United States
Environmental Protection
Agency
Office of Research and
Development
Washington DC 20460
EPA/600/P-93/004bF
July 1996
&EPA
Air Quality Criteria for
Ozone and Related
Photochemical Oxidants
Volume II of III
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EPA/600/P-93/004bF
July 1996
Air Quality Criteria for Ozone
and Related Photochemical Oxidants
Volume II of III
National Center for Environmental Assessment
Office of Research and Development
U.S. Environmental Protection Agency
Research Triangle Park, NC 27711
Printed on Recycled Paper
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Disclaimer
This document has been reviewed in accordance with U.S. Environmental
Protection Agency policy and approved for publication. Mention of trade names or
commercial products does not constitute endorsement or recommendation for use.
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Preface
In 1971, the U.S. Environmental Protection Agency (EPA) promulgated National
Ambient Air Quality Standards (NAAQS) to protect the public health and welfare from
adverse effects of photochemical oxidants. In 1979, the chemical designation of the standards
was changed from photochemical oxidants to ozone (O3). This document focuses primarily
on the scientific air quality criteria for O3 and, to a lesser extent, on those for other
photochemical oxidants such as hydrogen peroxide and the peroxyacyl nitrates.
The EPA promulgates the NAAQS on the basis of scientific information contained
in air quality criteria issued under Section 108 of the Clean Air Act. The previous O3 criteria
document, Air Quality Criteria for Ozone and Other Photochemical Oxidants, was released in
August 1986 and a supplement, Summary of Selected New Information on Effects of Ozone on
Health and Vegetation, was released in January 1992. These documents were the basis for a
March 1993 decision by EPA that revision of the existing 1-h NAAQS for O3 was not
appropriate at that time. That decision, however, did not take into account some of the newer
scientific data that became available after completion of the 1986 criteria document. The
purpose of this revised air quality criteria document for O3 and related photochemical
oxidants is to critically evaluate and assess the latest scientific data associated with exposure
to the concentrations of these pollutants found in ambient air. Emphasis is placed on the
presentation of health and environmental effects data; however, other scientific data are
presented and evaluated in order to provide a better understanding of the nature, sources,
distribution, measurement, and concentrations of O3 and related photochemical oxidants and
their precursors in the environment. Although the document is not intended to be an
exhaustive literature review, it is intended to cover all pertinent literature available through
1995.
This document was prepared and peer reviewed by experts from various state and
Federal governmental offices, academia, and private industry and reviewed in several public
meetings by the Clean Air Scientific Advisory Committee. The National Center for
Environmental Assessment (formerly the Environmental Criteria and Assessment Office) of
EPA's Office of Research and Development acknowledges with appreciation the contributions
provided by these authors and reviewers as well as the diligence of its staff and contractors in
the preparation of this document at the request of the Office of Air Quality Planning and
Standards.
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Air Quality Criteria for Ozone
and Related Photochemical Oxidants
Table of Contents
Volume I
1. Executive Summary 1-1
2. Introduction 2-1
3. Tropospheric Ozone and Its Precursors 3-1
4. Environmental Concentrations, Patterns, and Exposure Estimates 4-1
Appendix A: Abbreviations and Acronyms A-l
Volume II
5. Environmental Effects of Ozone and Related Photochemical
Oxidants 5-1
Appendix A: Abbreviations and Acronyms A-l
Appendix B: Colloquial and Latin Names B-l
Volume III
6. Toxicological Effects of Ozone and Related Photochemical Oxidants ... 6-1
7. Human Health Effects of Ozone and Related Photochemical Oxidants ... 7-1
8. Extrapolation of Animal Toxicological Data to Humans 8-1
9. Integrative Summary of Ozone Health Effects 9-1
Appendix A: Abbreviations and Acronyms A-l
l-v
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Table of Contents
Page
List of Tables II-xii
List of Figures II-xvi
Authors, Contributors, and Reviewers II-xxi
U.S. Environmental Protection Agency Science Advisory Board,
Clean Air Scientific Advisory Committee II-xxv
U.S. Environmental Protection Agency Project Team for Development
of Air Quality Criteria for Ozone and Related Photochemical Oxidants .... II-xxvii
5. ENVIRONMENTAL EFFECTS OF OZONE AND RELATED
PHOTOCHEMICAL OXIDANTS 5-1
5.1 INTRODUCTION 5-1
5.2 METHODOLOGIES USED IN VEGETATION RESEARCH ... 5-5
5.2.1 Fumigation Systems 5-5
5.2.1.1 Methodologies Discussed in the Air Quality
Criteria for Ozone and Other Photochemical
Oxidants 5-5
5.2.1.2 Methodologies Referenced Since the Air
Quality Criteria for Ozone and Other
Photochemical Oxidants 5-8
5.2.2 Experimental Design and Data Analysis 5-13
5.2.3 Mechanistic Process Models 5-15
5.2.4 Summary 5-16
5.3 SPECIES RESPONSE/MODE OF ACTION 5-18
5.3.1 Introduction 5-18
5.3.2 Ozone Uptake 5-19
5.3.2.1 Ozone Uptake by Plant Canopies 5-19
5.3.2.2 Ozone Absorption by Leaves 5-22
5.3.3 Resistance Mechanisms 5-24
5.3.3.1 Stomatal Limitation 5-24
5.3.3.2 Detoxification 5-26
5.3.4 Physiological Effects of Ozone 5-27
5.3.4.1 Carbohydrate Production and Allocation 5-30
5.3.4.2 Compensation 5-32
5.3.5 Role of Age and Size Influencing Response to Ozone . . 5-32
5.3.5.1 Summary 5-34
5.4 FACTORS THAT MODIFY PLANT RESPONSE 5-35
5.4.1 Modification of Functional and Growth Responses .... 5-35
5.4.2 Genetics 5-36
5.4.3 Environmental Biological Factors 5-47
I-VII
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Table of Contents (cont'd)
Page
5.4.3.1 Oxidant-Plant-Insect Interactions 5-47
5.4.3.2 Oxidant-Plant-Pathogen Interactions 5-51
5.4.3.3 Oxidant-Plant-Symbiont Interactions 5-56
5.4.3.4 Oxidant-Plant-Plant Interactions—
Competition 5-56
5.4.4 Physical Factors 5-57
5.4.4.1 Light 5-58
5.4.4.2 Temperature 5-58
5.4.4.3 Humidity and Surface Wetness 5-60
5.4.4.4 Drought and Salinity 5-60
5.4.5 Nutritional Factors 5-65
5.4.6 Interactions with Other Pollutants 5-67
5.4.6.1 Oxidant Mixtures 5-67
5.4.6.2 Sulfur Dioxide 5-68
5.4.6.3 Nitrogen Oxides, Nitric Acid Vapor,
and Ammonia 5-69
5.4.6.4 Hydrogen Fluoride and Other Gaseous
Pollutants 5-73
5.4.6.5 Acid Deposition 5-73
5.4.6.6 Heavy Metals 5-77
5.4.6.7 Mixtures of Ozone with Two or More
Pollutants 5-77
5.4.7 Interactions with Agricultural Chemicals 5-78
5.4.8 Factors Associated with Global Climate Change 5-79
5.4.9 Summary—Environmental Factors 5-82
5.5 EFFECTS-BASED AIR QUALITY EXPOSURE INDICES 5-84
5.5.1 Introduction 5-84
5.5.1.1 Biological Support for Identifying Relevant
Exposure Indices 5-84
5.5.1.2 Historical Perspective on Developing Exposure
Indices 5-85
5.5.2 Developing Exposure Indices 5-89
5.5.2.1 Experimental Design and Statistical Analysis . . 5-89
5.5.2.2 Studies with Two or More Different Patterns
of Exposure 5-91
5.5.2.3 Combinations of Years, Sites, or Species:
Comparisons of Yield Losses with Different
Exposure Durations 5-95
5.5.2.4 Comparisons of Measures of Exposure Based
on Reanalysis of Single-Year, Single-Species
Studies 5-105
I-VIII
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Table of Contents (cont'd)
Page
5.5.2.5 Comparison of Effects on Vegetation of
Cumulative "Peak" Versus "Mid-Level"
Ozone Exposures 5-117
5.5.3 Summary 5-136
5.6 EXPOSURE-RESPONSE OF PLANT SPECIES 5-137
5.6.1 Introduction 5-137
5.6.2 Summary of Conclusions from the Previous Criteria
Documents 5-137
5.6.3 Information in the Published Literature Since 1986 .... 5-142
5.6.3.1 Effects of Ozone on Short-Lived Species 5-144
5.6.4 Effects of Ozone on Long-Lived Plants 5-163
5.6.4.1 Perennial Agricultural Crops 5-164
5.6.4.2 Effects of Ozone on Deciduous Shrubs
and Trees 5-165
5.6.4.3 Effects of Ozone on Evergreen Trees 5-173
5.6.5 Assessments Using Ethylene Diurea as a Protectant .... 5-180
5.6.6 Summary 5-184
5.7 EFFECTS OF OZONE ON NATURAL ECOSYSTEMS 5-185
5.7.1 Introduction 5-185
5.7.2 Ecosystem Characteristics 5-186
5.7.3 Effects of Exposure to Ozone on Natural Ecosystems . . 5-188
5.7.3.1 The San Bernardino Forest Ecosystem—
Before 1986 5-188
5.7.3.2 The San Bernardino Forest Ecosystem—
Since 1986 5-193
5.7.3.3 The Sierra Nevada Mountains 5-196
5.7.3.4 The Appalachian Mountains—Before 1986 . . . 5-202
5.7.3.5 The Appalachian Mountains and the Eastern
United States—Since 1986 5-206
5.7.3.6 Rhizosphere and Mycorrhizal-Plant
Interactions 5-210
5.7.4 Ecosystem Response to Stress 5-215
5.7.4.1 Introduction 5-215
5.7.4.2 Forest Ecosystems 5-219
5.7.5 Summary 5-225
5.8 EFFECTS OF OZONE ON AGRICULTURE, FORESTRY,
AND ECOSYSTEMS: ECONOMICS 5-227
5.8.1 Introduction 5-227
5.8.2 Agriculture 5-228
5.8.2.1 Review of Key Studies from the 1986
Document 5-228
5.8.2.2 A Review of Post-1986 Assessments 5-231
l-ix
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Table of Contents (cont'd)
Page
5.8.2.3 Limitations and Future Research Issues 5-233
5.8.3 Forests (Tree Species) 5-234
5.8.4 Valuing Ecosystem Service Flows 5-235
5.8.4.1 Background 5-235
5.8.4.2 Nonmarket Valuation: Implications for
Ecosystem Service Flows 5-236
5.8.4.3 Challenges in Linking Valuation Techniques
to Ecosystem Service Flows 5-237
5.8.4.4 Valuing Ecosystem Service Flows:
Summary 5-237
5.8.5 Summary 5-238
5.9 SUMMARY AND CONCLUSIONS FOR VEGETATION AND
ECOSYSTEM EFFECTS 5-238
5.9.1 Introduction 5-238
5.9.2 Methodologies 5-240
5.9.3 Species Response/Mode of Action 5-241
5.9.3.1 Exposure Dynamics 5-242
5.9.3.2 Age and Size 5-243
5.9.4 Factors That Modify Plant Response to Ozone 5-243
5.9.4.1 Genetics 5-243
5.9.4.2 Environmental Factors 5-244
5.9.5 Effects-Based on Air Quality Exposure Indices 5-245
5.9.6 Exposure Response of Plant Species 5-248
5.9.6.1 Introduction 5-248
5.9.6.2 Predicted Crop Yield Losses 5-249
5.9.6.3 Predicted Biomass Changes in Trees 5-249
5.9.7 Effects of Ozone on Natural Ecosystems 5-250
5.9.8 Economic Assessments 5-252
5.10 EFFECTS OF OZONE ON MATERIALS 5-253
5.10.1 Introduction 5-253
5.10.2 Mechanisms of Ozone Attack and Antiozonant
Protection 5-253
5.10.2.1 Elastomers 5-253
5.10.2.2 Textile Fibers and Dyes 5-255
5.10.2.3 Paint 5-256
5.10.3 Exposure-Response Data 5-257
5.10.3.1 Elastomer Cracking 5-257
5.10.3.2 Dye Fading 5-264
5.10.3.3 Fiber Damage 5-271
5.10.3.4 Paint Damage 5-274
5.10.3.5 Cultural Properties Damage 5-276
l-x
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Table of Contents (cont'd)
Page
5.10.4 Economics 5-279
5.10.4.1 Introduction 5-279
5.10.4.2 Methods of Cost Classification and
Estimation 5-279
5.10.4.3 Aggregate Cost Estimates 5-280
5.10.5 Summary and Conclusions 5-282
REFERENCES 5-285
APPENDIX 5A: ABBREVIATIONS AND ACRONYMS A-l
APPENDIX 5B: COLLOQUIAL AND LATIN NAMES B-l
l-xi
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List of Tables
Number Page
5-1 Comparison of Fumigation Systems for Ozone Exposure-Plant
Response Studies 5-17
5-2 Examples of Intraspecific Variation of Foliar Symptoms in
Ozone Response 5-37
5-3 Examples of Intraspecific Variation in Growth Responses
Following Ozone Exposures 5-38
5-4 Mortality of Three Ozone Sensitivity Classes of Eastern White
Pine Trees During 1971 to 1986 5-44
5-5 Examples of Ozone Effects on Pollen Germination and Tube
Elongation 5-46
5-6 Ozone Effects on Insect Pests 5-49
5-7 Ozone-Plant-Pathogen Interactions 5-52
5-8 Field Studies of Ozone-Drought Stress Interactions in Crop
Species 5-62
5-9 Ozone-Soil Nutrient Interactions 5-66
5-10 Some Statistical Models of Combined Ozone and Sulfur Dioxide
Responses 5-70
5-11 References to Reports of Interaction or No Interaction Between
Ozone and Acid Rain or Acid Fog 5-74
5-12 A Summary of Studies Reporting the Effects of Ozone for Two
or More Exposure Patterns on the Growth, Productivity, or
Yield of Plants 5-94
5-13 A Summary of Studies Reporting the Effects of Ozone on the
Growth, Productivity, or Yield of Plants for Two or More
Replicate Studies Having Equal Total Exposures and Either
Varying or Similar Durations 5-97
I-XII
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List of Tables (cont'd)
Number Page
5-14 Summary of Ozone Exposures That Are Closest to Those
Predicted for 20 Percent Yield Reduction per SUM06 Exposure
Response Models Used by Lee et al. (1991) in Selected
National Crop Loss Assessment Network Experiments 5-107
5-15 Summary of Percentiles for Ozone Monitoring Sites in 1989
with a Maximum Three-Month SUM06 Value Less Than
24.4 ppm per Hour but with a Second Hourly Maximum
Concentration Greater Than or Equal to 0.125 ppm 5-109
5-16 Summary of Percentiles for Ozone Monitoring Sites in 1989
with a Maximum Three-Month SUM06 Value Greater Than
or Equal to 24.4 ppm per Hour but with a Second Hourly
Maximum Concentration Less Than 0.125 ppm 5-110
5-17 Ozone Concentrations for Short-Term Exposures That Produce
5 or 20 Percent Injury to Vegetation Grown Under Sensitive
Conditions 5-119
5-18 A Summary of Studies Reporting Effects of Peaks or Mid-Range
Concentrations 5-120
5-19 Estimates of the Parameters for Fitting the Weibull Model Using
the Seven-Hour Seasonal Mean Ozone Concentrations 5-140
5-20 Summary of Ozone Exposure Indices Calculated for Three- or
Five-Month Growing Seasons from 1982 to 1991 5-145
5-21 Comparison of Exposure-Response Curves Calculated Using the
Three-Month, 24-Hour SUM06 Values for 54 National Crop Loss
Assessment Network Cases 5-146
5-22 Comparison of Exposure-Response Curves Calculated Using the
24-Hour W126 Values for 54 National Crop Loss Assessment
Network Cases 5-149
5-23 The Exposure Levels Estimated to Cause at Least 10 Percent
Crop Loss in 50 and 75 Percent of Experimental Cases 5-152
5-24 SUM06 Levels Associated with 10 and 20 Percent Yield Loss
for 50 and 75 Percent of the National Crop Loss Assessment
Network Crop Studies 5-153
I-XIII
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List of Tables (cont'd)
Number Page
5-25 A Summary of Studies Reporting the Effects of Ozone on the
Growth, Productivity, or Yield of Annual Plants Published
Since U.S. Environmental Protection Agency (1986) 5-154
5-26 A Summary of Studies Reporting the Effects of Ozone on the
Growth, Productivity, or Yield of Perennial Crop Plants
Published Since U.S. Environmental Protection Agency (1986) . . . 5-161
5-27 A Summary of Studies Reporting the Effects of Ozone on the
Growth or Productivity of Deciduous Shrubs and Trees
Published Since U.S. Environmental Protection Agency (1986) . . . 5-166
5-28 Exposure-Response Equations That Relate Total Biomass to
24-Hour SUM06 Exposures Adjusted to 92 Days 5-169
5-29 SUM06 Levels Associated with 10 and 20 Percent Total Biomass
Loss for 50 and 75 Percent of the Seedling Studies 5-171
5-30 A Summary of Studies Reporting the Effects of Ozone on the
Growth or Productivity of Evergreen Trees Published
5-31
5-32
5-33
5-34
5-35
5-36
Since U.S. Environmental Protection Agency (1986)
Effects of Ethylene Diurea on Ozone Responses
San Bernardino Forest — Status 1972
Ecosystem Response to Pollutant Stress
Growing Season Summary Statistics for Ozone Monitoring Sites
in or Near Forests for the Period 1980 through 1988
Interactions of Ozone and Forest Tree Ectomycorrhizae
Interaction of Air Pollution and Temperate Forest Ecosystems
5-174
5-181
5-189
5-192
5-197
5-213
Under Conditions of Intermediate Air Contaminant Load 2-219
5-37 Properties of Ecological Systems Susceptible to Ozone at
Four Levels of Biological Organization 2-221
5-38 Recent Studies of the Economic Effects of Ozone and Other
Pollutants on Agriculture 5-230
l-xiv
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List of Tables (cont'd)
Number Page
5-39 Studies of the Economic Effects of Ozone and Other Pollutants
on Forests 5-235
5-40 Laboratory and Field Studies on Effects of Ozone on
Elastomers 5-258
5-41 Protection of Tested Rubber Materials 5-261
5-42 Effect of Ozone and Humidity on Interply Adhesion 5-263
5-43 Laboratory and Field Studies of the Effects of Ozone on Dye
Fading 5-265
5-44 Laboratory and Field Studies of the Effects of Ozone on
Fibers 5-272
5-45 Laboratory and Field Studies of the Effects of Ozone on
Architectural/Industrial Paints and Coatings 5-275
5-46 Laboratory Studies of the Effects of Ozone on Artists' Pigments
and Dyes 5-277
5-47 Summary of Damage Costs to Materials by Oxidants 5-281
ll-xv
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List of Figures
Number Page
5-1 Leaf absorption and possible functional changes that may occur
within the plant 5-3
5-2 Uptake of ozone from the atmosphere 5-20
5-3 Movement of gases into and out of leaves is controlled primarily
by the stomata 5-23
5-4 Simulation of the effects of diurnal variation in stomatal aperture
and in ozone concentration on ozone uptake: diurnal ozone
concentrations, simulated conductance, and ozone uptake 5-25
5-5 Effects of ozone absorption into a leaf 5-28
5-6 Effect of ozone on plant function and growth 5-29
5-7 The average injury index for visible foliar injury after exposure
of one-year-old seedlings to 50 pphm ozone for 7.5 hours 5-40
5-8 Frequency distribution showing the variability in ozone response
within one half-sib family of loblolly pine exposed to
increasing levels of ozone under chronic-level field conditions
over several growing seasons 5-41
5-9 Distribution pattern showing the number of ozone concentrations
within specified ranges for the 1983 winter wheat proportional-
addition experiment for the 1.4 times ambient air and 1.8 times
ambient air treatments and for San Bernardino, California,
in 1987 5-92
5-10 Comparison of the Weibull exposure-response functions and its
predicted relative yield loss curves using the seven-hour mean
exposure and daytime SUM06 for replicate years of National Crop
Loss Assessment Network Program's data for cotton, wheat,
kidney bean, and potato, respectively 5-100
l-xvi
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List of Figures (cont'd)
Number Page
5-11 Predicted relative yield losses for Acala SJ-2 cotton for four
sites and multiple years (1981, 1982, 1988, and 1989) relative
to 0.01 ppm for the seven-hour mean exposure, 0.035 ppm for the
second highest daily maximum concentration, 0 ppm per hour for SIGMOID,
and 0 ppm per hour for SUM06, which correspond to typical levels
in the charcoal-filtered chambers 5-101
5-12 Relative effect of ozone on growth and yield of spring wheat
cultivars from two growing seasons 5-102
5-13 Weibull exposure-response curves for the relative effect of
ozone on grain yield of spring wheat for three years,
individually and combined 5-103
5-14 Quadratic exposure-response curves for the relative effect of
ozone on grain yield of spring wheat in 1989 and 1990, using
four different exposure indices 5-104
5-15 Percent reduction in net photosynthesis of pines and
agricultural crops in relation to total ozone exposure,
for several ranges of peak concentrations 5-111
5-16 Percent reduction in net photosynthesis and biomass growth of
coniferous species in relation to total exposure and estimated
total ozone uptake 5-112
5-17 Percent reduction in net photosynthesis and biomass growth of
hardwood species in relation to total exposure and estimated
total ozone uptake 5-113
5-18 Percent reduction in net photosynthesis and biomass growth of
agricultural crops in relation to total exposure and estimated
total ozone uptake 5-114
5-19 Percent reduction in biomass growth of tree seedlings in
relation to total exposure 5-115
5-20 Reduction in volume production of loblolly pine seedlings in
relation to four exposure indices 5-116
I-XVII
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List of Figures (cont'd)
Number Page
5-21 A comparison between the resulting cumulative frequencies for
the exposure parameters, sum of all hourly average
concentrations and the sigmoidally weighted integrated exposure
index, W126 5-117
5-22 Fumigation schedule of uniform and simulated ambient ozone
concentration distributions at two equivalent dose levels 5-123
5-23 Fumigation schedule of uniform and simulated ambient ozone
concentration distributions at two dose levels 5-124
5-24 Experimental ozone exposure profiles 5-125
5-25 Ozone exposure profiles for 1983 season 5-127
5-26 Mean foliar injury on tobacco Bel W3 and mean ozone
concentrations for the years 1979 to 1988, mean foliar injury on
tobacco Bel W3 and ozone concentrations for weekly exposures
during the 1988 growing season, maximal foliar injury on
tobacco Bel W3 in relation to ozone concentrations for 1988, and
mean foliar injury on subterranean clover cv. Geraldton and
mean ozone concentrations for two weekly exposures during
the 1988 growing season 5-129
5-27 Maximum foliar injury on tobacco Bel W3 in relation to ozone
concentrations expressed in classes of 10 |ig/m3 for 1979 to
1983, and maximum foliar injury on two bean cultivars in
relation to ozone concentrations for 1982 and 1983 5-130
5-28 Summary hourly ambient ozone concentrations during nine
weeks of experimentation (1990) at Montague-Amherst,
Massachusetts, and summary hourly ambient ozone
concentrations during nine weeks of experimentation (1990)
at Mount Equinox 5-133
I-XVIII
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List of Figures (cont'd)
Number Page
5-29 Box-plot distribution of biomass loss predictions from Weibull
and linear exposure-response models that relate biomass and
ozone exposure as characterized by the 24-hour SUM06 statistic
using data from 31 crop studies from the National Crop Loss
Assessment Network and 26 tree seedling studies conducted at
U.S. Environmental Protection Agency's Environmental Research
Laboratory in Corvallis, Oregon; Smoky Mountains National
Park, Tennessee; Michigan; Ohio; and Alabama 5-160
5-30 Effects of ozone on plant function and growth 5-187
5-31 Total oxidant concentrations at Rim Forest in Southern California
during May through September, 1968 through 1972 5-190
5-32 Total basal area for each species as percent of the total basal
area for all species in 1974 and 1988 on plots with severe to
moderate damage, plots with slight damage, and plots with very
slight damage or no visible symptoms 5-194
5-33 Impact of a reduced supply of carbon to the shoot, or water and
nitrogen to the roots, on subsequent allocation of carbon 5-211
5-34 Carbon uptake through photosynthesis is made available to a
general pool of carbohydrates used in construction and
maintenance of various tissues 5-217
5-35 Organizational levels at which air pollutants have been shown to
affect the growth-related process of forest trees 5-218
5-36 Effects of environmental stress on forest trees are presented on a
hierarchial scale for leaf, branch, tree, and stand levels of
organization 2-222
5-37 Postulated mechanism for damage to elastomers by ozone 5-254
5-38 Reaction of anthraquinone dyes with ozone and with nitrogen
oxides 5-256
5-39 Relative decrease in stress with time as a function of ozone
concentration for polyisoprene vulcanizate 5-261
l-xix
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List of Figures (cont'd)
Number Page
5-40 Relaxation of rubber compounds in ozone is affected by the
combination of rubber formulation and type of ozone
protection 5-262
ll-xx
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Authors, Contributors, and Reviewers
Chapter 5. Environmental Effects of Ozone
and Related Photochemical Oxidants
Principal Authors
Dr. Richard M. Adams—Department of Agriculture and Resource Economics, Oregon State
University, Corvallis, OR 97331
Dr. Christian Andersen—Environmental Research Laboratory, U.S. Environmental Protection
Agency, 200 SW 35th Street, Corvallis, OR 97333
Dr. J.H.B. Garner—National Center for Environmental Assessment (MD-52),
U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Dr. Beverly A. Hale—Department of Horticultural Science, University of Guelph, Guelph,
Ontario, NIG 2W1, Canada
Dr. William E. Hogsett—Environmental Research Laboratory, U.S. Environmental Protection
Agency, 200 SW 35th Street, Corvallis, OR 97333
Dr. David F. Karnosky—School of Forestry and Wood Products, Michigan Technological
University, Houghton, MI 49931
Dr. John Laurence—Boyce Thompson Institute for Plant Research at Cornell University,
Tower Road, Ithaca, NY 14853
Dr. E. Henry Lee—ManTech Environmental Technology, Inc., 1600 W. Western Boulevard,
Corvallis, OR 97333
Dr. Allen S. Lefohn—A.S.L. & Associates, 111 Last Chance Gulch, Suite 4A,
Helena, MT 59601
Dr. Paul Miller—Pacific Southwest Forest and Range Experiment Station, USDA-Forest
Service Fire Lab, 4955 Canyon Crest Dr., Riverside, CA 92507
Mr. Doug Murray—TRC Environmental Corporation, 5 Waterside Crossing,
Windsor, CT 06095
Dr. Victor Runeckles—Department of Plant Science, University of British Columbia,
Vancouver, British Columbia, V6T 1Z4, Canada
l-xxi
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Authors, Contributors, and Reviewers (cont'd)
Dr. James A. Weber—Environmental Research Laboratory, U.S. Environmental Protection
Agency, 200 SW 35th Street, Corvallis, OR 97333
Dr. Ruth D. Yanai—Boyce Thompson Institute for Plant Research at Cornell University,
Tower Road, Ithaca, NY 14853
Reviewers
Ms. Vicki Atwell—Office of Air Quality Planning and Standards (MD-12),
U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Dr. Glen R. Cass—Environmental Engineering Science Department, Mail Code 138-78,
California Institute of Technology, Pasadena, CA 91125
Dr. Arthur Chapelka—Auburn University School of Forestry, Auburn, AL 36849-4201
Dr. Robert Goldstein—Electric Power Research Institute, 3412 Hillview Ave., Palo Alto, CA
94303
Dr. Marcia Gumpertz—Department of Statistics, North Carolina State University, Raleigh, NC
27695
Dr. Allen Heagle—U.S. Department of Agriculture, ARS, 1505 Varsity Drive,
Raleigh, NC 27606
Dr. Robert Heath—Dept. of Botany and Plant Science, University of California, Riverside, CA
92521
Dr. Thomas M. Hinckley—School of Forest Resources, University of Washington,
Seattle, WA 98195
Dr. Robert Kohut—Boyce Thompson Institute, Cornell University, Tower Road,
Ithaca, NY 14853-1801
Dr. Virginia Lesser—Department of Statistics, Oregon State University, Corvallia, OR 97333
Dr. Fred Lipfert—23 Carll Ct, Northport, NY 11768
Dr. Patrick McCool—SAPRC, University of California, Riverside, CA 92521
Dr. Delbert McCune—Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, NY
14853-1801
I-XXII
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Authors, Contributors, and Reviewers (cont'd)
Dr. Robert Musselman—U.S. Department of Agriculture, Forestry Service, Rocky Mountain
Experiment Station, 240 West Prospect Road, Fort Collins, CO 80526
Dr. Eva Pell—Pennsylvania State University, Department of Plant Pathology, 321 Buckhout
Laboratory, University Park, PA 16802
Dr. Phillip Rundel—Laboratory of Biomedical and Environmental Science, University of
California, LA, 900 Veterans Ave., Los Angeles, CA 90024
Dr. Jayson Shogren—School of Forestry and Environmental Studies, Yale University,
New Haven, CT 06511
Dr. James Shortle—Department of Agricultural Economics, Pennsylvania State University,
Armsby Building, 208C, University Park, PA 16802-5502
Dr. John Skelly—Pennsylvania State University, 108 Buckhout Laboratory,
University Park, PA 16802
Dr. Boyd Strain—Department of Botany, 136 Biology Science Building, Duke University,
Durham, NC 27708
Dr. George E. Taylor, Jr.—Biological Sciences Center, Desert Research Institute,
7010 Dandini Blvd., Reno, NV 89512
Dr. Patrick Temple—Statewide Air Pollution Research Center, University of California,
Riverside, CA 92521-0312
Dr. David Tingey—U.S. Environmental Protection Agency, Environmental Research
Laboratory, 200 SW 35th Street, Corvallis, OR 97333
Dr. Michael Unsworth—Department of Atmospheric Sciences, Oregon State University,
Corvallis, OR 97333
Dr. David Weinstein—Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, NY
14853-1801
Dr. John Yocom, 12 Fox Den Road, West Simsbury, CT 06092
I-XXIII
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U.S. Environmental Protection Agency
Science Advisory Board
Clean Air Scientific Advisory Committee
Ozone Review
Chairman
Dr. George T. Wolff—General Motors Corporation, Environmental and Energy Staff,
General Motors Bldg., 12th Floor, 3044 West Grand Blvd., Detroit, MI 48202
Members
Dr. Stephen Ayres—Office of International Health Programs, Virginia Commonwealth
University, Medical College of Virginia, Box 980565, Richmond, VA 23298
Dr. Jay S. Jacobson—Boyce Thompson Institute, Tower Road, Cornell University, Ithaca, NY
14853
Dr. Joseph Mauderly—Inhalation Toxicology Research Institute, Lovelace Biomedical and
Environmental Research Institute, P.O. Box 5890, Albuquerque, NM 87185
Dr. Paulette Middleton—Science & Policy Associates, Inc., Western Office, Suite 140,
3445 Penrose Place, Boulder, CO 80301
Dr. James H. Price, Jr.—Research and Technology Section, Texas Natural Resources
Conservation Commission, P.O. Box 13087, Austin, TX 78711
Invited Scientific Advisory Board Members
Dr. Morton Lippmann—Institute of Environmental Medicine, New York University Medical
Center, Long Meadow Road, Tuxedo, NY 10987
Dr. Roger O. McClellan—Chemical Industry Institute of Toxicology, P.O. Box 12137,
Research Triangle Park, NC 27711
Consultants
Dr. Stephen D. Colome—Integrated Environmental Services, University Tower, Suite 280,
4199 Campus Drive, Irvine, CA 92715
11-XXV
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U.S. Environmental Protection Agency
Science Advisory Board
Clean Air Scientific Advisory Committee
(cont'd)
Dr. A. Myrick Freeman—Department of Economics, Bowdoin College, Brunswick, ME 04011
Dr. Allan Legge—Biosphere Solutions, 1601 llth Avenue, NW, Calgary, Alberta T2N 1H1,
CANADA
Dr. William Manning—Department of Plant Pathology, University of Massachusetts, Amherst,
MA 01003
Dr. D. Warner North—Decision Focus, Inc., 650 Castro Street, Suite 300, Mountain View,
CA 94041
Dr. Frank E. Speizer—Harvard Medical School, Channing Lab, 180 Longwood Avenue,
Boston, MA 02115
Dr. George E. Taylor—Department of Environmental and Resource Sciences, 130 Fleischmann
Agriculture Bldg. 199, University of Nevada, Reno, NV 89557
Dr. Mark J. Utell—Pulmonary Disease Unit, Box 692, University of Rochester Medical
Center, 601 Elmwood Avenue, Rochester, NY 14642
Designated Federal Official
Mr. Randall C. Bond—Science Advisory Board (1400), U.S. Environmental Protection
Agency, 401 M Street, SW, Washington, DC 20460
Staff Assistant
Ms. Lori Anne Gross—Science Advisory Board (1400), U.S. Environmental Protection
Agency, 401 M Street, SW, Washington, DC 20460
I-XXVI
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U.S. Environmental Protection Agency
Project Team for Development of Air Quality Criteria
for Ozone and Related Photochemical Oxidants
Scientific Staff
Mr. James A. Raub—Health Scientist, National Center for Environmental Assessment
(MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Dr. A. Paul Altshuller—Physical Scientist, National Center for Environmental Assessment
(MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Mr. William G. Ewald—Health Scientist, National Center for Environmental Assessment (MD-
52), U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Dr. J.H.B. Garner—Ecologist, National Center for Environmental Assessment (MD-52),
U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Dr. Judith A. Graham—Associate Director, National Center for Environmental Assessment
(MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Ms. Ellie R. Speh—Secretary, National Center for Environmental Assessment (MD-52),
U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Ms. Beverly E. Tilton—Physical Scientist, National Center for Environmental Assessment
(MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC 27711
Technical Support Staff
Mr. Douglas B. Fennell—Technical Information Specialist, National Center for Environmental
Assessment (MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC
27711
Mr. Allen G. Hoyt—Technical Editor and Graphic Artist, National Center for Environmental
Assessment (MD-52), U.S. Environmental Protection Agency, Research Triangle Park, NC
27711
Ms. Diane H. Ray—Technical Information Manager (Public Comments), National Center for
Environmental Assessment (MD-52), U.S. Environmental Protection Agency, Research
Triangle Park, NC 27711
I-XXVII
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U.S. Environmental Protection Agency
Project Team for Development of Air Quality Criteria
for Ozone and Related Photochemical Oxidants
(cont'd)
Mr. Richard N. Wilson—Clerk, National Center for Environmental Assessment (MD-52), U.S.
Environmental Protection Agency, Research Triangle Park, NC 27711
Document Production Staff
Ms. Marianne Barrier—Graphic Artist, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Mr. John R. Barton—Document Production Coordinator, ManTech Environmental Technology,
Inc., P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Lynette D. Cradle—Word Processor, ManTech Environmental Technology, Inc., P.O. Box
12313, Research Triangle Park, NC 27709
Ms. Shelia H. Elliott—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Sandra K. Eltz—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Jorja R. Followill—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Sheila R. Lassiter—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Wendy B. Lloyd—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Carolyn T. Perry—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. Cheryl B. Thomas—Word Processor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Mr. Peter J. Winz—Technical Editor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
I-XXVIII
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U.S. Environmental Protection Agency
Project Team for Development of Air Quality Criteria
for Ozone and Related Photochemical Oxidants
(cont'd)
Technical Reference Staff
Mr. John A. Bennett—Bibliographic Editor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
Ms. S. Blythe Hatcher—Bibliographic Editor, Information Organizers, Inc., P.O. Box 14391,
Research Triangle Park, NC 27709
Ms. Susan L. McDonald—Bibliographic Editor, Information Organizers, Inc., P.O. Box 14391,
Research Triangle Park, NC 27709
Ms. Carol J. Rankin—Bibliographic Editor, Information Organizers, Inc., P.O. Box 14391,
Research Triangle Park, NC 27709
Ms. Deborah L. Staves—Bibliographic Editor, Information Organizers, Inc., P.O. Box 14391,
Research Triangle Park, NC 27709
Ms. Patricia R. Tierney—Bibliographic Editor, ManTech Environmental Technology, Inc.,
P.O. Box 12313, Research Triangle Park, NC 27709
l-xxix
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5
Environmental Effects of Ozone and
Related Photochemical Oxidants
5.1 Introduction
Analyses of photochemical oxidants in the ambient air have revealed the presence
of a number of phytotoxic compounds, including ozone (O3), peroxyacyl nitrates (PANs), and
nitrogen dioxide (NO2). Ozone, the most prevalent photochemical oxidant, has been studied
the most, and its effects are understood better than those of other photochemically derived
oxidants. Ozone affects vegetation throughout the United States, impairing crops, native
vegetation, and ecosystems more than any other air pollutant (Heck et al., 1980). The
phytotoxicity of nitrogen oxides has been assessed in Air Quality Criteria for Oxides of
Nitrogen (U.S. Environmental Protection Agency, 1993) and will not be discussed here.
On the basis of concentration, the PANs are more toxic than O3, with peroxyacetyl nitrate
(PAN) being about 10 times more phytotoxic than O3 (Darley et al., 1963; Taylor and
MacLean, 1970; Pell, 1976). Although more phytotoxic than O3, PANs generally occur at
significantly lower ambient concentrations and are distributed less widely than those of O3.
Ambient concentrations of O3 and PAN, as well as their concentration ratios, are discussed in
detail in Chapter 4.
The effects of photochemical oxidants were observed first as foliar injury on
vegetation growing in localized areas in Los Angeles County, CA (Middleton et al., 1950).
In these early reports, foliar injury was described as glazing, silvering, and bronzing of the
lower leaf surface of leafy vegetables and as transverse bands of injury on monocotyledonous
species. Subsequent studies showed that these symptoms of photochemical oxidant injury
were caused by PAN (Taylor et al., 1960). The characteristic O3 stipple on grape (Vitis
labruscana) leaves reported in the late 1950s was the first observation of O3 injury to
vegetation in the field (Richards et al., 1958). Subsequent studies with tobacco (Nicotiana
tabacum) and other crops confirmed that O3 was injuring vegetation at sites near urban
centers (Heggestad and Middleton, 1959; Daines et al., 1960). It now is recognized that
vegetation at rural sites may be injured by O3 transported long distances from urban centers
(Edinger et al., 1972; Heck et al., 1969; Heck and Heagle, 1970; Wolff et al., 1977a,b,c,
1980; Wolff and Lioy, 1980; Kelleher and Feder, 1978; Miller et al., 1972; Skelly et al.,
1977; Skelly, 1980; Garner et al., 1989; see also Chapters 3 and 4). Concentrations of O3 in
polluted air masses often remain high for prolonged periods in rural areas, increasing the
concern over possible effects on agriculture, forests, and native ecosystems.
Exposure to tropospheric O3 can cause injury and premature mortality of plant
tissues after entering the plant because O3 has strong oxidizing properties and reacts with
5-1
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cellular components. The effects of O3 on terrestrial ecosystems begin with the responses of
individual plants (Figure 5-1). Effects are initiated within the plant by reactions between
O3 or its metabolites and cellular constituents that influence biochemical and physiological
processes and alter plant growth. Plant sensitivity to O3 varies widely among individuals and
among species. Sensitivity is determined both by genetic composition of the plant and
environmental conditions. Plant response also is influenced by factors such as pollutant
concentration, duration of exposures, plant nutrition, developmental stage, climate, insects,
and diseases (See Sections 5.3 and 5.4).
Changes in foliar pigmentation and development of injured tissues are usually the
first visible sign of injurious O3 exposures and indicate impairment of physiological processes
with the leaves. To affect metabolic processes within the cell, sufficient amounts of O3 from
the atmosphere must be able to enter the plant through the leaf stomata and dissolve in the
aqueous layer lining the air spaces. Ozone and its decomposition products then diffuse
through the cell membrane, where they can react with cellular components (unless the plant is
able to detoxify or metabolize O3 or its metabolites) (Section 5.3; Tingey and Taylor, 1982).
Ozone can affect all aspects of plant growth (Figure 5-1). Plants accumulate,
store, and use carbon compounds to build their structure and maintain physiological processes
(Waring and Schlesinger, 1985). Within the leaf, carbon dioxide (CO2) absorbed from the
atmosphere is converted to carbohydrates during the process of photosynthesis. The water
and minerals necessary for growth are absorbed by plants from the soil. Growth and seed
formation depend not only on the rate of photosynthesis and uptake of water and nutrients,
but also on the subsequent metabolic processes and the allocation of the carbohydrates
produced during photosynthesis. Most plants require a balance of resources (i.e, energy,
water, mineral nutrients) to maintain optimal growth, but these are seldom available in natural
environments (Chapin et al., 1987). Plants compensate for injury or stress by allocating their
available resources to the point of injury or stress (McLaughlin et al., 1982; Miller et al.,
1982; Tingey et al., 1976b). Altering the allocation of carbohydrates has been shown to
decrease plant vigor, to increase susceptibility to insect pests and fungal pathogens, to
interfere with mycorrhizal formation, and to reduce plant growth and reproduction
(McLaughlin et al., 1982; Miller et al., 1982; U.S.Environmental Protection Agency, 1986;
Garner et al., 1989).
Most of the available information concerning the effects of O3 on vegetation is the
result of exposure-response studies of important agricultural crops and some selected forest
tree species, usually as seedlings. Through the years, crop plants, because of human food
demand, usually have been selected for their productivity. They are grown as monocultures,
fertilized, weeded, and frequently irrigated. In other words, competition for water nutrients,
space, and light is minimized greatly when compared with plants growing in natural
conditions, particularly in ecosystems. Trees for timber and paper also are grown on
plantations under conditions favoring the greatest production.
Some O3 exposures (concentration and duration) result in visible foliar injury to the
plant without growth reduction; other exposures result in growth reduction and decrease in
productivity without visible injury, whereas some exposures result in both. Data is presented
in Section 5.6 that deals with the impact of different concentrations and exposure durations
from many different experimental exposure-response studies on the growth of a variety of
cultivated crops, ornamental species, and natural vegetation.
5-2
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Atmospheric Processes
Canopy Processes
Leaf Processes/1
Ozone Uptake
Leaf Processes/
Mode of Action
| Plant Response)
Ecosystem Response
[Reduced Photosynthesis]
I
[Reduced Carbohydrate Production]
*
[Reduced Carbohydrate Allocation J
[Compensation)
'[Detoxification)
[Reduced Growth]
i
[Reduced Reproduction]
*
(Increased Susceptibility to]
Biotic and Abiotic Stresses]
Decrease in Mycorrhizael
Formation I
[ Individual Response)
[ Population Response)
I
[Community Response)
I
[ Ecosystem Response]
Figure 5-1. Leaf absorption and possible functional changes that may occur within the
plant. Ecosystem response begins at the level of the individual and is
propagated to the more complex level of organization.
5-3
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The number of crop species and cultivars for which information regarding
O3 effects exists encompasses a mere fraction of the total of those cultivated as crops or
found growing in natural communities. It is not possible to predict the sensitivity of the
species and cultivars that have not been investigated, except in very general terms, because of
the wide range of sensitivities to O3 known to exist among crop cultivars and species that
have been studied. Attempts to develop a general framework of response covering a range of
species using the fragmented knowledge available have not been successful.
For many years, attempts have been made to develop mathematical equations that
quantify the relationship between pollutant exposure and agricultural crop yield. The
advantages and limitations of the various indices that have been developed to aid in predicting
the effects of O3 on crop yield are discussed in Section 5.5.
Organisms, not ecosystems, respond to O3 exposure (Sigal and Suter, 1987). The
only well-documented study of ecosystem change is that of the San Bernardino Mixed Forest
ecosystem in Southern California where the impact of O3 on the keystone species, ponderosa
and Jeffrey pine (Pinns Jeffreyi), resulted in the reversion of the forest to a simpler stage
(Miller et al., 1982; Miller, 1984; U.S. Environmental Protection Agency, 1978, 1986).
In other regions of the United States, most of the data available for assessing ecosystem
responses deals with the responses of individuals to experimental O3 exposures. Studies
within the forests of the eastern United States, have dealt chiefly with the response in the
field of eastern white pine (Pinus strobus) (McLaughlin et al., 1982; Skelly, 1980; Skelly
et al., 1984). No long-term studies exist that deal with the impacts of O3 on the various
ecosystems components and how and whether these impacts alter ecosystem structure and
functions. Therefore, the determination of the impact of O3 on eastern forest ecosystems is
difficult, if not impossible (see Section 5.7).
Plant populations are affected if they include many sensitive individuals. Removal
of sensitive individuals within populations, or stands, if large in number, ultimately can
change community and ecosystem structure (Figure 5-1). Structural changes that alter the
ecosystem functions of energy flow and nutrient cycling can arrest or reverse ecosystem
development (Odum, 1985).
The sequential organization of this chapter begins first with the methodologies
(Section 5.2) that have been used to obtain the information presented and discussed in this
chapter. Next, Section 5.3 explains the known biochemical and physiological changes that
occur within the leaf cells after O3 entry into the plants and how these chemical responses
affect plant vigor, growth, and reproduction. Factors within and external to plants influence
their response to O3 and other stresses. These factors, as observed during experimental
exposures and in the field, can modify functional growth responses of plants to O3 (see
Section 5.4). The development of indices or exposure statistics that may be used in
quantifying and predicting crop responses to O3 exposures are found in Section 5.5. Data
obtained from many experimental exposure-response studies using methodologies presented in
Section 5.2 and the basis for the development of the indices discussed in Section 5.5 are
presented in Section 5.6. The information available on the ecosystem effects of O3 and the
data needed for more definitive assessments are found in Section 5.7. The costs to the nation
of O3 exposure of crops and ecosystems is discussed in Section 5.8. The scientific names of
the plants cited in this chapter are presented in Appendix B. Section 5.10 discusses the
effects of O3 on nonbiological materials.
5-4
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5.2 Methodologies Used in Vegetation Research
5.2.1 Fumigation Systems
The methodologies used in vegetation research have become more sophisticated
over the years as new technology has developed. New exposure systems have been devised
with pollutant dispensing systems that make it possible to more nearly duplicate the exposures
plants receive in the field. These systems and their good points and shortcomings are
discussed below.
Ozone fumigation plant-response studies require the fumigation of well-
characterized vegetation to varying O3 regimes. The variation in O3 regimes may be achieved
by controlled fumigation, chemical/mechanical exclusion or natural gradients of O3.
Controlled O3 fumigation systems are designed to maintain a modified gaseous atmosphere
around a plant for a period of exposure, for the purpose of monitoring plant responses to that
modified gaseous atmosphere. All fumigation systems share some common features: general
plant growth conditions (light, temperature, humidity, CO2, and soil moisture) must be met,
and differential concentrations of O3 generated either artificially or naturally must be supplied
to the vegetation and maintained during the exposure period. Exposure systems have been
established in controlled environments, greenhouses, and the field. Many of these were
described in the earlier criteria document, Air Quality Criteria for Ozone and Other
Photochemical Oxidants (U.S. Environmental Protection Agency, 1986). More recent reviews
of wet and dry deposition exposure systems have refined the knowledge of the strengths and
limitations of experimental approaches for studying the effects of O3, alone or in combination
with other pollutants, on crops and trees (Hogsett et al., 1987a,b; Griinhage and Jager, 1994a;
Manning and Krupa, 1992). Controlled fumigation systems may range from cuvettes, which
enclose leaves or branches (Bingham and Coyne, 1977; Legge et al., 1978), to a series of
tubes with calibrated orifices spatially distributed over a field to emit gaseous pollutants to a
plant canopy (Lee et al., 1978). Systems that exclude O3 by mechanical or chemical means
have been used, as have natural gradients of O3, to evaluate vegetation response to ambient
03.
5.2.1.1 Methodologies Discussed in the Air Quality Criteria for Ozone and Other
Photochemical Oxidants (U.S. Environmental Protection Agency, 1986)
Controlled Environment Exposure Systems
Controlled environment fumigation systems are those in which light sources and
control of temperature and relative humidity are artificial. Light quality and quantity are
likely to be lower than in ambient environments, usually resulting in lower photosynthetically
active radiation (PAR). Temperature and relative humidity likely will be more consistent in a
controlled environment than in ambient air. Controlled environment exposure systems are
typified by the widely used continuous stirred tank reactor (CSTR), a system originally
designed for mass balance studies of O3 flux to vegetation. The CSTR chambers have
distinct advantages for gas exchange studies because fluxes can be calculated readily when
controlling for environmental and pollutant conditions. The rapid air mixing minimizes
horizontal and vertical gradients within chambers as well as leaf boundary layer resistance.
Disadvantages of CSTR chambers include the following: the artificial pollution and growing
conditions may not represent natural exposure conditions, the rapid air movement may cause
wind injury to sensitive plants, the size of chambers restricts the study of large plants, and
lighting systems are problematic and provide subambient levels of PAR. Although CSTR
5-5
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chambers are useful for evaluating O3 effects on physiological processes, it is not possible to
extrapolate the data to field situations.
Greenhouse system designs are similar to those found in controlled environments,
except that light, temperature, and relative humidity conditions fluctuate with those occurring
in the greenhouse. Thus, greenhouse system designs are related more closely to field studies
than are controlled environments, but plant culture and environmental conditions are still quite
different from those of field exposure chambers, making direct extrapolation difficult. These
studies are, however, more applicable to phytotoxicity of O3 to greenhouse grown ornamental
and floriculture crops (U.S. Environmental Protection Agency, 1986). Some greenhouse
exposure systems use activated charcoal filtration to remove pollutants from the incoming air
prior to the addition of experimental O3 and either vent directly to the outside or use charcoal
filtration of the outgoing air to prevent contamination of the greenhouse air supply. Other
greenhouse exposure systems filter neither incoming nor outgoing air.
Field Exposure Systems
Fumigation of plants with O3 in the field is most frequently carried out using
open-top chambers (OTCs). There are many designs, each produces an environment that
differs in some degree from the ambient air (Unsworth et al., 1984a,b). The most widely
utilized design (U.S. Environmental Protection Agency, 1986) consists of a cylindrical
aluminum frame, covered with transparent film. The bottom half of the transparent covering
is double layered, with the inside panel perforated. Charcoal- and particulate-filtered air,
nonfiltered air, or O3-supplemented air is blown into the bottom layer, forced through the
perforations into the plant canopy, and then escapes through the top of the chamber. The
positive pressure maintained by the forced movement of air up through the chamber
minimizes influx of ambient air into the chamber through the open top. The design of these
chambers has been modified with frusta to reduce such incursions by ambient air, making the
chambers more viable under windy conditions. Moveable canopies have been added so that
rain exclusion studies can be carried out. Finally, these chambers have been modified in
shape or increased in size so that species such as mature trees and grapevines can be
enclosed. The OTC exposure system was employed in the National Crop Loss Assessment
Network (NCLAN) from 1980 to 1988, and a description and discussion of the chambers is
provided in Section 6.2.4 of the 1986 criteria document (U.S. Environmental Protection
Agency, 1986).
The main advantage of OTCs is the ability to provide an enclosed environmental
area for an increased range of treatments at near-ambient environmental conditions, while
excluding ambient pollutants. Most current OTC designs have been used widely and
successfully for studying the impact of O3 on crops over a growing season (e.g., NCLAN
program), but have diameters and heights that limit their use for larger plants. Although the
OTCs provide for the least amount of environmental modification of any outdoor chamber,
the OTC still may alter the microclimate sufficiently to have a significant effect on plant
growth under pollutant stress. The OTC effects on the microclimate include reductions in
light intensity, wind velocity, rainfall, and dew formation and persistence, and increases in air
temperature and possibly relative humidity (Hogsett et al., 1987a; Heagle et al., 1988a;
McLeod and Baker, 1988; Heck et al., 1994). For plants taller than 120 cm, there is more air
movement near the bottom of the plant canopy than near the top during calm periods (Heagle
et al., 1979c; Weinstock et al., 1982).
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Exhaustive comparisons have been made among plants grown in carbon-filtered
(CF) chambers, NF chambers, and similarly sized and located ambient air (AA) plots. Much
attention has been paid to the potential for differences in productivity between AA and NF
plants because of the modification of microclimate in OTCs (Manning and Krupa, 1992). For
NCLAN studies, plants in NF chambers were frequently taller than AA plants (Albaugh et al.,
1992; Olszyk et al., 1980; Heagle et al., 1979b). However, height was the only variable that
was consistently different between AA and NF (Heagle et al., 1988a). Krupa et al. (1994)
demonstrated that of 73 comparisons between NF and AA plants (NCLAN data), 56 showed
no statistical significance, due either to lack of chamber effect or to random compensation. A
more relevant question, whether OTCs change plant response to O3, has been addressed. A
comparison of plant growth and plant response to O3 exposure in OTCs, closed-top chambers,
and air-exclusion systems has been carried out (Olszyk et al., 1986a). The authors discovered
that there was interaction between plant response to O3 and type of exposure system for less
than 10% of the growth parameters measured in California, suggesting that plant response to
O3 was the same regardless of exposure system. Plants from exclusion systems were shorter
than those grown in OTCs and generally weighed more. Of the three groups of plants, those
in the control plots of the exclusion system (i.e., receiving ambient O3exposure) were most
similar in size to plants grown in field plots. Although this and another study (Olszyk et al.,
1992) indicate that environmental modification caused by chambers will affect plant growth
and yield, there is no evidence that there is a large effect of chambers on plant response to
O3. It is assumed that, because of the decreasing relative effects on plant environment caused
by controlled environment, greenhouse, closed-top field chambers, OTCs, open-air systems,
and ambient gradients, the system effects on plant response to O3 will decrease in the same
order. Microclimatic differences within an OTC can cause significant differences in yield, but
rarely were there significant interactions between position effect and plant response to O3
(Heagle et al., 1989a).
Considerable concern has been raised about plant response to trace pollutants in
OTCs, specifically nitrogen pentoxide (N2O5) and nitric oxide (NO) in chambers receiving O3
generated from dry air, and NO2 in chambers receiving AA. These trace pollutants may have
a direct effect (positive or negative) on plant processes or may change how plants respond to
O3, and, without careful evaluation, these effects may go undistinguished from those of O3. A
comparison of alfalfa (Medicago saliva) response to the same O3 exposure, generated either
electrostatically from air or through nonfiltration of AA, indicated that the generated O3
treatment was more phytotoxic than the ambient O3 treatment, probably due to the
co-generation of N2O5 and NO, along with O3 from dry air (Olszyk et al., 1990a). Open-top
chamber studies that use filtered versus NF ambient O3 have been proposed to avoid the
problems of generating O3. The drawback of this or any two treatment approaches is that
such plant responses to low ambient levels of O3, such as might occur in many years, is quite
subtle. To detect statistically significant differences between filtered- and NF-chamber-grown
plants when responses are subtle requires a high number of replications (Rawlings et al.,
1988a). This fact is illustrated in Heagle's own two-chamber work; as described in Heagle
(1989), some of the two-chamber studies had differences between AA and NF of greater than
10%. Such large differences reduce the number of replications needed to detect a significant
difference at p = 0.05. In any event, the differences either were not treated nor tested, or
were tested but were not significant, except in one case at Beltsville, MD, with soybean
(Glycine max). Heagle (1989) discussed the calculation of power and reviewed two-chamber
studies in great detail.
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Limited use (for O3 studies) has been made of chamberless field exposure systems,
which rely on ambient wind conditions to move O3 across an open-field canopy. The O3 is
emitted from vertical pipes, which are spaced in a circle around the experimental plot of
plants. The amount of O3 emitted from each vertical pipe, as well as the number and
compass direction of emitting pipes, depends on the wind direction and speed; this whole
process is usually being computer controlled.
5.2.1.2 Methodologies Referenced Since the Air Quality Criteria for Ozone and
Other Photochemical Oxidants (U.S. Environmental Protection Agency,
1986)
Branch and Leaf Chambers
Most of the developments in exposure systems since 1986 have been modifications
of existing systems. The tremendous interest in evaluation of mature tree response to O3 has
prompted the development of large branch chambers for estimating O3 flux to trees. These
branch chambers share many of the design characteristics of a CSTR. The chamber walls are
transparent film spread over a supporting frame. There is a fan to reduce boundary layer
resistance across the foliar surface, and an air inlet and outlet so that differential O3, CO2
(photosynthesis), and water vapor (leaf diffusive resistance) measurements can be taken
(Ennis et al., 1990; Houpis et al., 1991; Teskey et al., 1991). The advantages of this system
include the ease with which the Teflon® bag can be replaced; uniform light transmission can
be maintained; and the branch chamber can be moved from plant-to-plant, can be used in situ,
and can be modified for different sized branches. One of the disadvantages of the branch
chamber, and indeed of any such cuvette that isolates one part of the plant under different
environmental conditions than the rest of the plant, is that the isolation may lead to a
response different from that which would have been observed if the branch was under the
same environmental conditions as the rest of the plant. In addition, total tree growth cannot
be estimated using branch chambers because only part of the plant is treated with O3.
Flux Measurement
Estimation of O3 flux to foliage can be made directly by measuring the difference
in O3 concentration between air going into a leaf chamber and the same air stream exiting the
chamber after passing over the leaf. This estimation also can be inferred from measurements
of leaf diffusive resistance during exposure of a leaf to O3. The former method requires a
chamber or cuvette fumigation system with uptake of O3 that is quite small or extremely
nonvariable relative to the amount being taken up by the leaf. Otherwise, it is difficult to
detect O3 flux to a leaf with good precision. Such cuvettes can be adapted from those
commercially available for portable photosynthesis meters (Graham and Ormrod, 1989) or
constructed from a novel design, such as that developed by Fuentes and Gillespie (1992) to
estimate the effect of leaf surface wetness on O3 uptake of maple leaves. The criteria for flux
cuvette design include good light transmissibility, ease of leaf manipulation, minimal reaction
of chamber wall surface with O3, and good air mixing within the chamber. Good mixing of
air is necessary to avoid a gradient in pollutant concentration and to maintain a boundary
layer resistance, which is much less than stomatal resistance. Maintenance of leaf
temperature close to that of the surrounding air, so that transpiration rates are not abnormally
high, is another benefit of good air mixing. The physical design of the Fuentes and Gillespie
chamber was simple, consisting of two glass hemispheres that were clamped together and
separated by a Teflon® O-ring over the petiole of the leaf under investigation. Inlet and outlet
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air attachments were on opposite sides of the cuvette. Other cuvette designs have been used
to estimate leaf gas-exchange responses to O3; their principals of operation are similar, but
there are differences in materials and design (Amiro et al., 1984; Freer-Smith and Dobson,
1989; Laisk et al., 1989; Moldau et al., 1991a; Skarby et al., 1987).
Compared to the CSTR, which has been used for mass balance measurement of
gas flux by whole plants during fumigation (Le Sueur-Brymer and Ormrod, 1984), cuvette
systems usually determine flux to one leaf at a time. This results in a more precise
understanding of the interaction among leaf age, diffusive resistance, illumination and O3 flux.
However, these data are not particularly well adapted to estimating flux of O3 to a large
vegetated surface. Finally, regardless of the methodology used to determine O3 flux to
foliage, there exist only very sketchy mechanistic-process models that would link O3 fluxes to
decreases in growth and productivity of plants. These data primarily are useful for
developing a relationship between internal O3 dose and plant response and in estimating the
strength of vegetation as sinks for O3 flux on a large scale. Recent studies have estimated
fluxes of O3 to plant canopies by indirect methods. Ozone flux to oat (Avena sativa) in OTCs
(using mass balance principles and a resistance analogue model) was compared to that for oat
growing in the field, using an aerodynamic gradient method (Pleijel et al., 1994). Vertical
flux density calculations for O3 uptake by grassland vegetation (O3 based on radiometric
measurements) estimated exchange between the atmosphere close to the ground and the
ecosystem (Griinhage et al., 1994; Dammgen et al., 1994). Although fluxes of O3 to
vegetation cannot imply growth or O3 physiological responses, techniques such as these can
suggest whether plant responses to O3 in OTCs might differ from those in ambient field
culture because of micrometeorological-induced differences in O3 flux.
Pollutant-Dispensing Systems
Although exposure chambers have changed little in design in the last several years,
the profile characteristics and method of dispensing pollutant profiles have. Whereas early
studies utilized static or square-wave exposures, usually controlled by hand-set flowmeters,
many more recent systems expose plants with so-called dynamic exposures during which the
O3 concentration gradually reaches a maximum, thus simulating diurnal variation in
O3 concentration (Hogsett et al., 1985a). These profiles may be achieved by mass flow
controllers that are themselves computer controlled. Proportional-add systems such as that
used in NCLAN usually achieve ambient type profiles using rotameters instead of mass flow
controllers. The O3 concentration in each of the chambers is logged at preset intervals, so
that the integrated exposure for the entire fumigation period can be calculated. Deviations
from the planned O3 episode can occur, due to failure in dispensing or monitoring equipment,
as well as incursions of air through the tops of the chambers. The length of the interval
between determinations of O3 concentration in the chambers can be an important contribution
to the control of O3 profile. In general, longer intervals lead to less well-controlled and well-
characterized O3 exposure profiles (Lefohn et al., 1993). These deviations from the expected
profiles can be mathematically quantified and monitored among treatments and replications
(Hale-Marie et al., 1991).
Open-Air Field-Fumigation Systems
Open-air field-fumigation systems have the potential to estimate most closely field
losses due to O3, as the plants are grown and exposed under ambient field environmental
conditions. However, of all the fumigation systems, this is the least controllable and
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repeatable. It has been used in the past to expose plants to "static" concentrations (i.e.,
desired concentration is the same throughout the exposure period) of such pollutants as
sulphur dioxide (SO2) or hydrogen fluoride (HF) (Hogsett et al., 1987a). The Zonal Air
Pollution System (ZAPS) has been modified vastly and improved on to enable fumigation of
plants with a diurnally varying pattern of concentration (Runeckles et al., 1990). The system
represents a significant advancement over earlier open-air field fumigation systems in that
12 discrete seasonal treatments that simulate ambient patterns are achieved, rather than the
usual two or three. Ozone was supplied to 4-m plots, which were laid out in groups of four,
through a manifold suspended over the plant canopy. The wind speed and direction
determined the actual seasonal O3 exposures, although the O3 was released in concentrations
proportional to that observed at the time in the ambient environment. Although the
12 treatments are not repeatable over time, a regression relationship between pollutant
exposure and plant response can be established for each growing season.
The Liphook study in England of long-term responses of Picea sitchensis, Picea
abies, and Pinus sylvestris to SO2 and O3 in combination consisted of seven growth plots,
50 m in diameter, five of which were surrounded by 64 vertical pipes from which pollutant
gasses were emitted (McLeod et al., 1992). The 64 pipes were divided into four quadrants of
16 adjacent pipes, and each quadrant had diluted pollutant gases supplied to it from a
computer controlled mass flow controller. The emitting quadrants, as well as the rate at
which the gases were supplied to the quadrants, depended on wind speed and direction. The
gases were emitted from the vertical pipes into the plant canopy at two heights, 0.5 and 2.5 m
above a reference height, which was approximately two-thirds of tree height. This pattern of
gas dispersion resulted in a uniform horizontal distribution of hourly mean gas concentration
across each central 25-m diameter experimental plot. This exposure system, like all open-air
exposure systems, clearly simulates field plant growth conditions far better than open- or
closed-top chambers, and, with five enclosures and two nonenclosed ambient plots, this is by
far the largest of the very few of these systems that are in operation. Measured over a winter
wheat canopy, SO2 concentration differed by less than 1 nL.L"1 over a 5-h period of
measurement; measurement of consecutive 2-min mean values at five locations across the
plots demonstrated high uniformity (McLeod et al., 1985). The usefulness of the data is
limited, however, by the low number of treatments and lack of replication of those treatments.
Field Chamber Exposure Systems
Open-top field chambers are used in most field studies of plant response to
gaseous pollutants. The OTCs first were designed for studies on annual herbaceous crop
plants (Mandl et al., 1973), but enlarged versions also have been used successfully in tree
seedling and sapling studies (Adams et al., 1990a,b; Chappelka et al., 1990; Qiu et al., 1992;
Kress et al., 1992; Hogsett et al., 1989; Andersen et al., 1991; Karnosky et al., 1992a,b; Wang
et al., 1986a,b; Temple et al., 1992). Because the results from these studies using tree species
are extrapolated to predict the effects of O3 on forests, these studies require good exposure
control in order to replicate ambient O3 profiles characteristic of many low-elevation, rural
areas of eastern North America. This condition could have been met using an open-field
exposure system. Open-top chambers large enough for mature trees have been developed but
are expensive (Mandl et al., 1989; Albaugh et al., 1992).
Microclimatic modification by OTCs, as well as O3 exposure schedules that are
disconnected from typical O3 episode meteorology, have been addressed in a seasonal study
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of tree response to O3 in the United Kingdom (Wiltshire et al., 1992). This study uses OTCs
with roll-up sides, but, except for fumigation days, the plants are maintained in ambient
climatic conditions. The exposure episodes number between 27 and 30 throughout the
growing season and occur on days with ambient meteorology associated with naturally
occurring O3 episodes (i.e., high incident radiation and temperature, with little air movement)
(Wiltshire et al., 1992). The maintenance of near-ambient meteorological conditions during
both growth and exposure periods is an effort to make this study better represent field-grown
plant responses to O3, while maintaining control of O3 exposure.
Several designs of field fumigation chambers have been developed to overcome
some of the disadvantages of the OTCs, namely small plot size and incursion of ambient air.
Closed-top chambers first were developed in the 1950s; generally, their use diminished in
favor of OTCs. However, closed-top chambers smaller in dimension than the open-top design
have been constructed more recently in California to assess crop loss to O3. Closed-top
chambers were chosen because the authors wished to characterize the pollutant dose to the
plants very precisely; pollutant gradients within the chamber were minimal (Musselman et al.,
1986a). The chambers were octagonal in shape and covered with Teflon® film; the soil was
completely replaced with standard greenhouse mix. Temperatures in the chamber were higher
(2 to 4 °C at midday, 1 to 2 °C at night) than in the ambient air, and light levels were
reduced by 11% (spectral quality of the light in the chambers was not reported). The authors
concluded that, although the chambers were not suitable for studies destined for extrapolation
to plant response under field conditions, the chambers were very useful when tight control
over soil moisture and pollutant concentration was needed.
Closed-top chambers were constructed and installed in the United Kingdom to
study responses of shrubs and large herbaceous species to long-term, low (chronic)
concentrations of SO2, NO2, and O3 (Rafarel and Ashenden, 1991). These chambers were a
smaller version of an earlier design, because the larger chambers required pure gas sources of
NO2 and SO2 to be diluted into the ventilating air stream, which resulted in highly variable
exposure concentrations. The flow rate of the smaller chambers meant that premixed gases
were sufficient to maintain steady control of treatment concentrations. Because the gases
were discharged from the source at constant concentrations, different treatments were
achieved by placing one or more pollutant supply tubes in the fumigation chambers. Good air
circulation and moderate ambient temperatures maintained the chambers at near ambient
conditions; however, results cannot be extrapolated to predict plant response to O3 under
ambient air conditions.
Ambient Gradients for Evaluation of Plant Response to Ozone
The exposure system that utilizes ambient conditions of O3 exposure, temperature,
humidity, soils, and soil moisture is the ambient gradient system. By this method, plants are
grown along a transect of known differential pollutant concentrations, usually downwind of a
major point source or urban area. The concentration of pollutants is diluted as distance from
the source increases. The most well-defined O3 gradients exist in the Southern California Air
Basin and have been used in studies by Oshima et al. (1976, 1977a,b); unfortunately, outside
this region, few suitable gradients exist. A study using four different cultivars of red clover
(Trifolium praetense) and spring barley (Hordeum vulgare\ each differing in sensitivity to
SO2, NO2, and O3, was conducted along such a transect of gradient SO2, NO2, and
O3 concentrations in the United Kingdom (Ashmore et al., 1988). Ozone concentration was
inferred from injury to Bel W3 and Bel B cultivars of tobacco but was found to have very
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little relationship to cultivar performance. The authors cautioned that these results must be
interpreted with an understanding that differences among sites in other environmental
parameters could contribute to the detection of (or the failure to detect) O3 effects on the
crops. For ambient gradient studies to be interpretable, good characterization of site
parameters (rainfall, temperature, radiation, and soil type) is needed. Additionally, the
modeler needs to know how these factors should be used to adjust the apparent plant
response. In order to know that, a good knowledge base is needed of how all of these factors
modify plant response to O3.
Although Manning and Krupa (1992) assert that natural gradients are the "ideal
way to conduct O3/plant response studies in ambient air in field plots," they concede that few
gradients that meet statistical requirements for intermediate O3 concentrations exist outside
Southern California. It is possible, however, that more gradients will be identified as rural air
monitoring increases. They also concede that, although using artificial soils removes a
significant source of variation in plant response to O3, pot-grown plants do not closely
simulate the rooting environment found in the field (Manning and Krupa, 1992). Although
plants using gradients are commonly considered to be easily replicable in large numbers, they
should probably be considered as "repeats" rather than "replicates" in the conventional sense.
If treatments are replicated by locating them very close together at the same location in the
gradient, then they may better be considered as "sub-samples" of one replicate, if the climatic
and edaphic conditions are very similar, or as repeats of a study, if the conditions are not.
This argument is not just semantic; in data analysis, repeats and replicates should be handled
differently, because the sum of squares for repeats is likely much larger than for replicates
and may be composed significantly of plant response factors other than O3 concentration.
At this time, although some information is available, the relationships still are
incompletely understood. Many investigators consider that ambient gradients are impossible
to find without major differences in environmental conditions that may affect plant response
to O3 and, therefore, confound interpretation of the results.
Cultivar Comparisons
The comparison of isogenic lines of a particular species that differ only in their
tolerance to O3 is "the ideal way to determine the effect of ambient O3 on plants in the
field ...." (Manning and Krupa, 1992). Heagle et al. (1994) report on the use of a white
clover (Trifolium repens L.) system to estimate the effects of O3 on plants. A field
experiment conducted in 1984 and 1985 using white clover revealed a wide range of
sensitivity among the genotypes present in the commercial line "Regal" (Heagle et al., 1991a,
1993). Plants were screened for relative sensitivity to O3. Two clones were selected: one
ozone-sensitive (NC-S) and another ozone-resistant (NC-R). Subsequent studies suggested
that these clones could be useful as indicators of O3 sensitivity, if they routinely displayed
measurable differences in response to O3, while responding similarly to other factors (e.g.,
biotic, climatic, soil, chemical, and other pollutants). Experimentation indicated that the white
clover system can be used to indicate where and when ambient O3 concentrations cause foliar
injury and decrease growth. Hence, it can be inferred that other plant species sensitive to O3
also may be affected (Heagle et al., 1994).
Protective Chemicals
Chemicals that protect plants from O3 have been in use since the 1970s to evaluate
plant response to O3. Ethylene diurea (EDU) has been used in studies to modify the
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O3 sensitivity of several species (see Section 5.4.7). Ethylene diurea (and perhaps other
undetermined chemicals) has potential as a tool to evaluate field crop losses to O3 in the
absence of chambers, with their inherent modification of microclimate. A low-cost, simple
technique, EDU can be applied to larger plot sizes than currently are possible with OTCs,
thus reducing some of the uncertainty of extrapolating experimental results to a large scale.
Field protocols for the use of EDU have not been well established. Frequency and rate of
application that protects plants vary with species and edaphic and atmospheric conditions.
Depending on the method of application, EDU may have little effect on field-grown plant
response to O3 (Kostka-Rick and Manning, 1993). The basis for the year-to-year variation in
degree of protection of plants by EDU is not well understood, so drawing conclusions from
multi-year studies, which is the situation most relevant to evaluation of plant community
responses to ambient O3, is difficult. Two-treatment studies of EDU and plant response to O3
(Kostka-Rick and Manning, 1992a,b) indicate that protection is variable, suggesting that the
experimental system under investigation (soil, plant, and climate) would have to be extremely
well characterized and understood for interpretation of EDU studies to be complete. Manning
and Krupa (1992) point out that EDU is probably more useful in conjunction with OTCs so
that a factorial range of O3 can be administered to the plants. It is not clear that EDU
protection can be fine-tuned sufficiently into a range of discrete levels suitable for regression
analysis (Kostka-Rick and Manning, 1993). The mechanism by which EDU protects plants,
beyond being a systemic antioxidant, is unknown; understanding this mechanism has the
potential to contribute to the broader understanding of the mechanisms of O3 injury at the
cellular/metabolic level of the plant.
5.2.2 Experimental Design and Data Analysis
Experimental design strategies, including the number, kind, and levels of pollution
exposure; patterns of randomization; number of replicates; and experimental protocol are
crucial to the ability of the statistical approaches to test and model the effects of O3 on plant
response and to extrapolate experimental results to real world conditions. The experimental
design focuses an experiment on the specific objectives of the study and, so, may limit the
application of the data to other research goals. The various experimental design and analyses
for exposure-response data from controlled exposure studies have been well reviewed in the
1986 criteria document (U.S. Environmental Protection Agency, 1986) and will not be
repeated here. In summary, most field studies involving OTCs have used randomized block
or split-plot designs and pollution levels appropriate for regression analysis. These exposure-
response relationships generalize the mathematical relationship between the plant parameter of
interest and O3 exposure. Plant response to concentrations other than those used in the
experiment can be interpolated from these relationships, and thresholds of plant response can
be determined (Ormrod et al., 1988). In the latter half of the NCLAN program, the Weibull
model was chosen to characterize yield response to O3 because of its flexibility to describe a
wide range of data patterns (Rawlings and Cure, 1985) and, consequently, to allow a common
model to be fit when pooling data across years and sites (Lesser et al., 1990).
Experimental designs for exposure-response relationships can be expanded easily
so that plant response to O3 and another factor at multiple levels can be determined. Because
of the need to contain each O3 treatment by a chamber, incomplete factorial designs are more
efficient approaches to multi-factor studies, leading to exposure-response surfaces (Allen
et al., 1987). Choosing the appropriate incomplete factorial design for a response surface
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study requires forethought on whether all areas of the surface are of equal interest. For many
O3 plant response studies, this is not so because extremely high concentrations, although
increasing the precision with which plant response to lower concentrations is estimated, are
not as likely to occur in the ambient environment (see Chapter 4).
Because the U.S. Environmental Protection Agency (1986) decided to place greater
emphasis on damage (i.e., effects that reduce the intended human use of the plant) than on
injury, studies more frequently have used experimental designs that generate data suitable for
regression and treatment mean separation analyses for the purposes of modeling and testing
the impact of O3 on plant response. Although the impact at current O3 levels is of primary
interest and can be studied effectively using two O3 levels generated by CF and NF
treatments, the development of exposure-response models necessitates the use of additional
treatments at above ambient concentrations (Heagle et al., 1989a; Rawlings et al., 1988a).
The optimal number, range, and spacing of treatment levels depends on the anticipated
exposure-response model, but, in the case of the Weibull and polynomial models, greater
precision for estimation of relative yield loss at ambient O3 concentration is obtained when
the lowest treatment level is near zero and the highest treatment level is well above the
ambient concentration. For the Weibull model, the highest treatment should correspond to a
concentration for which yield loss is at least 63% of the yield at zero exposure (Dassel and
Rawlings, 1988; Rawlings et al., 1988b).
When studying the impact of mixtures of pollutants on plant processes in
chambers, response surfaces can be generated from complete or incomplete factorial designs.
These designs have been shown to increase the precision and efficiency of estimating relative
yield loss at ambient concentrations (Allen et al., 1987). The optimal design cannot be
specified a priori and necessitates the use of treatment levels from near zero to well above the
ambient concentration for each pollutant. However, response surface designs have not been
used widely in pollutant mixture studies, nor have these designs been used extensively to
study the interaction between pollutant exposure and quantitative environmental parameters,
such as light, temperature, and soil moisture. The interaction between O3 and phytotoxic
concentrations of other pollutants, in particular SO2, has not been studied extensively because
instances of co-occurrence of O3 and other pollutants are not common in the United States.
An analysis of pollution monitoring data showed fewer than 10 periods of co-occurrence
between O3 and phytotoxic concentrations of SO2 during the growing season at the sites
where the two pollutants were monitored (Lefohn and Tingey, 1984; U.S. Environmental
Protection Agency, 1986).
Design and analysis of pollutant effects studies have used various characterizations
of exposure to determine optimum spacings of treatment levels and to relate exposure to
response. Most notably, the daytime mean concentration index (i.e., either M7 or M12) was
adopted by the NCLAN program to determine the effects of O3 on plant response. However,
there has been considerable debate over the use of the mean index in exposure-response
modeling; the variety of ways to compute the characterizations of plant exposure will be
discussed in Section 5.5. When plant yield is considered, plant response is affected by the
concentration of exposure and by other exposure-dynamic factors (e.g., duration, frequency,
threshold, respite time), in combination with physiological, biochemical, and environmental
factors that may mask treatment effects over the growing period. Research goals to
understand the importance of exposure dynamic factors have utilized experimental designs
that apply two or more different patterns of exposure that are equal on some scaling (e.g.,
total exposure). Experiments designed specifically to address the importance of components
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of exposure may require the use of exposure regimes that are not typical of the ambient
environment.
The majority of chambered field studies use regression-based designs that focus on
developing exposure-response models but have limited application for testing the importance
of exposure dynamics (e.g., exposure duration) for evaluating exposure indices based on
statistical fit. When data from replicate studies of equal or varying duration are available, the
ability to test for duration effects on plant response may be enhanced using regression
analysis to combine data. The regression approach has been used to fit a common model to
combined data from replicate studies of the same species when it is reasonable to assume that
the primary cause of biological response is pollutant exposure, and that differences in
environmental, edaphic, or agronomic conditions among sites do not significantly change the
shape of the regression relationships. When pooling data across sites and years, additional
terms for site and year effects often are included in the model as either fixed or random
components, depending on the population of interest. Inferences over random environments
implies that the environments sampled by the experiments are representative of the population
of regions of interest under a variety of environmental conditions. In this case, site and year
effects are incorporated as random components when fitting a common model. The
appropriate analysis is to use a mixed model to fit an exposure response model with variance
components. This analysis has been used recently to combine data from replicate studies of
varying durations to test the importance of length of exposure in influencing plant response
(see Section 5.5).
5.2.3 Mechanistic Process Models
In addition to regression type models of plant response to O3, which are empirical
and statistical in nature, there are mechanistic-process models (Luxmoore, 1988; Kickert and
Krupa, 1991; Weinstein et al., 1991). The key difference between these two types of models
is how the changes are handled in the dependent variable over time. Empirical models treat a
time period (e.g., a growing season) as a single point and report the response of the dependent
variable as a single point as well. Regression models also may oversimplify the
characteristics of an O3 exposure, in that the description of the O3 exposure is compressed
over time to a single number. The variety of ways to compute this single number will be
discussed in Section 5.5.
Mechanistic-process models on the other hand describe the rate of change of a
variable in response to the treatment (such as O3) with change in time. The latter type of
model has the potential to capture the interaction among plant age or stage of development,
variability of ambient exposure concentrations, and plant response to O3. For this reason,
mechanistic-process models have been rated much more highly than regression models for
their realism, scientific value, and applicability to other locations (Kickert and Krupa, 1991).
However, compared to regression models, mechanistic-process models require more input
data, and the input data are less accessible. The mechanistic-process models are more
complex than regression models, requiring more computer time and memory to develop. The
precision of the output regression models is greater than mechanistic-process models (for
interpolative examinations only), as is their ability to estimate response probabilities. The
authors conclude that the popularity of single-equation, time-lumped models is related to the
fact that the studies of plant responses to O3 are oriented more to air quality standard setting
as an endpoint, rather than the physiological processes underlying plant responses. The
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problems with process-based models are the necessity for some large assumptions (in place of
real data) and the lack of validation. Without validation, using estimates from these models is
questionable; if the estimations are used, then the uncertainties associated with them must be
identified and quantified.
5.2.4 Summary
Each type of fumigation system is suited particularly well to certain types of
studies of plant response to O3; no one system is appropriate for all types of studies of plant
responses to O3 (Table 5-1). Each system has advantages and limitations that must be
evaluated in terms of the research objectives that it was designed to meet. Table 5-1 lists the
characteristics of the various exposure systems as they relate to experimental objectives,
including simulation of field conditions, replication, range of treatment levels possible, and
the ability to control extraneous environmental factors that may influence plant growth.
Controlled-environment chambers are well suited for mechanistic type studies at the molecular
or cellular level. Most plant cellular processes, as well as the equipment that measures them,
are quite sensitive to temperature and light, so good control and definition of these factors are
needed. Growth responses to O3 determined from controlled-environment chamber studies
cannot be extrapolated to the prediction of field losses to O3 because the culture conditions in
the two systems are just too dissimilar. Open-top chamber systems, although a compromise
in ability to simulate field conditions, have major advantages over other fumigation systems
for developing exposure-response functions (to develop a statistically robust surface requires
at least three or, better yet, five treatment levels) because (1) a range of pollution levels at
near-ambient environmental conditions can be generated to optimize the precision in empirical
modeling; (2) extrapolation of experimental results to probable field responses to ambient
exposure is possible to a certain extent because OTCs, although modifying microclimate,
appear not to affect relative plant response to O3; and (3) a semi-controlled environment is
created for plant growth with only O3 exposure level varied, thus it is valid to assume that the
primary cause of response is due to O3 exposure. Exclusion methods, particularly those using
chemicals such as EDU, are the least disruptive of ambient culture conditions in the field, so
these approaches most closely estimate real crop losses to O3. However, their application is
limited by the availability of ambient O3 in any particular year or location, as well as by
confounding by climatic and edaphic conditions. They are not well suited for establishing
exposure-response relationships because it is difficult to quantify the degree of protection
actually offered by the exclusion method in the field (Ashmore and Bell, 1994). In general,
open-field exposure systems or natural gradients are not replicable, nor can a range of
treatments be imposed to enable construction of a response function, which is necessary for
interpolation of O3 concentrations that cause plant response.
At the current time, OTCs represent the best technology for determination of crop
yield responses to O3; concentration and duration of the gas are well controlled, and the plants
are grown under near-field-culture conditions. There are several limitations and uncertainties
associated with the collected data: (1) the plot size is small relative to a field, (2)
microclimate differences may influence plant sensitivity to O3, and (3) air quality after
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Table 5-1. Comparison of Fumigation Systems for Ozone Exposure-Plant Response Studies
Fumigation System
Controlled-environment chambers
Greenhouse chambers
Closed-top field chambers
Open-top field chambers
Mechanical field exclusion
Open-field fumigation
Natural gradients
Simulation of
Field Losses
Low
Low
Medium
Medium to high
High
High
High
Replication of Range of
Experimental Unit Treatment Levels
Low
Medium
High
High
Low to medium
Low
Low
High
High
High
High
Low
Low
Low
Likelihood of Extraneous
Factors Affecting Response
Medium
Medium
Medium
Medium
Medium
High
High
i
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passage through a charcoal filter has not been widely characterized. These uncertainties are
not quantified, although there are preliminary data establishing their existence. There is
concern that these uncertainties are forgotten in the scaling of the plant response data to
national yields and their integration into larger cost-benefit models. However, because the
uncertainties are not yet quantified, they cannot be incorporated into the national estimates of
losses to O3. There is an urgent need to estimate these uncertainties so that the OTC data can
be used fully, with little doubt as to how well the data represents real crop losses. Further
comparisons of OTC and chemical exclusion plant responses, expanding the range of
environmental conditions and species for which they are compared, would help determine the
extent of the role of microclimate in modifying plant response to O3. Large scale exclusion
studies also could contribute to quantifying the uncertainty of extrapolating plot response to
field scale. Analysis of the atmospheric chemistry inside OTCs under various scenarios of
light, temperature, and humidity would address the question of what additional pollutants may
influence plant growth or plant responses to O3. Once these uncertainties are fully
characterized and quantified, existing models of crop loss can be constructed more precisely
and then incorporated into the national scale models with greater confidence.
5.3 Species Response/Mode of Action
5.3.1 Introduction
Plant adaptation to changing environmental factors or to stresses involves both
short-term physiological responses and long-term physiological, structural, and morphological
modifications. These changes help plants to minimize stress and to maximize the use of
internal and external resources. A great deal of information is available on the physiology of
single leaves; however, relatively little is known about whole-plant systems and whether the
physiological mechanisms involved are initiated wholly within the leaf or are the result of
whole-plant interactions (Dickson and Isebrands, 1991).
The many regulatory systems contained in leaves change both as a function of leaf
development and in response to different environmental stresses. Leaves function as the
major regulators of anatomical and morphological development of the shoot and control the
allocation of carbohydrates to the whole plant (Dickson and Isebrands, 1991). This section
discusses the movement of O3 into plant leaves and what is known about their biochemical
and physiological responses.
Movement of O3 into plant leaves involves both a gas and a liquid phase. The
phytotoxic effects of air pollution on plants appear only when sufficient concentrations of the
gas diffuse into the leaf interior and pass into the liquid phase within the cells. Therefore, to
modify or degrade cellular function, O3 must diffuse in the gas-phase from the atmosphere
surrounding the leaves through the stomata into the air spaces and enter into the cells after
becoming dissolved in the water coating the cell walls (U.S. Environmental Protection
Agency, 1986). The exact site or sites of action are not known. Biochemical pathways are
closely interrelated, and sufficient knowledge of all the control and regulatory mechanisms
does not exist (Heath, 1988). The previous criteria document summarized the overall
processes controlling plant response to O3.
"The response of vascular plants to O3 may be viewed as the culmination of a
sequence of physical, biochemical, and physiological events. Ozone in the
ambient air does not impair processes or performance, only the O3 that diffuses
5-18
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into the plant. An effect will occur only if a sufficient amount of O3 reaches
the sensitive cellular sites within the leaf. The O3 diffuses from the ambient air
into the leaf through the stomata, which can exert some control on O3 uptake to
the active sites within the leaf. Ozone injury will not occur if (1) the rate of
O3 uptake is sufficiently small that the plant is able to detoxify or metabolize
O3 or its metabolites; or (2) the plant is able to repair or compensate for the O3
impacts (Tingey and Taylor, 1982). The uptake and movement of O3 to the
sensitive cellular sites are subject to various physiological and biochemical
controls" (U.S. Environmental Protection Agency, 1986).
Responses to O3 exposure that have been measured include reduced net CO2
exchange rate (photosynthesis minus respiration), increased leaf/needle senescence, increased
production of ethylene, and changes in allocation patterns. Overall understanding of the
response of plants to O3 has been refined since the last criteria document (U.S. Environmental
Protection Agency, 1986). Increased emphasis has been placed on the response of the process
of photosynthesis to O3, on identification of detoxification mechanisms, and on changes in
biomass (sugar and carbohydrate) allocation.
As indicated above, entry of O3 into leaves involves the gas-phase external to the
plant and the liquid-phase within the leaf cells. A precondition for O3 to affect plant function
is that it be absorbed into the tissues. Ozone uptake will be divided into two components:
adsorption to surfaces and absorption into tissues. Adsorption will affect surface materials
(e.g., cuticles) but have little direct affect on physiological processes, whereas O3 absorption
can affect physiological function if O3 is not detoxified. In the following section, the
processes that control movement of O3 into the plant canopy and then into the leaf will be
examined.
5.3.2 Ozone Uptake
Uptake of O3 in a plant canopy is a complex process involving adsorption of O3 to
surfaces (stems, leaves, and soil) and absorption into tissues, primarily in the leaves
(Figure 5-2). Movement of O3 from the atmosphere to the leaf involves micrometeorological
processes (especially wind) and the architecture of the canopy (including the leaves). Within
the canopy, O3 can be scavenged by chemicals in the atmosphere (Kotzias et al., 1990;
Gab et al., 1985; Becker et al., 1990; Yokouchi and Ambe, 1985; Bors et al., 1989;
Hewitt et al., 1990); however, the products of these reactions themselves may be phytotoxic
(Kotzias et al., 1990; Gab et al., 1985; Becker et al., 1990; Hewitt et al., 1990). The extent to
which these scavenging processes affect O3 absorption by leaves is not well known. Uptake of
O3 by leaves is controlled, in large part, by the complex of microclimate and canopy
architecture, which control movement of O3 from the atmosphere to the leaf. Leaf
conductance is determined by leaf boundary layer conductance and stomatal conductance.
In this section, the theoretical and empirical studies on O3 uptake at the canopy and leaf
levels will be examined.
5.3.2.1 Ozone Uptake by Plant Canopies
Integration of O3 uptake at the stand level requires attention to several levels of
organization (Enders et al., 1992; Hosker and Lindberg, 1982) because uptake at this level
5-19
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Atmospheric Processes
I
/Ozone in the]
Atmosphere
I!
Canopy Processes
Leaf Processes/
Ozone Uptake
Leaf Processes/
Mode of Action
I
Plant Response
Ecosystem Response
J
Canopy
Boundary Layer!
Canopy
Conductance
Ozone in
Vegetation
Canopy
Leaf
Conductance
V*
Ozone Absorption I
into Foliage I
Stomatal I
Conductance
Figure 5-2. Uptake of ozone (OJ from the atmosphere. Ozone is moved from the
atmosphere above the canopy boundary layer into the canopy primarily by
turbulent flow of air. Canopy conductance, controlled by the complexity of the
canopy architecture and the wide distribution within the canopy, is a measure
of the ease with which gases move into the canopy. Within the canopy, O3 can
be adsorbed by surfaces as well as being absorbed into the foliage. Foliage
absorption is controlled by two conductances, leaf boundary layer and
stomatal, which together determine leaf conductance. The solid black arrows
denote O3 flow; dotted arrows indicate processes affecting uptake or response
to Oy Boxes at the left with double borders are those processes described in
the figure. The rounded box with a double border is the end of pathway on
this figure.
includes not only uptake by leaves but also adsorption by stems, the soil, and other structures
with which O3 can react. Although the actual pathway, and therefore conductance, will vary
within the canopy, depending on position and wind profile, an integrated average conductance
is frequently used to describe canopy conductance (Monteith and Unsworth, 1990). For most
tree species, canopy conductance tends toward high values, whereas, for crops, it tends to be
low.
5-20
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Two general approaches have been used to estimate O3 uptake by a plant stand:
(1) measurement of gradients over the canopy using micrometeorological methods and
(2) simulation of canopy conductance. The results of the two methods generally are different
because the micrometeorological techniques include O3 uptake by all surfaces, whereas
simulation accounts only for O3 absorbed by the surfaces simulated, primarily the foliage.
Two micrometeorological methods, (1) Bowen ratio and (2) eddy correlation, have
been used to calculate canopy O3 uptake. The Bowen ratio assumes a constant relationship
between heat and water vapor fluxes (i.e., sensible and latent heat), then calculates O3 uptake
assuming a constant relation between water vapor and O3 fluxes (Leuning et al., 1979a). The
eddy correlation technique requires more elaborate instrumentation for measurement of
variation in temperature, water vapor, and O3 concentration over time and has stringent site
requirements (Wesely et al., 1978).
Wesely et al. (1978), using eddy correlation, found a strong diurnal variation in the
deposition velocity (the inverse of canopy conductance) and O3 flux over a corn canopy.
They also found evidence that 20 to 50% of the flux was to the soil and to the surface of the
canopy. Ozone flux to a dead corn canopy also had a diurnal variation, but a lower
magnitude, probably reflecting the absence of uptake through the stomata. Single time
measures of deposition velocity, or canopy resistance, have been taken in a Gulf Coast pine
forest (54 s m"1; Lenschow et al., 1982) and in a New Jersey pine forest (120 and 300 s cm"1;
Greenhut, 1983). Ozone uptake in a maple forest varied diurnally in a pattern explainable by
variation in leaf conductance and O3 concentration (Fuentes et al., 1992). Ozone flux below
the tree canopy at 10 m was about 10% of the flux above the canopy at 33 m. Measurements
in specially constructed chambers showed that O3 uptake, as well as photosynthesis, could
occur when the foliage was wet (Fuentes and Gillespie, 1992). The fact that wet leaves could
take up significant CO2 is evidence that the stomata were not blocked by the water on the leaf
surface. This result is counter to assumptions made in earlier work (Baldocchi et al., 1987) in
which water on the surface of the leaf was presumed to interfere with O3 uptake.
Simulation of canopy conductance requires scaling uptake from individual leaves
to individual trees to that of a stand using a combination of canopy models (one for each
species) and a stand model to handle interactions among individuals. Several assumptions are
required for this approach: the primary sink for O3 is the foliage, variation in stomatal
conductance can be simulated through the canopy using either direct measurements or models,
and canopy and plant models adequately simulate response when competition is occurring.
Leuning et al. (1979a,b) used a simple model to estimate canopy uptake in corn
(Zea mays) and tobacco. Comparison of the results of these simulations with estimates using
the Bowen ratio technique indicated that about 50% of the O3 absorbed by the stands entered
the leaves. Baldocchi et al. (1987) presented a model for canopy uptake of O3 that
incorporated stomatal function, some aspects of canopy architecture, and soil uptake. The
results of the simulation of O3 uptake by a corn canopy correlated well with estimations using
the Bowen ratio, but tended to overestimate the magnitude. These authors point out that
results of model simulation are quite sensitive to the assumptions used. As part of a series of
simulations, Reich et al. (1990) explored the effects of different O3 exposures (daily average
O3 concentrations of 0.035, 0.05, 0.065, and 0.080 ppm) on canopy carbon gain in a mixed
oak-maple forest. Depending on the response function and O3 exposure used, reductions in
carbon gain were between 5 and 60%. An important result of these simulations is that the
effect of O3 was strongest in the upper layer of the canopy, where most of the photosynthesis
occurred. Although all these simulations provide some interesting insights into how
5-21
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O3 uptake (and response) varies with time and exposure, data for validating the models are
still needed.
Griinhage and Jager (1994a,b), using information gathered from a
micrometeorological study of O3 flux observations above a natural grassland in Germany,
developed a mathematical model to describe the flux and to estimate the potential injury to
the grassland. The aim of the paper was to explain how both vertical flux and stomatal
conductance changed during the day and influenced the uptake of air pollutants. For this
reason, under ambient conditions, exposures cannot be expressed as a simple function of the
pollutant concentration in air.
In summary, O3 uptake (absorption to surfaces and absorption by tissues) by plant
canopies has been measured only a few times. The results are consistent with the hypothesis
that stomatal conductance plays a major role in the process. Modeling of O3 absorption by
leaves provides a means of assessing the understanding of the processes controlling
O3 absorption. Combining direct measurements over canopies with modeling will provide a
means for assessing the dynamics of O3 uptake in a canopy.
5.3.2.2 Ozone Absorption by Leaves
The importance of stomatal conductance for the regulation of O3 uptake by a
canopy has been hypothesized for some time (Heck et al., 1966; Rich et al., 1970). Uptake of
O3 by leaves is controlled primarily by stomatal conductance, which varies as a function of
stomatal aperture (Figure 5-3). Kerstiens and Lendzian (1989) found that the permeability of
cuticles by O3 from several species was about 0.00001 that of open stomata. Movement of
guard cells, which control stomatal opening, are affected by a variety of environmental and
internal factors, including light, humidity, CO2 concentration, and water status of the plant
(Zeiger et al., 1987; Kearns and Assmann, 1993). Air pollutants, including O3, also may
affect stomatal function (U.S. Environmental Protection Agency, 1986). The pattern of
diurnal stomatal conductance is produced by the integrated response of guard cells to a
variety of factors.
As the primary "gate keepers" for gas exchange between the atmosphere and the
leaf, stomata perform the vital function of controlling the movement of gases, including air
pollutants such as O3, to and from the leaf. The complexity of the response of stomata to
environmental (microclimatic and edaphic) factors is indicated by the large amount of
research on stomatal physiology and response to changing conditions (for reviews, see Zeiger
et al., 1987; Schulze and Hall, 1982) and on developing models to simulate stomatal response
(Avissar et al., 1985; Ball et al., 1987; Collatz et al., 1991; Eamus and Murray, 1991; Friend,
1991; Gross et al., 1991; Johnson et al., 1991; Kuppers and Schulze, 1985). The magnitude
and diurnal pattern of stomatal conductance depends on both internal, species-specific factors
and on the external environment, including soil fertility and nutrient availability, as well as
microclimate (Schulze and Hall, 1982; Beadle et al., 1985a,b). Mid-day stomatal closure is
observed frequently under conditions of high temperature and low water availability (Helms,
1970; Tenhunen et al., 1980; Weber and Gates, 1990). As an example of the variability in
diurnal gas exchange, Tenhunen et al. (1980) present nine graphs of diurnal photosynthesis
for apricot (Prunus armeniaca) measured from July to September 1976. Although there is a
general pattern of increase in the morning and of decline in the evening, the path of
photosynthesis and conductance are quite different among
5-22
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X
X
X
X
Internal Factors:
Water Stress
Carbohydrate Levels
Mineral Nutrients
Humidity <
Figure 5-3. Movement of gases into and out of leaves is controlled primarily by the
stomata (small openings in the leaf surface whose aperture is controlled by two
guard cells). Guard cells respond to a number of external and internal
factors, including light, humidity, carbon dioxide (COJ, and water stress. In
general, the stomata open in response to light and increasing temperature and
close in response to decreasing humidity, increased CO2, and increasing water
stress. They also may close in response to air pollutants, such as ozone.
of days. The inherent variability in stomatal opening makes using a set time period for
O3 exposure problematic. This variability makes determining the effects of a given diurnal
O3 exposure pattern difficult without reference to physiological, meteorological, and edaphic
information, as well as to the sensitivity of individual species exposed.
To be absorbed, O3 must be present in the atmosphere surrounding the leaf and the
stomata must be open. Any factor that affects stomatal opening affects O3 absorption
(Figure 5-3). Under drought conditions, when stomatal conductance is reduced, the relative
effect of O3 is less when compared with well-watered controls (Tingey and Hogsett, 1985;
Flagler et al., 1987; Temple et al., 1993, also see Section 5.4). Low humidity has been
shown to modify plant response to O3 (McLaughlin and Taylor, 1981), presumably due to
reduced O3 absorption (Wieser and Havranek, 1993).
5-23
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To calculate O3 absorption, some estimate of the internal O3 concentration must be
made. In earlier work, a finite O3 concentration was assumed to exist in the intercellular air
space of the leaf (Bennett et al., 1973; Tingey and Taylor, 1982; Lange et al., 1989).
Estimating this concentration is difficult because the rate of O3 absorption into the leaf must
be known. Recently Laisk et al. (1989) presented evidence that this concentration is near
zero, a result that is consistent with the highly reactive nature of O3. Further studies on other
species must be made to test the hypothesis that internal O3 concentration is negligible in
leaves.
The other component of absorption, O3 concentration outside the leaf, may vary
greatly with time of day and season (Chapter 4). Data on the effect of variations in
O3 profile (from constant concentrations to equal daily peaks to variable [episodic] peaks),
based on greenhouse and OTC chamber studies using simulated exposures, suggest that those
profiles that have periodic high concentrations have a greater effect than those with low peaks
even though the exposure is equivalent (Hogsett et al., 1985a; Musselman et al., 1986b; see
Section 5.6). Taylor and Hanson (1992) show how variations in conductance can affect O3
absorption and conclude that conductances in and near the leaf surface have a major influence
on absorption of O3. Figure 5-4 shows a simulation of the effect of diurnal variation in
stomatal conductance and O3 concentration on the O3 absorbed into the leaf. Amiro and
Gillespie (1985) found that cumulative O3 absorption correlated with visible injury in
soybean. Weber et al. (1993) found that rate of uptake may play an important role in the
response of ponderosa pine (Pinus ponderosd). The roles of cumulative uptake versus uptake
rate have not been clarified and need further study.
Absorption of O3 by leaves depends on variations in both stomatal conductance
and O3 concentration. The highly reactive nature of O3 makes measuring its absorption
difficult; therefore, models of stomatal conductance are used, along with O3 concentrations, to
estimate O3 absorption. The relative importance of absorption rate versus cumulative
absorption is not known at present.
5.3.3 Resistance Mechanisms
Resistance mechanisms can be divided into two types: (1) exclusion from
sensitive tissue and (2) detoxification near or in sensitive tissue. For leaves, the former
involve response and cuticles, and the latter involve various potential chemical and
biochemical reactions that chemically reduce O3 in a controlled manner. Although these
systems potentially provide protection against O3 injury to tissue physiology, they come at
some cost, either in the reduction in photosynthesis, in the case of stomatal closure, or in
carbohydrate used to produce detoxification systems.
Injury to leaf and needle cuticles does not appear to have a major effect on leaf
function, based on the inconsistent data. Barnes et al. (1988a) found that O3 exposure could
damage leaf cuticles; however, Liitz et al. (1990) found no consistent changes in cuticle
structure in Norway spruce (Picea abies).
5.3.3.1 Stomatal Limitation
As noted above, stomata can be affected by a wide variety of environmental
factors (Section 5.3.2.2), by occurrences of stress (Section 5.4), and by age. In addition,
5-24
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Ozone Profiles
5 10 15
Time (h)
20
| — 14:00 peak —12:00 peak—-16:00 peak —constant
£ 0.06
E
o 0.04
c 0.02
1
I <
o
O
Variation in Conductance
Simulation
B
10 15
Time (h)
20
Simulated Absorption
-------
stomatal response can vary among species. These multiple interactions make accurate
prediction of uptake under field conditions difficult. Some early research showed a decrease
in leaf conductance (Figure 5-3), with O3 exposure implying a direct effect of O3 on stomatal
conductance (U.S. Environmental Protection Agency, 1986). In studies at high
O3 concentrations (>0.3 ppm), stomatal response was rapid (Moldau et al., 1990). In other
studies, reduction in conductance in response to O3 required hours to days of exposure (Dann
and Pell, 1989; Weber et al., 1993). Several studies have shown that discrimination against
C13 in C3 plants decreases with O3 fumigation (Okano et al., 1985; Martin et al., 1988;
Greitner and Winner, 1988; Saurer et al., 1991; Matyssek et al., 1992). These data are
consistent with an increased restriction of diffusion of CO2 into the leaf (Farquhar et al.,
1989). However, Matyssek et al. (1992) and Saurer et al. (1991) found that internal CO2
increased with O3 exposure, and that water-use efficiency decreased, both the opposite of
expectation, indicating that photosynthesis decreased relatively more than conductance.
Although stomata limit O3 uptake and may respond directly to high O3 concentrations
(e.g., >0.2 ppm, U.S. Environmental Protection Agency, 1986; Moldau et al., 1990), the
relative importance of this response, compared to indirect effects induced by reductions in
photosynthetic performance, has not been fully assessed.
5.3.3.2 Detoxification
When O3 enters a cell, several highly reactive compounds can be produced (e.g.,
superoxide, free radicals, peroxides) (Heath, 1988). The effects of these compounds depends
on their reactivity, mobility, and half-life. For detoxification to occur, oxidant and antioxidant
must occur proximately. In addition, the rate of production of antioxidant must be a
significant portion of the rate of oxidant entry into the system for effective detoxification to
occur. Two general kinds of detoxification systems have been reported in plants: (1) those
that utilize reductants (e.g., ascorbate) to reduce O3 and (2) those that utilize enzymes
(superoxide dismutase). In either case, excess oxidizing power is dissipated in a controlled
manner, effectively protecting the tissue from damage. These protective systems probably
developed in response to photooxidation, which can occur, for example, at low temperatures
(Powles, 1984).
Several antioxidants have been reported, the most studied being ascorbate and
glutathione (GSH). Much of this work has occurred since the 1986 criteria document
(U.S. Environmental Protection Agency, 1986). Alscher and Amthor (1988) reviewed the
literature in this area. In the chloroplast, the process requires dihydronicotinamide adenine
dinucleotide phosphate and may be a cause for the transient reduction in photosynthesis
observed in some studies (Alscher and Amthor, 1988).
Evidence for the participation of antioxidants in protecting cells from O3 injury is
primarily indirect (i.e., changes in levels of antioxidants or of associated enzymes). In red
spruce (Picea rubens), GSH levels increased in year-old needles in response to O3, but not in
current-year needles (Hausladen et al., 1990; Madamanchi et al., 1991). Dohmen et al. (1990)
found increased concentrations of reduced glutathione in Norway spruce in response to
long-term O3 fumigation. In a poplar hybrid (Populus maximowiczii x P. trichocarpa), total
GSH increased with O3 fumigation; however, the ratio of reduced forms to oxidized forms
declined, indicating that oxidation of GSH possibly was stimulated by O3 (Gupta et al., 1991).
Mehlhorn et al. (1986) found that both GSH and ascorbic acid (AH2) increased with O3
fumigation in silver fir (Abies alba) and Norway spruce. The potential for AH2 to protect
cells from O3 damage was explored by Chameides (1989), who concluded that such protection
5-26
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was possible if AH2 occurred in the apoplast at sufficient concentrations and production rates;
however, experimental data are needed to test this hypothesis.
The response of enzymes involved in detoxification is not clear. Activities of
enzymes involved in antioxidant production increased in response to O3 in one study (Price
et al., 1990); however, in several others, no effect was found (Madamanchi et al., 1992;
Pitcher et al., 1991; Anderson et al., 1992; Nast et al., 1993). Activity of superoxide
dismutase (SOD), an enzyme that can reduce one of the products of O3 interaction with the
cytoplasm, can be increased by O3 fumigation (Alscher and Amthor, 1988; Gupta et al.,
1991). There are both cytosolic and chloroplastic forms of this enzyme, but the role the
different forms play in detoxification of O3 is not clear. Teppermann and Dunsmuir (1990)
and Pitcher et al. (1991) found that increased production of SOD had no effect on resistance
to O3 in tobacco.
The extent to which these detoxification systems can protect tissue from
O3 damage is unknown. However, "if plants have detoxification mechanisms which are
kinetically limited, the rate of O3 uptake may be important, so that even an integrated
absorbed dose may be insufficient to account for observed responses" (Cape and Unsworth,
1988). Potential rates of detoxification for given tissues are needed to estimate the
importance of these systems to overall O3 response. In addition, the sites in which the
detoxification systems occur need to be identified.
5.3.4 Physiological Effects of Ozone
The initial reactions of O3 with cellular constituents are not known. The high
reactivity and nonspecificity of O3 reactions, coupled with the absence of a useful isotopic tag
for O3, make studies of the initial reactions difficult at best. The data on changes in
biochemical function resulting from O3 exposure probably represent effects one or more steps
beyond the initial reactions. Nonetheless, data is available that indicate the wide range of
cellular processes that can be affected by O3.
Ozone that has not been neutralized by one of the detoxification systems
(Figure 5-5) acts first at the biochemical level to impair the functioning of various cellular
processes (Tingey and Taylor, 1982; U.S. Environmental Protection Agency, 1986). The
result of these impairments are reflected in integrated changes in enzyme activities, membrane
function, and energy utilization (Queiroz, 1988). Several related papers have shown that the
activity of the primary carboxylating enzyme (RuBP-carboxylase) is reduced by O3 exposures
in the range of those measured at some sites (Dann and Pell, 1989; Enyedi et al., 1992; Pell
et al., 1992; Landry and Pell, 1993). Membrane injury has been found in some experiments
using acute levels of O3 (Heath, 1988). Chronic exposure can lead to changes in lipid
composition and in cold resistance (Brown et al., 1987; Davison et al., 1988; DeHayes et al.,
1991; Lucas et al., 1988; Wolfenden and Wellburn, 1991). Recently, Floyd et al. (1989) have
shown that O3 can affect nuclear deoxyribonucleic acid (DNA).
Changes in the in vivo concentrations of various growth regulators in response to
O3 exposure could have important consequences for plant function. However, the effects of
O3 on levels and activities of growth regulators have not been studied extensively. Ozone has
been shown to stimulate ethylene production, and inhibitors of ethylene production have been
found to reduce the effects of O3 in short-term experiments (Pell and Puente, 1986; Rodecap
and Tingey, 1986; Taylor et al., 1988b; Mehlhorn et al., 1991; Telewski, 1992; Langebartels
et al., 1991; Mehlhorn and Wellburn, 1987; Kargiolaki et al., 1991; Reddy
5-27
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Atmospheric Processes
Canopy Processes
Leaf Processes/
Ozone Uptake
Leaf Processes/
Mode of Action
Plant Response
Ecosystem Response
Absorption of
Ozone into Leaf
Reduced
Photosynthesis
Physiological Response to Ozone
Detoxification
Increased
Foliage
Senescence
Repair
I Replacement
Reduced Canopy
Carbon Gain
Respiratory
Losses
"-•A
Reduced Carbon Export
Figure 5-5. Effects of ozone (OJ absorption into a leaf. Once inside the leaf, O3 can have
a number of effects, all of which affect carbohydrate production and
utilization. Reduced photosynthesis, increased leaf senescence, production of
detoxification systems, and increased respiration (both maintenance and
growth) reduce the amount of carbohydrate available for allocation.
Compensation through production of new leaves, for instance, can counter
some or all of these effects, depending on the O3 exposure, the physiological
state of the plant, and the species. Integration of these processes leads to
changes in the amount of carbohydrate available for allocation from the
canopy. Solid black arrows denote O3 flow, and dotted arrows show the
cascade of effects of O3 absorption on leaf function. Boxes at the left and at
the top with double borders indicate leaf processes; the box at the bottom with
a dark border indicates the impact
et al., 1993). Ethylene is produced during ripening of fruit, during periods of stress, and
during senescence (Abeles et al., 1992). Increased levels of ethylene in the leaves could play
a role in the early senescence of foliage. In some cases, there is a correlation between
ethylene production and O3 sensitivity; however, the relationship is complex and makes use of
ethylene production as an index of sensitivity problematic (Pell, 1988).
5-28
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Abscisic acid (ABA) plays an important role in stomatal function (Davies et al.,
1980). Atkinson et al. (1991) found that stomata from O3 fumigated leaves were less
sensitive to ABA than control leaves. Maier-Maercker and Koch (1991a,b; 1992a,b) found
that exposure to ambient pollutants, including O3 and SO2, caused histological changes in
guard cells and resulted in some loss in stomatal control. Results from studies on European
white birch (Betulapenduld) also indicate some change in stomatal function (Matyssek et al.,
1992). These data could explain the observation that stomatal function may be impaired by
long-term O3 exposure (Walmsley et al., 1980). Kobriger et al. (1984) found no effect of
O3 on whole-leaf content of ABA, but changes in compartmentation could not be ruled out.
Physiological effects of O3 uptake are manifest in two ways: (1) reduced net
photosynthesis and (2) increased senescence (Figure 5-5). Both decreased photosynthesis and
increased leaf senescence result in the loss of capacity for plants to form carbohydrates,
thereby potentially having a major impact on the growth of the plant (Figure 5-6). The exact
response of a given individual will depend on its ability to compensate for O3 injury.
Atmospheric Processes
Reduced
Carbohydrate
Production
Ozone Effects
Canopy Processes
Leaf Processes/
Ozone Uptake
Leaf Processes/
Mode of Action
Carbohydrate
Allocation
r ^^^^^^^^^^^a^^^^^^fc
/ J^ Reproduction 1
"** ' 1 \ ,L,
Plant Response
Compensation
Ecosystem Response
f Other
Stresses
Figure 5-6. Effect of ozone (OJ on plant function and growth. Reduction in carbohydrate
allocation affects the pool of carbohydrates available for growth. Changes in
relative growth rate of various organs as a function of O3 exposure suggest
that allocation patterns of carbohydrate are affected. Solid black arrows
denote where O3 absorption affects the allocation processes of the plant; dotted
arrows show the cascade to plant growth. Boxes with dark borders indicate
site of impact The box with a double border, at left, indicates the location of
response.
5-29
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Ozone-induced reduction in net photosynthesis has been known for some time
(U.S. Environmental Protection Agency, 1986). Changes in stomatal conductance,
photosynthetic capacity, carbohydrate allocation, and respiration have been documented. The
relationship between O3 exposure and photosynthesis is not well known. Photosynthesis
provides plants with the energy and structural building blocks necessary for their existence.
The photosynthetic capacity of a plant is an important aspect of plant response to stresses in
natural environments and is strongly associated with leaf nitrogen content and with water
movement. Both resources are essential if the process is to occur and involves the allocation
of carbohydrates from the leaves to the roots for nitrogen acquisition and water uptake. Leaf
photosynthetic capacity is also age dependent. As the plant grows, the canopy structure
changes altering the amount and angle of light hitting a leaf. Allocation of carbohydrates and
nutrients to new leaves is especially important in stimulating growth production (Pearcy et al.,
1987). Reductions in photosynthesis are likely to be accompanied by a shift in growth pattern
that favors shoots and by an increase or decrease in leaf life span (Winner and Atkinson,
1986). Therefore, alteration of the processes of photosynthesis and carbohydrate allocation
affects plant response to stresses such as O3. Reduction in photosynthesis (reduced
carbohydrate formation and allocation to leaf repair or to new leaf formation decreases the
availability of carbohydrates) potentially alters the normal allocation pattern and, therefore, all
aspects of plant growth and reproduction (Figure 5-6). The effects of a reduction in
photosynthesis on growth and reproduction was discussed in the previous criteria document
(U.S. Environmental Protection Agency, 1986).
Carbohydrate production by a single plant is controlled not only by photosynthetic
capacity of the foliage but also by the amount and distribution of that foliage. Stow et al.
(1992) and Kress et al. (1992) found that O3 exposure affected needle retention in loblolly
pine (Pinus taedd). Similar data have been reported for slash pine (Pinus elliotti) (Byres
et al., 1992a). Keller (1988) and Matyssek et al. (1993a,b) reported increased senescence
with increased O3 exposure in trembling aspen, as did Wiltshire et al. (1993) in apple (Mains
spp). Replacement of injured leaf tissue has been reported for some species when they are
exposed to low O3 concentrations (Held et al., 1991; Temple et al., 1993). Temple et al.
(1993) also found increased photosynthetic capacity of new needles in O3 treatments
compared to controls.
Few direct effects of O3 have been found outside leaves. Kargiolaki et al. (1991)
found that intumescences (lesions) appear on stems of three species of poplar (Populus) after
72 days of O3 fumigation (70 to 80 ppb). Ozone probably enters the stem through the
lenticles that occur on the surface of the stem and allow direct exchange of gases between the
stem and the air. The consequence of this response to O3 is not clear; however, it may be
related to the reduction in phloem transport rate observed in loblolly pine (Spence et al.,
1990).
5.3.4.1 Carbohydrate Production and Allocation
The importance of photosynthesis and carbohydrate allocation in plant growth and
reproduction has been pointed out previously. The patterns of carbohydrate allocation directly
affect growth rate. Plants require a balance of resources to maintain optimal growth;
however, in natural environments optimal conditions seldom occur. Therefore, some plants
compensate for differences in resource availability and for environmental stresses. They do
this by changing the way they allocate carbohydrates (Chapin et al., 1987). Each response to
stress affects the availability of carbohydrates for allocation from the leaves (Figure 5-5).
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The carbohydrate pool is affected both by a reduction in the carbohydrate produced and by a
shift of carbohydrate to repair and replacement processes. The effect is particularly
noticeable in the roots where O3 exposure significantly reduces available carbohydrate
(Andersen et al., 1991; Andersen and Rygiewicz, 1991). Effects on leaf and needle
carbohydrate content have varied from a reduction (Barnes et al., 1990b; Miller et al., 1989c)
to no effect (Alscher et al., 1989) to an increase (Luethy-Krause and Landolt, 1990). Cooley
and Manning (1987) reviewed the literature on carbohydrate partitioning and noted that
"storage organs ... are most affected by O3-induced partitioning changes when
O3 concentrations are in the range commonly observed in polluted ambient air." Friend and
Tomlinson (1992) found that O3 exposure increased retention of 14C-labeled photosynthate in
needles of loblolly pine, and modified the distribution of labels among starch, lipids, and
organic acids (Edwards et al., 1992b; Friend et al., 1992).
The above discussion supports the information in the previous criteria document
(U.S. Environmental Protection Agency, 1986), which pointed out that roots usually were
affected more by O3 exposures than were the shoots. Studies by Miller et al. (1969), Tingey
et al. (1976b), McLaughlin et al. (1982), and Price and Treshow (1972) were cited in support
of this view. Miller et al. (1969) noted that reduction in photosynthesis was accompanied by
decreases in sugar and polysaccharide fraction in injured needles of ponderosa pine seedlings,
as well as by altered allocation of carbohydrates. Exposures were for 30 days, 9 h/day, to
concentrations of 0.15, 0.30, or 0.40 ppm. These exposures reduced photosynthesis by 10,
70, and 85%, respectively. The observations of Tingey et al. (1976a) indicated that
O3 exposures differentially affected metabolic pools in the roots and tops of ponderosa pine
seedlings grown in OTCs. Further, this study indicated that the amounts of soluble sugars,
starches, and phenols tended to increase in the tops and decrease in the roots of ponderosa
pine seedlings exposed to 0.10 ppm O3 for 6 h/day for 20 weeks. The sugars and starches
stored in the tree roots were significantly less than those in the roots of controls. In another
study cited in the 1986 document, McLaughlin et al. (1982) also observed the reduced
availability of carbohydrate for allocation to the roots and stated that the result was reduced
vigor and enhanced susceptibility of trees to root diseases. Loss of vigor was due to a
sequence of events that was associated with exposure to O3, including premature senescence,
loss of older needles, lower gross photosynthetic productivity, and reduced photosynthate
(carbohydrates) available for growth and maintenance. Carbon-14 transport patterns also
indicated changes in carbon allocation. Older needles were found to be the source of
photosynthate for new needle growth in the spring and were storage sinks in the fall.
Retention of 14C-photosynthate by foliage and branches of sensitive trees indicated that
allocation to the trunks and roots was reduced.
Lost carbohydrate production has effects throughout the plant (Figure 5-6). The
roots and associated mycorrhizal fungi are especially susceptible to reduced carbohydrate
availability and, quite frequently, show the greatest decline in growth (Adams and O'Neill,
1991; Edwards and Kelly, 1992; McQuattie and Schier, 1992; Meier et al., 1990; Taylor and
Davies, 1990). However, in some cases, increased mycorrhizal formation has been reported
(Gorissen et al., 1991b; Reich et al., 1985). It might be expected that reduced allocation to
roots would affect shoot growth through increased susceptibility to water stress, reduced
nutrient availability (Flagler et al., 1987), and reduced production of growth factors (Davies
and Zhang, 1991; Letham and Palni, 1983). Effects on production and retention of leaves and
needles were described above. Effects on stem growth have been found in tree species
(Hogsett et al., 1985b; Mudano et al., 1992; Pathak et al., 1986; Matyssek et al., 1992;
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Matyssek et al., 1993b). Changes in canopy density, root/shoot ratio, and stem growth will
affect the functioning of the plant and may make plants more susceptible to environmental
stresses, such as drought and nutrient limitation, that are characteristic of many ecosystems.
5.3.4.2 Compensation
Compensatory responses occur as plants attempt to minimize the effects of stress.
Responses include adjustments to changes in physiological processes (e.g., photosynthetic
performance and foliage production) that tend to counteract the effects of O3 absorption by
the leaves. Pell et al. (1994) have reviewed the extensive literature produced in the Response
of Plants to Interacting Stresses (ROPIS) experiment (Goldstein and Person, 1994). A wide
range of compensatory responses have been identified, especially reallocation of resources
leading to increased relative growth in the shoot compared to the root (see above).
Compensation can take the form of production of new tissue (e.g., leaves) to replace injured
tissue or of biochemical shifts, including increased photosynthetic performance in new foliage.
Changes in respiratory rate have been attributed to such repair processes (U.S.
Environmental Protection Agency, 1986). Recent studies have found stimulation of dark
respiration in Norway spruce (Barnes et al., 1990b; Wallin et al., 1990) and pinto bean
(Amthor, 1988; Amthor and Cumming, 1988; Moldau et al., 1991b). Repair of membranes
(Sutton and Ting, 1977; Chevrier et al., 1988, 1990) and replacement of impaired enzymes
are two probable reasons for increased respiration. Ozone has been shown to increase the
adenosine triphosphate/adenosine diphosphate (ATP/ADP) ratio, which is consistent with
increased respiratory activity (Weidmann et al., 1990; Hampp et al., 1990). As in the case of
detoxification, the importance of repair processes in the overall carbohydrate budget of the
plant and of their influence of apparent threshold is unknown.
Recovery of photosynthetic performance after O3 exposure has been noted in some
studies. Early work indicated that recovery of photosynthetic capacity could occur after
exposure of high concentrations (>0.25 ppm) of O3 (e.g., Botkin et al., 1971, 1972). Dann
and Pell (1989) found that photosynthetic rate, but not Rubisco activity, recovered within a
few days in potato (Solanum tuberosum) after exposure to 0.2 ppm O3. In ponderosa pine,
photosynthetic rates in O3 treated needles recovered to that of controls within 40 to 50 days
(Weber et al., 1993). To what extent this recovery can offset losses in carbohydrate gain is
not known, nor is the mechanism.
Replacement of injured foliage (see Section 5.3.4) is another method to counteract
the effects of O3 exposure. The extent to which increased leaf and needle production and
increased photosynthetic performance in the new foliage compensates for O3 injury is not
known.
The importance of various compensatory mechanisms is not sufficiently well
known to allow an estimate of the degree to which they might mitigate the effect of O3. The
fact that increases in photosynthesis and in leaf production have been measured indicates that
these processes, at least, may be important.
5.3.5 Role of Age and Size Influencing Response to Ozone
Plant age, physiological state, and frequency of exposure play important roles in
plant response to O3. In annual species, effects of O3 on production will occur through
changes in allocation of carbohydrates over the years, resulting in reduced seed production.
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In perennial species, plant growth will be affected by reduction in storage of carbohydrates,
which may limit growth the following year (carry-over effects). Carry-over effects have been
documented in the growth of tree seedlings (Hogsett et al., 1989; Sasek et al., 1991; Temple
et al., 1993) and roots (Andersen et al., 1991). Accumulation of these effects will affect
survival and ability to reproduce. Data on cumulative effects of multiple years of
O3 exposures have been, for the most part, the result of 2- to 3-year studies.
A tacit assumption in much of the research on O3 effects on trees is that seedling
response to O3 is a good predictor of large-tree response. This assumption has been
necessitated by the difficulty in exposing large trees to O3 for long periods. Pye (1988)
reviewed the problems of extrapolation from seedling/sapling experiments to large trees and
noted several areas of difference between seedling/saplings and large trees: (1) microclimate
(especially radiation), (2) transport distances, (3) ratio of photosynthetic to respiratory tissue,
and (4) potential for storage. Cregg et al. (1989) also argued that these differences in scale
can affect growth responses seen. Some studies have indicated that seedlings may be more
sensitive (i.e., greater visible injury) than large trees (Kozlowski et al., 1991); however,
Samuelson and Edwards (1993) found that leaves on large red oak trees (Quercus rubrd) are
more sensitive than those on seedlings. It is likely that a variety of factors determines
sensitivity to O3, including stomatal function and presence of detoxification systems, so that,
in some cases, seedlings will be more sensitive and, in others, large trees will be. Although
each of the four differences between small and large trees mentioned above can be supported
on theoretical grounds, little direct information is available to evaluate the importance of these
differences, especially with respect to O3.
The microclimate of the canopy of mature trees is quite different from that of
seedlings, as is that of a stand of trees compared to a single tree in a field. Light intensity
through the multilayer canopy can vary by an order of magnitude or more (Jones, 1992).
In addition, gradients of other important microclimatic variables (temperature, humidity, and
wind speed) exist within the canopy. These will all affect stomatal conductance, and some
(e.g., wind speed) will affect canopy conductance. In addition, leaf development will be
affected by these microclimatic variables (especially light intensity), leading to leaves with
different physiological capacity and sensitivity to O3 (Samuelson and Edwards, 1993; Waring
and Schlesinger, 1985).
The effect of plant size on transport processes and the subsequent response to O3 is
unknown. The simple fact of greater distance over which transport must occur will affect the
timing of response of organs distant from the primary site of O3 impact, the foliage. Studies
using methods that integrate functions over the whole tree could provide useful information.
For example, combinations of porometer measurements on foliage and whole-plant water use
measured (Schulze et al., 1985) on individuals of different sizes could provide very useful
information on the coupling of leaf-level processes to whole-canopy and whole-plant
response. Greater evaporative demand in large trees as the result of greater leaf area and
different microclimate than in small trees could lead to transient water stress and stomatal
closure because of insufficient water transport capacity.
As a tree grows from a seedling to a large tree, the ratio between photosynthesis
and respiration declines as a greater portion of the plant tissue becomes nonphotosynthetic. It
is reasonable to assume that such a change could result in less resource being available for
detoxification and repair as the plant grows. How this change affects the ability of a plant to
survive O3 (or any other stress) is not known. Recently, Samuelson and Edwards (1993)
presented data on northern red oak that show O3 decreased photosynthetic performance more
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on lower leaves within the canopy of large trees than on leaves near the top of the canopy
(a result apparently counter to the model results of Reich et al., 1990). Seedling
photosynthesis was not affected by the same O3 exposure. A more interesting result of this
work is the reduction in total canopy biomass found in large trees exposed to O3. It is not
possible to assess directly the relative importance of reduced photosynthesis versus loss of
canopy from these data, but the data do show that differences may exist between large trees
and seedlings in their response to O3. These differences may be due to changes in carbon
budgets, stomatal characteristics, microclimate, and flushing patterns that develop as seedlings
become trees. The ability of northern red oak seedlings to produce three flushes and thus
replace injured foliage may be an important defense mechanism in the seedling stage. The
physiological basis of these findings need further investigation.
In evergreen perennial plants, foliage must be maintained from one year to the
next, frequently through periods unfavorable to growth. In evergreen species that retain a few
to several years of leaves, increased susceptibility to stress (e.g., frost) could further reduce
potential canopy photosynthesis in subsequent years (Brown et al., 1987; Davison et al., 1988;
DeHayes et al., 1991; Lucas et al., 1988). Fincher (1992) found that O3 decreased frost
tolerance in red spruce in both seedlings and trees; the consequences of this change in
seedlings and large trees needs of further study.
The effect of O3 on storage of carbohydrates in large compared to small trees is
not known. Changes in storage could affect the ability of the plant to withstand other stresses
or to produce adequate growth during each growing season.
Dendrochronology (tree-ring analysis) provides the opportunity to do retrospective
studies over the life of large trees. Reduction in annual radial growth has been found in the
southern Sierra Nevada for Jeffrey pine but not for ponderosa pine (Peterson et al., 1987,
1989, 1991; Peterson and Arbaugh, 1988). One difficulty with using tree-ring data to
estimate O3-related effects is that it is not always possible to separate reductions due to
O3 from other effects (e.g., drought).
Development of reliable methods for scaling from small to large trees is crucial to
the prediction of the long-term effects of O3 on forest function. Measurement of the response
of different size trees to O3 could provide useful data on the relative responses of small and
large trees. However, problems exist in giving similar exposures to trees of widely different
sizes. The most direct method is to fumigate trees over a significant portion of their life
span. Time is the primary obstacle to these studies because they would require decades to
complete. Whatever methods are used must be based on a good understanding of the
physiological changes that occur as trees grow.
5.3.5.1 Summary
In the previous criteria document, it was concluded that the "critical effects,
including reduction in photosynthesis and a shift in the assimilation of photosynthate, will
lead to reduced biomass, growth, and yield" (U.S. Environmental Protection Agency, 1986).
In addition, changes in carbohydrate allocation patterns and effects on foliage were noted as
important. Since that report, additional information has been developed, especially on the
effects of O3 on photosynthetic performance. However, at present there is still no clear
understanding of the initial biochemical changes resulting within the leaf cells after the entry
of O3 and how these changes interact to produce the observed responses. Much of the earlier
research used very high (>0.25 ppm) O3 concentrations, which produced what could be
characterized as acute responses. More recent research has used lower concentrations, usually
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including near ambient (0.04 to 0.06 ppm) O3 levels, so that the observed responses may be
more relevant to field conditions. One characteristic of these more recent data is that a longer
exposure (days to weeks, instead of hours) is needed to show a response.
As a result of the research since the last criteria document (U.S. Environmental
Protection Agency, 1986), the way in which O3 exposure reduces photosynthesis, especially
its effects on the central carboxylating enzyme (ribulose-6-P-carboxylase/oxygenase), is better
understood. The rate of senescence of leaves has been shown to increase as a function of
increasing O3 exposure. At near-ambient exposures, leaf production has been shown to
increase in some species, thereby off-setting the increased loss to due senescence. The
mechanism of the increase in senescence is not known, hence deserves further study. Finally,
the role that changes in allocation of resources play in plant response to O3 is now better
understood. Most studies have shown that allocation of photosynthate to roots is decreased
by O3. In some cases, allocation to leaf production has increased. Whether these changes are
driven entirely by changes in carbohydrate availability or are controlled by other factors (e.g.,
hormones) is not known.
Some potentially significant processes have been investigated since the last criteria
document, especially detoxification and compensatory processes. The role of detoxification in
providing a level of resistance to O3 has been investigated; however, it is still not clear to
what degree these processes can provide protection against O3 injury. Data are needed
especially on the potential rates of antioxidant production and on the subcellular localization
of the antioxidants. Potential rates of antioxidant production are needed to assess whether
they are sufficient to detoxify the O3 as it enters the cell. The localization is needed to assess
whether the antioxidants are in a location (cell wall or plasmalemma) that permits contact
with the O3 before it has a chance to damage subcellular systems. Ozone exposure has been
shown to decrease cold tolerance of foliage in some species. This response could have a
major impact on long-lived evergreen species that retain leaves for several years. Various
forms of compensation, especially stimulation of production of new leaves and higher
photosynthetic performance of new leaves, have been reported. Although these processes
divert resources away from other sinks, compensation may counteract the reduction in canopy
carbon fixation caused by O3. The quantitative importance of these processes is still in need
of investigation.
The major problem facing researchers trying to predict long-term O3 effects on
plants is how the plant integrates all of the response to O3 into the overall response to the
environment, including naturally occurring stresses. Little is now known about how response
to O3 changes with increasing age and size. This information is crucial to predicting the
long-term consequence of O3 exposure in forested ecosystems.
5.4 Factors That Modify Plant Response
5.4.1 Modification of Functional and Growth Responses
Plant response to oxidants may be modified by various biological, physical, and
chemical factors. Biological factors that modify plant response include those within the plant,
as well as those external to the plant. The genetic makeup and the developmental stage play
critical roles in the way individual plants respond to O3 and other external stresses. For
example, different varieties or cultivars of a particular species are known to differ greatly in
their responses to a given exposure to O3, whereas the magnitude of the response of a
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particular variety, in turn, depends on environmental factors such as temperature and
humidity, soil moisture and nutrition, the presence of pests or pathogens, and exposure to
other pollutants or agricultural spray chemicals. In other words, response will be dictated by
the plant's present and past environmental milieu, which also includes the temporal pattern of
exposure and the plant's stage of development. The corollary is also true: exposure to
oxidants can modify response to other environmental variables. For example, exposure to
O3 reduces the ability of trees to withstand winter injury caused by exposure to freezing
temperatures (Davison et al., 1988) and influences the success of pest infestations (Hain,
1987; Lechowicz, 1987). Hence, both the impact of environmental factors on response to
oxidants and the effects of oxidants on responses to environmental factors have to be
considered in determining the impact of oxidants on vegetation in the field. These
interactions are summarized as the involvement of "other stresses" in the scheme shown in
Figure 5-6 (Section 5.3). In the following review, the environmental factors are grouped into
three categories: (1) biological (including genetic and developmental components), (2)
physical, and (3) chemical.
Runeckles and Chevone (1992) have provided a general review of the interactive
effects of environmental factors and O3. The subject also is treated in a National Acid
Precipitation Assessment Program (NAPAP) report (Shriner et al., 1991). The numbers of
publications that have appeared since the previous criteria document and supplement vary
widely among the different environmental factors reviewed. As a result, in several sections,
material covered in these earlier documents has been repeated in order to provide
comprehensive coverage and to place new findings into context.
5.4.2 Genetics
The response of an individual plant within a species and at a given age is affected
both by its genetic makeup and the environment in which it grows. This section examines the
role of genetics in plant response to O3 and its implication for both managed and natural
ecosystems. In addition, major knowledge gaps in the understanding of genetic aspects of
O3 responses are pointed out.
The responses of plants to O3 are strongly influenced by genetics, as was
summarized in the air quality criteria document for O3 (U.S. Environmental Protection
Agency, 1986). Thus, the plants of a given population or family will not respond to O3 in the
same way, even if they are grown in a homogenous environment. This has been
demonstrated amply through intraspecific comparisons of O3 sensitivity as determined by
foliar sensitivity of ornamental plants, the aesthetic value of which is decreased by visible
foliar injury, and of woody plants that are important components of natural ecosystems
(Table 5-2). Ornamental plants and plants growing in wilderness areas, for example, have an
intrinsic worth, apart from any economic value related to growth (Tingey et al., 1990).
Considerable genetic variation in O3 sensitivity also has been demonstrated for growth
responses of crop plants (Table 5-3). The range of responses displayed for visible foliar
injury and growth, biomass, or yield vary from species to species and from study to study.
However, it is not uncommon to have genotypes varying from no response to well over 50%
leaf area injured or 50% growth or yield reductions in the same study. Additional examples
of genetic variation in O3 response are shown in Figure 5-7 for visible foliar injury and in
Figure 5-8 for growth. From Figure 5-7, one can see that, depending on what population has
been examined, white ash (Fraxinus americand) and green ash (F. penmylvanicd) could
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Table 5-2. Examples of Intraspecific Variation of Foliar Symptoms
in Ozone Response
Species
Ornamental,
Non-woody
Plants
Petunia sp.
(Petunia)
Poa pratensis L.
(Kentucky bluegrass)
Genetic Ozone Range of
Unit3 Concentration Duration Response15 Reference
Cultivars 400 ppb
4h/day
Cultivars 400 ppb
300 ppb
4 days 20 to 60% (3) Elkiey and Ormrod
(1979a,b),
Elkiey et al. (1979)
2 h 0 to 90% (3) Murray et al. (1975),
4 h 30 to 60% (3) Wilton et al. (1972)
Trees
Acer rubrum L.
(Red maple)
Fraxinus americana L.
(White ash)
Fraxinus pennsylvanica
Marsh. (Green ash)
Populations 750 ppb 3 days 19 to 34% (2) Townsend and
7 h/day Dochinger (1974)
Half-sib 500 ppb 7.5 h 0 to 50% (3) Karnosky and Steiner
families 250 ppb 6 h 2 to 33% (2) (1981),
Steiner and Davis
(1979)
Half-sib 500 ppb 7.5 h 0 to 40% (3) Karnosky and Steiner
families 250 ppb 6 h 2 to 39% (2) (1981),
Steiner and Davis
(1979)
Gleditsia triacanthos L.
(Honeylocust)
Pinus ponderosa
Dougl. ex P.
Laws and C. Laws
(Ponderosa pine)
Pinus strobus L.
(Eastern white pine)
Pinus taeda L.
(Loblolly pine)
Populus tremuloides
Michx. (Trembling
aspen)
Cultivars
Half-sib
families
Clones
Half-sib
families
Clones
Ambient
1.5 x ambient
300 ppb
250 ppb
ambient +
60 ppb
200 ppb
150 ppb
1 growing
season
3 growing
seasons
6h
8h
1 growing
season
3 h
6h
0 to 34% (3)
0 to 28% (2)
0 to 60% (3)
3 to 29% (2)
1 to 42% (1)
7 to 56% (1)
10 to 91% (1)
Karnosky (198 la)
Temple et al. (1992)
Houston (1974)
Kress et al. (1982a),
Adams et al. (1988)
Karnosky (1977),
Berrang et al. (1991)
aCultivars = a variety of agricultural or horticultural crops produced by selective breeding or a vegetatively
propagated tree selection; Half-sib = seedlings with one parent in common; Clones = vegetatively propagated
individual genotypes; and Populations = seedlings derived from a common gene pool.
bRange of response is expressed as (1) percentage of leaves showing visible symptoms, (2) percentage of leaf
area injured, or (3) percentage from a leaf injury rating scheme.
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Table 5-3. Examples of Intraspecific Variation in Growth Responses
Following Ozone Exposures
Species
Crops and
Non-woody
Plants
Agrostis capillaris L.
(Bentgrass)
Begonia semperflorens
Hort. (Bedding
begonia)
Festuca arundinacea
Schreb. (Fescue)
Lycopersicon
esculentum L.
(Tomato)
Phaseolus vulgaris L.
(Snapbean)
Plantago major L.
(Common plantago)
Raphanns sativus L.
(Radish)
Silene cucabalus
(Bladder campion)
Solanum tuberosum L.
(Potato)
Spinacia oleracea L.
(Spinach)
Trees and Other
Woody Plants
Acer rubrum L.
(Red maple)
Abies alba Mill.
(Silver fir)
Pinus elliottii
Engelm. (Slash pine)
Genetic
Unita
Populations
Cultivars
Cultivars
Cultivars
Cultivars
Populations
Within
cultivar
Populations
Cultivars
Cultivars
Populations
Populations
Half-sib
families
Ozone
Concentration
60ppb
500 ppb
4 h/day
250 ppb
4 h/day
400 ppb
6 h/day
400 ppb
1.5 x ambient
60 ppb
7h
72 ppb
7h
80 ppb
7 h/day
70 nL/
1-7 h/day
0.1 uL/
1-4 h/day
3 days/week
35 ppb
12 h/day
150 ppb
6 h/day
130 ppb
7 h/day
750 ppb
7 h/day
250 ppb
7 h/day
3 x ambient
Duration
4 weeks
2 days
4 days
7 days
2h
1 growing
season
mean -
44 days
mean -
54 days
42 days
2 weeks
3 weeks
4 weeks
8 days
38 days
3 days
10 days
3 growing
seasons
Range of
Response15
-45 to +20% (2)
-59 to 0% (2)
-16 to +10% (2)
-53 to -35% (2)
-50 to -4% (2)
-54 to -17% (3)
-26 to -2% (3)
-73 to -44% (3)
-68 to -50% (3)
-24 to 0% (1)
-40 to -5% (2)
-75 to -48% (2)
-10 to 0% (2)
-40 to 0% (2)
-56 to -28% (2)
-36 to -17% (1)
-18 to +3% (1)
-20 to 0% (1)
Reference
Dueck et al.
(1987;
Reinert and Nelson
(1979),
Reinert and Nelson
(1980)
Flagler and
Younger (1982)
Reinert and
Henderson (1980),
Temple (1990a)
Heck et al. (1988),
Temple (1991),
Eason and Reinert
(1991)
Reiling and
Davison (1992a)
Gillespie and
Winner (1989)
Ernst et al. (1985)
Pell and Pearson
(1984),
Ormrod et al.
(1971)
Heagle et al.
(1979a)
Townsend and
Dochinger (1974)
Larsen et al.
(1990)
Dean and Johnson
(1992)
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Table 5-3 (cont'd). Examples of Intraspecific Variation in Growth Responses
Following Ozone Exposures
Species
Pinus taeda L.
(Loblolly pine)
Pinus taeda L.
(Loblolly pine)
Populus tremuloides
Michx. (Trembling
aspen)
Rhododendron
obtusum
(Lindl) Planch.
(Azalea)
Genetic
Unif
Full-sib
families
Half-sib
families
Clones
Cultivars
Ozone
Concentration
50 ppb
6h/day
1.9 x ambient
Ambient +
60 ppb
2.5 x ambient
250 ppb
26.4 ppm-h
ambient
250 ppb -
3 h/day
Duration
28 days
2 growing
seasons
1 growing
season
1 growing
season
8h
92 days
3 growing
seasons
6 days
Range of
Response15
-18 to 0% (1)
-19 to 0% (2)
-27.5 to +3% (2)
-19 to -2% (2)
-22 to +30% (2)
-74 to -5% (2)
-24 to -12% (2)
-43% to 0% (2)
Reference
Kress et al.
(1982b),
Shafer and
Heagle (1989)
Adams et al.
(1988),
Qiu et al. (1992),
Winner et al.
(1987)
Karnosky et al.
(1992a),
Wang et al.
(1986a,b)
Sanders and
Reinert (1982)
aCultivars = a variety of agricultural or horticultural crops produced by selective breeding or a vegetatively
propagated tree selection; Half-sib = seedlings with one parent in common; Clones = vegetatively propagated
individual genotypes; and Populations = seedlings derived from a common gene pool.
bRange of response is expressed as (1) decrease compared to charcoal-filtered-air control plants in terms of
growth, (2) biomass, or (3) yield.
have been classified as either O3 sensitive or O3 tolerant. Also noticeable from this figure is
the large amount of variation in O3 tolerance of individual half-sib (one parent in common)
families from a given population. From Figure 5-8, the heterogeneity within a given loblolly
pine half-sib family in terms of growth is displayed. This variability has some interesting
implications. First, because plants of a given species vary widely in their response to
O3 exposure, response relationships generated for a single genotype or small group of
genotypes may not represent adequately the responses of the species as a whole (Temple,
1990a). Second, because of the genetic variability and differential fitness extant among
different genotypes in a population of plants, O3 imposes a selective force favoring tolerant
genotypes over sensitive ones (Roose et al., 1982; Treshow, 1980). Each of these
implications will be discussed in this section.
Mechanisms and Gene Numbers
Little is known about the genetic bases for O3 resistance mechanisms or about the
numbers of genes involved in these mechanisms (Pitelka, 1988). Most O3 resistance
mechanisms involve a physiological cost that will result in decreased growth and productivity
of resistant plants grown under O3 stress. Partial or complete stomatal closure in the presence
of O3 is an example of a mechanism of resistance that has been demonstrated for several
plants (Engle and Gabelman, 1966; Thorne and Hanson, 1976; Reich, 1987;
5-39
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250-
200
A. F. americana
4567
Provenance
8
10
x
250
200
c 150
^
.5,100-
50-
B. F. pennslvanica
1
12345
6 7 8 9 10 11 12 13 14 15 16
Provenance
Figure 5-7.
The average injury index for visible foliar injury after exposure of 1-year-old seedlings to 50 pphm
ozone for 7.5 h. Each mean shown represents the average of five trees per family. There were
either four or five half-sib families for each white ash (Fraxinus americana L.) provenance
(geographic location) and either three or four families for each green ash (F. pennsylvanica Marsh.)
provenance. The specifics of the experimental design are reported in Karnosky and Steiner (1981).
5-40
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Figure 5-8.
113 137 163 188 213 237 263 288 313 337 363 388 413 437 463 488 513
Midpoint of Biomass Class (g)
Frequency distribution showing the variability in ozone (O3) response
(midpoint of whole-plant biomass) within one half-sib family of
loblolly pine (P. taeda L.) exposed to increasing levels of O3 under
chronic-level field conditions over several growing seasons (Adams
et al., 1988). The arrows show the mean response for each of the
three O3 treatments (subambient, ambient, and above-ambient O3).
The specifics of the experimental design are reported by Adams
et al. (1988). This figure was developed by Taylor (1994).
Sumizono and Inoue, 1986; Tingey and Taylor, 1982) and that involves a high physiological
cost because plants that have reduced stomatal conductivity also will have reduced carbon
assimilation for growth (Ehleringer, 1991). Tolerance of internal leaf tissues to O3 may
involve the production of antioxidant defense compounds (Lee and Bennett, 1982; Gupta
et al., 1991) or other types of biochemical defense systems. The extent to which these
internal tolerance mechanisms have physiological costs associated with them is not yet
understood, but it is likely that increased defense compound production, triggered by O3, will
impact the amount of carbon available for growth (Ehleringer, 1991). The genetic regulation
of these or other O3 resistance mechanisms has not yet been characterized thoroughly.
Whether or not O3 resistance is due to single gene or multi-gene control will affect
the rate and extent of resistance development (Roose, 1991). Rapid stomatal closing in the
presence of O3 appears to be under the control of either a single gene or a few genes in onion
(Allium cepct) (Engle and Gabelman, 1966), some bean (Phaseolus vulgaris) cultivars
5-41
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(cultivated varieties) (Knudson-Butler and Tibbitts, 1979), soybean (Damicone et al., 1987b),
and petunia (Petunia spp.) (Elkiey and Ormrod, 1979a,b; Elkiey et al., 1979). Generally,
resistance mechanisms appear to be more complex (Karnosky, 1989a) and seem to involve
multiple gene control as has been demonstrated in tobacco (Aycock, 1972; Huang et al., 1975;
Povilaitis, 1967), some bean cultivars (Mebrahtu et al., 1990a,b,c), corn (Cameron, 1975), tall
fescue (Festuca arundinaced) (Johnston et al., 1983), potato (De Vos et al., 1982; Dragoescu
et al., 1987), and loblolly pine (Weir, 1977; Taylor, 1994).
Genetic Implications of Ozone Effects: Managed Ecosystems
Because of the high cost involved in conducting long-term growth studies to
determine O3 effects on plants, only a small proportion of the total number of commercial
crop cultivars and important tree seed sources, families, clones, and cultivars have been
examined adequately for O3 sensitivity. Still, a tremendous amount of variation has been
found, as was described in the previous O3 criteria document (U.S. Environmental Protection
Agency, 1986) and in Tables 5-2 and 5-3.
Plant breeders and nurserymen working in locations with high O3 concentrations
have inadvertently developed selections more tolerant to O3 than those developed in locations
with low O3 exposures (Reinert et al., 1982; Roose et al., 1982). The cultivars Team alfalfa
and Kennebec, Pungo, and Katahdin potatoes were developed at the U.S. Department of
Agriculture Research Center at Beltsville, where 0.120 ppm O3 frequently is exceeded
(Lefohn and Pinkerton, 1988; Ludwig and Shelar, 1980). These cultivars have proven to be
more O3 tolerant than cultivars developed elsewhere (Reinert et al., 1982). Similarly, cotton
(Gossypium spp.) and sugar beet (Beta spp.) cultivars developed in Southern California, where
O3 levels are among the highest in the country, are more O3 tolerant than cultivars developed
in low O3 areas (Reinert et al., 1982).
Nurserymen, Christmas tree growers, and seed orchard managers all routinely have
discarded pollution-sensitive chlorotic dwarf and tip-burned white pine trees because of their
slow growth in areas with high O3 exposures (Umbach and Davis, 1984). Thus, they have
contributed to the selection of more O3-tolerant commercial forests.
Although these examples suggest that selection of O3-tolerant genotypes is
possible, the general consensus of the scientific community is that top priority should be
given to solving pollution problems at their source (Karnosky et al., 1989) and not in
selecting pollution-tolerant cultivars.
An interesting set of experiments by Barnes et al. (1990c) and Velissariou et al.
(1992) have described a concern about the modern crop varieties that have been developed in
clean-air environments but are being grown routinely in areas with elevated O3 exposures.
These authors speculated that breeders of spring wheat (Triticum aestivum) grown in Greece
inadvertently had selected varieties with increased O3 sensitivity due to their higher rates of
stomatal conductivity (Velissariou et al., 1992). Velissariou et al. (1992) found a significant
correlation between year of introduction and stomatal conductance, with stomatal
conductance, increasing with the more modern introductions. The authors suggested that the
selection for higher yields had resulted in a higher O3 uptake for the modern spring wheat
cultivars, contributing to their increased O3 sensitivity. When they compared the relative
growth rates of spring wheat cultivars released over the period from 1932 to 1980, the
modern cultivars had more foliar injury and more growth decrease when grown in the
presence of O3 (Barnes et al., 1990c; Velissariou et al., 1992).
5-42
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Genetic Implications of Ozone Effects: Natural Ecosystems and Biodiversity
Air pollutants can affect the genetics of plant populations in two ways: (1) they
may increase mutation rates or (2) they may apply selection pressures that eventually may
lead to adaptive responses (Cook and Wood, 1976). The issue of O3-induced changes in
mutation rate has not been studied adequately, but recent evidence by Floyd et al. (1989)
suggests that DNA may be affected by O3 to induce mutation in plants. However, there is
evidence that O3 may be affecting plant populations via natural selection. According to
Bradshaw and McNeilly (1991), there are three stages of selection-driven population change:
Stage I, elimination of the most sensitive genotypes; Stage II, elimination of all genotypes
except the most resistant; and Stage III, interbreeding of the survivors.
The first report of O3 as a selective force in plant populations was that involving
lupine (Lupinus bicolor) populations in the greater Los Angeles area (Dunn, 1959). Local
Los Angeles area populations were more O3 resistant than populations originating from
cleaner-air areas. Berrang et al. (1986, 1989, 1991) have presented evidence for population
change in trembling aspen (Populus tremuloides). Aspen clones from across the United States
were sampled randomly from populations in polluted and nonpolluted areas. Aspen from
areas with high ambient O3 concentrations were injured visibly to a lesser extent by
experimental O3 exposures than clones from areas with low O3 concentrations (Berrang et al.,
1986, 1991). Similar results were seen for field trials of O3 injury (Berrang et al., 1989).
More recently, growth rate and biomass differences have been reported for aspen clones
differing in O3 tolerance (Karnosky et al., 1992b). Berrang et al. (1989) suggest that sensitive
genotypes are not killed directly by O3, but are eliminated through intraspecific competition
for light, nutrients, and water with their resistant neighbors. Spatial (population) variation in
O3 resistance that is related to background O3 pollution also has been demonstrated in British
populations of plantago (Plantago major) (Reiling and Davison, 1992a,b).
There have been three concerns raised regarding the spatial variation studies of
O3 resistance. First, because O3 generally does not show steep concentration gradients, spatial
studies must involve populations that are great distances from one another, so it is difficult to
determine whether geographical differences in O3 resistance are related primarily to local
O3 exposures or to other environmental factors (Reiling and Davison, 1992a). Second, spatial
studies are limited by the general absence of historical records of ambient O3 concentrations
at the sites where the populations were sampled (Bell et al., 1991). Third, no O3 study has
collected plants from the same population over time to demonstrate O3-induced population
change over time (Bell et al., 1991), as has been demonstrated for other pollutants. However,
Karnosky (1981b, 1989b) studied the O3 symptom expression and survival of over 1,500
eastern white pine trees growing in southern Wisconsin and found that O3-sensitive genotypes
had a 10-times-higher rate of mortality than did the O3-resistant genotypes over a 15-year
study (Table 5-4). This is direct evidence of the occurrence of Stage I natural selection.
Further evidence of this type was presented by Heagle et al. (1991a), who found a population
change in O3 sensitivity over 2 years with white clover (Trifolium repens) exposed to O3 in
OTCs. A high O3 dose at the end of the study caused significantly less foliar injury in plants
that survived two seasons of exposure to high O3 concentrations than in plants that had
survived low O3 concentrations.
The rate of evolution is dependent on the selection pressure, the magnitude of the
genetically controlled variability, and the number of genes involved (Roose, 1991).
Long-lived species, such as trees, will evolve more slowly than annuals or biennials
5-43
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Table 5-4. Mortality of Three Ozone Sensitivity Classes of
Eastern White Pine (Pinus Strobus L.) Trees During 1971 to 1986
Sensitivity Classa Number Trees Number Trees Dead Percent Mortality
Resistant
Intermediate
Sensitive
1,386
98
57
34
3
14
2.4%
3.1%
24.6%
aResistant = not showing visible foliar injury during the study; Intermediate = showing visible injury, including
foliar tip burn during 1 or 2 years; Sensitive = showing visible injury, including foliar tip burn, short needles,
and poor needle retention for 3 or more years of the study.
Source: Karnosky (1989b).
(Barrett and Bush, 1991). Gillespie and Winner (1989) found O3 to be a strong and rapid
selective force with radish (Raphanus sativus). Ozone resistance was expressed within one
generation following a series of artificial pollinations with various populations from the radish
cultivar "Cherry Belle".
Whether or not the loss of some genotypes from plant populations is important is a
debatable question. However, it is likely that sensitive genotypes are being lost from natural
ecosystems with current O3 exposures. Field studies documenting differential growth rates of
O3-sensitive and tolerant genotypes of eastern white pine in natural ecosystems influenced by
O3 were summarized in the previous air quality criteria document for O3 (U.S. Environmental
Protection Agency, 1986). Similar findings subsequently have been reported for O3-sensitive
and tolerant Jeffrey pine trees in California (Peterson et al., 1987). It is likely that these
growth-rate differences affect the competitive ability of O3-sensitive genotypes and increase
their mortality rate (Karnosky, 1989b).
Although some loss of rare alleles (one of a series of genes that are alternative in
inheritance) and change in gene frequency is likely with loss of sensitive genotypes, the
significance of these effects on biodiversity is unknown (Barrett and Bush, 1991). If the
remaining population of O3-resistant plants is less adaptable to subsequent change due to a
reduced redundancy, as has been predicted by Gregorius (1989), or if O3 sensitivity is linked
to other traits such as rapid growth or high productivity, as has been suggested because of the
inherently higher gas-exchange rates of some O3-sensitive genotypes (Barnes et al., 1990c;
Thorne and Hanson, 1976; Turner et al., 1972; Velissariou et al., 1992), then losing these
sensitive genotypes is both biologically and economically important. This remains a point of
scientific debate. Although the evolution of resistance to air pollution is hypothesized to
contribute to the loss of genetic variability (Scholz et al., 1989; Karnosky, 1991), other
scientists suggest that there is little experimental evidence for concluding that genetic
diversity is actually threatened by air pollution and that air pollution has less important
implications for plant populations than do factors such as global climate change and habitat
fragmentation (Parsons and Pitelka, 1991; Taylor and Pitelka, 1992). Clearly, there is a need
for additional research in this area of O3 effects in plant biodiversity (Karnosky et al., 1989).
5-44
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Reproductive Aspects and Related Genetic Implications
In the previous discussion in this section, only natural selection at the whole-plant
level has been mentioned. This type of selection occurs as plants compete with their
neighbors for survival and the ability to reproduce. Selection is thought to occur also during
the reproductive process (Feder and Sullivan, 1969; Krause et al., 1975), and this is referred
to as gametophytic selection (Mulcahey, 1979; Wolters and Martens, 1987) or fertility
selection (Venne et al., 1989). The ability of gametophyte (haploid part of the plant-life
cycle) selection to modify the sporophytic generation depends on two critical issues:
(1) pollen genes should be expressed after meiosis (cell divisions leading to production of
gametes), and (2) those same genes also should be expressed in the sporophytes (diploid part
of the plant-life cycle) (Mulcahey and Mulcahy, 1983). This genetic overlap has been
demonstrated in some species (Mulcahy, 1979; Searcy and Mulcahy, 1985; Walsh and
Charlesworth, 1992). Indirect evidence for O3-induced gametic selection was presented for
Scot's pine (Pinus sylvestris) by Venne et al. (1989). Based on their studies of the effects of
O3 on the pollen germination and tube elongation of some 30 Scots pine clones, they found
that O3 could change markedly the relative male contribution to successful fertilization.
However, this study did not actually examine offspring, as would be needed to positively
prove O3-induced gametophytic selection.
Studies of O3 effects on pollen germination and tube elongation generally have
found a negative impact of O3 on this critical element of reproduction (Table 5-5). Whether
or not selection is occurring at the pollen level because of a selective disadvantage of the
pollen from sensitive genotypes is a debatable issue. Feder (1986) and Krause et al. (1975)
found that the pollen from O3-sensitive genotypes of petunia and tomato (Lycopersicon
esculentum) was more severely affected by O3 than pollen from tolerant genotypes, suggesting
that gametophytic selection could be occurring. Similar results were found for Scots pine
clones by Venne et al. (1989). These authors found that the relative male contribution for
charcoal-filtered air versus O3-treated conditions was very different and potentially could lead
to a strong gametophytic selection response caused by O3. However, Hanson and Addis
(1975) did not see any differences in the effect of O3 on the pollen from sensitive and tolerant
petunia (Petunia hybridd) genotypes, and Benoit et al. (1983) found no apparent differences
in the susceptibility of eastern white pine pollen from O3-sensitive or tolerant genotypes.
Clearly, the question of whether O3-induced gametophytic selection is occurring has not been
resolved.
Reduced flowering as the result of prolonged fumigation with O3 has been shown
in bladder campion (Silene cucabalus) (Ernst et al., 1985). Decreased floral initiation and
decreased floral productivity under long-term O3 exposures also have been reported in
geranium (Pelargonium spp.) and carnation (Dianthus caryophyllus) (Feder, 1970).
Ozone-induced impairment of flowering will reduce the fitness of the affected genotypes,
populations or species and may result in the eventual loss of these genetic units from the
O3-stressed ecosystem. Reduced eastern white pine fecundity in air-pollution-stressed
ecosystems has been reported by Houston and Dochinger (1977).
Genetic Summary
Plant species, cultivars, populations, and individuals within populations display
variable responses to O3. Variability in O3 responses among and within species was described
in the previous O3 criteria document (U.S. Environmental Protection Agency, 1986).
An important component of this variation is genetically controlled. The specific
5-45
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Table 5-5. Examples of Ozone Effects on Pollen Germination
and Tube Elongation
Species
Nicotiana tobacum L.
(Tobacco)
Petunia hybrida
(Petunia)
Pinus strobus L.
(Eastern white pine)
Zea mays L.
(Corn)
Pollen
Germination
Decrease
Not tested
No effect
Decrease
Pollen Tube
Elongation
Decrease
Decrease
Decrease
Not tested
Reference
Feder (1968)
Feder and Shrier (1990)
Feder and Shrier (1990)
Benoit et al. (1983)
Mumford et al. (1972)
genes controlling O3 response and involved in mechanisms of O3 tolerance are largely
unknown. However, control of stomatal conductance and internal biochemical defense
systems are among the most commonly described tolerance mechanisms. Ozone tolerance is
generally thought to be controlled by multiple genes.
There are implications of genetic variation in O3 response, both for managed and
natural ecosystems. These are summarized below along with the relative degree of
uncertainty attached to each.
It is known, with a great deal of certainty, that plants have a high degree of
genetic variation in O3 response. Thus, exposure-response equations and yield-loss equations
developed for a single or small number of cultivars, genotypes, families, or populations may
not represent adequately the response of the species as a whole.
The issue of O3 effects on biodiversity via natural selection is a topic of debate
within the scientific community. The potential for natural selection for O3 tolerance and
associated loss of sensitive genotypes is regional in nature, unlike well-known, point-source
pollution impacts that occur on local plant populations. However, the intensity of
O3 selection generally is thought to be quite low, 0.3 or less (Taylor and Pitelka, 1992), in the
majority of the United States. The extent that germplasm has been, or continues to be,
affected, in terms of allele loss or gene frequency changes by O3, and how this might be
impacting the genetic adaptability of populations, are open and important research questions.
Although it is well known that individual plants within a species vary in their
O3 tolerance, the physiological costs to tolerant plants are not known in terms of carbon
assimilation and allocation. Tolerance mechanisms based on reduced stomatal conductivity in
the presence of O3 would likely reduce growth of tolerant plants. Similarly, tolerance
mechanisms based on the productivity of antioxidant compounds likely will shunt plant
resources away from growth to the production of the defense compounds. The
characterization of the extent and types of physiological costs involved in O3 tolerance
remains an important research question.
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5.4.3 Environmental Biological Factors
The previous criteria document (U.S. Environmental Protection Agency, 1986)
discussed pollutant-plant-pest and pollutant-plant-pathogen interactions together, and provided
a tabular summary of pathogen effects. However, in light of the numerous studies of insect
and pathogen interactions that have appeared in recent years, the topics are dealt with
separately below. Nevertheless, it is worth reiterating several points made in the previous
criteria document.
• Pests and diseases are natural components of managed and natural ecosystems.
• Significant crop and timber losses result from pests and pathogens.
• The establishment of disease and pest infestations and their subsequent
development involve complex interactions among the host plant, the
environment, and the causal organism.
• The generalized disease (or pest infestation) cycle involves the arrival of the
pathogen or pest on the host plant surface or its introduction into the host plant
tissues through wounds or as a result of insect feeding activity.
• Growth and development or propagation of the pathogen or pest only occurs if
all environmental conditions are favorable.
• Such development leads to various degrees of host tissue destruction or
malfunction, and usually culminates in the causal organism entering a
reproductive stage and producing propagules (e.g., spores or eggs) that facilitate
its spread.
Ozone may modify any stage of the disease cycle directly, by affecting the causal
organism itself, or indirectly, by effects on the host plant (Lechowicz, 1987). Conversely, the
plant-pest interaction may modify the sensitivity of the host plant to O3.
The roots of many members of the pea family (including many important crops
such as soybeans, beans, and peas [Pisum sativum]) are infected by symbiotic nitrogen-fixing
bacteria (Rhizobium spp.), leading to the formation of bacteria-rich nodules that contribute to
the nitrogen economy of the plant through their ability to fix and convert atmospheric
nitrogen to biologically useful forms. Other nitrogen-fixing microorganisms are associated
with the roots of several species, and, in many cases, roots are invaded by species of soil
fungi to form mycorrhizal symbioses that assist in root functioning. These symbioses
constitute micro-ecosystems and are discussed more fully in Section 5.7 as they relate to
forest tree species.
Biological interactions also affect the growth of plants in populations (pure stands)
and communities (mixtures of species) through the individual plants' competition for available
resources (light, CO2, water, and nutrients). Such plant-plant interactions are features of all
managed and natural ecosystems, but they operate at the individual plant level. Hence, the
effects of oxidants on these interactions are discussed in this section, as well as in Section
5.7, which deals with ecosystem responses.
5.4.3.1 Oxidant-Plant-lnsect Interactions
The previous criteria document (U.S. Environmental Protection Agency, 1986)
concluded that little was known at that time about O3-insect interactions. Since then, the
topic has been covered in several reviews: Fluckiger et al. (1988), Hughes (1988), Manning
and Keane (1988), and Hain (1987). Relevant studies of the effects of O3 on the feeding
preference of herbivorous insects and on their growth, fecundity, and survival are presented in
5-47
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Table 5-6. As can be seen readily in this summary, the information is scattered widely
among a wide range of host plants and pests. Nevertheless, there appears to be a general
trend in the observations suggesting that O3-induced changes in the host plants frequently
result in increased feeding preference of a range of insect species, although this may or may
not be reflected in effects on the growth of the insect.
However, in most studies, the effects have been far from clear-cut. For example,
variable responses were observed with the aphid, Aphis fabae, on broad bean (Viciafabd)
(Brown et al., 1992); with the aphids, Acyrthosiphon pisum and Aphis rumicis, on pea and
dock (Rumex obtusifolius), respectively; with the beetle, Gastrophysa viridula, on dock
(Whittaker et al., 1989), with the Mexican bean beetle, Epilachna varivestis, on Corsoy
soybean (Endress and Post, 1985); and with the gypsy moth, Lymcmtria dispar, on white oak
(Quercus alba) (Jeffords and Endress, 1984). Although statistically significant effects were
observed frequently, they did not provide any consistent pattern of insect growth response to
different levels or patterns of exposure.
Brown et al. (1992) observed that the response of Aphis fabae depended on the
dynamics of exposure: growth was stimulated in short-term (<24 h) continuous exposures or
in episodic exposures over several days, whereas longer continuous exposures caused
decreased growth. Chappelka et al. (1988c) found that O3 consistently enhanced the feeding
preference and larval growth of the Mexican bean beetle on soybean, leading to increased
defoliation. Although the cultivar Forrest was significantly more sensitive to O3 than Essex,
this difference did not lead to any differences in insect behavior and development. Similarly,
clear stimulatory responses were observed with pinworm, Keiferia lycopersicella, on tomato
(Lycopercicon esculentum) (Trumble et al., 1987); with an aphid, Phyllaphis fagi, and a
weevil, Rhynchaenus fagi, on European beech (Fagus sylvatica) (Braun and Fluckiger, 1989;
Hiltbrunner and Fluckiger, 1992); with the monarch butterfly, Danaus plexippus, on milkweed
(Asclepias syriacd) (Bolsinger et al., 1991, 1992); and with infestation by the willow leaf
beetle, Plagiodera versicolora, on cottonwood (Populus deltoides) (Coleman and Jones,
1988). However, there was less egg-laying by Plagiodera on O3-treated foliage, and
treatment had no effect on beetle growth rates and survival (Jones and Coleman, 1989).
In view of previous experiments in which it was demonstrated clearly that aphid
growth was stimulated significantly by ambient pollutant mixtures containing O3, SO2, and
NO2 and, in light of other reports of O3-induced stimulations of insect growth, the inhibitory
effects of O3 on the growth of Aphis fabae on broad bean (Dohmen, 1988) or kidney bean
(Braun and Fluckiger, 1989) may be anomalous. The inhibitory effects on broad bean were
observed only at low O3 levels; exposure to higher concentrations resulted in a stimulation of
aphid growth, which Dohmen (1988) attributed to the increased rate of leaf senescence of the
host plant. The effects observed on kidney bean could not be accounted for by differences in
the amino acid composition of the plant sap, although differences in other constituents or
direct effects of O3 on the pea aphid itself could not be ruled out (Braun and Fluckiger,
1989).
A well-established indirect stimulatory effect is the predisposition to bark beetle
attack of ponderosa pine injured by exposure to O3. However, the infested trees do not favor
good brood production; O3 injury results in a more susceptible but less suitable host (Hain,
1987).
In all of these studies, the focus was on direct or indirect effects of O3 on the
insect. With the exception of the work of Braun and Fluckiger (1989), any effects on the
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Table 5-6. Ozone Effects on Insect Pests
Oi
-L
CD
Host Plant/Insect
CROP SPECIES
Broad bean/aphid
Pea/aphid
Kidney bean/aphid
Soybean/beetle
(cv. Corsoy)
(cvs. Essex, Forrest)
Tomato/pinworm
NATURAL
VEGETATION
Milkweed/monarch
butterfly
Dock/aphid
Dock/beetle
TREES SPECIES
European beech/aphid
European beech/weevil
Exposure3
3 day, 0.085 ppm
<24 h, 0.1 ppm
>24 h, 0.1 ppm 8 h/day,
episodic
4-8 day, var.
14 day, var.
16 day, var.
21 day, 7 h/day, var.
2-4 day, 3 h/day
0.28 ppm
17-19 day, 7 h/day
0.150-0. 178 ppm
15 day, var.
15 day, var.
2 mo, var.
72 h, var.
Experimental Conditions15
Chamber, whole plant
Chamber, whole plant
Chamber, whole plant
Chamber, whole plant
Chamber, whole plant
OTC
Chamber
OTC
Chamber, detached leaf
Chamber, whole plant
Chamber, whole plant
Chamber, whole plant
Chamber, whole plant
OTC
OTC
Effect of Ozone on Insect
3-13% decreased growth rate
17% increased growth rate
12% decreased growth rate
15% increased growth rate
Variable effects on growth
15-50% reduction in growth of
insect
Variable feeding preference
0.11>0.0>0.05>0.03 ppm;
feeding preference increased and
greater larval growth
80% increase in larval
development; no effect on
fecundity
No feeding preference but greater
larval growth rate
10% increased growth rate
10% larger egg batches; fourfold
greater larval survival
75% increase in number
Twofold increase in feeding
preference
Reference
Dohmen (1988),
Brown et al. (1992)
Whittaker et al. (1989)
Braun and Fluckiger (1989)
Endress and Post (1985),
Chappelka et al. (1988c)
Trumble et al. (1987)
Bolsinger et al. (1991, 1992)
Whittaker et al. (1989)
Whittaker et al. (1989)
Braun and Fluckiger (1989)
Hiltbrunner and Fluckiger (1992)
-------
Oi
dn
o
Table 5-6 (cont'd). Ozone Effects on Insect Pests
Host Plant/Insect
Exposure*
Experimental Conditions15
Effect of Ozone on Insect
Reference
TREE SPECIES
(cont'd)
Cottonwood^eetle
5 h, 0.2 ppm
Ponderosa pine/bark Natural
beetle
White oak/gypsy moth 11 day, 7 h/day, var.
OTC
None, field
Chamber, leaf disks
22-60% greater consumption of
foliage but decreased fecundity
Increased infestation but
decreased survival
Variable feeding preference
0.15 > 0.03 >0.09 ppm
Jones and Coleman (1988),
Coleman and Jones (1988)
Hain (1987)
Jeffords and Endress (1984)
Var. indicates a range of exposures.
bChamber indicates closed chamber; OTC indicates open-top field chamber.
-------
host plant that were reported were confined to observations on visible symptoms of foliar
injury. The only report of an O3-insect interaction affecting the response of the host plant
appears to be that of Rosen and Runeckles (1976). This study showed that exposure to
subacute levels of O3 and infestation with the greenhouse whitefly, Trialeurodes
vaporariomm, acted synergistically (i.e., more than additively) in causing leaf injury and
accelerated senescence of kidney bean. However, the extent to which other insects with
sucking mouthparts, such as aphids, might be involved in similar interactive responses is
unknown, as is the nature of any interactions that involve pests that ultimately invade and
develop within the host plant, such as those that cause the formation of galls.
The reports of O3-insect-plant interactions are thus scattered among a wide range
of host plant and insect species, and represent only a minute fraction of the plant-insect
interactions that involve crop and native species. Although there appears to be a trend in the
limited data available that suggests that exposures to moderate O3 levels may increase the
likelihood of insect attack and its consequences, there is insufficient information to decide
whether extrapolation of this generalization is warranted or not. Even if the generalization is
valid, it is not possible to generate any quantitative measure of response. Before such
estimates will be possible on a broad scale, studies of a much wider range of plant insect-
systems will be needed, together with systematic, in-depth studies of individual systems,
aimed at determining the long-term effects on both the host plant and the insect. Such studies
should include investigations of biological control systems employing beneficial insects,
which are used increasingly as alternatives to chemical insecticides and herbicides.
5.4.3.2 Oxidant-Plant-Pathogen Interactions
Plant disease is the result of infection by fungi, bacteria, mycoplasmas, viruses,
and nematodes. Recent reviews of pathogen-plant-O3 interactions have been published by
Dowding (1988) and Manning and Keane (1988) and extend the coverage of the previous
criteria document (U.S. Environmental Protection Agency, 1986), in which the results of
published studies of the effects of O3 on disease development were summarized in tabular
form. Interactions involving fungal pathogens occupied most of that review, and more recent
studies have maintained this emphasis.
The previous criteria document concluded that it was "impossible to generalize and
predict effects in particular situations" (U.S. Environmental Protection Agency, 1986).
However, Dowding (1988) since has concluded that pathogens that can benefit from injured
host cells or from disordered transport mechanisms are enhanced by pollution insult to their
hosts, whereas those that require a healthy mature host for successful invasion and
development are depressed by pollutant stress to their host.
This conclusion is supported by evidence that the development of diseases caused
by obligate parasites such as the rust fungi and bacterial pathogens usually is reduced by
O3. As shown by the observations summarized in Table 5-7, reductions in disease
development were observed in five of the nine studies of obligate fungal parasites listed,
whereas increases were observed in all but four of the studies of facultative fungal pathogens.
Similarly, in four of the five bacterial systems, O3 reduced infection or disease development.
It should be noted that, in three of the four studies of obligate fungi on which exposure to
O3 either had no effect or that resulted in stimulated fungal growth, the pathogen was a
powdery mildew (Erysiphe, Microsphaera). As discussed by Tiedemann et al. (1991), these
species constitute a special case because they are ectoparasites whose hyphae merely penetrate
the surface epidermal cells of the host plant's leaves rather than the mesophyll
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Table 5-7. Ozone-Plant-Pathogen Interactions3
Host Plant
OBLIGATE FUNGI
Kidney bean
Barley
Cottonwood
Lilac
Oats
Wheat
Oi
fe
FACULTATIVE FUNGI
Barley
Cabbage
Corn
Pathogen
Uromyces phaseoli
Erysiphe graminis
Melampsora medusae
Microsphaera alni
Puccinia coronata
Erysiphe graminis
Puccinia graminis
Puccinia graminis
Puccinia recondita
Drechslera teres
Gerlachia nivalis
Helminthosporium
sativum
Fusarium oxysporum
Helminthosporium
maydis
Effect of O3 on Disease
Increased number of
smaller pustules
Reduced infection but
greater spore production
Reduced infection and
development
No effect
Reduced infection and
development
Increased infection and
development
Reduced infection and
development
Reduced development
Reduced infection and
development
Increased infection
Increased infection
No effect
Decreased development
Increased development
Effect of Disease on O3 Response
Reduced injury on severely
diseased leaves
Not reported
Not reported
Not reported
No effect
Not reported
Reduced leaf injury
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Reference
Resh and Runeckles (1973)
Heagle and Strickland (1972)
Coleman et al. (1987)
Hibben and Taylor (1975)
Heagle (1970)
Tiedemann et al. (1991)
Heagle and Key (1973a,b)
Heagle (1975)
Dohmen (1987)
Tiedemann et al. (1990)
Tiedemann et al. (1990)
Tiedemann et al. (1990)
Manning et al. (197 la)
Heagle (1977)
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Table 5-7 (cont'd). Ozone-Plant-Pathogen Interactions3
Host Plant
Pathogen
Effect of O3 on Disease Effect of Disease on O3 Response
Reference
Oi
61
CO
FACULTATIVE FUNGI (cont'd)
Cottonwood Marssonina brunnea
Geranium Botrytis cinerea
Onion Botrytis (3 spp.)
Potato
Soybean
Wheat
Jeffrey pine
Ponderosa pine
White pine
Botrytis cinerea
Alternaria solani
Alternaria solani
Fusarium oxysporum
Gerlachia nivalis
Helminthosporium
sativum
Helminthosporium
sativum
Septoria (2 spp.)
Septoria (2 spp.)
Heterobasidium annosum
Heterobasidium annosum
Vertcicladiella procera
Lophodermium pinastre
Increased infection
Decreased infection
Increased infection and
development
Increased infection and
development
Increased infection
Increased infection
Increased infection
Increased infection
No effect
Increased infection
Increased infection
Increased infection
Increased development
Increased development
Slightly increased incidence
Slightly increased incidence
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Increased leaf injury
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Not reported
Coleman et al. (1988)
Krause and Weidensaul (1978)
Wukasch and Hofstra (1977a,b)
Manning et al. (1969)
Holley et al. (1985)
Bisessar (1982)
Damicone et al. (1987a)
Tiedemann et al. (1990)
Tiedemann et al. (1990)
Tiedemann et al. (1991)
Tiedemann et al. (1990)
Tiedemann et al. (1991)
James et al. (1980a)
James et al. (1980b)
Costonis and Sinclair (1972)
Costonis and Sinclair (1972)
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Oi
o,
Tobacco
Table 5-7 (cont'd). Ozone-Plant-Pathogen Interactions3
Host Plant
BACTERIA
Alfalfa
Soybean
White bean
Wild strawberry
NEMATODES
Begonia
Soybean
Pathogen
Xanthomonas alfalfae
Pseudomonas glycinea
Pseudomonas spp.
Xanthomonas phaseoli
Xanthomonas fragariae
Aphelenchoides
fragariae
Belonolaimus
longicaudatus
Heterodera glycines
Paratrichodorus minor
Effect of O3 on Disease
Reduced development
Reduced incidence
Reduced infection
No effect
Reduced incidence
Reduced nematode
reproduction
Stimulation or no effect
Reduced nematode
reproduction
Reduced nematode
Effect of Disease on O3 Response
Reduced leaf injury
No effect
Reduced leaf injury
Reduced leaf injury
No effect
Reduced leaf injury
Not reported
Not reported
Reduced leaf injury
Reference
Howell and Graham (1977)
Laurence and Wood (1978a)
Pell et al. (1977)
Temple and Bisessar (1979)
Laurence and Wood (1978b)
Weber et al. (1979)
Weber et al. (1979)
Weber et al. (1979)
Weber et al. (1979)
Pratylenchus penetrans
Meloidogyne hapla
reproduction
No effect
Possible stimulation15
Not reported
Increased leaf injury
Weber et al. (1979)
Bisessar and Palmer (1984)
"See Appendix A for abbreviations and acronyms.
bBased on studies using the protectant EDU (see Section 5.2.1.2).
-------
tissues within the leaves. They noted that Heagle and Strickland (1972) observed greater
pustule development of Erysiphe on exposed barley once infection was established, although
the pathogen was sensitive during the early stages of infection. Tiedemann et al. (1991)
suggest that the observed stimulations result from a differential weakening of the host's
resistance response to the pathogen.
In a few of the studies summarized in Table 5-7, effects of disease development on
the sensitivity of the host plant to O3 were noted. Heagle and Key (1973b) and Resh and
Runeckles (1973) confirmed the earlier observation of Yarwood and Middleton (1954) that
infection with obligate rust fungi could reduce the severity of acute injury caused by exposure
to O3. However, with Uromyces on bean, the "protection" was noted only on severely
infected leaves (Resh and Runeckles, 1973), and Heagle (1970) observed no such effect with
crown rust, Puccinia coronata, on oats.
Infection with bacterial pathogens and nematodes also tends to reduce the impact
of O3, and almost all studies of the interactions of O3 with virus infections appear to do so.
The previous criteria document (U.S. Environmental Protection Agency, 1986) reviewed the
supporting evidence from numerous studies with a range of host plants and viruses, and noted
only two studies in which O3 injury was apparently increased by virus infection (Ormrod and
Kemp, 1979; Reinert and Gooding, 1978). However, with tomato infected by mosaic viruses,
injury was reduced in the leaves of plants in which viral infection was well established
(Ormrod and Kemp, 1979). Two more recent studies have indicated either no effect or
variety-dependent increased sensitivity to relatively high O3 levels. Heagle et al. (199la,
1992) found no effects of infection with several viruses on the response of two clonal strains
of white clover. On the other hand, Reinert et al. (1988) reported that three cultivars of
burley tobacco responded differently to O3 when infected with either tobacco etch virus or
tobacco vein mottling virus (TVMV). Although tobacco etch virus infection resulted in the
protection of cultivars from O3-induced growth suppression, TVMV infection enhanced the
suppression of the growth of two cultivars, Burley 21 and Greenville 131, but had no effect
on the third, Burley 49.
With the exception of one field study demonstrating the suppression of O3 injury
on tobacco infected with tobacco mosaic virus (Bisessar and Temple, 1977), the other
investigations of virus interactions all have been conducted in laboratory or greenhouse
chambers, which raises the question of the relevance of these investigations to field
conditions. As noted in the previous criteria document (U.S. Environmental Protection
Agency, 1986), with few exceptions, the reports of viral protection are probably of little
commercial significance but may provide information at the mechanistic level of plant
response. The same caveat is equally applicable to the significance of protective effects of
other obligate pathogens.
No studies appear to have been conducted of interactions involving disease-causing
mycoplasmas.
As in the case of plant-insect interactions, much more systematic study is needed
before it will be possible to provide any quantitative estimates of the magnitude of the
interactive effects. The patterns of pollutant modification of plant-pathogen relations
suggested by Dowding (1988) are supported partly by the limited evidence available for
O3, but studies of a wider range of plant-pathogen systems will be needed before it will be
possible to provide quantitative generalizations.
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5.4.3.3 Oxidant-Plant-Symbiont Interactions
Exposure to O3 can modify the symbiotic relationships between plants and
microorganisms. In the case of Rhizobium, the important nitrogen-fixing symbiont of many
leguminous species, the adverse effects of exposure of the host plant reviewed in the previous
criteria document (U.S. Environmental Protection Agency, 1986) all were observed at
O3 levels of 0.3 ppm or greater. However, Flagler et al. (1987) observed a consistent decline
in total nitrogen-fixing activity of nodulated soybean roots with increasing O3 concentrations
up to 0.107 ppm (7-h/day seasonal average), with no effect on specific nodule activity. In a
greenhouse study of soybean plants exposed at three different growth stages to a 12-h
treatment in which the peak O3 concentration (at 6 h) was 0.2 ppm, Smith et al. (1990)
observed a 40% decrease in specific nodule activity. Hence, there is limited evidence to
indicate adverse effects on Rhizobial nitrogen-fixation at O3 levels experienced in polluted air.
The effects of O3 on mycorrhizal fungal symbioses have been reviewed by
Manning and Keane (1988) and McCool (1988). Seasonal exposures averaging 0.079 ppm
O3 resulted in a 40% reduction in the growth of the vesicular-arbuscular endomycorrhizal
fungus, Glomus fasciculatus., on soybean roots; however, mycorrhizal infection lowered the
O3-induced reduction in pod yield from 48 to 25% (Brewer and Heagle, 1983). Once-weekly
exposures of tomato plants to 0.3 ppm for 3 h retarded the early development of the same
fungus on tomato seedling roots, leading to reduced seedling growth (McCool et al., 1982).
Greitner and Winner (1989) reported that the increased availability of nitrogen to alder (Alnus
serrulata) seedlings resulting from the presence of root nodules containing the nitrogen-fixing
actinomycete, Frankia, enabled plants to recover their photosynthetic integrity rapidly after
exposure to O3; however, they did not investigate effects on symbiont.
In spite of the inconsistencies in the available evidence, it appears that rhizobial
and mycorrhizal growth is likely to be impaired as a consequence of long-term exposure to
oxidant stress, probably because of reduced allocation of photosynthate to the root system
(Chapter 7, U.S. Environmental Protection Agency, 1986). However, the implications of such
effects on mycorrhizae are particularly difficult to predict because of an inadequate
understanding of the functioning of the tree root-mycorrhiza-soil system.
5.4.3.4 Oxidant-Plant-Plant Interactions—Competition
In the field, the growth of any plant is to some extent dependent on its ability to
compete for resources with its neighbors. Some are better competitors than others for light,
water, nutrients, and space. Grime (1979) characterized as "competitors" those with a rapid
growth rate associated with a capacity to adjust to rapidly changing conditions. Factors such
as light or soil nutrients are not available ad libitum, because of the mutual shading of leaves
within the canopy and root competition. Competition may be either intra- or interspecific,
(i.e., the interference may be caused by neighboring members of the same or other species).
The planting densities and row spacings adopted for agricultural crops represent compromises
between maximizing the number of plants per unit area and the adverse effects of
intraspecific competition. Weeds are typical interspecific competitors; interspecific
competition also occurs in mixed plantings, such as grass-clover forage and pasture plantings
and is an important feature of natural ecosystems.
Although competition from weeds may contribute more to crop losses on a global
scale than any other factor, no studies appear to have been conducted on the effects of
oxidant pollution on such competition. On the other hand, a few crop mixtures have been
studied. A consistent finding with grass-clover mixtures has been a significant shift in the
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mixture biomass in favor of the grass species (Bennett and Runeckles, 1977; Blum et al.,
1983; Kohut et al., 1988a; Rebbeck et al., 1988; Heagle et al., 1989b).
As the number of competing species increases, the interactions more appropriately
are dealt with at the ecological level, but, as demonstrated by the work of Evans and
Ashmore (1992), it is important to recognize that, because of the differential stresses imposed
by competition, the impact of O3 on the components of a mixture may not be predictable on
the basis of knowledge of the responses of the individual species grown in isolation.
A similar caution must be stated about extrapolating to field conditions the results obtained in
laboratory studies in which competition may be minimal. However, the development and use
of field exposure systems have permitted many recent studies of crop species to be conducted
at normal planting densities and, hence, have incorporated interspecific competition as an
environmental factor. On the other hand, most forest tree studies have tended to be
"artificial" in their use of individual seedlings or saplings or spaced trees, even when exposed
in open-air systems (McLeod et al., 1992).
The significance of the effects of competitive interactions on the O3 response of
the competing species is thus largely unknown except for a few cases involving grass-legume
mixtures. However, these are far from typical because they only involve two species, one of
which is a legume with unique nitrogen nutrition conferred by the nitrogen-fixing capabilities
of Rhizobial symbionts. Hence, the lack of knowledge of the effects of O3 on competitive
interactions leads to considerable uncertainty in attempting to assess the impact of O3 on both
managed and natural ecosystems by extrapolation from effects on individual species.
5.4.4 Physical Factors
The physical components of the plant's aerial environment are light, temperature,
humidity, air turbulence, and surface wetness, whereas the physical, edaphic components
affecting the plant roots are temperature, soil moisture, and soil salinity. The previous criteria
document (U.S. Environmental Protection Agency, 1986) also included soil fertility under this
heading; in the present review, this topic is dealt with separately in Section 5.4.5, which deals
with chemical factors. The effects of the physical climatic factors (light, temperature,
atmospheric turbulence, and the availability of water) on plant growth and survival are major
determinants of the geographic distribution of the earth's natural vegetation and of the
distribution of agricultural lands and the suitability of the crops grown on them. Because of
the control that these factors exert over plant growth, their variation, especially in the short
term, can be expected to influence the magnitude of plant responses to oxidants. As in the
previous criteria document, the factors are discussed individually, although their actions on
plant growth and sensitivity are interrelated closely. Ozone uptake and the effect of air
turbulence on boundary layer processes is discussed in Section 5.3.2. A brief integration of
their effects is presented in Section 5.4.8, which discusses the effects of global climate
change.
At the time of the previous criteria document, much of the knowledge of the
effects of these factors came from laboratory and greenhouse experimentation that focused the
foliar injury response of high exposures to O3, which exceeded those likely to be encountered
in ambient air. Since then, more information has become available on growth effects,
especially with regard to the key area of the interactions involving drought stress.
5.4.4.1 Light
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Light influences plant growth through its intensity, quality (i.e., the distribution of
wavelengths), and duration (i.e., daylength or photoperiod). Much of the early work on
light-oxidant interactions is largely of academic interest because light intensity and daylength
are uncontrolled in natural field situations. However, reduced intensities are needed for the
production of shade-grown cigar wrapper tobacco and in many commercial greenhouse
floriculture operations, in which photoperiod also may be controlled in order to induce
flowering. The general conclusion reported previously (U.S. Environmental Protection
Agency, 1986) is that susceptibility to foliar injury is increased by low intensities and short
photoperiods, although unpredictable responses had been observed when plants were subjected
to increased or decreased intensities during and after exposure to O3. One aspect of increased
susceptibility to low light intensities that needs to be emphasized concerns the fact that many
studies of oxidant effects have been conducted in controlled-environment chambers in which
the light intensities used have rarely approached those of natural sunlight and, hence, may
have magnified the observed responses. Significant differences in the amounts of foliar injury
were observed on soybean plants grown in a growth chamber, a shaded greenhouse, or in an
OTC in the field, when subsequently treated with a standard O3 exposure, although the
growing conditions other than light intensity and quality were comparable (Lewis and
Brennan, 1977). Factors other than light intensity must have contributed to the observed
differences because the descending order of sensitivity was greenhouse-growth chamber-field
chamber, although the average light intensities in the greenhouse and growth chamber were
81 and 18%, respectively, of those in the field chamber.
Reduced light intensities have been measured in OTCs in the field, resulting from
the build-up of dust on the walls. However, Heagle and Letchworth (1982) could detect no
significant effects on soybean growth and yield in a comparison of plants grown in unshaded
OTCs and chambers to which shading cloth was applied.
At the mechanistic level, Darrall (1989) has reviewed the effects of light intensity
and suggests that, at high intensities, the potential for endogenous oxyradical production is
greatest, and that this, combined with the production of oxyradicals from O3, might exceed
the leafs detoxification ability. However, at lower intensities, decreased carbon assimilation
would limit the availability of energy for use in cellular repair.
In most species, light indirectly plays a major role in the opening and closing of
stomata. Because stomata, therefore, tend to close at night and open during the day, light
duration, to some extent, dictates whether or not O3 can be taken up by foliage from the
ambient air.
5.4.4.2 Temperature
Temperature affects almost all physical processes and chemical reactions within the
plant. Hence, it is the temperature within the plant tissues that is important. Although air
temperature dictates the overall heat balance in the surrounding air, the temperature of the
leaf also is determined by the absorption of infrared radiation during the photoperiod (which
increases the leaf temperature) and the loss of water vapor through transpiration (which
provides evaporative cooling). Hence, the effects of air temperature per se must be viewed in
the context of these other physical factors. It therefore is not surprising that the few early
studies of the effects of air temperature alone, using controlled environment chambers, led to
variable and conflicting results, as noted in the previous criteria document (U.S.
Environmental Protection Agency, 1986). In most of these studies, the RH and light intensity
were held constant. In water-saturated air with a RH of 100%, the absolute humidity (or
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water vapor pressure) increases with temperature. Such increases occur at all RHs.
Therefore, at constant RH, the increase in absolute humidity, or vapor pressure with
temperature, in turn, increases the vapor-pressure deficit (VPD) (i.e., the difference between
the absolute humidity, or vapor pressure) and that of completely saturated air at the same
temperature. Because VPD controls the rate of evaporation of water, at constant RH, the
effects of temperature are unavoidably confounded with effects on VPD. In a recent study
with tomato seedlings, in which differences in VPD at different temperatures were minimized,
Todd et al. (1991) showed that, out of 11 growth variables measured, the only significant
modifications of the effects of O3 caused by temperature were on stem fresh weight and
specific leaf area (leaf area/leaf dry weight). The authors suggest that VPD probably plays a
more important role in determining sensitivity to O3 than temperature.
Although transpiration rate is dependent on VPD, it also is regulated by the
opening and closing of stomata on the leaf surface, vertical wind velocities, and factors, such
as O3, that cause stomatal closure indirectly will cause leaf temperature to rise. Such stomatal
and temperature changes have been observed during exposure to O3 (Matsushima et al., 1985;
Temple and Benoit, 1988).
An important O3-temperature interaction affecting trees and other woody perennials
is winter hardiness. Several studies have shown that exposures to O3 at realistic levels may
reduce the cold- or frost-hardiness of plants, as reviewed by Davison et al. (1988). Using the
pea plant as a laboratory model, Barnes et al. (1988b) showed that daily 7-h exposures to
0.075 or 0.09 ppm O3 for 7 days significantly reduced plant survival after exposure to
night-time temperatures that fell from 2 to -4 °C over a 2-h period and then were held at
-4 °C for a further 4 h.
Various responses of coniferous trees to the exposure to O3 during the growing
season and freezing temperatures during the following winter have been reported. With
Norway spruce, Eamus and Murray (1991) found that the recovery of photosynthetic rates
after freezing was slower in O3-treated seedlings. Brown et al. (1987) and Barnes and
Davison (1988) observed severe necrosis of the older needle classes of seedlings of some
Norway spruce clonal saplings exposed to O3 and then to freezing temperatures, although
other clones showed no effect. Increased winter injury on plants exposed to O3 also was
observed with Sitka spruce (Picea sitchemis) (Lucas et al., 1988) and red spruce (Fincher
et al., 1989). With loblolly pine, Edwards et al. (1990a) observed variable results, but
Chappelka et al. (1990) reported that a late winter frost resulted in severe tip die-back of the
youngest needles of seedling trees exposed to 1.7 (350 ppm-h) and 2.5 (433 ppm-h) times
the ambient (272 ppm -h) O3 concentration during the previous growing season (in contrast to
the effects observed on Norway spruce). The response also varied with plant genotype.
A reason for the difference may be that, in the study with Norway spruce, the freezing period
occurred soon after exposure to elevated O3 levels, whereas in the loblolly pine study, the
frost occurred in late winter. The diversity of results led Eamus and Murray (1991) to
develop a conceptual framework that recognizes that, even in severe winters, there are brief
periods of mild temperatures that induce partial dehardening. Ozone decreases frost
hardiness, per se, and it also increases the trees' predisposition to dehardening during winter;
such dehardening puts O3-exposed trees at greater risk from subsequent low temperatures.
In a greenhouse study with 1-year-old red spruce seedlings, Neighbour et al.
(1990) reported that decreasing the level of NO at the time of exposure to O3 prevented the
appearance of O3-induced frost injury. They suggest that the effects attributed to O3 are
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probably due to the combination of O3 with traces of NO above a critical level. However,
this effect apparently has not been investigated further.
In a study of the subtropical trees, Volkamer lemon (Citrus volkamericana) and
avocado (Persea americana), in Florida, Eissenstat et al. (1991a) found that, although
O3 could reduce frost hardiness, the effects were subtle, and the authors concluded that the
likelihood that frost resistance is adversely affected by current O3 levels is slight.
The general consequences of global warming on O3 responses are discussed in
Section 5.4.8.
5.4.4.3 Humidity and Surface Wetness
A review of early investigations led to the conclusion that, in general, high RH
tends to sensitize plants to O3 (U.S. Environmental Protection Agency, 1986). Such a
conclusion is supported on mechanistic grounds. A study by McLaughlin and Taylor (1981)
indicated that measured O3 uptake by bush bean plants (Phaseolus vulgaris) increased with
RH, and there are several reports that, at high RH, the rapid decrease in stomatal conductance
caused by O3 at lower RHs is inhibited (Otto and Daines, 1969; Rich and Turner, 1972;
Elkiey and Ormrod, 1979a; Elkiey et al., 1979). However, stomatal responses to O3 show
considerable variability among species and even among cultivars of the same species (Elkiey
and Ormrod, 1979a; Elkiey et al., 1979), and, hence, it is to be expected that the patterns of
the O3-RH interaction may not always be as clear. Thus, with yellow poplar (Liriodendron
tulipifera), five consecutive daily exposures to 0.15 ppm for 7 h at either 40 or 80% RH
revealed considerable variation in stomatal conductance (Jensen and Roberts, 1986). At 40%
RH, there was a tendency for O3 to cause a decrease in conductance during the later
exposures. Nevertheless, at 80% RH, the conductances generally were greater and tended to
increase during the later exposures.
Surface wetness also influences the foliar uptake of O3, although there appear to
have been no studies undertaken to investigate the consequences of such uptake. Until
recently, it has been suggested that O3 uptake is reduced when foliage is wet because the
stomata may be covered with water (Hicks et al., 1987). However, Fuentes and Gillespie
(1992) reported that both wetness from dew or raindrops on the upper surface of red maple
leaves can increase O3 uptake significantly. Although this may be due partly to a stomatal
response to resulting increases in RH, the fact that increased uptake occurred in darkness,
when the stomata largely were closed led the investigators to suggest that direct uptake into
the surface water is the more important mechanism. However, no information is available as
to the consequences of such deposition.
5.4.4.4 Drought and Salinity
Short- and long-term variations in the availability of soil water have a profound
influence on plant growth. In some agricultural situations, the use of irrigation may eliminate
drought stress. However, the growth of crops and natural vegetation in many areas will be
affected adversely by the varying degrees of water shortage that occur, both during a growing
season and from year to year. The previous criteria document (U.S. Environmental Protection
Agency, 1986) summarized earlier studies and concluded that drought stress reduced the
magnitude of adverse effects of O3, including injury and growth and yield reductions. The
effect was attributed to an increased rate of stomatal closure in drought-stressed plants in
response to O3 that effectively reduced uptake of the pollutant. These conclusions were based
almost exclusively on studies with crop species. Since then, a number of studies with tree
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seedlings and further studies with crops species have shown that the interaction between
drought and O3 is more complex and variable than originally thought.
Heagle et al. (1988a) summarized the results of investigations into the
drought-O3 interaction in six soybean studies, three cotton studies, one study each of alfalfa
and a clover-fescue mixture. These studies were undertaken as part of NCLAN (Heck et al.,
1984). The results of these investigations are included in Table 5-8. Significant interactions
between O3 and drought stress (soil moisture deficit, [SMD]) were reported only in three
soybean studies, two cotton studies, and the alfalfa study. The interaction was usually
revealed by the fact that the clear negative relationships between yield and O3 exposure
observed with watered plants were either much reduced or could not be demonstrated with
drought-stressed plants, bearing in mind that, in most of these situations, the yields already
were depressed by the SMD. As a result, the lack of any significant response to O3 in some
cases with such stressed plants reflects the decreased range of yield responses within which
an O3 effect could operate. However, as shown in Table 5-8, Heggestad et al. (1988) found
with Forrest soybean that SMD significantly enhanced the effects of low O3 exposures.
Heagle et al. (1988a), therefore, concluded that the suppression of the response to O3 caused
by drought appeared to be dependent on the severity of the SMD-induced stress.
Brennan et al. (1987) suggested that the normal experimental protocols used in
most NCLAN studies, which called for the use of irrigation to avoid possible complications
due to drought, might have biased the yield loss data for soybean because it increased plant
sensitivity to O3. However, Heggestad and Lesser (1990) found no evidence to support this
suggestion, in view of the comparable estimates of yield losses predicted by the O3-response
curves.
Bytnerowicz et al. (1988) found no interaction between SMD and O3 in 18 desert
annual species. However, moderate SMD rendered the tropical fiber plant, kenaf (Hibiscus
cannabinus\ less sensitive to O3, although sensitivity was enhanced by severe water stress
(Kasana, 1992). A field survey of milkweed plants in two areas in the mid-Ohio River
Valley revealed much less foliar injury attributable to O3 in 1988, a dry year in which the
maximum concentration recorded nearby reached 0.2 ppm, than in 1989, a year with ample
precipitation and a nearby maximum of 0.12 ppm (Showman, 1991).
Although there have been several recent studies of the effects of O3 exposure and
drought stress on tree species, they have little in common with respect to the treatments
applied or the measurements made. However, clear demonstrations of significant interactions
have been obtained with beech, poplar, and loblolly pine seedlings. Davidson et al. (1992)
found that, although O3 reduced root growth in well-watered plants, SMD reversed this
inhibition and led to slight O3-induced stimulations. Drought reduced foliar injury caused by
O3 to poplar (Harkov and Brennan, 1980), ponderosa pine (Temple et al., 1992), and loblolly
pine (Meier et al., 1990). In poplar, the effect was attributed to the reduced stomatal
conductance observed, which reduced O3 uptake. Similar effects on stomatal conductance
were observed in Norway spruce and sitka spruce (Dobson et al., 1990). In ponderosa pine,
SMD also countered the inhibitory effects of O3 on needle growth and retention (Temple
et al., 1993). Tseng et al. (1988), however, observed no effects of O3 on Fraser fir (Abies
balsamea) grown under three levels of SMD. No consistent patterns were found with various
physiological measurements made on red spruce seedlings subjected to both O3 and drought
(Roberts and Cannon, 1992). Lee et al. (1990b) observed reduced root conductivity in the
second drought cycle following exposure to O3. Thus, there is some
5-61
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Table 5-8. Field Studies of Ozone-Drought Stress Interactions in Crop Species3
(Adapted in part from Heagle et al., 1988a)
Oi
Estimated Yield Loss (%) per Seasonal Mean
O3 Concentration (ppm)b
Crop/Cultivar
Soybean
Williams
Williams and
Corsoy 79
Williams
Forrest
Davis
Davis
Corsoy 79
Young
Cotton
Acala SJ-2
Acala SJ-2
McNair 235
Acala SJ-2
Year
1982
1983
1982
1983
1984
1986
1986
1981
1982
1985
1986
Response
Yield
Yield
Yield
Root length
Root length
Yield
Yield
Yield
DS
Yield
DS
Yield
Yield
Yield
Yield
Yield
Yield
Yield
Yield
Shoot dry mass
Shoot dry mass
Shoot dry mass
Significant
Interaction0
No
WW
DS
WW
DS
WW
DS
WW
No
WW
DS
No
WW
DS
No
No
wwe
DSe
DS (severe)6
0.04
7
7
6
3
13
4
4
2
0
6
3
1
6
7
0.05
13
13
11
No si|
[33
9
21
7
No si|
7
4
0
11
7
2
15
13
[22
[20
[+14
0.06
19
18
15
mificant O3
36
21
28
12
mificant O3
12
8
0
17
13
o
J
26
21
26
37
+22
0.07
24
24
19
effect
52]d
39
35
16
effect
18
13
0
25
21
7
40
30
42]f
44]f
27]f
0.08
30
30
23
60
41
21
24
21
1
34
30
12
55
40
Reference
Heggestad et al. (1985)
Heggestad and Lesser (1990)
Heggestad and Lesser (1990)
Heggestad et al. (1988)
Heggestad et al. (1985)
Heggestad and Lesser (1990)
Heagle et al. (1987a)
Heagle et al. (1987a)
Irving et al. (1988)
Miller et al. (1989b)
Temple et al. (1985)
Temple et al. (1985)
Heagle et al. (1988b)
Temple et al. (1988b)
-------
Table 5-8 (cont'd). Field Studies of Ozone-Drought Stress Interactions in Crop Species3
(Adapted in part from Heagle et al., 1988a)
Estimated Yield Loss (%) per Seasonal Mean
O3 Concentration (ppm)b
Crop/Cultivar
Alfalfa
WL-514
WL-514
Year
1984
1985
Response
Yield
Yield
Significant
Interaction0
No
Nog
0.04
6
4
0.05 0.06
9 13
7 10
0.07
17
14
0.08
20
18
Reference
Temple et al. (1988a)
Tall Fescue-Ladino Clover
Kentucky 31
and Regal
1984
1984
Yield
Yield
No
No
5
6
8 12
11 17
17
24
22
32
Heagle et al. (1989b)
"See Appendix A for abbreviations and acronyms.
bWhere a significant interaction was observed, separate responses are listed for well-watered (WW) and drought-stressed (DS) plants; otherwise, the pooled
01 response is listed.
O) "Based on Weibull model estimates (Heagle et al., 1988a)
dData presented are percent reductions in root length per soil core at seasonal mean O3 exposures of 0.074, 0.107, and 0.132 ppm relative to 0.052 ppm. Increased
root lengths in DS treatments ranged from 136 to 11% with increasing O3 exposure.
Interaction not significant by analysis of variance, but significant suppression of O3 response in DS (severe).
fWeibull model data not available. Data presented are actual percent yield losses at seasonal mean O3 exposures of 0.074, 0.094, and 0.111 ppm relative to
0.015 ppm.
Polynomial regression analysis showed slightly greater response in WW than DS plots.
-------
evidence from tree species to support the view that drought stress may reduce the impact of
O3. However, the work with trees provides no additional information to help in resolving the
quantitative nature of the drought-O3 interaction.
Although drought stress may be the result of insufficient rainfall, conditions of
effective SMD also may be induced by excessive soil salinity. Laboratory studies reviewed in
the previous criteria document (U.S. Environmental Protection Agency, 1986) showed that
increased salinity could reduce the impact of O3 on injury and yield of various crops.
However, in a more recent field study with alfalfa, Olszyk et al. (1988) found no overall
interaction between O3 and salinity on growth or yield. Although salinity decreased the
number of empty nodes caused by exposure to above-ambient levels of O3, the effect was
statistically significant only for the second of four harvests. In general, salinity was found to
be more harmful to alfalfa growth than exposure to O3, but, as pointed out by Olszyk et al.
(1988), the amount of information available is insufficient to permit the development of
models for estimating losses due to O3-salinity combinations.
The bulk of the available evidence supports the view that drought stress may
reduce the impact of O3 on plants. However, it must be emphasized that, in terms of growth
and productivity, any "protective" benefit will be offset by the effects of SMD per se, as
noted in the previous criteria document (U.S. Environmental Protection Agency, 1986).
The O3-water interaction is not confined to the effects of SMD on direct plant
response to O3. Numerous studies have shown that O3 may affect various aspects of plant
water status, including water-use efficiency (WUE), the ratio of the rates of photosynthetic
carbon gain and transpirational water loss. For example, Reich et al. (1985) observed that
daily exposures to 0.13 ppm O3 for 6.8 h resulted in a 25% reduction in WUE in well-
watered Hodgson soybean, when compared to exposure to 0.01 ppm. Similar findings have
been reported for alfalfa (Temple and Benoit, 1988) and radish (Barnes and Pfirrmann, 1992).
However, WUE is a complex resultant of both stomatal conductance and the activity of the
photosynthetic system, both of which may be independently affected by O3. Genetic or
environmentally induced difference in the relative sensitivities of the stomatal and
photosynthetic components will dictate the nature and magnitude of any effect of O3 on
WUE. Thus, with radish and soybean, Greitner and Winner (1988) observed effects on
stomatal conductance and photosynthetic CO2 assimilation that translated into O3-induced
increases in WUE; however, they point out, that this advantageous increase far outweighed
the adverse effects of O3 on growth.
However, these reports concern herbaceous weedy species, and there appears to be
only one report concerning tree species. Johnson and Taylor (1989) reported that exposure to
higher than ambient levels of O3 results in adaptation to a more efficient use of water by the
foliage of loblolly pine seedlings. The corollary to this observation is that trees exposed
continuously to low O3 levels may be more sensitive to recurrent drought stress than are those
grown under higher exposure levels. As with most studies of tree species, these observations
were made on tree seedlings, and the relevance to mature trees is still to be established.
It therefore is clear that not only does drought have a pronounced effect on the
response of most species to O3, but that O3 also may modify plant water relations, including
conferring drought tolerance. However, more study will be needed before it will be possible
to generalize about the implications of the latter effect and its importance to forest
ecosystems.
5-64
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5.4.5 Nutritional Factors
All land plants require an adequate supply of essential mineral elements from the
soil in order to avoid adverse effects on growth and survival resulting from mineral
deficiencies. Two of the essential elements needed for growth are nitrogen and sulfur, and
although these are normally obtained from the soil through the root system, the plant's needs,
at least in part, also can be met by the uptake of pollutant gases such as NO2 and SO2. Other
nutrients such as phosphorus, potassium, magnesium, and calcium generally are available only
from the soil.
A supply of elements such as nitrogen, potassium, phosphorus, sulfur, magnesium,
and calcium is essential for plant growth, but optimal growth requires that the supply be
balanced; with insufficiency (or excess) of any of them, growth will be suboptimal. Not
surprisingly, therefore, nutrient imbalance has been shown to affect response to O3, although
the previous criteria document (U.S. Environmental Protection Agency, 1986) concluded that
work to that date had not clarified the relationship between soil fertility and sensitivity to O3,
largely because of the differences in nutrients and species selected for study and the
experimental conditions used. This conclusion is still valid, in spite of the results of a limited
number of more recent studies, and is not surprising in view of the vast number of possible
permutations and combinations of nutrient elements and their levels that may exert effects on
O3 response. A comprehensive summary of the relevant studies is presented in Table 5-9.
Most information concerns nitrogen. However, inspection of Table 5-8 shows that,
in four of the 13 studies, increased nitrogen supply increased susceptibility to foliar injury or
enhanced adverse effects on growth; two of the studies showed opposite effects; in three
studies, injury was greatest at normal nitrogen levels and less at higher or lower levels; and,
in one study, injury was least at normal nitrogen levels. No interactions were observed with
soil nitrogen in three studies. Knowledge of the tissue nitrogen levels resulting from the
fertilizer treatments, as recommended by Harkov and Brennan (1980), might resolve these
contradictions, but these were not reported in most studies. The contradictory evidence for
tobacco may reflect different responses of different cultivars, as suggested by Menser and
Hodges (1967).
The possibilities of response to O3 being modified as a result of significant dry
deposition of nitric acid (HNO3) vapor or of wet deposition of nitrate ion in acid precipitation
are discussed in Sections 5.4.6.3 and 5.4.6.5, respectively.
The limited evidence for phosphorus, potassium, and sulfur consistently indicated a
decrease in sensitivity with increased nutrient level. With respect to general fertility, both
studies listed in Table 5-8 revealed decreased sensitivity to O3 at high levels of nutrient
supply, although, with soybean, nutrient-deficient plants also showed decreased sensitivity.
Heagle (1979) found that, although injury and growth reductions tended to be greatest at
normal levels of fertility, the effects were dependent on the rooting medium used; in media
containing peat, the impact of O3 on growth was least at the lowest fertility level.
Cowling and Koziol (1982) have suggested that, in spite of the apparent
contradictory evidence regarding the effects of nutrition on O3 response, there is evidence to
support the hypothesis that differences in sensitivity are ultimately linked to changes in the
status of soluble carbohydrates in the plant tissues (Dugger et al., 1962). However, this
hypothesis has yet to be tested systematically.
5-65
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Table 5-9. Ozone-Soil Nutrient Interactions
(Based in part on Cowling and Koziol, 1982)a
Species
Response to Increase in
Nutrient Level
Reference
Nitrogen
Loblolly pine
Ponderosa pine
Poplar
Yellow poplar
Ladino clover/tall fescue
Mangel
Radish
Spinach
Tobacco
Decreased reduction of growth due
toO3
No injury or growth interactions
Maximum injury in mid-range but
no growth interaction
No growth interaction
No growth interaction
Increased injury
Increased reduction of growth
due to O3
Increased reduction of growth
due to O3
Increased injury
Decreased injury
Minimum injury in mid-range
Maximum injury in mid-range
Maximum injury in mid-range
Tjoelker and Luxmoore (1991)
Bytnerowicz et al. (1990)
Harkov and Brennan (1980)
Tjoelker and Luxmoore (1991)
Monies et al. (1982)
Brewer et al. (1961)
Ormrod et al. (1973)
Pell et al. (1990)
Brewer et al. (1961)
Menser and Street (1962)
MacDowall (1965)
Leone et al. (1966)
Menser and Hodges (1967)
Phosphorus
Radish
Tomato
No growth interaction
Increased injury
Ormrod et al. (1973)
Leone and Brennan (1970)
Potassium
Norway spruce
Pinto bean
Soybean
Decreased reduction of CO2
assimilation due to O3
Decreased injury
Decreased injury
Keller and Matyssek (1990)
Dunning et al. (1974)
Dunning et al. (1974)
Sulfur
Bush bean
Decreased injury
Adedipe et al. (1972)
Magnesium
Loblolly pine
No growth interaction
Edwards et al. (1992b)
General Fertility (nitrogen,
phosphorus, and potassium)
Bush bean
Soybean
Decreased injury
Maximum injury and growth
reduction in mid-range
Heck et al. (1965)
Heagle (1979)
aSee Appendix A for abbreviations and acronyms.
5-66
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Nutritional nitrogen and sulfur also can be supplied directly to foliage in the form
of nitrogen and sulfur oxides. The interactions of these gaseous pollutants with O3, dealt with
in the next section, focus on toxic rather than nutritional effects. However, one example of a
beneficial effect concerns N2O5. Because N2O5 is produced in trace amounts by high-voltage,
corona-discharge O3 generators, it may contaminate O3 produced from air by such generators
for use in studies of effects of O3 on vegetation, unless the O3 stream is passed first through a
water scrubber. Brown and Roberts (1988) reported that deposition of the nitrate formed by
hydration of trace amounts of N2O5 in unscrubbed O3 significantly increased the nitrogen
status of the exposed plants, which may have confounded the effects attributed to O3.
5.4.6 Interactions with Other Pollutants
The concurrent or sequential exposure of vegetation to different gaseous air
pollutants has been found to modify the magnitude and nature of the response to individual
pollutants. Some of the early work reviewed in the previous criteria document (U.S.
Environmental Protection Agency, 1986) on the effects of gaseous pollutant combinations is
of academic interest, with little relevance to the present review because of the levels of
exposure and the exposure profiles used and the fact that the experimental regimes usually
involved concurrent exposures to two or more pollutants repeated daily. Lefohn and Tingey
(1984) and Lefohn et al. (1987b) reviewed the patterns of co-occurrence of O3, SO2, and NO2
in urban, rural, and remote sites in the United States for the years 1978 to 1982 and found
that co-occurrences were usually of short duration and occurred infrequently. They noted that
the most frequent types of co-occurrence were either purely sequential or a combination of
sequential and overlapping exposures of short duration. Accordingly, the present review will
focus on the evidence from experiments that simulated these naturally occurring patterns of
combined exposure or, at least, that used exposure levels in the ranges of those occurring in
polluted air. An exception is the co-occurrence of O3 and PAN, which are both components
of photochemical oxidant.
Over the past decade, the effects of pollutant mixtures have been reviewed by
Wolfenden et al. (1992), Shriner et al. (1991), Mansfield and McCune (1988), Torn et al.
(1987), Lefohn and Ormrod (1984), Reinert (1984), and Runeckles (1984).
5.4.6.1 Oxidant Mixtures
Because of their photochemical origins, elevated levels of O3 and PAN can occur
simultaneously. There appear to have been no further investigations of the effects of
simultaneous or sequential exposures since the limited number of studies reviewed in the
previous criteria document (U.S. Environmental Protection Agency, 1986). Hence, there is no
reason to question the general conclusion, based on the work of Tonneijck (1984) and Nouchi
et al. (1984), that the two gases tend to act antagonistically in both concurrent and sequential
exposures. Hydrogen peroxide (H2O2) is also a component of photochemically polluted
atmospheres. Although Ennis et al. (1990) reported reduced stomatal conductances in red
spruce needles exposed to a mixture of O3, SO2, and H2O2, no studies have been made of
O3/H2O2 interactions.
5-67
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5.4.6.2 Sulfur Dioxide
Because SO2 originates from point sources of combustion, the occurrence of high
ambient concentrations at a given location is usually episodic because of its dependence on
wind speed and direction and the distance from the source. However, aggregations of point
sources can lead to more widespread but less marked increases in ambient SO2 levels. Thus,
the potential exists for elevated O3 exposures to be superimposed on patterns of SO2, ranging
from severe fluctuations to almost steady low-level concentrations. Concern over the
importance of O3-SO2 interactions dates from the observations of Menser and Heggestad
(1966) that simultaneous exposures of tobacco to SO2 and O3 acted synergistically (i.e., the
effects of the mixture were greater than the sum of the responses to either pollutant alone).
Indeed, in the Menser and Heggestad study, foliar injury was found to result from exposure to
mixtures, although exposures to either gas alone at the same concentrations as in the mixtures
did not result in injury.
Although much of the early work was concerned with foliar injury responses to
simultaneous exposures to high levels of O3 and SO2, more recent studies have tended to
focus on the consequences of growth and yield of repeated exposures to lower level mixtures
or sequences. Several studies have been aimed at obtaining statistical evidence for the
existence of interactions. For example, Ashmore and Onal (1984), studying six cultivars of
barley, found that SO2 at 0.065 ppm for 6 h, an exposure that induced no adverse effects,
acted antagonistically to a 6-h exposure to 0.18 ppm O3, causing significant decreases in foliar
injury, ranging from 46% to as much as 95%. However, only one cultivar, Golden Promise,
showed a significant interaction on yield, with SO2 completely reversing the decrease caused
by O3 alone. The results could not be explained by effects on stomatal uptake because
stomatal conductances were found to be highest in the mixture. In contrast, with pea, Olszyk
and Tibbitts (1981) reported that O3 + SO2 caused the same degree of stomatal closure as SO2
alone. An antagonism similar to that observed on Golden Promise also was observed in field
studies of Arena barley (Adaros et al., 199la) and spring rape (Brassica napus) (Adaros et al.,
1991b). However, with Tempo spring wheat, a synergistic interaction was observed: the
adverse effect of O3 on yield (-26%) was increased to -38% by SO2, which, by itself, only
reduced yield by 7% (Adaros et al., 1991a). On the other hand, neither Amundson et al.
(1987) nor Kohut et al. (1987) observed any interaction in a field study with Vona winter
wheat. Irving et al. (1988) observed no interaction on field corn.
In a series of experiments in which exposure to O3 or an O3/SO2 mixture was
preceded by exposures to SO2 alone, an antagonistic response was observed on foliar injury to
white bean (Hofstra and Beckerson, 1981). In contrast, the responses of cucumber (Cucumis
sativus) and radish were synergistic, whereas there was no interaction on soybean or tomato.
However, when followed by exposure to an O3/SO2 mixture, SO2 pretreatment resulted in an
increase in injury to white bean, decreases in cucumber and tomato, and no effect on soybean
and radish.
Field studies with soybean using an air-exclusion system to provide a range of
exposures to O3 and SO2 at ambient and subambient levels revealed an antagonistic
interaction on yield at low concentrations (Jones et al., 1988). However, Kress et al. (1986)
found no interaction in a soybean field study using OTCs. No interactions were found with
potato (Pell et al., 1988) or with a red clover-timothy (Phleum pratense) forage mixture
(Kohut et al., 1988b).
5-68
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From the foregoing, it is apparent that no clearer pattern of the interactive effects
of O3 and SO2 on crops has emerged since the previous criteria document (U.S.
Environmental Protection Agency, 1986). The same is true for the responses of tree species.
With tree seedlings, Chappelka et al. (1988a) observed no interaction on white ash.
Although a synergistic interaction was found on root growth of yellow poplar (Chappelka
et al., 1985), only additive interactions were found on the growth of other parts of the plant.
In a unique study, Kargiolaki et al. (1991) noted that SO2 reduced the accelerated leaf
senescence caused by O3 on two poplar clones, but had no effect on other clones. They also
observed additive or less than additive interactions on the formation of intumescences, due to
hypertrophy of the stems and bark cracking. They attributed the differences in clonal
response to differences in the levels of pollutant-induced ethylene evolution.
Sulfur dioxide reversed the inhibition of photosynthesis caused by exposure to
O3 in two lichen species, Flavoparmelia caperata and Umbilicaria mammulata (Eversman and
Sigal, 1987).
Several studies have attempted to quantify the magnitudes of joint responses to
O3 and SO2. The earliest (Macdowall and Cole, 1971) showed that the synergistic injury
response of tobacco occurred at concentrations of SO2 less than the threshold for SO2 injury,
but not less than the O3 threshold. Oshima (1978), working with kidney bean, found that the
synergistic reduction due to intermittent exposures to O3 was linear through a range of
O3 concentrations achieved by varying degrees of filtration of ambient air (expressed as 10 to
90 ppm-h of concentrations greater than zero), although the threshold for an O3 response was
approximately 47 ppm-h.
A selection of statistical models of injury- or yield responses to O3/SO2 is listed in
Table 5-10. It is immediately apparent that the models reveal no consistent patterns of
response. In part, this is because they were developed on the basis of individual experiments
conducted under different environmental conditions at different locations in different years.
Although each model was statistically significant, it was based on a unique data set. One
study with soybean indicated an antagonistic interaction (Heagle et al., 1983b), but another
indicated no interaction (Kress et al., 1986). Cucumber (Hofstra et al., 1985) and snap bean
(Heggestad and Bennett, 1981) were reported to respond synergistically, whereas white bean
responded antagonistically (Hofstra et al., 1985).
All that can be concluded from these studies is that the type of interaction, and
whether or not one exists, is probably highly dependent on species and cultivar, and possibly
dependent on other environmental variables. The available evidence is insufficient to be able
to decide in which way, and to what extent, SO2 exposure will influence the effects of O3 on
a particular species or cultivar at a particular location. The synergism originally observed
(Menser and Heggestad, 1966) is not a general response.
5.4.6.3 Nitrogen Oxides, Nitric Acid Vapor, and Ammonia
As discussed in Chapter 3, the photochemical formation of O3 involves a complex
series of reactions in which NO, NO2, and HNO3 participate as intermediates or reaction
products. Of these, the limited number of reports of interactive effects with O3 is confined to
NO2. Some of the few studies of O3/NO2 interactions that have utilized realistic
concentrations have involved mixtures of the pollutants. Adaros et al. (1991a) found in a
2-year study of two cultivars each of barley and spring wheat that significant interactions
could be detected only on wheat yield in one growing season. With both cultivars, the
5-69
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Table 5-10. Some Statistical Models of Combined Ozone and Sulfur Dioxide Responses3
Oi
-------
Table 5-10 (cont'd). Some Statistical Models of Combined Ozone and Sulfur Dioxide Responses3
Type of
Species Interaction Model Reference
Tomato
New Yorker Injury = -75.78 + 20.481n[PI] - 29.16[O3] + 1,016[O3]2 + 9.02[SO2] - 17.29[SO2]2 + 258.76 Deveau et al.
[O3][SO2] (PI = plastochron index, used as a covariate; [O3] and [SO2]: ppm) (1987)
b
Oi
aSee Appendix A for abbreviations and acronyms.
bReport includes models for other growth variables.
-------
interaction was antagonistic. Nitrogen dioxide also reduced the adverse effect of O3 on the
yield of spring rape (Adaros et al., 1991b). Foliar injury to sunflower (Helianthus annum)
caused by daily exposures to O3 (0.1 ppm, 8 h) was increased by continuous exposure to
0.1 ppm NO2 (Shimizu et al., 1984). Plant dry weight was decreased by O3 + NO2 relative to
growth in O3 alone, but because O3 exposure resulted in a slight increase in dry weight
relative to the controls, the growth in the mixture and in the controls did not differ
significantly.
The results of a study of seven tree species exposed to 0.1 ppm O3 and/or 0.1 ppm
NO2 for 6 h/day for 28 days (Kress and Skelly, 1982) were reported in detail in the previous
criteria document (U.S. Environmental Protection Agency, 1986). However, although several
growth interactions were noted in the review, the only statistically significant effect was on
top growth of pitch pine (Pinus rigida), in which NO2 reversed a growth stimulation caused
by exposure to O3. In contrast, although Yang et al. (1982) also observed an antagonistic
interaction on the needle dry weights of two eastern white pine clones, in these cases NO2,
reversed the adverse effect of O3.
There appear to have been only three studies using sequential exposures of O3 and
NO2. Runeckles and Palmer (1987) exposed radish, wheat, bush bean, and mint (Mentha
piperita) daily to 0.08 to 0.1 ppm NO2 for 3 h (0900 to 1200 hours), to 0.08 to 0.1 ppm
O3 for 6 h (1200 to 1800 hours), or to the two gases in sequence. With each species except
mint, pretreatment with NO2 significantly modified the growth responses to O3. In radish and
wheat, the two gases acted conjointly to reduce growth more than O3 alone, whereas in bean
NO2 was antagonistic. In studies with tomato, Goodyear and Ormrod (1988) found that
sequential exposure to 0.08 ppm O3 for 1 h, followed by 0.21 ppm NO2 for 1 h, significantly
reduced growth. No significant effects were found when the sequence was reversed or the
two gases were used as a mixture. However, because the study did not include a treatment
with O3 alone, no information was obtained as to how NO2 may have influenced the response
to O3. Bender et al. (1991) exposed kidney beans in OTCs in the field to the sequence:
O3 (0800 to 1600 hours, ambient + 0.50 ppm) followed by NO2 (1600 to 0800 hours, ambient
+ 0.3 ppm), during two growing seasons. No significant treatment effects on growth were
observed in 1988, but in 1989 a significant interaction on total plant biomass was noted after
48 days; the overnight NO2 exposures negated the inhibition caused by O3 with a change from
-32 to +14%, relative to the controls. This type of response is similar to that observed on
bean by Runeckles and Palmer (1987).
With such limited information, it is not possible to generalize, particularly because
antagonistic and additive responses have been reported even for individual species. However,
because, on a daily basis, changes in NO2 levels tend to lead to maxima at times when
O3 levels are lowest, the evidence is sufficiently compelling to indicate that modifications of
the O3 response, as a result of increased NO2, are highly probable. Direct interactive effects
of O3 and NO virtually are precluded because of their rapid reaction to form NO2.
In Southern California, O3 levels have been correlated with levels of HNO3 vapor
(Fenn and Bytnerowicz, 1993). No studies of possible interactive effects between O3 and
HNO3 have been reported. However, Taylor et al. (1988a) suggest that HNO3 is largely
deposited on foliar surfaces and, hence, may be leached to the soil by rainfall. Such leaching,
together with rates of dry deposition to soil that have been conservatively estimated to range
between 5.7 and 29.1 kg nitrogen ha"1 year"1, would lead to nitrogen additions to the soil at
rates considerably less than agricultural rates of nitrogen-application to crops. However, such
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additions to forest soils could increase nitrogen levels significantly and lead to interactive
effects with O3 via changes in soil fertility, as discussed in Section 5.4.5.
Ammonia (NH3) can contribute significantly to total nitrogen deposition in some
locations. However, virtually nothing is known of its interactive effects with O3. Tonneijck
and van Dijk (1994) reported that, although NH3 and O3 showed a significant antagonism with
regard to foliar injury of O3-sensitive bean cv. Pros, no interactions occurred with regard to
growth effects.
5.4.6.4 Hydrogen Fluoride and Other Gaseous Pollutants
The adverse effects of HF released from the aluminum smelting process and
superphosphate fertilizer manufacture are well documented, but information about possible
HF/O3 interactions are limited to a single study. MacLean (1990) reported that exposures of
corn plants on alternate days to 4 h at l|ig/m3 fluorine as HF or 0.06 ppm O3 showed reduced
rates of senescence, compared with plants exposed only to O3.
5.4.6.5 Acid Deposition
Any impact that acid deposition has on crops or natural ecosystems occurs either
through direct effects on foliage or indirectly through the soil. Soil effects may result from a
change in pH or to the deposition of sulfate or nitrate onto the soil. The effects of acidic
deposition have been reviewed extensively by Shriner et al. (1991). Although concerns over
the possible role of exposures to acid rain or acid fog and O3 in the forest-decline syndrome
led to several studies with forest tree species, studies also have been conducted on crops.
Of over 80 recent reports of studies on over 30 species, more than 75% of the reports
indicated no significant interactions between O3 and acidity of simulated acid rain (SAR) or
acid fog. The reports are summarized in Table 5-10. In 63 studies, there was either no effect
of one or other of the pollutants (usually acid rain) or the effects of both pollutant stresses
were simply additive.
However, in other studies, statistically significant interactions have been reported
for several species, as also shown in Table 5-11. For example, although a large number of
studies of loblolly pine revealed no interaction, Qiu et al. (1992) reported significant
interactions on foliar and stem and root biomass with seedling trees of an O3-sensitive family.
However, because the study failed to show a significant main effect of acidity of the SAR,
the authors question whether the interaction is meaningful.
With Norway spruce, antagonistic interactions were noted on stomatal conductance
(Barnes et al., 1990a) and dark respiration (Barnes et al., 1990b). In contrast, Eamus and
Murray (1991) reported greater than additive effects of O3 and acid mist on photosynthetic
rates. However, no interactions were noted in nine other investigations (Table 5-11).
Kohut et al. (1990) observed significant interactions on needle and shoot growth of
red spruce. In both cases the inhibition caused by O3 and SAR at pH 5.1 was reversed by
more acidic rain at pH 3.1. However, there were unexplained inconsistencies in the trends
because the combination of intermediate O3 levels and low pH resulted in the greatest
reductions in dry matter. Percy et al. (1992), also working with red spruce, observed an
unexplained statistically significant interaction on the thickness of the needle epidermal cell
cuticular membrane: at intermediate O3 exposures, increased acidity led to reduced membrane
thickness, whereas lower or higher O3 levels led to thicker membranes.
Shelburne et al. (1993) reported that, in two growing seasons, needle biomass of
shortleaf pine (Pinus echinatd) was reduced significantly in tree seedlings receiving the
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Table 5-11. References to Reports of Interaction or No
Interaction Between Ozone and Acid Rain or Acid Fog
Species >
Tree Species
CONIFERS
Jeffrey pine
Loblolly pine
Ponderosa pine
Shortleaf pine
Slash pine
White pine
Douglas fir
Norway spruce
Red spruce
Sequoia
Totals
HARDWOODS
Green ash
White ash
European beech
Paper birch
Sugar maple
Red oak
Yellow poplar
Totals
Crop Species
FORAGES AND FIELD CROPS
Alfalfa
Sorghum
Soybean
Wheat
Totals
HORTICULTURAL CROPS
Snap bean
Celery
Corn
Pepper
Interaction
To. References
0 —
1 41
0 —
1 52
2 9, 13
1 47
0 —
1 3,4
2 31,39
1 63
9
0 —
0 —
1 14
1 29
0 —
0
3 11, 12, 27
5
1 59
1 51
1 67
0 —
2
0 —
0 —
0 —
0 —
No.
1
13
2
1
0
3
1
9
5
0
35
1
1
1
0
2
2
1
8
4
0
4
1
5
1
1
1
2
No Interaction
References
62
1, 10, 16-21, 26, 32, 43, 47, 49, 55
65, 66
8
—
44, 46, 56
25
2, 5-7, 15, 24, 30, 36, 50
33, 34, 38, 40, 62
—
23
23
35
—
44, 45
44, 45
48
42, 53, 59, 64
—
28, 37, 53, 57
53
53
60
60
58, 60
5-74
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Table 5-11 (cont'd). References to Reports of Interaction or No
Interaction Between Ozone and Acid Rain or Acid Fog
Interaction No Interaction
Species No. References No. References
HORTICULTURAL CROPS (cont'd)
Strawberry 0 — 2 60, 61
Tomato 0 — 2 53, 60
Avocado 1 22 0 —
Citrus 1 22 0 —
Totals 2 9
Others
Ivy
Lichen (Lobaria)
Totals
TOTALS
0 —
0 —
0
19
1
1
2
63
30
54
References:
1. Adams and O'Neill (1991). 2. Barnes and Brown (1990). 3. Barnes et al. (1990a). 4. Barnes et al. (1990b).
5. Blank et al. (1990a). 6. Blank et al. (1990b). 7. Blaschke and Weiss (1990). 8. Boutton and Flagler (1990).
9. Byres et al. (1992a,b). 10. Carter et al. (1992). 11. Chappelka et al. (1985). 12. Chappelka et al. (1988b).
13. Dean and Johnson (1992). 14. Eamus and Murray (1991). 15. Ebel et al. (1990). 16. Edwards and Kelly
(1992). 17. Edwards et al. (1990b). 18. Edwards et al. (1991). 19. Edwards et al. (1992a). 20. Edwards et al.
(1992b). 21. Edwards et al. (1992c). 22. Eissenstat et al. (1991b). 23. Elliott et al. (1987). 24. Ftihrer et al.
(1990). 25. Gorissen et al. (1991b). 26. Hanson et al. (1988). 27. Jensen and Patton (1990). 28. Johnston and
Shriner (1986). 29. Keane and Manning (1988). 30. Kerfourn and Garrec (1992). 31. Kohut et al. (1990).
32. Kress et al. (1988). 33. Laurence et al. (1989). 34. Lee et al. (1990b). 35. Leonardi and Langebartels
(1990). 36. Magel et al. (1990). 37. Norby et al. (1986). 38. Patton et al. (1991). 39. Percy et al. (1992).
40. Pier et al. (1992). 41. Qiu et al. (1992). 42. Rebbeck and Brennan (1984). 43. Reddy et al. (1991a,b).
44. Reich and Amundson (1985). 45. Reich et al. (1986b). 46. Reich et al. (1987). 47. Reich et al. (1988).
48. Roberts (1990). 49. Sasek et al. (1991). 50. Senser (1990). 51. Shafer (1988). 52. Shelburne et al. (1993).
53. Shriner and Johnson (1987). 54. Sigal and Johnston (1986). 55. Somerville et al. (1992). 56. Stroo et al.
(1988). 57. Takemoto et al. (1987). 58. Takemoto et al. (1988a). 59. Takemoto et al. (1988b). 60. Takemoto
et al. (1988c). 61. Takemoto et al. (1989). 62. Taylor et al. (1986). 63. Temple (1988). 64. Temple et al.
(1987). 65. Temple et al. (1992). 66. Temple et al. (1993). 67. Troiano et al. (1983).
highest O3 exposures (2.5 x ambient) and SAR at pH 3.3. However, there were no effects at
lower O3 exposure levels or at higher pHs.
A 3-year study of slash pine revealed a significant interaction on stem volume
increment in each year (Dean and Johnson, 1992). This was attributed to a high rate of
increase observed with increasing acidity in trees exposed to an intermediate O3 level
(2 x ambient). In contrast, at higher or lower O3 exposures, acidity of the SAR applied had
little effect. Although another study with slash pine indicated a significant interaction on
photosynthetic rates, no information was provided about its nature (Byres et al., 1992b).
The mineral status (potassium, calcium, and manganese) of white pine showed
antagonistic interactions between O3 and SAR (Reich et al., 1988). Increased acidity nullified
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the increase in foliar potassium and the decreases in root calcium caused by O3, whereas
increased O3 nullified the increase in root manganese that resulted from increased acidity.
Temple (1988) reported a synergistic response to O3 and SAR of root growth of
giant sequoia. Yellow poplar showed no interactions in one study (Table 5-11), but a greater
than additive response of root growth was observed by Chappelka et al. (1985). Chappelka et
al. (1988b) found that, although neither O3 nor the pH of SAR caused any significant effects
on growth, at intermediate O3 levels, increased acidity caused significant decreases in stem
and leaf biomass. Jensen and Patton (1990), on the other hand, reported significant
antagonistic interactions on yellow poplar leaf and shoot growth. Based on estimates from
growth models derived from experimental data, increased acidity (pH 5.5 to 3.0) of SAR
reduced the decreases caused by O3 by almost 50%.
Adverse effects of O3 on the leaf area and shoot, leaf, and root biomass of paper
birch (Betula papyriferd) were reversed by increased acidity of SAR (Keane and Manning,
1988). Similarly, in both avocado and lemon (Citrus volkameriand) trees, Eissentstat et al.
(1991b) found that increased acidity offset the negative effects of O3 on leaf growth.
Although there are four reports of no interactions on alfalfa, Takemoto et al.
(1988b) observed significant interactions on leaf drop. In charcoal-filtered air, leaf drop
increased by a factor of 6 as the pH of the fog treatment changed from 7.24 to an extremely
acid pH 1.68, the lowest level recorded in the field in Southern California. In unfiltered air,
in contrast, leaf drop increased only 20%.
Several studies with soybean revealed no significant interactions. However,
Troiano et al. (1983) reported a 42% reduction in seed yield between CF and unfiltered air
with SAR at pH 2.8 versus a 6% reduction at pH 4.0. Increased acidity thus multiplied the
effect of O3, due largely to a stimulation of seed yield caused by increased acidity. Shafer
(1988) observed a stimulation of shoot growth of sorghum at pH 2.5 of SAR over growth at
pH 5.5, as a result of which, greater growth occurred at low O3 exposure levels, although
there was no effect of acidity at the highest O3 level (0.3 ppm).
In summary, although the majority of studies have not demonstrated the existence
of interactions between O3 and SAR, where statistically significant interactions on growth or
physiology have been reported, the interactions were mostly antagonistic. The only
synergistic interactions reported are in two studies of yellow poplar and single studies of
sequoia and shortleaf and slash pines. In most cases where significant interactions were
noted, the authors have had difficulty in providing any mechanistic explanation. It appears
that, although the effects may have passed normally accepted tests of statistical significance,
they may nevertheless have been spurious findings. Overall, it appears that exposure to acidic
precipitation is unlikely to result in significant enhancement of the adverse effects of O3 in
most species. In the few cases of antagonistic interactions, the suggestion was made that
these may have reflected a beneficial fertilizer effect due to the nitrate and sulfate present in
the SAR applied.
The preceding review has focused on interactive effects of O3 and wet hydrogen
ion deposition. With regard to the anionic constituents of acid deposition, studies with SAR
have tended to use dilute mixtures of nitric and sulfuric acids, together with other anions and
cations, to achieve the desired pH levels. However, no studies appear to have been
undertaken to separate any interactive effects of the individual cations (nitrates or sulfates)
from those involving hydrogen ions. However, given the limited and variable information on
interactive responses of O3 and nitrogen and sulfur as soil nutrients, it is not possible to
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predict the nature of any possible interactions of O3 with the wet deposition of these elements.
5.4.6.6 Heavy Metals
Interactions of O3 with several heavy metal pollutants were reviewed in the
previous criteria document (U.S. Environmental Protection Agency, 1986). The limited data
for pollutants such as cadmium, nickel, and zinc almost invariably showed that they enhanced
the adverse effects of O3, usually additively, but occasionally more than additively. To the
results with cadmium, nickel, and zinc on garden cress (Lepidium sativum), lettuce (Lactuca
sativa)., pea, tomato, and aspen, reviewed at that time, should be added similar findings with
zinc on pinto bean (Mcllveen et al., 1975); increased zinc results in significantly increased
foliar injury and decreased mycorrhizal infection. However, in a study of the effects of O3,
nickel, and copper on tomato, Prokipcak and Ormrod (1986) found that, as the levels of both
O3 and nickel increased, the interaction changed from additive to less than additive. Complex
interactions were observed when the treatments included both nickel and copper.
No information appears to be available about possible interactions with lead.
Although qualitatively heavy metals appear to increase plant sensitivity to O3, the limited
information available precludes defining any quantitative relationships.
5.4.6.7 Mixtures of Ozone with Two or More Pollutants
Pollutant-pollutant interactions are not limited to mixtures or sequences of two
pollutants. Several studies have been made of interactions of O3 with various combinations of
SO2, NO2, and acid rain. However, in some of these investigations, no treatment with O3 was
included in the experimental design, and, therefore, no information was obtained on effects in
response to O3. Some studies using only repeated daily exposures to high levels (>0.3 ppm)
of one or more pollutants are excluded from this review.
Adaros et al. (1991b), in a field study of spring rape using open-top chambers,
found no significant interactions between O3 and NO2 (sequential exposures) and SO2
(continuous exposures). In a 2-year study on spring barley and spring wheat, some
statistically significant interactions were noted, but they were scattered through the different
growth measurements, cultivars, and years with no consistent pattern (Adaros et al., 1991c).
Additive effects with no interactions were observed in studies of shore juniper (Junipems
confertd) (Fravel et al., 1984), radish (Reinert and Gray, 1981), and azalea (Rhododendron
spp.) (Sanders and Reinert, 1982). Yang et al. (1982) reported a less than additive interaction
on injury to white pine.
No significant three-way interactions were found in studies of soybean (Norby
et al., 1985), yellow poplar (Chappelka et al., 1985, 1988b), or any other hardwood species
(Davis and Skelly, 1992a; Jensen and Dochinger, 1989; Reich et al., 1985) exposed to O3,
SO2, and SAR.
No information was collected on interactions in the few published studies
involving O3, SO2, NO2, and SAR.
The limited data make it difficult to draw any firm conclusions, but, in general, the
consequences of such exposures appear to be dictated largely by the dominant individual
two-way interaction.
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5.4.7 Interactions with Agricultural Chemicals
Agricultural chemicals are used for the control of insect pests, diseases, and weeds
and for the control of growth in specialized situations, such as the selective thinning of fruit
on orchard trees. The potential for some agricultural chemicals to modify plant response to
O3, first noted with certain fungicides on pinto beans (Kendrick et al., 1954), led to numerous
field and laboratory studies. As noted in the previous criteria document (U.S. Environmental
Protection Agency, 1986), protection against O3 injury was found to be conferred by
applications of numerous commercial fungicides, herbicides, and growth regulators.
The available information is derived from studies involving a number of different
commercial chemicals and species. No comprehensive and systematic studies have been
reported, but the weight of evidence indicates that certain fungicides are consistent in
providing protection. In particular, there have numerous reports of protection conferred by
applications of benomyl (benlate; methyl-l-[butylcarbamoyl]-2-benzimidazolecarbamate).
In addition to the studies reviewed in the previous criteria document (U.S. Environmental
Protection Agency, 1986), benomyl protection of grape (Musselman and Taschenberg, 1985)
and bean cultivars (Pell, 1976; Pellisier et al., 1972) also has been reported. It is of interest
to note that, although several nematocides were found to increase sensitivity of tobacco and
pinto bean to O3, applications of benomyl overcame this response and conferred resistance
(Miller et al., 1976). However, benomyl was found to increase the injury caused by PAN
(Pell and Gardner, 1979). It also should be noted that many of the effective fungicides are
carbamates and have been used as antioxidants in other applications, such as rubber
formulations.
The need to distinguish between protective action against O3 injury and fungicidal
activity per se is shown by a study of fentin hydroxide (Du-Ter; tetraphenyltin hydroxide) on
potato (Holley et al., 1985). The fungicide reduced foliar injury in the field and also the
colonization of injured leaf tissue by the early blight fungus, Alternaria solani. However,
yield increases appeared to result from the reduction of disease rather than from diminished
O3 injury.
The triazoles are a family of compounds with both fungicidal and plant growth
regulating properties. Fletcher and Hofstra (1985) reported on the protective action of
triadimefon [ 1 -(4-chlorophenoxy)-3,3-dimethyl-1 -(1H-1,2,4-triazo-1 -yl)-2-butanone], and
Musselman and Taschenberg (1985) found that triadimefon and the triazole, etaconazole
(l-[(2,4-dichlorophenyl)-4-ethyl-l,3-dioxolan-2-yl]methyl-lH-l,2,4-triazole), were as effective
as benomyl in protecting grape from oxidant injury; cultivar differences were noted, with the
fungicides being more effective on Concord than on Ives foliage. Seed treatment with
triazole S-3307 ([E]-l-[4-chlorophenoxy]-3,3-dimethyl-2-[l,2,4-triazol-l-yl]- l-penten-3-ol)
resulted in a 50% reduction in the size of wheat plants but provided complete protection from
an excessive exposure to 0.5 ppm O3 for 6 h that resulted in severe necrosis on the leaves of
untreated plants (Mackay et al., 1987).
A range of commercial plant growth regulating compounds was studied by Cathey
and Heggestad (1972). The plant growth retardants, CBBP (Phosfon-D; 2,4-dichloro-
benzyltributyl phosphonium chloride) and SADH (Alar®; succinic acid, 2,2-dimethyl-
hydrazide) and several of its analogs, were found to be more effective than benomyl in
reducing O3 injury on petunia.
Conflicting reports of the effects of herbicide-O3 interactions were reviewed in the
previous criteria document (U.S. Environmental Protection Agency, 1986). Recent studies of
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metolachlor (2-chloro-jV-[2-ethyl-6-methlphenyl]-jV-[2-methoxy-l-methylethyl] acetamide)
(Mersie et al., 1989) and atrazine (2-chloro-4-ethylamino-6-isopropylamino-5-triazine) (Mersie
et al., 1990) revealed species-dependent effects: metolachlor sensitized corn to O3 but offered
protection to bean and soybean. The effects of atrazine on corn were additive to those
induced by exposure to 0.2 ppm O3 for 6 h/day, twice weekly, for three weeks, but
antagonistic to exposures to 0.3 ppm. Mersie et al. (1990) also observed a protective action
of the commercial antioxidant, w-propyl gallate, on corn.
In spite of reports to the contrary (Teso et al., 1979), Rebbeck and Brennan (1984)
found that the insecticide, diazinon (O,O-diethyl-O-[2-isopropyl-4-methyl-6-pyrimidinyl]
phosphorothioate), did not protect alfalfa from O3 injury in a greenhouse study.
The knowledge of the interactions of these different types of agricultural chemicals
with O3 is still too fragmentary to enable any general conclusions to be drawn, other than to
note the general efficacy of the carbamate fungicides. As noted in the previous criteria
document (U.S. Environmental Protection Agency, 1986), it is premature to recommend their
use specifically for protecting crops from the adverse effects of O3, rather than for their
primary purpose.
5.4.8 Factors Associated with Global Climate Change
This section focuses solely on the ways in which features of global climate change
may be expected to affect the impact of oxidants on vegetation. It is not intended to provide
a comprehensive review of the issues and components of climate change per se.
The magnitudes and causes of some of the changes in features of the global
climate that have been observed or are predicted to occur are currently the subject of
controversy. However, there is clear evidence of increases in mean CO2 levels (Keeling
et al., 1989), which, together with other anthropogenic emissions of radiatively active gases,
may contribute to the upward trend in mean surface-level temperatures observed over the past
century (Jones, 1989) and to changes in precipitation patterns throughout the world (Diaz et
al., 1989). In addition, depletion of the stratospheric O3 layer in the polar regions, caused by
halofluorocarbons, results in increased penetration of the atmosphere by solar ultraviolet-B
(UV-B) radiation (280- to 320-nm wavelengths). However, the intensity of UV-B radiation
reaching the earth's surface may be attenuated by O3-pollution in the lower troposphere
(Briihl and Crutzen, 1989). Differences in the degree of this attenuation probably contribute
to the discrepancies between recently observed trends in surface-level UV-B intensities
(Scotto et al., 1988; Blumenthaler and Ambach, 1990).
Independent of any effects of ambient temperature, CO2 level affects plant-water
relations through effects on stomatal aperture and conductance, leading to effects on leaf and
canopy temperature and the uptake of gaseous pollutants. The effects of UV-B on numerous
growth processes have been reviewed by Tevini and Teramura (1989) and Runeckles and
Krupa (1994). Individual interactive effects of O3 and several effects of global climate
change have been reviewed in the previous sections. However, it is important to recognize
that, because of the interactions among the different components of climate change
themselves, a holistic approach is essential, which includes the potential of interactions for
modifying plant response to oxidants. Overall reviews of the interactions involving the
factors of climate change and O3 have been presented by Krupa and Kickert (1989) and
Ashmore and Bell (1991).
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The effect of increased CO2 in stimulating photosynthetic rates also may lead to
increased leaf area, biomass, and yield (Allen, 1990). Increased CO2 also leads to stomatal
closure. However, with regard to water use, the result of decreased stomatal conductance in
reducing transpiration is offset partly by the increase in leaf and canopy temperature, resulting
from reduced evaporative cooling, and the increase in leaf area. The net result is that
increased CO2 may lead to only slight increases in water-use efficiency, which are attributable
more to increased photosynthetic activity than to reduced transpiration (Allen, 1990). On the
other hand, because the primary route of entry into the leaf of a gaseous pollutant such as
O3 is through the stomata, increased CO2 levels would be expected to decrease the impact of
O3 by reducing uptake as a consequence of reduced stomatal conductance. The effects of
increasing CO2 levels discussed above relate to plants with the C3 pathway of carbon fixation.
These include the following major broad-leaved crops: wheat, rice (Oryza sativa), legumes,
potato, and cole crops. Plants with the C4 pathway tend to have greater water-use efficiencies
(WUEs) than C3 plants, but show less response to increased CO2 levels. Major C4 crops are
corn and sorghum. However, no studies appear to have been conducted on O3/CO2
interactions in C4 species.
Allen (1990) provides a simulation of the effect of doubling the average ambient
CO2 level from 340 to 680 ppm on soybean yield, based on the Weibull response model to
O3 and SO2 of Heagle et al. (1983b) and the model of stomatal conductance developed for
soybean by Rogers et al. (1983):
gs = 0.0485 - 7.00 x 1Q-5[CO2] + 3.40 x 1Q-8[CO2]2,
where gs is stomatal conductance (in meters per second), and [CO2] is CO2 concentration
(in parts per million). According to this model, a doubling of the CO2 level would reduce
gs by a factor of 0.69, effectively reducing the O3 and SO2 concentrations to 0.038 and
0.018 ppm, respectively. At the current 340 ppm CO2 level, the Weibull model predicts a
yield of 340.5 g/m of row. Reduced pollutant entry at 680 ppm CO2 gives a predicted yield
of 390.6 g/m of row, an increase of 14.7%. This is a conservative estimate because it ignores
the direct effect of the increased CO2 level on soybean growth.
Although the calculation makes numerous assumptions, it is supported qualitatively
by evidence from the few studies published to date on CO2/O3 interactions. Barnes and
Pfirrmann (1992) reported that an increased CO2 level of 765 ppm countered the adverse
effects of O3 on photosynthesis, shoot growth rate, leaf area, and water-use efficiency of
radish. Protection against the adverse effects of O3 on soybean by elevated CO2 also was
reported by Kramer et al. (1991). The yield loss due to O3 at ambient CO2 was 11.9%,
whereas, in the presence of ambient +150 ppm CO2, the loss was only 6.7%.
Although these studies support the prediction of Allen (1990), they were conducted
in growth chambers (Barnes and Pfirrmann, 1992) or OTCs (Kramer et al., 1991; Mulchi et
al., 1992), as were the studies on which Allen's model was based. Hence, the plants would
not have been subjected to the environmental conditions typical of the open field, particularly
with respect to wind speed and its effects on transpiration and temperature. Nevertheless,
these studies support the view that increased CO2 levels will reduce adverse effects of O3 on
crops.
It is unclear as to whether such CO2-induced reductions of the impact of O3 also
apply to the long-term growth of trees, and it is equally unclear as to how increased CO2 will
affect the impact of O3 on ecosystems. These uncertainties arise because of the numerous
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compensatory feedback mechanisms that play important roles in both long-term perennial
growth and in the behavior of ecosystems. Such feedback includes changing demands for
nutrients, increased leaf area and potential water loss, and changes in litter quality and
quantity. For example, in terms of the effects of increased CO2 alone, long-term studies of
several species suggest that, although photosynthesis may be demonstrably stimulated, there
may be little or no net response at the ecosystem level (Bazzaz, 1990).
The consequences of global warming as a feature of climate change are difficult to
assess because, as discussed in Section 5.4.4, the information on the effects of temperature on
O3-response is conflicting. However, as Ashmore and Bell (1991) point out, concerns over
the effects of O3 on sensitivity to freezing temperatures will become increasing unimportant
as warming occurs.
Various models of climate change scenarios have indicated that changed
precipitation patterns will lead to increased drought in some mid-latitude regions of the world.
The bulk of the evidence reviewed in Section 5.4.4 suggests that this would reduce the impact
of O3. However, because of the major direct impact of drought per se, such protection would
be of little practical significance.
Greater certainty surrounds the likelihood that global warming will increase the
incidence and severity of losses caused by pests and diseases. Concurrent increases also may
favor the competitiveness of many weed species. At present, it is not possible to quantify
such changes or to determine how they would influence the interactions discussed in
Section 5.4.3.
With regard to possible interactions of O3 and UV-B, Runeckles and Krupa (1994)
point out that, because of the episodic nature of O3 pollution, including its typical diurnal
pattern, surface-level exposures to UV-B also will be episodic. They have described various
possible O3/UV-B scenarios that need to be considered. With low surface-O3 levels and
increased UV-B irradiation due to stratospheric O3 depletion, effects of UV-B will
predominate. On the other hand, elevated surface-O3 levels will cause increased attenuation
of UV-B resulting in reduced surface intensities. With no stratospheric O3 depletion, this
condition implies that surface effects of O3 will predominate over the effects of UV-B; with
stratospheric O3 depletion, the resulting surface level irradiation will be dependent on the
concentration and thickness of the surface O3 layer, and both O3 and UV-B effects may occur.
To date, there have been no experiments conducted specifically to simulate these
different scenarios. However, Miller et al. (1994) exposed soybean in field OTCs, within
which lamps were suspended to provide increased intensities of UV-B. The O3 treatments
were ambient and 1.5 x ambient. No significant O/UV-B interactions were noted; the effects
on growth were solely attributable to the O3 exposure. However, increased UV-B irradiation
resulted in increases in the foliar content of UV-absorbing constituents. In contrast, Miller
and Pursley (1990) reported that a preliminary experiment revealed a less than additive
interaction of O3 and UV-B on soybean growth.
It is clear overall that the effects of O3 on vegetation will be modified to some
degree by various components of the complex mix of factors that constitute climate change.
Considerably more research will need to be undertaken before quantitative assessments of the
magnitudes of the changes will be possible.
5.4.9 Summary—Environmental Factors
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Since the previous criteria document (U.S. Environmental Protection Agency,
1986), additional studies have been published on a wide range of biological, physical, and
chemical factors in the environment that interact with plant response to O3.
Biological components of the environment of individual plants include pests,
pathogens, and plants of the same or other species in competition. With regard to insect
pests, although only a very limited number of plant-insect systems have been studied, there is
a general trend in the observations that suggests that some pests have a preference for and
grow better when feeding on plants that have been impacted by O3. Unfortunately, because
there is no knowledge of how the vast majority of plant-insect systems will be affected by O3,
it is not possible to offer any quantitative overall assessment of the consequences of such
interactions on the growth of crops and natural vegetation. At best, there is a reasonable
likelihood that some insect pest problems will increase as a result of increased ambient
O3 levels, but there is no evidence to suggest that O3 may trigger pest outbreaks.
Plant-pathogen systems also are affected by O3, but, here too, the available
evidence is far from representative of the wide spectrum of plant diseases. Nevertheless, the
suggestion of Dowding (1988) that diseases caused by obligate pathogens tend to be
diminished by O3, whereas those caused by facultative pathogens tend to be favored, generally
is supported by the limited evidence available. In terms of its broader implications, this
suggests that continued exposure to O3 may lead to a change in the overall pattern of the
incidence and severity of specific plant diseases affecting crops and forest trees. However, it
is not possible, with the limited evidence currently available, to predict whether the net
consequences of O3 exposure would be more or less harmful.
A major level of uncertainty concerns the effects of O3 at the population and
community levels within natural ecosystems. Very few studies have been conducted on
multi-species systems, and Woodward (1992) has pointed out the hazards of attempting to
extrapolate from responses of the individual plant to responses of a population of such plants.
This is borne out by the observations of Evans and Ashmore (1992) who showed that the
behavior to O3-exposure of a species growing in mixture with other species is not predictable
from its behavior when grown in isolation. This has serious implications with regard to
complex natural ecosystems and identifies a serious gap in the knowledge of the effects of
O3 that can be filled only by a substantial research effort.
With regard to the physical environment, the combination of light, temperature, air
turbulence, and water availability largely determines the success of plant growth because of
the influence of these factors on the processes of photosynthesis, respiration, and
transpiration. Air turbulence plays an important role in O3 uptake because it determines the
amount of O3 to which a plant is exposed, as well as when exposure will occur. For
agricultural crops, perhaps the most important of these potential interactions with O3 concerns
water availability and use. There is consistent evidence that drought conditions tend to
reduce the direct adverse effects of O3 on growth and yield. Conversely, the ready
availability of soil water tends to increase the susceptibility of plants to O3 injury. However,
a lack of water should not be viewed as a potentially protective condition, because of the
adverse effects of drought per se. The combination of drought conditions and exposure to
O3 is likely to result in adverse effects on growth and yield that are largely the result of lack
of water. However, with perennial trees, there is evidence that prolonged exposures to
O3 may lead to greater water use efficiency, which would enable such trees to be better able
to survive drought conditions.
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In contrast with crop species, with tree species, the relative roles of light,
temperature, and water are shifted somewhat because of the differences in plant form.
In particular, the photosynthetic function of the leaves is carried out by a much smaller
proportion of the plant's biomass. Conversely, a larger demand is placed on temperature-
dependent respiratory processes to maintain and support the tissues of the stem and root
systems. In addition, in temperate regions, the perennial habit brings with it the requirement
for storage of carbohydrates and other reserves, in order to permit survival during the winter
season and to facilitate renewed spring growth. Hence, with tree species it becomes
important to distinguish between the immediate effects of exposure to O3 and the longer term
consequences of these effects.
Of particular importance in northern latitudes and at higher elevations is the
demonstrated role of O3 in adversely affecting cold hardiness by reducing carbohydrate
storage. Independent of effects on winter hardiness, there is also evidence to indicate that
adverse effects on storage also may be a component of changes in growth occurring in
subsequent seasons (Hogsett et al., 1989; Andersen et al., 1991; Sasek et al., 1991).
However, it is not yet possible to assemble these observations into a general quantitative
model.
The plant's environment also contains numerous chemical components, ranging
from soil nutrients and other air pollutants to agricultural chemicals used for pest, disease, and
weed control. With regards to plant nutrients and their influence on plant response to O3, the
available evidence is highly fragmentary and frequently contradictory and, hence, does not
permit the drawing of any general conclusions. A large number of studies have been
conducted on the effects of O3 in conjunction with other gaseous air pollutants such as SO2
and NO2, although the information obtained in several of the studies is of no more than
academic interest because of the unrealistic exposure conditions used. Although there is clear
evidence to show that O3 and SO2 may act synergistically in increasing foliar injury in some
species, the available evidence indicates that this type of response is not universal. Several
empirical models of the O3-SO2 interaction have been developed, but they have little in
common and are highly specific to the crop and exposure conditions used. Furthermore, the
frequently observed lack of interaction implies that in many cases the impact of O3 is
probably best assessed on its own. The same is true of the situation with regard to
combinations of O3 and acid rain or acid fog and of O3 and NO2.
Numerous agricultural chemicals have been found to influence the responses of
plants to O3. In particular, several fungicides have been shown to provide protection against
visible injury, although none has been adopted for commercial application for this purpose.
On the other hand, the experimental chemical EDU has been found consistently to provide
protection of a wide range of species, both in the laboratory and in the field.
Because increased tropospheric O3 is a component of global climate change, results
from studies on the interactions of O3 with increased levels of CO2 and UV-B radiation are
beginning to appear. Initial work with CO2 suggests that increased CO2 levels may ameliorate
the effects of O3. However, it is too soon to be able to generalize on the outcome of this
interaction. At the present time, no investigations of the compound interactions involving O3,
CO2, UV-B, increased temperature, and changed soil-moisture status have been reported.
In conclusion, in spite of the amount of work carried out on the interactions of
O3 with environmental factors, there exists only a very fragmented understanding from which
to draw conclusions. This is probably inevitable in view of the vast scope of the possible
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interactions between O3 and all the other environmental variables. It is also a result of the
fact that most of the published work consists of studies resulting from personal interests of
the investigators, rather than from coordinated programs of research that focus on systematic
investigations. The consequence is that, although information has been reported about
magnitudes of many interactions of O3 with environmental variables (or the lack thereof), the
fragmented and nonsystematic nature of the information prevents the drawing of general
conclusions and of defensible estimates of the uncertainties associated with these interactions.
5.5 Effects-Based Air Quality Exposure Indices
5.5.1 Introduction
5.5.1.1 Biological Support for Identifying Relevant Exposure Indices
The effects of O3 on individual plants and the factors that modify plant response to
O3 are complex and vary with species, environmental conditions, and soil and nutrient
conditions. Because of the complex effect of O3 and its interactions with physical and genetic
factors that influence response, the development of exposure indices to characterize plant
exposure and to quantify the relationship between O3 exposure and ensuing plant response has
been, and continues to be, a major problem. At best, experimental evidence of the effect of
O3 on biomass production can refine the knowledge of those factors of O3 exposure that affect
the ability to predict plant response using exposure indices. The impacts of measured O3
concentrations on plant response are discussed and evaluated to determine the key factors of
exposure that account for the variations in plant response and, if possible, to develop
measures of pollutant exposure that relate well with plant response.
Considerable evidence of the primary mode of action of O3 on plants (e.g., injury
to proteins and membranes, reduction in photosynthesis, changes in allocation of
carbohydrate, early senescence), which eventually impacts biomass production, identifies
O3 uptake as the measurement of plant exposure (Section 5.3). Ozone uptake is controlled by
canopy and stomatal conductance and by ambient O3 outside the leaf (see Figure 5-3). Any
factor that will affect stomatal conductance (e.g., light, temperature, humidity, soil and
atmospheric chemistry, air turbulence, nutrients, time of day, phenology, biological agents)
will affect O3 uptake and, consequently, plant response (i.e., yield or biomass). Biochemical
mechanisms describe the mode of action of O3 on plants as the culmination of a series of
physical, biochemical, and physiological events leading to alterations in plant metabolism.
Ozone-induced injury is cumulative, resulting in net reductions in photosynthesis, changes in
allocation of carbohydrate, and early senescence, which ultimately lead to reductions in
biomass production. In most cases, increasing the duration of exposure increases the effect of
O3 on plant response. Peak concentrations, when they occur during daylight (when stomatal
conductance is high), can have more influence in determining the impact of O3 on plant
response than lower concentrations or night concentrations because of a greater likelihood of
intracellular impairment.
From a toxicological perspective, duration and peak concentrations above some
level have value in determining plant response but interact with other factors such as respite
time, temporal variation, phenology, canopy structure, physiological processes, environmental
conditions, and soil and nutrient conditions in different fashions, depending on species.
Effects occur on vegetation when the amount of pollutant absorbed exceeds the ability of the
plant to detoxify O3 or to repair the initial impact (Tingey and Taylor, 1982).
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Although O3 uptake integrates the above factors with atmospheric conditions and
relates well with plant response, it is difficult to measure. Several empirical models to predict
stomatal conductance have been developed for particular species (Losch and Tenhunen, 1981)
but have not been used to estimate O3 uptake or to develop exposure indices. Based on
atmospheric measurements of deposition and diurnal patterns of O3 and gas exchange in a
natural grassland ecosystem, Griinhage and Jager (1994a,b) and Griinhage et al. (1993a,b)
proposed an ambient O3 exposure potential for characterizing O3 uptake and related it to the
damaged-leaf area (DLA) of leaf No. 4 of Bel W3 tobacco (Griinhage et al., 1993a,b).
5.5.1.2 Historical Perspective on Developing Exposure Indices
For almost 70 years, air pollution specialists have explored alternative
mathematical approaches for summarizing ambient air quality information in biologically
meaningful forms that can serve as surrogates for dose for vegetation effects purposes. Some
of the indices introduced have attempted to incorporate some of the factors (directly or
indirectly) described above. Recognizing the importance of duration and peak concentrations
in conjunction with stomatal conductance, the optimum exposure index can be written as
Index =
where Q is the hourly mean concentration, f(C;) is some function of Q, and w; is some
weighting scheme that relates ambient condition and internal O3 flux. The optimal weights
are difficult to develop because of the complex relationship among exposure, environmental
condition, and species.
Equation 5-1 represents a taxonomy of exposure indices that have been proposed
as surrogates of dose in the literature. The exposure indices differ in the ways in which the
values are assigned to w;. Based on the weighting function, the exposure indices can be
arranged into the categories described below (description from Lee et al., 1989).
• One Event: w; = 0 for all C;, except for the few concentrations where w; = 1 .
Examples of such indices are the second highest daily maximum 1-h
concentration (2HDM), the maximum of 7-h (P7) and 1-h (PI) maximum daily
averages, and the 90th or higher percentiles of hourly distribution.
• Mean: w; = 0 for all Q outside the period of interest (P) and w; = v;/£i=1 " v;
for all Q inside the period P, where v; is a function of C; or some
environmental variable. Examples are the seasonal mean of 7-h daily means
(M7) (Heagle et al., 1979b); the effective mean (me), where mev is the index in
Equation 5-1 with f(C;) = C;"1/v and w; = 1 for some parameter v (Larsen and
Heck, 1984); the solar-weighted mean where v; is the hourly solar radiation
value (Rawlings et al., 1988b).
• Cumulative: w; = 1 for all C;. An example is the seasonal sum of all hourly
concentrations (i.e., total exposure, denoted as SUMOO).
• Concentration Weighting: w; = g(C;) where g() is a monotonically
nondecreasing function. Examples are the seasonal sum of hourly
concentrations at or above a threshold level such as 0.06 ppm (SUM06) or
0.08 ppm (SUM08); the seasonal sum of the difference between an hourly
concentration above a threshold level, less the threshold value, such as
0.08 ppm (AOT08); the total impact with w; = C/"1"17^ for some v (Larsen et al.,
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1983); the index with the allometric function, g(C;) = C;a, a > 0; the index with
sigmoidal weighting function, g(C;) = 1/[1 + M x exp(-AxQ)], where M =
4,403 and A = 126, denoted as W126 by Lefohn et al. (1988a), and M = 500
and A = 100, denoted SIGMOID by Lee et al. (1989); total hours with
concentrations at or above a threshold level, such as 0.08 ppm (HRS08), g(Q) =
0 for Q < 0.08 ppm and w; = 1/Q for Q > 0.08 ppm.
• Multicomponent: w; = g(C;, i). Examples are indices that incorporate several
characteristics of exposure and crop development stage, including the
phenologically weighted cumulative impact indices (Lee et al., 1987).
Oshima (1975) and Oshima et al. (1976) proposed an exposure index, where the
difference between the value above 0.10 and 0.10 ppm was summed. This is referred to as
the AOT10 exposure index with f(C;) = Q - 0.10 and w; = 0 for Q < 0.10 ppm and w; = 1
for C; > 0.10 ppm in Equation 5-1. Alternatively, Lefohn and Benedict (1982) introduced an
exposure index based on the hypothesis that, if the higher O3 concentrations had greater value
in predicting adverse effects on agricultural crops than did the lower values, then the higher
hourly mean concentrations should be given more weight than the lower values. This index
summed all hourly concentrations equal to and above a 0.10-ppm threshold level. This index
is referred to as the SUM10 exposure index, with f(Q) = Q and w; = 0 for Q < 0.10 ppm and
w; = 1 for Q > 0.10 ppm. The SUM indices are not concentration weighting but threshold
weighting, in that all concentrations at or above a threshold level have equal weight rather
than increasing weight to higher concentrations.
A 6-h, long-term, seasonal mean, O3 exposure index was used by Heagle et al.
(1974). Also, Heagle et al. (1979b) reported the use of a 7-h experimental period mean. The
7-h (0900 to 1559 hours) mean, calculated over an experimental period, was adopted as the
statistic of choice by the U.S. Environmental Protection Agency's (EPA's) NCLAN program
(Heck et al., 1982). The 7-h daily daylight period was selected by NCLAN because the index
was believed to correspond to the period of greatest plant susceptibility to O3 pollution. In
addition, the 7-h period of each day (0900 to 1559 hours) was assumed to correspond to the
time that the highest hourly O3 concentrations would occur. However, not all monitoring sites
in the United States experience their highest O3 exposures within the 0900 to 1559 hours 7-h
time period (Lefohn and Jones, 1986; Lefohn and Irving, 1988; Logan, 1989). Toward the
end of the program, NCLAN redesigned its experimental protocol and applied proportional
additions of O3 to its crops for 12-h periods. The expanded 12-h window reflected NCLAN's
desire to capture more of the daily O3 exposure. In the published literature, the majority of
NCLAN's experiments were summarized using the 7-h experimental-period average.
Based on the concept that higher concentrations of O3 should be given more
weight than lower concentrations (summarized in U.S. Environmental Protection Agency,
1986), concerns about the use of a long-term average to summarize exposures of O3 began
appearing in the literature (Lefohn and Benedict, 1982; Tingey, 1984; Lefohn, 1984; Lefohn
and Tingey, 1985; Smith et al., 1987). Specific concerns were focused on the fact that the
use of a long-term average failed to consider the impact of peak concentrations. The 7-h
seasonal mean contained all hourly concentrations between 0900 to 1559 hours; this long-term
average treated all concentrations within the fixed window in a similar manner. A large
number of hourly distributions within the 0900- to 1559-hours window could be used to
generate the same 7-h seasonal mean, ranging from those containing many peaks to those
containing none. Larsen and Heck (1984) pointed out that it was possible for two air
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sampling sites with the same daytime arithmetic mean O3 concentration to experience
different estimated crop reductions.
In the late 1980s, the focus of attention turned from the use of long-term seasonal
means to cumulative indices (i.e., exposure indices that sum the products of concentrations
multiplied by time over an exposure period). As indicated previously, the cumulative index
parameters proposed by Oshima (1975) and Lefohn and Benedict (1982) were similar. Both
parameters gave equal weight to the higher hourly concentrations but ignored the
concentrations below a subjectively defined minimum threshold (e.g., 0.10 ppm). Besides the
cumulative indices proposed by Oshima (1975), Oshima et al. (1976), and Lefohn and
Benedict (1982), other cumulative indices were suggested, including the number of
occurrences of daily maximum hourly averaged concentrations greater than a threshold level
(Ashmore, 1984) and the use of exponential functions (Nouchi and Aoki, 1979; Larsen and
Heck, 1984) to assign unequal weighting to O3 concentrations.
A possible disadvantage of applying an integrated exposure index, as defined by
Oshima (1975) and Lefohn and Benedict (1982), is that the use of an artificial threshold
concentration as a cutoff point eliminates any possible contribution of the lower
concentrations to vegetation effects. Although this disadvantage may not be important when
considering O3 exposures that occur in the California South Coast Air Basin, where repeated
high concentrations are experienced from day to day, and there are relatively short periods
between episodes, it is important when assessing the typical exposures experienced in other
parts of the United States.
Recognizing the disadvantage, Lefohn and Runeckles (1987) suggested a
modification to the Lefohn and Benedict (1982) exposure index by weighting individual
hourly mean concentrations of O3 and summing over time. Lefohn and Runeckles (1987)
proposed a sigmoidal weighting function that was used in developing a cumulative integrated
exposure index. The index included the lower concentrations in the integrated exposure
summation.
None of the exposure indices mentioned above fully characterize the potential for
plant uptake of O3 because the indices, being measures of ambient condition, ignore the
biological processes controlling the transfer of O3 from the atmosphere through the leaf and
into the leaf interior (U.S. Environmental Protection Agency, 1986, 1992). Early studies with
beans and tobacco, reviewed in the previous criteria document (U.S. Environmental Protection
Agency, 1986), showed that short-term, higher peak exposures induced more visible injury
than longer term, lower peak exposures of the same total exposure, indicating that
concentration has more value than exposure duration in eliciting a response, at least for short-
lived species. Other studies with soybean, tobacco, and bean, conducted prior to 1983 and
described in U.S. Environmental Protection Agency (1986), showed that the foliar injury
response to subsequent peak exposures varies with temporal pattern. Predisposition to low
levels of O3 for a few days increases plant sensitivity to subsequent peaks (Johnston and
Heagle, 1982; Heagle and Heck, 1974; Runeckles and Rosen, 1977). Tobacco plants exposed
to 2 consecutive days of peak exposures showed greater injury on the first day (Mukammal,
1965). Plants exposed to a series of successive short exposures suffered more injury than did
those plants that received a continuous uniform exposure, with all plants receiving equal total
exposure (Stan and Schicker, 1982).
When yield or growth are considered, "not only are concentration and time
important, but the dynamics of the O3 exposure are also important" (U.S. Environmental
Protection Agency, 1986). Musselman et al. (1983) were the first to demonstrate that plants
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exposed to variable concentrations showed greater effect on plant growth than those exposed
to a fixed or daily peak concentration of equal total exposure but lower peak concentrations.
The Hogsett et al. (1985b) study also reported a greater effect on plant growth of variable
concentrations; however, no plant response data is presented in the paper. Musselman et al.
(1986b), in a subsequent experiment, exposed kidney bean plants to either a simulated
ambient or a uniform concentration that had equal total exposure and peak concentration
(at two levels of 0.30 and 0.40 ppm) and found that the effects of the two distributions did
not differ significantly. Consequently, when peak concentrations and total exposures are
equal, the diurnal distribution of concentrations appears to be unimportant.
More recent studies with bean (Kohut et al., 1988b), soybean (Heagle et al.,
1986b), and tobacco (Heagle et al., 1987b) (reviewed in U.S. Environmental Protection
Agency, 1992) showed conflicting evidence of no significant differences in response to
different exposure patterns of equal total exposure but varying peak concentrations. The
value of peak concentrations in influencing response was inconclusive. For the study with
beans, plants exposed to peak exposures showed significant impairment in the early harvests,
but, at the final harvest, O3 effects on growth and yield were not statistically significant. For
the NCLAN studies with soybean and tobacco, differences in yield between the constant and
proportional 7-h O3-addition exposures were not significant, even though the proportional-
addition treatments had greater peak concentrations. In reanalysis of the soybean and tobacco
studies, Rawlings et al. (1988b) stated that the differences between the constant and
proportional O3 additions were relatively small, thus limiting the power of the comparison
test. However, 12-h exposures caused greater effects than 7-h exposures, but the decrease in
yield loss was not directly proportional to the increased length of exposure (Rawlings et al.,
1988b).
Considerable research since the publication of the previous criteria document (U.S.
Environmental Protection Agency, 1986) has been directed at developing measures of
exposure that were consistent with then-current knowledge of the mode of action of O3 on
plants, as well as on factors such as concentration, duration, and temporal dynamics of
exposure influencing response. A number of retrospective studies of existing data to evaluate
and compare exposure indices based on statistical fit (Rawlings et al., 1988b; Adomait et al.,
1987; Cure et al., 1986; McCool et al., 1986, 1987; Smith et al., 1987; Lee et al., 1987, 1988;
Lefohn et al., 1988a; Tingey et al., 1989; Musselman et al., 1988) have been summarized in
the literature between 1986 and 1988 and reviewed by the U.S. Environmental Protection
Agency (1992). Studies using O3 exposures in chambers suggest the following conclusions:
O3 effects are cumulative, peak concentrations may be more important than lower
concentrations in eliciting a response, and plant sensitivity to O3 varies with time of day and
crop development stage. Exposure indices that cumulate the exposure and preferentially
weight the peaks yield better statistical fits to response than do the mean and peak indices.
Because the mean exposure index treats all concentrations equally and does not
specifically include an exposure duration component, the use of a mean exposure index for
characterizing plant exposures appears to be inappropriate for relating exposure with
vegetation effects (U.S. Environmental Protection Agency, 1992). In particular, the weighting
of the hourly O3 concentrations of the mean is inconsistent with the weighting function of
plant exposure to O3 in Equation 5-1, which attempts to relate O3 flux to ambient condition.
The total exposure index includes an exposure duration component but does not adequately
relate pollutant exposure with plant response because the index weights all concentrations
equally and focuses on the lower concentrations.
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Evidence supporting the use of peak-weighted, cumulative indices in relating
O3 exposure and plant response is based on statistical reanalyses of NCLAN data. However,
it is unlikely that the empirical modeling of plant response will determine the optimal
weighting function of hourly O3 concentrations for use in characterizing plant exposure, which
varies with environmental factors and species. The development and comparison of exposure
indices based on statistical fits is difficult because only a limited number of experiments have
been designed specifically to test and evaluate the various exposure indices.
Although much research has been conducted on O3 effects on crops and trees since
1988, the overall understanding of the mode of action of O3 on plants and factors that modify
plant response remains unchanged since the previous criteria document (U.S. Environmental
Protection Agency, 1986) and its supplement (U.S. Environmental Protection Agency, 1992).
Additional studies further support the value of concentration, duration, and temporal pattern of
exposure in describing plant exposure and its relation to plant response. Studies that applied
two or more different exposure patterns of equal exposure but possibly different peak
concentrations are reviewed in Section 5.5.2.2 to substantiate the value of exposure structure
in influencing the magnitude of plant response. Recent papers that report results from
replicate studies over time and space are summarized in Section 5.5.2.3 to test the value of
duration and its relation to plant response. In addition, a few recent studies that provide
additional insight to those factors that modify plant response are reviewed in Sections 5.5.2.4
and 5.5.2.5.
5.5.2 Developing Exposure Indices
5.5.2.1 Experimental Design and Statistical Analysis
Controlled and field exposure-response studies, where extraneous factors
influencing response are controlled or monitored, allow the study of concentration, duration,
respite time, and temporal fluctuations at various stages of crop development in influencing
response. These studies provide insight on the efficacy of exposure indices in explaining
variation of response. A small number of experiments have been designed specifically to
study the components of exposure and have applied two or more different patterns of
exposure that measure the same SUMOO values. These designs provide the best evidence to
determine whether plants respond differentially to temporal variations in O3 concentrations;
however, they may have limited application in developing a statistical relationship between O3
exposure and plant response. Other design considerations, including the number, kind, and
levels of O3 exposure; the patterns of randomization; the number of replicates used in the
experiment; and experimental protocol, determine the strength of the statistical analysis that is
applied to the treatment mean comparison tests and the range of ambient and environmental
conditions over which generalizations may be made. These designs have been used
successfully to test the value of components of exposure, particularly concentration, in
influencing response (Musselman et al., 1983, 1986b, 1994; Hogsett et al., 1985b). Different
approaches that include either a mean separation procedure or a regression procedure have
been used to identify those important components of exposure that influence response.
To identify the importance of exposure in contributing to variation of plant
response, the majority of pollutant effects studies use regression-based designs that apply a
single pattern of exposure at varying concentration levels. However, if these designs are
used, the application of the results is limited; plant response (i.e., plant yield) with respect to
exposure is unchanged with different measures of exposure. The relative position and spacing
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between exposure levels is a function of how the exposure index weights the hourly O3
concentrations and governs the statistical fit to response. The regression approach has been
used to compare and evaluate various exposure indices, but the ability to discriminate among
indices is low for these studies. By their nature, those studies that have used regression-based
designs that utilize data from single patterns of exposure cannot distinguish between mean
exposure indices and sums constructed from means (i.e., mean x duration) and, consequently,
cannot be used to test the value of duration in explaining the variation of response.
Evidence to substantiate the value of duration in explaining the experimental
variation of plant response may be obtained when combining data from replicate studies of
the same species and cultivar over time and space. Pooling of data from replicate studies of
the same species to evaluate duration effects and to compare various exposure indices
assumes that the primary cause of biological response is pollutant exposure. This assumption
may or may not be valid, particularly when plants from replicate studies are grown under
varying environmental, edaphic, and agronomic conditions that tend to mask the treatment
effects during the growth of the plant (Section 5.3). Hence, it is more difficult to substantiate
the importance of exposure-dynamic factors from retrospective analyses of combined data
from replicate studies of the same species than from experiments designed specifically to
address the components of exposure. The comparison of environmental conditions, as well as
the yields of plants exposed to CF air over replicate studies, is a simple check of interaction
but does not ensure that O3 effects on response can be isolated. In addition, when the main
effect of O3 is insignificant, the data may be limited for determining the value of duration or
other components of exposure in predicting response. Nonetheless, if an air pollutant is the
primary source of variability in plant response, the relationship between exposure and
response should be consistent when data sets for the same crop are combined over several
years or locations.
Sets of replicate studies of equal and varying duration are readily available in the
published literature, but only a few reports have combined the data to test specifically the
value of duration in explaining variation of plant response or to evaluate exposure indices
based on statistical fit. Lefohn et al. (1988a) were the first to fit a common response model
to combined data from two replicate studies of varying duration using various exposure
indices. Greater yield losses occurred when plants were exposed for the longer duration,
indicating that the duration component of exposure was important in influencing response, and
that a cumulative-type index was able to describe adequately the relationship between
exposure and yield. More recent papers have reported results of the 2 years of replicate
studies, and a few papers have used the regression approach, with and without variance
components for sites and years, to evaluate various exposure indices based on the adequacy of
fit of a common response model.
A number of the papers relevant to the study of components of exposure
influencing plant response report only the mean and total exposure (SUMOO) indices.
Because exposure indices weight hourly O3 concentrations differently, it is almost impossible
to convert one index to another. The original data, which in many cases are not available,
would be necessary to generate alternative exposure indices. Therefore, unless adequate
information is given to allow calculation of exposure indices, the analysis of reported results
from individual and combined data to evaluate different exposure indices is not possible,
although it may be possible to perform retrospective evaluation of the structure of exposure in
altering plant response.
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Another concern relates to the experimental design, particularly the number, kind,
and levels of exposure used in the study. Generalization of experimental results is largely
dependent on the degree to which atmospheric and biospheric conditions mimic those of the
target population when growing under ambient conditions. However desirable the need to
mimic the real world, understanding the relationship between exposure and the ensuing
response (i.e., plant yield) and identifmg those components of exposure that influence
response may require the use of exposure regimes with temporal pattern, concentration, or
structure that are not observed in nature. Such data requires the comparison of exposure
levels between CF and near-NF conditions, but the mathematician who attempts to model an
experiment requires higher than NF levels of O3 to better determine the nature of plant
response to O3. A discussion of the advantages and disadvantages of OTCs and the types of
NCLAN exposures is discussed in the section on methodologies (Section 5.2.1.1). The
O3 exposures utilized by the NCLAN program have been described as producing artificial
regimes that do not mimic actual conditions.
In addition to the CF concentration regimes, Lefohn et al. (1988a) have reported
that the highest treatments have a tendency to display bimodal distributions that are unrealistic
(Figure 5-9). At this time, there is no evidence to suggest whether or not these higher NF
exposures provide realistic information on the impact of O3 on plant response.
Studies that utilize exposures with peak concentrations above 0.40 ppm may not
provide realistic evidence of O3 impact on plant response in the United States. These studies
provide limited evidence for substantiating the value of peak concentrations in influencing
response. Consequently, these studies are not included in this section.
5.5.2.2 Studies with Two or More Different Patterns of Exposure
Experiments using chambers that focused on the structure of exposure have shown
that plant response is differential to temporal patterns of O3 exposure. For crop species, there
is evidence to suggest that plant response is influenced more by higher concentrations than by
lower concentrations or exposure duration. Greater response to concentration occurred when
plants were predisposed to low concentrations for a few days or when peaks occurred just
prior to or at maximum leaf expansion (U.S. Environmental Protection Agency, 1978, 1986).
Plants exposed to two (or more) different exposure patterns of equal exposure (i.e., same
SUMOO value) showed greater foliar injury response to:
(1) the short-term, high-concentration exposure than to the longer term exposure
with lower peak concentrations (Heck et al., 1966; Heck and Tingey, 1971;
Bennett, 1979; Nouchi and Aoki, 1979; Amiro et al., 1984; Ashmore, 1984;
Tonneijck, 1984); and
(2) the exposure that predisposes plants to low O3 concentrations for a few days
prior to a high O3 concentration than to exposures that have a set diurnal
pattern of O3 concentrations or less than 2 days of respite time between high
concentrations (Heck and Dunning, 1967; Johnston and Heagle, 1982; Heagle
5-91
-------
150
g> 100
50
I
A. 1.4 X Ambient Ozone
I I I I I I I I I I I
50 100 150
200
\ i i i i i \
250 300
150-1
M
8
100 H
8
o
"5 50
B. 1.8 X Ambient Ozone
i I I I I I
0 50
nfl,
100
\ i i i i i i i r
150 200
250
300
800-1
600
400-
200
C. San Bernardino, CA, 1987
0 iiiiir~
0 50
flo
100
\ i i i i i r
150 200
250
300
Ozone Concentration (ppb)
Figure 5-9. Distribution pattern showing the number of ozone concentrations
within specified ranges for the 1983 winter wheat proportional-
addition experiment for the (A) 1.4 * ambient air and (B) 1.8 *
ambient air treatments and for (C) San Bernardino, CA, in 1987.
5-92
-------
and Heck, 1974; Runeckles and Rosen, 1977; Mukammal, 1965; Stan and
Schicker, 1982).
The studies that applied the same exposure but used different patterns of exposure
have been reviewed in previous criteria documents (U.S. Environmental Protection Agency,
1978, 1986, 1992) and substantiate the role of concentration, temporal dynamics, respite time,
and predisposition in influencing the magnitude of plant response to O3.
Musselman et al. (1983) and Hogsett et al. (1985b) were among the first to
demonstrate that variable concentrations produced greater effect on plant growth than did
fixed or set diurnal patterns of exposure of equal total exposure but with lower peak
concentrations (Table 5-12). Musselman et al. (1986a), in a subsequent experiment, exposed
kidney bean plants to either a variable or a uniform concentration of equal total exposure and
equal peaks (at two levels of 0.30 and 0.40 ppm) and found that the effects of the two
distributions were not significantly different (Table 5-12). Musselman et al. (1994), in a third
experiment, exposed kidney bean plants to four different patterns of equal total exposure and,
like Musselman et al. (1983), found that patterns with higher peak concentrations or longer
duration of high concentrations (>0.16 ppm) produced significantly greater effect on top dry
weight than the square wave pattern. Cumulative, peak-weighted exposure indices with an
allometric weighting parameter between 2 and 3.5 gave the best fit for dry weight, necrosis,
and number of pods. These results provide evidence that: total exposure (i.e., SUMOO),
being unable to differentiate among the exposure patterns, is a poor predictor of plant
response; the peak concentrations or sequence of peak concentrations (>0.16 ppm) are
important in determining plant response; and greater weight should be given to higher
concentrations when describing exposure. Consequently, when peak concentration and total
exposure are equal, the diurnal distribution of concentrations (e.g., sequence of peak
concentrations >0.16 ppm) may be an important factor.
One recent study exposed bean plants to two consecutive exposures of 0.30 ppm
for 3 h/day in the rapid vegetative growth stage and showed greater reductions in total dry
weight when exposures were 3 to 6 days apart (McCool et al., 1988) (Table 5-12); this
finding is consistent with earlier results on the role of predisposition in influencing response
(e.g., Hogsett et al., 1988). Predisposition to a high concentration above the level that causes
visible injury may increase plant sensitivity over time (Mukammal, 1965). As a result, the
subsequent response to a high concentration following recovery may be greater than
experienced in prior exposures. In future modeling efforts, this phenomenon may have to be
taken into consideration, by the weighting of hourly concentrations, for properly
characterizing plant exposure.
Sensitivity of plants to O3 is a function of stomatal conductance and varies with
the cultivar, time of day, and phenology. To test the role of phenology, Heagle et al. (1991b)
applied 16 patterns of exposure in combinations of either CF or NF air for each quarter of the
experimental period (31 days/quarter) (Table 5-12). The authors concluded that the
phenological stage of development played a role in plant response, and that exposures during mid-
to late-growth stages caused greater yield losses than did exposures during earlier
developmental stages. For crops, foliage appears to be most sensitive to O3 just prior to or
during maximum leaf expansion (U.S. Environmental Protection Agency, 1978). These
results are consistent with earlier studies (Lee et al., 1987) that reported better statistical fits
to response using exposure indices that preferentially weighted hourly O3 concentrations
during the period of anthesis to seed fill.
5-93
-------
Table 5-12. A Summary of Studies Reporting the Effects of Ozone for Two or More
Exposure Patterns on the Growth, Productivity, or Yield of Plants3
Species
Glycine max L.
Merrill cv. Davis,
Forrest, Bragg,
and Ransom
Medicago sativa L.
Phaseolus vulgaris
L.
cv. Calif. Dark
Red Kidney Bean
i Phaseolus vulgaris
CD T
j^ L.
cv. Calif. Dark
Red Kidney Bean
Phaseolus vulgaris
L.
cv. Calif. Dark Red
Kidney Bean
Phaseolus vulgaris
L.
cv. Calif. Dark
Red Kidney Bean
Facility11
OTC in
pots
OTC in
pots
GC in
pots
GC in
pots
GCin
pots
GCin
pots
Total Number
of Chambers Exposure Patterns0
24 16 combinations of CF
or NF + over 4 quarters
(3 1 -days/quarter)
8 E, DP
8 U, V
8 U, V
8 Square wave (SW),
Triangular (T),
Flattened triangular (FT),
Rhomboid (R)
10 Initial exposure of 0.3 ppm
for 3-h and second exposure
of 0.3 ppm at 2-6 (or 1-5)
days after initial exposure
Exposure
Duration
124 days
133 days
3 weeks
(1 day/
week)
3 weeks
(1 day/
week)
7 weeks
(3 days/
week)
2-6 days
in 1984
and
1-5 days
in 1985
Concentration (ppmyExposure11
(ppm-h)
M7 (ppm): CF range from 0.016 to
0.038 over the 4 quarters, NF+range
from 0.096 to 0.098 over the
4 quarters
Equal SUM07 (ppm-h): DPH=113,
DPL=63, EH=117, EL=72
Equal SUMOO (ppm-h): DPH=183,
DPL=140, EH=193, EL=145
M7 (ppm): DPH=0.099, DPL=0.074,
EH=0.084, EL=0.064
Equal SUMOO (ppm-h/day):
UL=VL=0.69; UH=VH=0.92
Equal Max concentration (ppm):
UL=VL=0.30, UH=VH=0.40
Equal SUMOO (ppm-h/day):
UL=VL=1.20; UH=VH=1.68
Max concentration, (ppm): UL=0.20,
VL=0.50,UH=0.28, VH=0.715
Equal SUMOO (ppm-h/day):
Variable
Total
seed
weight
Shoot
dry
weight
Pod and
seed dry
weights
Pod and
seed dry
weights
Top dry
SW=T=FT=R=0.60. Max concentrationweight
(ppm): SW=0.12, T=0.36,
FT=R=0.24.
Equal maximum concentration of
0.30 ppm.
Total dry
weight
Effect'
Forrest: greater effect in Q3 than in other
quarters. Davis: no consistent effect Ql,
significant but similar effects for Q2, Q3, and
Q4. Ransom: no significant O3 effects in Ql
or Q2, and equal responses in Ql, Q3, and Q4.
Bragg: no significant O3 effects in Ql or Q2,
significant decreases in Q3 and Q4.
91 and 67% reductions for EH and DPH.
Significant difference between E and
DP regimes. Treatment means are ordered
CF
-------
There is very limited information on the effect of O3 on mature trees. Most of the
information available deals with the nature of seedling response to O3 (see Section 5.6.4);
however, much less is known about the role of exposure-dynamic factors (e.g., concentration,
duration, respite time, temporal variation) in influencing biomass response in long-lived
species.
When yield is considered, a number of exposure-dynamic factors, including
concentration, temporal pattern, predisposition, and respite times, as well as phenological
stage of plant development, have been shown to influence the impact of O3 on plant response.
Evidence from studies of kidney bean (Musselman et al., 1983, 1994), alfalfa (Hogsett et al.,
1985b), tobacco (Heagle et al., 1987b), soybean (Heagle et al., 1986b), ponderosa pine, and
aspen suggests that concentration and temporal variation of exposure are important factors in
influencing biomass production and, consequently, become considerations in measures of
exposure. Because the SUMOO index weights all concentrations equally, the SUMOO is
inadequate for characterizing plant exposure to O3 (Lefohn et al., 1989). Other factors,
including predisposition time (McCool et al., 1988) and crop development stage (Heagle
et al., 1991b), contribute to variations in biological response, which suggests the need for
weighting O3 concentrations to account for predisposition time and phenology. However, the
roles of predisposition and phenology in influencing plant response vary with species and
environmental conditions and are not understood well enough to allow specification of a
weighting function for use in characterizing plant exposure.
5.5.2.3 Combinations of Years, Sites, or Species: Comparisons of Yield Losses
with Different Exposure Durations
Duration has not been a focus in experimental designs of studies that applied two
or more exposure regimes over the growing season. Several lines of evidence suggest that the
ultimate yield depends on the cumulative impact of repeated peak concentrations (U.S.
Environmental Protection Agency, 1986, 1992), and that O3-induced reductions in growth are
linked to reduced photosynthesis, which is impaired by the cumulative O3 exposure (Reich
and Amundsen, 1985; Reich, 1987; Pye, 1988). In EPA reviews of the literature (U.S.
Environmental Protection Agency, 1986, 1992), EPA concluded that "When plant yield is
considered, the ultimate impact of an air pollutant on yield depends on the integrated impact
of the pollutant exposures during the growth of the plant." As a measure of plant exposure,
the appropriate index should differentiate between exposures of the same concentration but of
different duration. For example, a mean index calculated over an unspecified time cannot
accomplish this (Lefohn et al., 1988a; Hogsett et al., 1988; Tingey et al., 1989, 1991; U.S.
Environmental Protection Agency, 1986, 1992).
The paper by Lefohn et al. (1988a), reviewed previously in U.S. Environmental
Protection Agency (1992), along with published criticisms and responses, was the first to fit a
common response model to combined data from two replicate studies of unequal duration (71
and 36 days for the 1982 and 1983 wheat studies, respectively, conducted at Ithaca, NY) to
test specifically for the importance of duration in influencing plant response. Greater yield
losses occurred in 1982, which can be attributed partially to the longer duration. Because the
mean index ignores the length of the exposure period, the year-to-year variation in plant
response was minimized by the use of several cumulative indices rather than the mean.
Lefohn (1988) and Lefohn et al. (1988b) concluded that duration has value in explaining
variation in plant response, and that a cumulative-type index was preferred over a mean or
peak index based on statistical fit.
5-95
-------
When O3 effects are the primary cause of variation in plant response, plants from
replicate studies of varying duration showed greater reductions in yield or growth when
exposed for the longer duration (Lee et al., 1991; Olszyk et al., 1993; Adaros et al., 1991a)
(Table 5-13, Part A). Using NCLAN data for wheat, cotton, kidney bean, and potato from
replicate studies with markedly different exposure durations, Lee et al. (1991) showed that
year-to-year variations in the magnitude of relative yield loss were minimized by the use of
exposure indices that are cumulative and weight peak concentrations more than low
concentrations, indicating that O3 effects are cumulative (Figure 5-10). Olszyk et al. (1993),
using the two NCLAN cotton studies summarized by Temple et al. (1985) and Lee et al.
(1991), in addition to cotton studies replicated at four sites in California's San Joaquin Valley
over 2 years, tested and compared various exposure indices (SIGMOID, SUM06, M7, and
2HDM) based on statistical fit of a common response model. A Weibull response model with
variance components was fit to the combined data and used to test for a common response
(Gumpertz and Rawlings, 1991, 1992; Gumpertz and Pantula, 1992). The likelihood ratio test
of parallel exposure-response curves was statistically significant for M7 and 2HDM for at
least one set of cotton data, indicating significant differences in the magnitude of response
across years or sites. On the other hand, the SIGMOID and SUM06 indices resulted in
consistent patterns of response for both sets of cotton data, as well as between sets of cotton
data (Figure 5-11). The authors concluded that the peak-weighted, cumulative indices
minimized the temporal and spatial variations in crop yield and better predicted cotton yield
responses than the M7 or 2HDM indices. The mean and peak indices did not differentiate
between exposure seasons of differing duration and could not account for year-to-year
differences in response.
The results of European studies with wheat (Adaros et al., 1991a,c), spring rape
(Adaros et al., 1991b), barley (Adaros et al., 1991c), and kidney beans (Bender et al., 1990),
using data from replicate studies with varying duration, are less conclusive as to the role of
duration in determining plant response (Table 5-13, Part A). Exposures are reported using a
mean index. Adaros et al. (199la) showed a greater reduction in above-ground dry weight
when exposed for the longer duration for the wheat cultivar Star but not for the cultivar
Turbo (Figure 5-12). Adaros et al. (1991c), in another 2-year study with barley (cv. Arena
and Alexis) and wheat (cv. Star and Turbo), involving mixtures of O3, SO2, and NO2, showed
greater reductions in yield when exposed for the longer duration for all species and cultivars
except barley cv. Alexis (Table 5-13, Part A). Ozone effects were insignificant in both years
for barley cv. Alexis. The authors did not attribute the differential response in growth and
yield to any single factor, but the data suggested that O3 effects are cumulative. When
O3 exposure is the primary source of response, the mean exposure index of unspecified
duration could not account for the year-to-year variation in response.
The role of duration in influencing growth or yield is unclear for the other studies
because of the following limitations in the data:
(1) Treatment levels were below the levels necessary to induce injury or damage
to kidney bean plants in 2 of the 3 years. None of the years produced a
significant O3 effect at or below 70 ppb concentration (Bender et al., 1990).
Similarly, the study with barley showed no significant O3 effects.
5-96
-------
Table 5-13. A Summary of Studies Reporting the Effects of Ozone on the Growth, Productivity,
or Yield of Plants for Two or More Replicate Studies Having Equal Total
Exposures and Either Varying Durations (Part A) or Similar Durations (Part B)a
Oi
cb
Species
Total No.
Facility11 of Plots
Duration
[dates and (days)]
Concentration (ppm)/ Exposure (ppm-h)°
Variable
Effect"1
Reference
PART A
Brassica OTC
napus L. in pots
var. Napus
cv. Callypso
Gossypium OTC
hirsutum L.
cv. Acala SJ2
Hordeum OTC
vulgare L. in pots
cf. Arena
and Alexis
Phaseoulus OTC
vulgaris L.
cv. Calif. Dark
Red Kidney
Bean
Phaseolus
vulgaris L.
cf. Rintintin
Solarium
tuberosum L.
cv. Norchip
Triticum
aestivum L.
cv. Vona
OTC
in pots
OTC
OTC
1987: 18 1987: 05-13 to 08-10 (89)
1988: 24 1988: 05-02 to 08-24 (113)
1989: 16 1989: 05-08 to 08-01 (84)
1981: 12 1981: 07-06 to 09-15 (72)
1982: 12 1982: 06-04 to 09-09 (98)
1988: 24 1988: 04-29 to 08-15 (108)
1989: 16 1989: 05-08 to 08-15 (99)
1980: 20 1980: 08-20 to 09-10 (22)
1982: 20 1982: 08-11 to 10-06 (57)
19881:4 1988 I: 06-15 to 08-04(51)
1988 II: 6 1988 II: 07-24 to 08-29 (37)
1989 III: 8 1989 III: 06-04 to 07-25 (52)
1985: 15 1985: 06-14 to 08-22 (70)
1986: 39 1986: 06-20 to 08-20 (62)
1982: 20 1982: 05-18 to 07-17 (61)
1983: 12 1983: 06-12 to 07-17 (36)
1987: M24 (M8) in ppb range from 5 (9) to 16 (43). Seed
1988: M24 (M8) in ppb range from 3 (5) to 16 (48). dry
1989: M24 (M8) in ppb range from 6 (5) to 22 (62). weight
1981: M7 (SUM06) range from 18 ppb (0 ppm-h) to 138Lint
(68). dry
1982: M7 (SUM06) range from 12 ppb (0 ppm-h) to 111 weight
(71).
1988: M8 (max 8-h mean) in ppb range from 5 (15) Seed
to 48 (89). dry
1989: M8 (max 8-h mean) in ppb range from 11 (27) weight
to 62 (101).
1980: M7 (SUM06) range from 24 ppb (0 ppm-h) to 139 Seed
(19). dry
1982: M7 (SUM06) range from 19 ppb (0 ppm-h) to 110 weight
(40).
I. M8 (max) in ppb range from 3 (19) to 48 (70). Pod
II. M8 (max) in ppb range from 2 (19) to 50 (105). dry
III. M8 (max) in ppb range from 6 (26) to 109 (159). weight
1985: M7 (SUM06) range from 22 ppb (0 ppm-h) to Tuber
85 (47). weight
1986: M7 (SUM06) range from 24 ppb (0 ppm-h) to
88 (38).
1982: M7 (SUM06) range from 21 ppb (0 ppm-h) Seed
to 95 (41). dry
1983: M7 (SUM06) range from 26 ppb (0 ppm-h) weight
to 96 (22).
1987: 27% reduction at M8 = 43 ppb (***). Adaros et al.
1988: 18% reduction at M8 = 48 ppb (***). (1991b)
1989: 11% reduction at M8 = 62 ppb (***).
45 and 66% reductions at M7 =111 ppb. Lee et al.
57 and 60% reductions at SUM06 = (1991),
68 ppm-h. Olszyk et al.
(1993)
Arena: 14% (*) and 6% (NS) reductions at Adaros et al.
M8 = 48 ppb. (1991c)
Alexis: No reductions at M8 = 48 ppb (NS).
13 and 59% reductions at M7 = 110 ppb. Lee et al.
28 and 8% reductions at SUM06 = (1991)
19 ppm-h.
I. 2% reduction at M8 = 48 ppb (NS). Bender et al.
II. 0% reduction at M8 = 50 ppb (NS). (1990)
III. 0% (NS) and 47% (*) reductions at
M8 = 50 and 109 ppb.
42 and 25% reductions at M7 = 85 ppb. Lee et al.
32 and 27% reductions at 12-h SUM06 = (1991)
38 ppm-h.
74 and 49% reductions at M7 = 95 ppb. Lefohn et al.
49 and 62% reductions at SUM08 = (1988a),
21 ppm-h. Lee et al.
55 and 60% reductions at 7-h SUM06 = (1991)
22 ppm-h.
-------
Table 5-13 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth, Productivity,
or Yield of Plants for Two or More Replicate Studies Having Equal Total
Exposures and Either Varying Durations (Part A) or Similar Durations (Part B)a
Species
Total No. Duration
Facility11 of Plots [dates and (days)]
Concentration (ppm)/ Exposure (ppm-h)°
Variable
Effect"1
Reference
PART A (cont'd)
Triticum OTC
aestivum L. in pots
cv. Star
and Turbo
1988:6 1988: 04-27 to 08-23 (118) 1988: M8 (max,SUM06) in ppb range from
1989: 10 1989: 05-09 to 08-15 (98) 4 (58,0) to 51 (106,8.2).
1989: M8 (max,SUM06) in ppb range from
10 (34,0) to 113 (162,87).
Seed Star: 20% (*) and 9% (NS) reductions at Adaros et al.
dry M8 = 51 ppb. (1991a)
weight Turbo: 25% (*) and 31% (*) reductions at
M8 = 51 ppb.
Triticum
aestivum L.,
cv. Star
and Turbo
PART B
Glycine max L.
Merr. cv. Davis
01
CD Glycine max L.
00 Merr.
cv. Williams
Medicago
sativa L.
cv. WL-514
Pinus rigida
Mill.
Pinus taeda L.
OTC 1988: 24
in pots 1989: 16
OTC 1977: 8
in pots 1978: 8
OTC 1981: 31
1982: 31
1983: 31
OTC 1984: 30
1985: 30
OTC Exp. 1: 4
in pots Exp. 2: 4
GC 1986: 15
in pots 1987: 15
1988:
1989:
1977:
1978:
1981:
1982:
1983:
1984:
1985:
Exp.
Exp.
1986:
1987:
: 04-29 to
08-15
: 05-08 to 08-15
: 06-17 to
: 06-28 to
: 07-20 to
: 07-14 to
: 07-23 to
: 03-16 to
: 03-23 to
10-10
10-21
09-22
09-22
09-23
10-10
10-09
(108)
(99)
(116)
(116)
(65)
(71)
(63)
(209)
(201)
1: 13 weeks
2: 13 weeks
: 09-15 to
: 07-27 to
12-04
10-15
(81)
(81)
1988: M8 (max 8-h mean) in ppb range from
5 (15) to 48 (89).
1989: M8 (max 8-h mean) in ppb range from
11 (27) to 62 (101).
1977: M7 (max) in ppb range from 27 (78) to
154 (277).
1978: M7 (max) in ppb range from 28 (84) to
131 (241).
1981: M7 in ppb range from 15 to 64.
1982: M7 in ppb range from 17 to 99.
1983: M7 in ppb range from 19 to 132.
1984: M12 in ppb range from 16 to 109.
1985: M12 in ppb range from 10 to 94.
1: M8 in ppb range from 0 to 200 (U).
2: M8 in ppb range from 0 to 200 (U).
1986: SUMOO in ppm-h range from 0 to 99 (U).
1987: SUMOO in ppm-h range from 0 to 99 (U).
Seed
dry
weight
Seed
dry
weight
Bean
dry
weight
Top dry
weight
Total
dry
weight
Total
dry
weight
Star: 26% (*) and 12% (*) reductions at M8 = 48 Adaros et al.
ppb.
(1991c)
Turbo: 34% (*) and 17% (*) reductions at
M8 = 48 ppb.
47 and 37% reductions at M7 = 131
ppb.
28, 20, and 32% reductions at M7 = 64 ppb.
43 and 41% reductions at M7 = 99 ppb in
1982 and 1983
29% (*) and 25% (*) reductions at
M12 = 94 ppb.
49 and 46% reductions at M8 = 200
43 and 28% reductions at SUMOO =
averaged across all families.
Individual families show similar
ppb.
99 ppm-h
Cure et al.
(1986),
Heagle et al.
(1983a)
Heggestad and
Lesser (1990),
Heggestad et al.
(1988)
Temple et al.
(1988a)
Schier et al.
(1990)
Shafer et al.
(1993)
reductions (e.g., 35 and 33% reductions at
SUMOO = 99 ppm-h for family 5.56,
14 and 12%
reductions at SUMOO = 99 ppm-h for family
1.68).
-------
Table 5-13 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth, Productivity,
or Yield Of Plants for Two or More Replicate Studies Having Equal Total
Exposures and Either Varying Durations (Part A) or Similar Durations (Part B)a
Species
Facility11
Total No.
of Plots
Duration
[dates and days]
Concentration (ppm)/ Exposure (ppm-h)°
Variable
Effect"1
Reference
cb
CD
PART B (cont'd)
Picea mbens OTC
Sarg. in pots
Pisum sativum L. ZAPS
cv. Puget
Populus
tremuloides
Michx clones
Triticum
aestivum L.
cv. Albis
Triticum
aestivum L.
cv. Albis
Triticum
aestivum L.
cv. Severn,
Potomac, Oasis,
MD5518308
OTC
in pots
OTC
1987: 12 1987: 05-30 to 12-15 (199) 1987: SUMOO in ppm-h are 32, 61, 91, and 119. Total
1988: 12 1988: 06-01 to 12-01 (184) 1987: SUMOO in ppm-h are 36, 70, 101, and 135. dry
weight
1986: 14 1986: last 58 days
1987: 14 1986: last 52 days
1988: 18 1988: 07-19 to 09-27 (71)
1989: 18 1989: 07-20 to 09-20 (64)
1986: 12 1986: 05-06 to 07-31 (86)
1987: 16 1987: 04-27 to 08-10 (92)
1988: 16 1988: 05-04 to 08-01 (89)
OTC 1989: 24 1989: 05-16 to 08-14 (91)
1990: 24 1990: 05-14 to 08-09 (88)
OTC 1984: 20 1984: 05-14 to 06-22 (40)
1985: 20 1985: 05-06 to 06-15 (41)
M12 and D25 (numbers of days with 1-h Pea
concentrations >25 ppb) used in simple linear fresh
regression. weight
1988: SUMOO in ppm-h are 5.0, 10.0, and Stem
19.4 (U). and leaf
1989: SUMOO in ppm-h are 7.7, 15.4, and dry
26.4 (U). weights
1986: M24 (max) in ppb range from 12 (61) to Seed
47 (181). dry weight
1987: M24 (max) in ppb range from 12 (54) to
45 (175).
1988: M24 (max) in ppb range from 17 (65) to
45 (148).
1989: M7 (SUM06) range from 18 ppb (0 ppm-h) Seed dry
to 62 (3.8). weight
1990: M7 (SUM06) range from 17 ppb (0 ppm-h)
to 71 (5.6).
1984: M4 (AOT03) in ppb (ppb-h) range from Seed dry
32 (0) to 93 (10). weight
1985: M4 (AOT03) in ppb (ppb-h) range from
30 (0) to 86 (9).
0% (NS) reduction in biomass after first year, Alscher et al.
8% (*) reduction at SUMOO = 135 ppm-h (1989)
after second year of exposure. Amundson et al.
(1991)
0% reductions at M12 = 100 ppb Runeckles et al.
based on linear regression models. (1990)
36% (*) and 40% (*) reductions at Karnosky et al.
SUMOO = 19.4 ppm-h. (1992b)
1986: 61% reduction at M24 = 47 ppb. Fuhrer et al.
1987: 27% reduction at M24 = 45 ppb. (1989)
1988: 65% reduction at M24 = 45 ppb.
29 and 22% reduction at M7 = 62 ppb. Fuhrer et al.
29 and 17% reduction at SUM06 = (1992)
3.8 ppm-h.
31% (*) and 9% (NS) reductions at Slaughter et al.
M4 = 86 ppb. (1989)
"See Appendix A for abbreviations and acronyms.
bGC = Controlled environmental growth chamber, or CSTR; OTC = open-top chamber; ZAPS = zonal air pollution system.
°U = Uniform.
d* = Significant at the 0.05 level; NS = not significant.
-------
1,000i
Cotton
Wheat
M7 (ppm)
20 40 60
SUM06 (ppm-h)
M7 (ppm)
20 40
SUM06 (ppm-h)
Kidney Bean
Potato
0.05 0.10 0.15 0 20 40
M7 (ppm) SUM06 (ppm-h)
0.03 0.06 0.09
M7 (ppm)
0 20 40
SUM06 (ppm-h)
Figure 5-10.
Comparison of the Weibull exposure-response functions and its
predicted relative yield loss (PRYL) curves (relative to 0 ozone)
using M7 and daytime SUM06 for replicate years of National Crop
Loss Assessment Network Program's data for (A) and (B) cotton
(var. Acala SJ-2), (C) and (D) wheat (var. Vona), (E) and (F) kidney
bean (var. California light red), and (G) and (H) potato (var. Norchip),
respectively. Mean dry weights and the Weibull exposure-response
functions for replicate studies are given in the top portion of the
graphs (Lee et al., 1991).
5-100
-------
10 20 30 40
SIGMOID (ppm-h)
50
B
0.10 0
0.1
2HDM (ppm)
0.2
10 20 30 40 50
SUM06 (ppm-h)
Figure 5-11. Predicted relative yield losses (lint weight) for Acala SJ-2 cotton for four sites
and multiple years (1981, 1982, 1988, and 1989) relative to 0.01 ppm for M7,
0.035 ppm for 2HDM, 0 ppm-h for SIGMOID, and 0 ppm-h for SUM06,
which correspond to typical levels in the charcoal-filtered chambers.
Predicted losses are based on M7 (A), 2HDM (B), SIGMOID (C), and
SUM06 (D) exposure indices. Abbreviations: DI = Dinuba, FP = Five
Point, HA = Hanford, and SH = Shafter (Olszyk et al, 1993).
5-101
-------
120
90
•? 60
30
Star
Total Biomass
1988
1989
Grain Yield
1988
1989
I
I
Turbo
0.015 0.03 0 0.015
Ozone Concentration (ppm)
0.03
0.045
Figure 5-12. Relative effect of ozone on growth and yield of spring wheat cultivars (var.
Star and Turbo) from two growing seasons (Adaros et al, 199la).
(2) Differences in growing conditions and varying kinds of interactions among O3,
SO2, and NO2 resulted in different sizes of control plants of spring rape over
years and affected the magnitude of response to O3. Compared to 1987, yield
of control plants increased by 32% in 1988 and by 94% in 1989 (Adaros
et al., 1991b). Consequently, the evidence of duration as the primary cause of
differences in response over years was difficult to substantiate.
When durations were nearly equal, plant response to O3 were similar for 2- or
3-year studies with alfalfa (Temple et al., 1988a), pea (Runeckles et al., 1990), soybean
(Heagle et al., 1983a; Heggestad and Lesser, 1990; Cure et al., 1986), wheat (Fuhrer et al.,
1989, 1992), aspen clones (Karnosky et al., 1992b), loblolly pine (Shafer et al., 1993), and
pitch pine (Schier et al., 1990) (Table 5-13, Part B). For example, year-to-year variations in
wheat yield response to O3 were small for the 3 years having durations between 86 and
92 days, allowing pooling of the data to fit a common Weibull model using Rawling's
solar-radiation-weighted mean index (Fuhrer et al., 1989) (Figure 5-13). Different growing
conditions were reported in studies of Shafer et al. (1993), Fuhrer et al. (1989), but no
5-102
-------
1.2
1.0
0.8
0.6
0.2
0.00 0.02 0.04 0.06 0.08 0.10 0.12
Mean Weighted Ozone Concentration (ppm)
Figure 5-13.
Weibull exposure-response curves for the relative effect of ozone
on grain yield of spring wheat for 3 years, individually and
combined (Fuhrer et al., 1989).
interaction between O3 and climatic effects was found. On the other hand, Slaughter et al.
(1989) reported reductions in wheat grain yield of 69 and 9% in a 2-year study having equal
exposure durations, which the authors attribute to differences in rainfall and temperature.
Environmental conditions in 1985 favored greater photosynthate partitioning for grain
development rather than for vegetative growth, resulting in larger plants in 1985. Air
pollution effects may not have been the primary source of variation in response, and,
consequently, the data do not substantiate the role of duration in influencing response.
These studies report plant response as a function of a mean exposure index and do
not evaluate or compare various exposure indices, based on statistical fit. In a series of
papers that examined the response of spring wheat to O3 at higher elevations, Grandjean
Grimm and Fuhrer (1992a,b) and Fuhrer et al. (1992) conducted a 2-year study in which the
flux of O3 was determined in OTCs. Plants were exposed to O3 for periods lasting 44 and
50 days in 1989 and 1990, respectively, and flux measurements were taken repeatedly over
the experimental period. In addition to O3 flux, exposures were characterized using M7, M24,
SUM06, and the solar-radiation-weighted mean index (Rawlings et al., 1988b). The quadratic
response curves relating the various indices with grain yield showed that year-to-year
variations were minimized using the mean O3 flux index (Figure 5-14). The other three
exposure indices showed slightly greater yield losses in 1989 than in 1990, in contrast with
longer exposure in 1990 and drier conditions in 1989. The authors concluded that the O3 flux
related well with yield because the mean flux incorporated environmental factors, canopy
structure, and physiological processes, which affected the uptake of O3 from the air to the leaf
interior. The measurements of pollutant concentrations ignored these factors and,
5-103
-------
consequently, were unable to account for all of the year-to-year variability in wheat response.
The authors suggested that O3 flux was a surrogate of Fowler and Cape's
5-104
-------
1.2
1.0
0.8
0.6
04
0.2
1.2
1.0
0.8
0.6
04
0.2
0
1.2
1.0
0.8
0.6
0.4
0.2
0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.08 0.09 .S>
7 h day"1 (ppm)
.i
0.01 0.02 0.03 0.04 0.05 0.06 0.07
SUM06 (ppm-h)
0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.080.09
Radiation-Weighted Mean (ppm)
1.2
1.0
0.8
0.6
0.4
0.2
0
20 40 60 80 100
Ozone Flux (\ig m"2min"1)
120
Figure 5-14.
Quadratic exposure-response curves for the relative effect of ozone
on grain yield of spring wheat in 1989 and 1990, using four different
exposure indices (A through D).
Source: Modified from Fuhrer et al. (1992).
(1982) "pollutant absorbed dose" and appeared to be the relevant measure for use in relating
exposure and plant response.
Alscher et al. (1989) and Amundson et al. (1991) report on the impact of O3 on
growth, injury, and biomass response of 2-year-old red spruce seedlings after 1 and 2 years of
exposure, respectively. Exposures were characterized using the M12 (or M7), M24, and
SUMOO indices. No significant O3 effects on biomass were detected in 1987 (Alscher et al.,
1989) because stomatal conductances in red spruce are inherently low and, consequently,
result in low rates of pollutant uptake (Seller and Cazell, 1990). However, in the second
year, O3 reduced leaf and root starch, increased foliar antioxidant content, and reduced
biomass of 1988 fixed-growth foliage. However, O3 effects on biomass were slight in the
second year. The authors concluded O3 effects are cumulative because the onset of damage
occurred in the second year rather than the first year of exposure.
Plant response is influenced by exposure duration and O3 concentration.
Regardless of whether concentrations are above or below levels at which injury has been
observed, plant responses are determined by the cumulative effects of the number of times
exposures have occurred. The results of these studies are in general agreement that O3 effects
are cumulative, and the ultimate impact of long-term exposures to O3 on crops and seedling
biomass response depends on the integration of repeated peak concentrations during the
growth of the plant. Consequently, the mean or peak indices are inappropriate because the
length of exposure is unspecified, and these indices cannot differentiate among exposures of
5-105
-------
the same concentration but of various durations. These results support the conclusion that an
appropriate O3 index should cumulate all hourly concentrations in some fashion to reflect the
nature of O3 on plant response. Fuhrer et al. (1992) suggested that the weighting function
should reflect the relationship between ambient pollutant concentration and internal O3 flux,
consistent with the mode of action of O3 on plants and with earlier findings that
peak-weighted, cumulative indices give better predictions of plant response than mean or peak
indices.
5.5.2.4 Comparisons of Measures of Exposure Based on Reanalysis of Single-
Year, Single-Species Studies
Studies cited in previous sections focused on the role of the structure of exposure
in influencing plant response but do not identify specifically the weighting function for use in
characterizing plant exposure to O3. In addition to these types of studies, other studies have
focused on comparison of measures of exposure based on reanalysis of single-year,
single-species studies. The variety of statistical approaches used to relate exposure and plant
response range from informal description of the distributions of O3 concentrations associated
with response to more formal regression-based procedures.
The regression approach is designed to select those exposure indices that properly
order and space the treatment means along the horizontal axis to optimize the fit of a linear or
curvilinear model. However, because the experimental designs are not intended to evaluate
various indices, the power of the regression approach to identify the important exposure-
dynamic factors influencing plant response is less desirable (Lefohn et al., 1992a).
Consequently, these retrospective studies provide less substantiating evidence of the role of
exposure-dynamic factors (e.g., concentration, duration, temporal pattern, respite time) than do
those studies with experimental designs and analyses that focus on specific components of
exposure.
Most of the early retrospective studies reporting regression results using data from
the NCLAN program or from Corvallis, OR (Lee et al., 1987, 1988; Lefohn et al., 1988a;
Tingey et al., 1989), or using data collected by Oshima (U.S. Environmental Protection
Agency, 1986; Musselman et al., 1988) were in general agreement and consistently favored
the use of cumulative peak-weighted exposure indices. These studies have been reviewed
previously by EPA (U.S. Environmental Protection Agency, 1992). Lee et al. (1987)
suggested that exposure indices that included all the data (24 h) performed better than those
that used only 7 h of data; this is consistent with the conclusions of Heagle et al. (1987b) that
plants receiving exposures for an additional 5 h/day showed 10% greater yield loss than those
exposed for 7-h/day. In a subsequent analysis using more of the NCLAN data, Lee et al.
(1988) found the "best" exposure index was a general phenologically weighted,
cumulative-impact index, with sigmoid weighting on concentration and a gamma weighting
function as surrogate of time of increased plant sensitivity to O3. For most cases, Lee et al.
(1987) computed their exposure indices based on the daylight exposure periods used by the
NCLAN investigators. The exposure indices with minimum residual sum of squares were
those indices that cumulated hourly O3 concentrations over the growth of the plant, gave
preferential weighting to peak concentrations, and phenologically weighted the exposures to
emphasize concentrations during the plant growth stage. The paper by Tingey et al. (1989) is
a summarization of the results in Lee et al. (1988) and shows the limitations of the mean
index.
5-106
-------
Lefohn and Foley (1992) characterized the NCLAN exposures that had a SUM06 level closest to those
that predicted a 20% yield loss, using the exposure-response equations as reported in Lee et al. (1991) and Tingey
et al. (1991). Lefohn and Foley (1992) characterized the hourly average concentrations using percentiles, HRS06,
HRS10, SUM06, and W126 for each of 22 NCLAN studies. The authors noted that the frequent occurrence, in many
cases, of high hourly concentrations (>0.10 ppm) may have been partly responsible for the 20% yield loss. The
number of hourly average concentrations ranged from 0 to 515 with only one of the 22 NCLAN experiments
experiencing no hourly average concentrations >0.10 ppm, whereas the remaining experiments experienced multiple
occurrences >0.10 ppm. The repeated occurrences of high hourly average concentrations were a result of the NCLAN
protocol (Table 5-14). As a result of their analysis, Lefohn and Foley (1992) and Lefohn et al. (1992b) stressed that,
because the NCLAN experiments contained peak hourly average concentrations, it is important that any index selected
to characterize those regimes responsible for growth reduction adequately capture the presence of these peak
concentrations when attempting to predict biological responses using actual ambient air quality data.
For example, Tingey et al. (1991), using mostly NCLAN data, identified 24.4 ppm-h as the SUM06
value, calculated over a 3-mo period, that would protect 50% of the NCLAN crops analyzed at the 10% yield
reduction level. These predicted relative yield loss (PRYL) calculations assume that the crops being protected will be
grown using NCLAN protocol. There are monitoring sites in the United States that experience 3-mo cumulative
SUM06 values greater than 24.4 ppm-h, but do not experience frequent occurrences of hourly average concentrations
>0.10 ppm. For example, 24% (1987), 10% (1988), 30% (1989), 25% (1990), and 31% (1991) of the rural
agricultural sites listed in the EPA Aerometric Information Retrieval System (AIRS) database experienced 3-mo
cumulative SUM06 values greater than 24.4 ppm-h but experienced fewer than 11 hourly average concentrations equal
to or greater than 0.10 ppm. Lefohn and Foley (1992) noted that agricultural crops grown at a site experiencing a 3-
mo cumulative SUM06 value greater than 24.4 ppm-h, but with infrequent high hourly average concentrations (e.g.,
>0.10 ppm), might experience less yield reduction than predicted using NCLAN experimental results. For rural forest
sites, 21% (1987), 23% (1988), 54% (1989), 50% (1990), and 52% (1991) of the sites exhibited 3-mo cumulative
SUM06 values greater than 24.4 ppm-h, but fewer than 11 hourly average concentrations equal to or greater than
0.10 ppm. Tables 5-15 and 5-16 illustrate that sites that experience 3-mo SUM06 values >24.4 ppm do not
necessarily have peaks, whereas sites that experience values <24.4 ppm-h do have peaks.
Reich (1987) reviewed 44 studies on 45 species to study the effects of O3 on net photosynthesis (Pn)
and growth of crops and tree species. Plants responded differently to equivalent total exposures (i.e., SUMOO), when
peak concentrations differed widely, with greater loss of Pn for increasing concentrations (Figure 5-15). Short-term,
high concentrations above 0.40 ppm (e.g., 0.50 ppm for 8 h) caused rapid and significant reduction in Pn. Longer
term exposures (for weeks) to lower concentrations had a significant effect on Pn; the observed reductions were less
severe than at the higher concentrations. Based on short-term, high concentration studies, SUMOO alone was an
inadequate descriptor of exposure for predicting response. However, for assessing the effects of long-term, low
concentrations typical of ambient condition, SUMOO may be adequate, because the response of field-grown plants to
SUMOO was roughly linear. SUMOO explained much, although not all, of the variation in Pn and the growth of
conifers, hardwood trees, and agricultural crops (Figures 5-16 through 5-18). Unexplained variation can be attributed
to biological variation, inherent experimental error, experimental conditions, and differences
5-107
-------
Table 5-14. Summary of Ozone Exposures That Are Closest to Those Predicted for
20% Yield Reduction per SUM06 Exposure Response Models Used by
Lee et al. (1991) in Selected National Crop Loss Assessment Network Experiments3
(Concentrations are in parts per million.)
Experiment1"
SOYBEAN
A80SO - Corsoy
A83SO - Amsoy
A83SO - Corsoy
A85SO - Corsoy-79 D
A85SO - Corsoy-79 W
A86SO - Corsoy-79 D
A86SO - Corsoy-79 W
B83SO - Corsoy-79 D
B83SO - Corsoy-79 W
B83SO - Williams D
^ B83SO - Williams W
A 18 ISO - Hodgson
g R81SO - Davis
R82SO - Davis
R83SO - Davis Dry
R83SO - Davis Wet
R84SO - Davis Dry
R84SO - Davis Wet
R86SO - Young Dry
R86SO - Young Wet
SORGHUM
A82SG - Dekalb
WHEAT
A82WH - Abe
A82WH - Arthur-71
A83WH - Abe
A83WH - Arthur-71
BTI82WH - VONA
BTI83WH - VONA
Chamber
NF+0.03-1
NF+0.03-1
NF+0.03-1
NFx2.00-lD
NFx2.00-lW
NFx2.5-lD
NFx2.0-lW
NF-1D
NF+0.03-1 W
NF+0.03-1D
NF+0.03-1 W
NF+0.06-1
NF-1
NF+0.02-1
NF+0.02-1D
NF+0.02-1 W
NF+0.015-1D
NF+0.015-1W
NFxl.3-lD
NFxl.3-lW
NF+0.10-1
NF+0.03-1
NF+0.06-1
NF+0.06-1
NF+0.06-1
NF-1
NF-1
Min.
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
10
0.000
0.001
0.001
0.000
0.000
0.002
0.002
0.002
0.002
0.002
0.002
0.004
0.003
0.001
0.002
0.002
0.006
0.006
0.003
0.003
0.001
0.002
0.002
0.004
0.004
0.011
0.006
30
0.011
0.014
0.014
0.008
0.011
0.016
0.015
0.006
0.006
0.006
0.006
0.007
0.015
0.013
0.015
0.015
0.018
0.018
0.013
0.013
0.010
0.015
0.015
0.019
0.019
0.025
0.021
50
0.026
0.028
0.028
0.023
0.026
0.035
0.033
0.018
0.019
0.019
0.019
0.015
0.026
0.026
0.030
0.030
0.030
0.029
0.024
0.023
0.023
0.027
0.027
0.032
0.032
0.034
0.036
Percentiles
70 90
0.045
0.049
0.049
0.051
0.063
0.085
0.065
0.037
0.049
0.049
0.049
0.031
0.043
0.047
0.055
0.054
0.047
0.046
0.047
0.046
0.055
0.047
0.053
0.054
0.054
0.042
0.049
0.077
0.083
0.083
0.110
0.114
0.137
0.105
0.063
0.084
0.084
0.084
0.083
0.066
0.080
0.089
0.087
0.077
0.075
0.089
0.087
0.145
0.079
0.109
0.108
0.108
0.057
0.071
95
0.090
0.098
0.098
0.129
0.134
0.161
0.124
0.074
0.097
0.098
0.097
0.090
0.075
0.091
0.104
0.101
0.089
0.089
0.107
0.101
0.160
0.094
0.121
0.123
0.123
0.064
0.083
99
0.111
0.123
0.123
0.160
0.162
0.207
0.161
0.087
0.118
0.118
0.118
0.105
0.088
0.123
0.126
0.119
0.113
0.110
0.137
0.129
0.185
0.113
0.144
0.159
0.159
0.072
0.097
Max
0.123
0.168
0.168
0.194
0.199
0.279
0.242
0.111
0.135
0.137
0.135
0.132
0.145
0.203
0.155
0.138
0.140
0.159
0.206
0.198
0.223
0.149
0.170
0.186
0.186
0.098
0.116
Number
of Obs.
1,344
1,992
1,992
2,352
2,352
2,040
2,040
1,512
1,512
1,512
1,512
1,680
2,664
2,160
2,640
2,640
2,496
2,496
2,568
2,568
2,040
1,344
1,344
1,296
1,296
1,464
864
Number of Occurrences
>0.06 >0.08 >0.10
263
467
467
657
729
784
719
184
359
364
359
323
421
471
721
698
512
486
597
573
599
300
373
365
365
114
165
113
223
223
495
547
654
510
51
198
204
198
191
79
218
378
359
208
193
345
323
557
130
293
295
295
2
51
35
90
90
319
358
515
271
5
70
66
70
29
6
56
163
140
59
62
175
136
516
43
186
186
186
0
4
SUM
06 08
(ppm-h)
21.1
39.1
39.1
67.5
75.1
92.1
69.6
13.5
30.1
30.5
30.1
26.7
30.2
39.0
61.6
58.7
41.2
38.9
53.7
50.2
79.1
24.1
37.4
37.4
37.4
7.6
12.4
10.7
22.1
22.1
56.2
62.5
83.2
55.1
4.4
18.9
19.5
18.9
17.4
7.0
21.4
37.7
35.0
19.9
18.6
36.2
32.8
76.3
12.5
31.8
32.5
32.5
0.2
4.7
W126
(ppm-h)
17.7
33.2
33.2
63.0
70.0
88.6
63.7
10.6
25.8
26.0
25.8
22.9
22.6
33.1
53.1
50.7
34.8
32.6
47.7
44.1
78.2
19.8
35.3
35.6
35.6
6.2
9.8
-------
cn
CD
Table 5-14 (cont'd). Summary of Ozone Exposures That Are Closest to Those Predicted for
20% Yield Reduction per SUM06 Exposure Response Models Used by
Lee et al. (1991) in Selected National Crop Loss Assessment Network Experiments3
(Concentrations are in parts per million.)
Experiment1"
CORN
A81MA - PAG 397
A81MA - Pioneer
COTTON
R82CO - Stoneville
R85CO - McNair Dry
R85CO - McNair Wet
PEANUT
R80PN - NC-6
TOBACCO
R83TO - McNair 944
Chamber
NF+0.06-2
NF+0.06-2
NF-1
NFxl.99-lD
NFxl.33-lW
NF+0.015-1
NF+0.020-1
Min.
0.000
0.000
0.000
0.000
0.000
0.000
0.000
10
0.000
0.000
0.003
0.003
0.003
0.004
0.003
30
0.008
0.008
0.018
0.012
0.012
0.017
0.018
50
0.020
0.020
0.029
0.024
0.024
0.029
0.037
Percentiles
70 90
0.052
0.052
0.044
0.052
0.041
0.043
0.061
0.111
0.111
0.065
0.117
0.073
0.066
0.089
95
0.126
0.126
0.074
0.154
0.091
0.076
0.104
99
0.150
0.150
0.087
0.221
0.129
0.091
0.121
Max
0.187
0.187
0.152
0.291
0.166
0.112
0.155
Number
of Obs.
1,968
1,968
2,856
3,000
3,000
2,688
1,968
Number of Occurrences
>0.06 >0.08 >0.10
552
552
390
810
487
369
611
461
461
64
609
226
101
288
306
306
7
407
118
5
117
SUM
06 08
(ppm-h)
57.5
57.5
28.2
92.9
41.4
27.2
50.7
51.0
51.0
5.8
78.9
23.5
8.8
28.4
W126
(ppm-h)
55.1
55.1
22.7
88.2
35.9
22.0
42.6
"See Appendix A for abbreviations and acronyms.
""Separate analyses were performed for each water stress level, dry (D) and well-watered (W).
-------
cn
Table 5-15. Summary of Percentiles for Ozone Monitoring Sites in 1989
(April through October) with a Maximum Three-Month SUM06 Value <24.4 ppm-h
but with a Second Hourly Maximum Concentration >0.125 ppm
AIRS Site
060010003
060371301
060374002
060375001
060830008
060830010
060833001
090010113
090091123
220191003
220330003
220330004
220331001
220470002
220770001
230052003
471630009
481410027
481990002
482010024
482010062
482011034
482011037
490350003
490353001
Name
Livermore, CA
Lynwood, CA
Long Beach, CA
Hawthorne, CA
Santa Barbara, CA
Santa Barbara, CA
Santa Barbara County, CA
Bridgeport, CT
New Haven, CT
Westlake, LA
Baton Rouge, LA
Baton Rouge, LA
East Baton Rouge, LA
Iberville Parish, LA
New Roads, LA
Cape Elizabeth, ME
Kingsport, TN
El Paso, TX
Kountze, TX
Harris County, TX
Houston, TX
Houston, TX
Houston, TX
Salt Lake County, UT
Salt Lake City, UT
Min.
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.001
0.001
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
10
0.000
0.000
0.010
0.000
0.010
0.010
0.010
0.002
0.003
0.003
0.001
0.002
0.003
0.005
0.001
0.017
0.001
0.010
0.000
0.000
0.000
0.000
0.000
0.001
0.002
30
0.010
0.010
0.020
0.020
0.020
0.020
0.020
0.011
0.010
0.013
0.009
0.008
0.012
0.014
0.011
0.027
0.005
0.020
0.010
0.010
0.010
0.010
0.010
0.008
0.014
50
0.030
0.020
0.020
0.030
0.030
0.030
0.030
0.022
0.019
0.022
0.021
0.016
0.022
0.023
0.021
0.034
0.017
0.030
0.020
0.020
0.020
0.010
0.010
0.029
0.029
Percentiles
70 90
0.040
0.030
0.030
0.040
0.040
0.040
0.040
0.033
0.029
0.033
0.034
0.028
0.034
0.034
0.033
0.042
0.032
0.040
0.030
0.030
0.030
0.030
0.030
0.042
0.041
0.050
0.050
0.050
0.060
0.050
0.050
0.050
0.048
0.045
0.052
0.059
0.047
0.056
0.057
0.052
0.055
0.054
0.050
0.050
0.060
0.050
0.050
0.050
0.056
0.053
95
0.060
0.070
0.060
0.060
0.060
0.060
0.060
0.059
0.056
0.061
0.069
0.057
0.066
0.068
0.062
0.064
0.062
0.060
0.060
0.070
0.070
0.060
0.060
0.062
0.061
99
0.090
0.100
0.080
0.080
0.080
0.080
0.080
0.091
0.091
0.082
0.094
0.078
0.092
0.093
0.083
0.093
0.078
0.080
0.080
0.110
0.110
0.100
0.110
0.083
0.079
Max
0.140
0.140
0.160
0.190
0.190
0.220
0.140
0.156
0.156
0.137
0.168
0.138
0.171
0.149
0.141
0.146
0.125
0.260
0.130
0.230
0.170
0.220
0.250
0.125
0.140
Maximum
Uncorrected
SUM06
(ppm-h)
17.0
18.1
13.6
18.1
17.1
13.3
12.3
16.5
12.9
12.2
17.4
8.4
14.4
15.9
12.0
16.7
13.4
14.9
10.6
19.2
16.8
14.0
16.3
17.4
13.0
Number of
Observ.
Over 7-mo
Period
5,067
4,793
4,876
4,894
4,823
4,663
5,077
4,865
4,502
4,811
4,964
4,791
4,890
5,040
4,964
4,627
4,252
4,484
4,630
4,728
4,600
4,595
4,729
4,585
4,544
-------
cn
Table 5-16. Summary of Percentiles for Ozone Monitoring Sites in 1989
(April Through October) with a Maximum Three-Month SUM06 Value > 24.4 ppm-h
but with a Second Hourly Maximum Concentration <0.125 ppm
AIRS Site
040132004
060070002
060170009
060430004
060710006
061011002
120094001
170190004
170491001
180970042
240030014
240053001
310550032
350431001
360310002
370270003
370810011
371470099
390030002
391510016
420070003
420770004
470090101
510130020
510610002
511870002
550270001
551390007
Name
Scottsdale, AZ
Chico, CA
South Lake Tahoe, CA
Yosemite National Park, CA
San Bernardino County, CA
Yuba City, CA
Cocoa Beach, FL
Champaign, IL
Effmgham County, IL
Indianapolis, IN
Anne Arundel, MD
Essex, MD
Omaha, NE
Sandoval County, NM
Essex County, NY
Lenoir, NC
Guilford County, NC
Farmville, NC
Allen County, OH
Canton, OH
New Brighton, PA
Allentown, PA
Smoky Mountain National Park,
TN
Arlington County, VA
Fauquier County, VA
Shenandoah National Park
(Dickey Ridge), VA
Horicon, WI
Oshkosh, WI
Min.
0.000
0.000
0.000
0.000
0.000
0.000
0.002
0.000
0.000
0.001
0.000
0.000
0.002
0.000
0.016
0.000
0.004
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.004
0.002
0.002
10
0.006
0.010
0.020
0.008
0.020
0.000
0.017
0.008
0.009
0.006
0.006
0.002
0.021
0.010
0.033
0.007
0.010
0.010
0.007
0.008
0.008
0.003
0.025
0.001
0.009
0.027
0.019
0.016
30
0.018
0.020
0.030
0.022
0.040
0.020
0.024
0.020
0.023
0.021
0.021
0.010
0.030
0.020
0.042
0.019
0.023
0.023
0.022
0.019
0.021
0.016
0.036
0.010
0.021
0.037
0.029
0.028
50
0.031
0.030
0.040
0.035
0.050
0.030
0.032
0.029
0.036
0.034
0.032
0.024
0.037
0.030
0.050
0.032
0.034
0.034
0.032
0.030
0.032
0.028
0.044
0.023
0.033
0.045
0.037
0.038
Percentiles
70 90
0.045
0.040
0.050
0.049
0.060
0.040
0.042
0.039
0.046
0.046
0.045
0.038
0.047
0.040
0.056
0.045
0.046
0.044
0.043
0.042
0.043
0.039
0.053
0.037
0.045
0.054
0.047
0.048
0.062
0.060
0.060
0.065
0.070
0.060
0.059
0.065
0.063
0.063
0.064
0.059
0.062
0.060
0.067
0.062
0.063
0.062
0.060
0.060
0.062
0.060
0.065
0.059
0.061
0.065
0.062
0.063
95
0.071
0.070
0.070
0.072
0.080
0.070
0.068
0.072
0.070
0.072
0.073
0.069
0.067
0.060
0.073
0.067
0.070
0.070
0.068
0.070
0.070
0.070
0.070
0.071
0.069
0.071
0.070
0.070
99
0.084
0.080
0.080
0.083
0.090
0.080
0.077
0.078
0.081
0.085
0.090
0.089
0.075
0.070
0.086
0.078
0.083
0.083
0.086
0.088
0.087
0.087
0.081
0.088
0.084
0.082
0.088
0.084
Maximum
Uncorrected
Max SUM06 (ppm-h)
0.107
0.100
0.100
0.111
0.100
0.100
0.094
0.088
0.104
0.103
0.120
0.121
0.098
0.090
0.106
0.092
0.113
0.100
0.107
0.110
0.102
0.102
0.098
0.116
0.122
0.100
0.111
0.121
31.7
33.5
44.8
37.6
70.5
29.0
28.7
32.0
25.3
25.4
25.5
25.2
24.9
25.1
45.6
25.8
27.7
26.4
24.5
26.3
29.4
25.1
35.9
25.7
24.6
59.0
24.6
27.9
Number of Observ.
Over 7-mo
Period
5,070
4,690
4,768
4,853
4,856
4,623
5,012
5,091
4,600
4,592
4,360
5,028
4,160
5,059
4,070
4,806
4,853
4,833
4,854
4,875
5,055
5,040
4,764
5,029
5,050
4,454
4,142
4,206
-------
20-
0-
.E .20-
o>
O
0)
-40-
-60-
-80-
-100-
Pines
0.05-0.06 pi_,
0.10-0.20 pp
0.30-0.45 pp
0.55-0.95 pp
-20
20 40 60 80 100 120
c
Q_
8>
20 -I
0-
-20-
-40-
O
*-•
I
o>
Q- -60
-80 -I
-10
Crops
0.05-0.15 ppm
0.50-0.75 ppm
10 20
SUMOO (ppm-h)
30
Figure 5-15. Percent reduction in net photosynthesis (Pn) of (A) pines (including one
point for red spruce) and (B) agricultural crops in relation to total ozone
exposure (SUMOO), for several ranges of peak concentrations (Reich, 1987).
5-112
-------
o
10-
0-
-10-
-20-
-30-I
Pines
30
60
90
30-
I
o 1
II
°>'5
(65-10-
8 -30-
-50-
Pines
40 80 120
SUMOO (ppm-h)
160
10 -
0 •
-10-
-20-
-30.
-40
20 -
0-
-20
-40-
-60-
B
Pines
D D
10
20
Pines
10 20 30
Uptake (mg/cm2)
40
Figure 5-16. Percent reduction in net photosynthesis (Pn) and biomass growth of
coniferous species in relation to (A) total exposure (SUMOO) and
(B) estimated total ozone uptake (Reich, 1987).
in O3 uptake. Imputed O3 uptake calculated as the product of SUMOO and mean diffusive
conductance (ks) for each species better correlated with Pn and growth than did SUMOO.
Kickert and Krupa (1991) criticized Reich's (1987) findings on the basis of
insufficient reporting of statistical model parameters, possible nonnormality of Pn and growth
variables, exclusion of ks terms for imputing O3 uptake for each species, and the absence of
implication for any individual plant species. However, Reich's synthesis of Pn and growth,
using the SUMOO index, would not necessarily be invalidated by nonnormality of the
variables. Reich's use of a mean diffusive conductance to impute O3 uptake is questionable
because leaf diffusive conductance measurements vary with time of day, season, and
environmental condition. In addition, the timing of an O3 exposure and stomatal conductance
is of utmost importance because they determine whether a plant will respond to O3 exposure
or not. Consequently, numerous measurements of conductance are required to weight hourly
O3 concentrations to calculate O3 uptake over the growth of a plant.
Pye (1988) reviewed 15 studies on 26 seedling species and found reductions in
biomass response increased with SUMOO (Figure 5-19). Seasonal sum of hourly
5-113
-------
5
o
(3
c
O
?
5
o
s.
20-
0-
-20-
8 -40-
S.
-60-
20-
Hardwoods
20 •
o.
-20
-40
-60 i
10
20
30
-80-L-r
B
Hardwoods
10
15
20
20
40 60
SUMOO (ppm-h)
10 20 30 40
Uptake (mg/cm2)
50
Figure 5-17.
Percent reduction in net photosynthesis (Pn) and biomass growth
of hardwood species in relation to (A) total exposure (SUMOO) and
(B) estimated total ozone uptake (Reich, 1987).
concentrations values ranged from 4 to 297 ppm-h. However, there was substantial variation
in response. Pines, poplars, sycamore (Platanus occidentalis), ash, and maple (Acer
saccharuni) are all relatively sensitive. Both concentration and duration are important factors
governing impact on growth and photosynthesis, but they probably are not equally important.
The biomass data suggest a nonlinear response to fumigation, and the presence of convexity
of response implies that for similar mean O3 exposures, damage will be greater when
O3 concentrations are more variable.
There is limited information for assessing the relative performance of exposure
indices for relating to vegetation effects. Lefohn et al. (1992a) reported that it was not
possible to differentiate among the SUMOO, SUM06, SUM08, and W126 exposure indices
because the indices were highly correlated with one another in the experiment (Figure 5-20).
However, results based on biological experiments, reported by Musselman et al. (1983, 1994)
and Hogsett et al. (1985b) have shown that different exposure regimes with similar SUMOO
5-114
-------
values resulted in those exposures experiencing peak concentrations exhibiting the greater
effects. The authors demonstrated that plants exposed to variable O3 concentrations
5-115
-------
Q_
Q>
10
6
CD
_c
Q
?
3
o
20
40 60 80
SUMOO (ppm-h)
10 20 30 40
Uptake (mg/cm2)
50
Figure 5-18. Percent reduction in net photosynthesis (Pn) and biomass growth of
agricultural crops in relation to (A) total exposure (SUMOO) and
(B) estimated total ozone uptake (Reich, 1987).
in chambers showed greater effect on plant growth than did those exposed to a fixed or daily
peak concentration of equal SUMOO, but with lower peak concentrations.
Building on the above cited results of chamber studies that indicated a greater
biological response to the higher hourly average concentrations, Lefohn et al. (1989)
concluded that the SUMOO index did not appear to perform adequately. Using air quality
data, Lefohn et al. (1989) showed that the magnitude of the SUMOO exposure index was
largely determined by the lower hourly average concentrations (Figure 5-21). Figure 5-21
illustrates that the slope of the curve that described the cumulative frequency for the SUMOO
index (referred to as TOTDOSE) was greater than the slope of the curve for the W126 index
until approximately 0.06 ppm; thereafter, the reverse was true. This occurred because the
W126 index weighted the higher concentrations more heavily than the lower ones, whereas
the TOTDOSE index did not.
Supplementing the results in Lefohn et al. (1989), Lefohn et al. (1992a), using
loblolly pine data exposed at Auburn, AL, to varying levels of O3 over 555 days (Lefohn
et al., 1992a) reported that the magnitude of the SUMOO values in the CF chamber, although
5-116
-------
50
25
£ °
D)
1-25
0>
CO
.c
O
-75
-100
Figure 5-19.
fl
*
-A v
0 25 50 75 100 125 150 175 275 300
Ozone Exposure (|j,L1 h)
Percent reduction in biomass growth of tree seedlings in relation to
total exposure (Pye, 1988).
experiencing hourly average values greater than those at the South Pole or Pt. Barrow, AK,
was about 50% less than the SUMOO values experienced at the South Pole and Pt. Barrow.
In a similar analysis using ambient data, Lefohn et al. (1992a) identified a separate
set of ambient sites that experienced SUMOO values similar to those of the ambient treatments
at Auburn; these ambient sites experienced fewer hourly concentrations above 0.07 ppm than
did the ambient chambers. Similar to the results cited above, the authors noted that the
magnitude of the SUMOO index was unable to capture the occurrence of the higher hourly
average concentrations in the ambient treatments. The authors indicated that the SUMOO
index was inadequate because of the observed inconsistencies of the SUMOO value between
chambers and selected monitoring sites.
When taken by themselves, the importance of these findings may be debatable
because the clean sites are not representative of loblolly growing regions, and there is no
substantiating evidence of differing effects at these levels. However, the coupling of the air
quality considerations, as described by Lefohn et al. (1989, 1992a), with the biological
findings reported by Musselman et al. (1983, 1994) and Hogsett et al. (1985b), builds a
consistent picture that the SUMOO index does not describe properly the occurrence of the
higher hourly average concentrations.
5-117
-------
1
0.8
0.6
0.4
0.2
n
A
X
o
o
o
o
X
X
X
1
0.8 :
I
0.6
0.4
0.2
n
c
o
>
o
o
X
X
' X
SUMOO (ppm-h)
SUM06 (ppm-h)
1
0.8
0.6
0.4
0.2
B
'0 100 200 300 400 500 600 700
W126 (ppm-h)
1
0.8 >
0.6
0.4
0.2
D
'0 100 200 300 400 500 600 700
SUM08 (ppm-h)
Figure 5-20.
Reduction in volume production of loblolly pine seedlings (family
91) in relation to four exposure indices (A through D) (Lefohn et al.,
1992a).
As noted earlier in this section (see also Section 5.4), the sensitivity of vegetation
at time of exposure varies with species and is a function of several factors (e.g., soil moisture,
light conditions, humidity, air turbulence). Assuming all factors are held constant
(a condition not found in the ambient atmosphere), the results reported by Musselman et al.
(1983, 1994), and Hogsett et al. (1985b), imply that, given any distribution of hourly average
concentrations, higher hourly average concentrations should be given greater weight than
lower hourly average concentrations. This statement provides only guidance concerning the
potential of each hourly average concentration to affect one type of vegetation relative to
5-118
-------
-------
Griinhage and Jager (1994b) concluded that mid-level hourly average O3 concentrations of
0.05 to 0.09 ppm are of greater importance than are higher hourly average concentrations in
affecting vegetation.
It is clear from the studies over the years that the cumulative effects of exposure to
all concentrations, peak and mid-range included, can play an important role in producing plant
growth responses. The apparent difference in viewpoints is based on whether cumulative
peak concentrations play a greater role in producing growth responses than do cumulative
mid-range concentrations. As emphasized later, these views are based on experimental results
that are not comparable. The studies that support the importance of peaks are chamber
studies primarily using peak exposures, whereas the majority of the studies emphasizing that
mid-range concentrations must be considered in plant response base their conclusions on both
OTC and ambient field data. The key to plant response is timing because peak and mid-range
concentrations do not occur at the same time. The greatest potential effect of O3 on plants
will occur when stomatal conductance is highest. If peaks do occur when stomatal
conductance is greatest, the contribution of mid-range exposures will not be observable
because they are masked. Associated with this is the importance of atmospheric conductivity
(i.e., the O3 concentration must reach the leaf surface if it is to be taken up by a plant).
Many studies over the years, depending on the duration of exposures and
sensitivity of the plants have shown that injury to crops and other vegetation could occur
when exposed to O3 concentrations that ranged from 0.04 to either 0.4 or 0.5 ppm, with the
higher concentration usually causing injury in the shortest period of time (Table 5-17;
U.S. Environmental Protection Agency, 1978, 1986). This range encompasses both peaks and
mid-range concentrations reported in the studies with the differing viewpoints cited above
(Musselman et al., 1983, 1986b, 1994; Hogsett et al.,1985b; Tonneijck and Bugter, 1991;
Tonneijck, 1994; Krupa et al., 1993, 1994, 1995; Griinhage et al., 1993b; Griinhage and Jager,
1994b).
Unfortunately, the terms "high" and "low" concentrations and "peak" and
"cumulative peak" concentrations are often used in publications (e.g., the majority of those
cited above) without any explanation or the concentration being specified or, when specified,
varying terminology has been applied with regard to what constitutes high concentrations or
categories of lower values. For example, in an early paper discussing the development of
vegetation effects exposure indices, Hogsett et al. (1988) termed 0.05 to 0.09 ppm as "mid-
range", whereas >0.10 was considered as being "relatively high". In a recent paper, Krupa
et al. (1995) term the concentrations of 0.05 to 0.09 as "moderately enhanced" and those
>0.09 ppm as high. For consistency within this present review, concentrations ranging from
0.05 to 0.09 ppm are termed mid-range and those above 0.10 ppm as high or peaks.
When evaluating the results of the studies cited above, most attention has been
focused on the concentrations used in the experiments (whether peaks or mid-range) by those
espousing a particular viewpoint, whereas little mention has been accorded to duration of
exposure, number of peaks during the exposure, whether or not there were peaks, and whether
the experiments were conducted in chambers in the greenhouse, in the field, or in OTCs in
the field. In the introduction to their paper, Musselman et al., (1983) describe the major
problem plant scientists have encountered when attempting to relate exposures to plant
responses in stating: "Pollutant dose, a quantitative description of pollutant exposure, has
been defined as a product of concentration and exposure duration. The components of
5-118
-------
Table 5-17. Ozone Concentrations for Short-Term Exposures That Produce
5 or 20% Injury to Vegetation Grown Under Sensitive Conditions3
Ozone Concentrations That May Produce 5% (20%) Injury (ppm):
Exposure time (h) Sensitive Plants'3
0.5
1.0
2.0
4.0
8.0
0
(0
0
(0
0
(0
0
(0
0
0
.35 -
.45 -
.15 -
.20 -
.09 -
.13 -
.04 -
.10 -
.02 -
.06 -
0.
0.
0.
0.
0.
0.
0.
0.
0.
0.
.50
.60)
.25
.35)
.15
.25)
.09
.15)
.04
.12
Intermediate Plants0
0
(0
0
(0
0
(0
0
(0
0
0
.55
.65
.25
.35
.15
.25
.10
.15
.07
.13
- 0.
- 0.
- 0.
- 0.
- 0.
- 0.
- 0.
- 0.
- 0.
- 0.
.70
.85)
.40
.55)
.25
.35)
.15
.30)
.12
.25
Less Sensitive Plants'1
>0
>0
>0
>0
>0
.70
.40
.30
.25
.20
(0.85)
(0.55)
(0.40)
(0.35)
(0.30)
The concentrations in parenthesis are for the 20% injury level.
bExamples of sensitive plants: oat, bean, and tobacco.
"Examples of intermediate plants: legumes, clover, and wheat.
dExamples of less sensitive plants: vegetables, woody plants, and cucumber.
Source: U.S. Environmental Protection Agency (1978, 1986).
pollutant dose are now recognized to be much more complex. Exposure concentration should
consider distribution, peaks, and means, whereas exposure duration includes length of time
exposed to zero concentration to indicate time intervals between exposures as well as the
duration of individual exposures. Sequence and patterns of intermittent pollutant exposures
also are involved when describing dose."
The papers on which the differing viewpoints are based represent attempts by the
various scientists to address the problems noted in the preceding paragraph. When reading
these papers, it soon becomes clear that each study is unique, some exposures were conducted
in chambers in the greenhouse or in the field on plants growing in pots, and others were
conducted in ambient air with plants grown in pots (See Table 5-18). None of the studies,
even those in which the same scientists exposed the same plant species or cultivar, replicates
a previous study. No two of the studies have exposed plants in the same manner or under
similar conditions (Table 5-18). The O3 concentrations, the duration, the conditions under
which exposures were made, and the medium in which the plants were grown all vary. When
similar exposure methods have been used, the exposures (concentration x duration [C x T])
and the plant species exposed have been different, and, when the same species or cultivar has
been used, the exposure methods have been different, and plants were grown in a different
medium. Therefore, the data presented in each paper were obtained under the particular set
of circumstances applicable to that given study. Attempting to extrapolate the data from these
studies to a broader scale causes many problems. Several of the authors of the above papers
have recognized this fact (Musselman et al., 1983, 1986b, 1994; Tonneijck and Bugter, 1991;
Krupa et al.,1993) and state that their studies have limited applicability,
5-119
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cn
Table 5-18. A Summary of Studies Reporting Effects of Peaks or Mid-Range Concentrations3
Species
Concentration (ppm) Exposure Pattern
Exposure Duration
Methodology Response
Reference
Kidney Bean cv.
California Dark
Red Phaseolus
vulgaris L.
Kidney Bean cv.
California Dark
Red
Phaseolus
vulgaris L.
Kidney Bean cv.
California Dark
Red Phaseolus
vulgaris L.
Alfalfa, Medicago
sativa L.
0.28
0.2
0.1-0.5
0.14-0.7
0.3
0.4
0.06-0.3
0.08-0.4
1. 0.12
2. 0.36 peak, max
1-h avg = 0.28
3. 0.24
4. 0.24 1-h peak
Daily 7-h mean:
0.063, 0.064,
0.083, 0.084,
peaks " 0.2
7-h mean
0.074,
0.094, 0.099,
peaks = 0.10-0.15
UHb
ULC
Simulated ambient:
diurnal, variable
diurnal, variable
UL "square wave"
UH "square wave"
Ambient, variable
Ambient, variable
Uniform
Narrow-based triangle
Broad based pyramid
Trapezoid
Daily for 30 days:
low episodic,
high episodic,
peaks at 1400-1500 h
30 days:
low daily peak,
high daily peak,
peaks at 1400 h
One 6-h (0915-1515 h)
exposure/week
1/3 plants: at 6 weeks;
1/3 plants: at 6 and 7 weeks;
1/3 at 6, 7, and 8 weeks plants
harvested at end of exposure period
One 2-h (1051-1309 h)
exposure/week for 6, 7, or 8 weeks
One 6-h (900-1500) exposure/week
1/3 plants: at 6 weeks;
1/3 plants: at 6 and 7 weeks;
1/3 at 6, 7, and 8 weeks plants
harvested at end of exposure period
7 weeks
3 days/week
5 h daily
0900-1600 h;
30 days x 5
8 CSTR, in
pots in soil
8 negative
pressure
chambers, in
pots in soil
CSTR,
15 plants
per chamber
8 OTC, in
pots;
alfalfa cut
3* during
exposure
period
Greatest injury
at 6 and
7 weeks;
senescence at
8 weeks
Square wave
vs. ambient: no
difference in
response if total
dose equivalent
Least injury:
profiles 2 and 4
Greatest injury:
3 > 1 but less
than 2 and 4
Growth reduced
more for alfalfa
under episodic
exposures
Growth reduced
less than with
episodic
exposures
Musselman
et al. (1983)
Mussleman
et al. (1986b)
Musselman
et al. (1994)
Hogsett et al.
(1985b)
-------
cn
Table 5-18 (cont'd). A Summary of Studies Reporting Effects of Peaks or
Mid-Range Concentrations3
Species
Tobacco cv. Bel W3
Nicotiana tobacum L.
Tobacco cv. Bel W3,
Nicotiana tobacum L.
Bean, Phaseolus
vulgaris L. cv.
Stratego cv. Groffy
Tobacco cv. Bel W3
Bel B Nicotiana
tobacum L.
Concentration (ppm)
Yearly mean range
1979-88: 0.025-0045
Weekly mean range
1988: 0.01-0.055
Years, 1979-1983
0.005-0.15, combined
in classes of 10 ug/m3
Years 1982-1983
0.015-0.075, combined
in classes of ug/m3
0.06-0.100
0.06-0.103
Exposure Pattern
Ambient, daily not
given
Ambient, daily not
given
Ambient, daily not
given
Ambient, daily not
given
Montague weekly
max
Mt. Equinox weekly
max
Exposure Duration
1 week
1 week
1 week
1 week
1 week
1 week
Methodology
4 pots in soil in
field: 17 locations
4 pots in soil in
field: 17 locations
4 pots in soil in
field: 40 locations
4 pots in soil in
field: 10 locations
OTC (CF); OTC
(NF); ambient
6 plants in pots in
peat and Perlite
6 plants in pots in
peat and Perlite
Response
Foliar injury
Foliar injury
Foliar injury
Foliar injury on
Stratego
Foliar injury on
bottommost
expanded leaf
Reference
Tonneijck and
Bugter (1991)
Tonneijck (1994)
Krupa et al.
(1993)
"See Appendix A for abbreviations and acronyms.
bUH = Uniform high.
°UL = Uniform low.
-------
and that caution should be used in applying their results on a broader scale. Had this advice
been adhered to, then many apparent discrepancies in conclusions across the papers would
likely not have arisen.
Musselman et al. (1983) exposed bean plants (Phaseolus vulgaris cv. California
Red Kidney) grown in pots in soil in CSTR chambers in a greenhouse with CF air to
simulated ambient O3 concentration distributions specific for their region (Riverside, CA), as
well as to two uniform concentration levels (Table 5-18). Plants were exposed to a
6-h O3 fumigation from 0915 to 1515 Pacific Standard Time (PST) at 6, 7, and 8 weeks of
age. The four exposure regimes were (1) uniform high, 0.28 ppm; (2) uniform low, 0.2 ppm;
(3) variable low concentrations ranging from 0.1 to 0.5 ppm that simulated ambient exposures
distributions (i.e., O3 concentrations increased during the morning, peaked in the afternoon,
and then decreased in the evening); and (4) variable high exposures ranging from 0.14 to 0.71
ppm that also simulated ambient concentration distributions (Table 5-18; Figure 5-22). Six
days after each of the three fumigations, one-third of the plants were measured for leaflet
oxidant stipple and destructively analyzed for leaf area and dry weight of plant parts.
Therefore, one-third of the plants received one fumigation, the second third received two
fumigations, and the remaining third received three fumigations at 6, 7, and 8 weeks of age.
Simulated ambient O3 distribution treatment produced significantly greater leaf injury and
reduced growth and yield response than the uniform low or high exposure patterns. In
addition, the simulated Riverside ambient O3 concentration distribution reduced the total dry
weight at both the 6- and 7-week fumigations; both pod and seed weights were reduced. The
reduction in dry weights of pods resulted after the first fumigation at 6 weeks and did not
change with subsequent fumigations. At 8 weeks, plants had begun to senesce. In this
experiment, levels of concentration ranged from the lowest, 0.1 ppm, to the highest, 0.5 ppm.
No exposure concentration, therefore, was below the "peak" level. Musselman et al. (1983)
pointed out that the simulated ambient pollutant distribution used in their studies was specific
for their geographic region. They also suggested that other studies determining the responses
of additional species at different developmental stages to ambient O3 distributions typical of
other regions of the country were needed to put their findings in perspective.
Exposures in the Musselman et al. (1986b) study were designed to compare plant
response to simulated ambient and uniform O3 concentration distributions at two equivalent
dose levels under controlled conditions (Table 5-18; Figure 5-23). Plants were fumigated in
eight negative pressure chambers located within the greenhouse and received either one
ambient or one uniform O3 treatment during Week 6, during Weeks 6 and 7, or during Weeks
6, 7, and 8. Therefore, as in the previous study, one-third received one fumigation, the
second third received two fumigations, and the other third received three fumigations. Plants
were harvested 6 days after their last fumigation (Musselman et al., 1986b).
The uniform distribution in the above study was selected so that the constant
concentration matched the total dose and peak concentration of the ambient distribution.
Matching the peak concentration and the total dose required that plants exposed to the
uniform distribution be exposed to the peak concentration (either 0.3 or 0.4 ppm) during the
entire fumigation period, whereas plants in the ambient distribution were exposed to the same
peak for only half an hour. The O3 concentrations during the ambient exposure distribution
had a fluctuating rising and falling pattern and were of longer duration overall, and the time
of the peak exposure was shorter when compared with the uniform O3 concentration
5-122
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0.70-
~ 0.60-
f 0.50-
.0
| 0.40-
§ 0.30
O
cf 0.20-
Oin
.1U
r\ f\r\
8 9 10
....
Uniform High
Uniform Low
.
|
i
i i i
11 12 13 14 15 1
Time of Day
Figure 5-22. Fumigation schedule of uniform and simulated ambient ozone
concentration distributions at two equivalent dose levels.
Source: Musselman et al. (1983).
treatment. Total exposure time for the uniform distribution was 2 h and 18 min, and, for the
ambient distribution, it was 6 h (Figure 5-23). Simulated ambient O3 concentrations for the
low dose ranged from 0.058 to 0.30 ppm, and for high dose, from 0.077 to 0.40 ppm.
The authors point out that ambient air quality data are generally reported as hourly
average concentrations, and the dynamics of changes in O3 concentrations during the hour are
not considered in the summaries of air quality data, although these have been considered
important in plant response. They also state that the results of this experiment demonstrate
that, when peak O3 concentrations and total dose are equivalent, the shape of the
O3 distribution (normal versus square wave) had no effect on the magnitude of response.
Beans responded similarly to both an ambient and a uniform O3 concentration distribution.
No significant difference in injury, growth, or yield was observed. The authors conclude with
the statement that "Further research is needed to examine whether peak concentration is the
most important component of the concentration distribution causing plant response"
(Musselman et al., 1986b).
In a further attempt to determine the response of plants to different exposure
profiles but equal total exposures (C * T), Musselman et al. (1994) exposed the same bean
cultivar, California Red Kidney, grown as in the previous studies, in CSTRs in a CF
greenhouse to four different profiles having the same total cumulative exposure and the same
5-123
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0.50 -I
i 0.30
8
0.20
om
0.10
0.00
Ambient High -•
Ambient Low
Uniform High
Uniform Low
I I I I I
8 9 10 11 12 13
Time of Day
14 15
I
16
Figure 5-23. Fumigation schedule of uniform and simulated ambient ozone
concentration distributions at two dose levels.
Source: Musselman et al. (1986b).
7-, 12-, and 24-h seasonal means (Table 5-18; Figure 5-24). Ozone exposures began 21 days
after germination. Plants were exposed for approximately 5 h, three times a week over the
seven-week growing season. The first profile used was a "square-wave" concentration of 0.12
ppm; the second exposure resembled a narrow-based triangle, during which the
O3 concentrations rose rapidly to a peak of 0.36 ppm with a maximum 1-h average of
0.28 ppm and then dropped off rapidly; the third profile was in the shape of a broad-based
pyramid, during which the O3 concentration rose slowly to a peak of 0.24 ppm and then
slowly dropped off; the fourth profile rose rapidly to a plateau with a peak of 0.24 ppm that
lasted for 1 h and then dropped off slowly. The maximum 1-h average concentrations of 0.22
ppm for Profiles 3 and 4 simulated the more typical summer patterns for Southern California,
where hourly peaks of >0.2 ppm occurred with regularity. Each of the last three profiles had
the same total O3 exposure, but at least 1 h of each daily exposure had at an average peak
concentration that exceeded 0.12 ppm.
Significant differences were found for all measured variables. Plants exposed
using the 0.12-ppm square-wave exposure (Profile 1) exhibited the least injury. Profile 3,
with the mean hourly pyramidal peak of 0.22-ppm exposure, exhibited significantly less
necrosis than did Profiles 2 and 4, which also had peak exposures. Plants responded similarly
to Profiles 2 and 4. There were no significant differences in plant responses for any of the
measured response variables, even though the mean 1-h peak for Profile 2 (0.28 ppm) was
higher than the 1-h peak mean (0.22) for Profile 4. Both of these profiles had higher peaks
or a longer duration of high concentrations, those above 0.16 ppm, than did
5-124
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Q.
8
c
0
O
O
o
8
o
0.36
0.30
0.24
0.18
0.12
0.06
0.36
0.30
0.24
0.18
0.12
0.06
0.36
0.30
0.24
0.18
0.12
0.06
0.36
0.30
0.24
0.18
0.12
0.06
Profile 1
Profile 2
1
Profile 3
Profile 4
12345
Fumigation Length (hours)
Figure 5-24. Experimental ozone exposure profiles.
Source: Musselman et al. (1994).
5-125
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Profile 3. The three exposure profiles that incorporated peaks impacted plant response more
severely than the steady-state profile, thus providing evidence of the importance of peak
concentrations in defining an exposure index (Musselman et al., 1994). Total exposure,
however, could not relate O3 impact to plant response unless the exposure shape was held
constant. The authors caution against the application of summary exposure statistics that do
not give increased weight to higher concentrations for comparison of plant response in areas
with differing exposure regimes. In addition, the authors state that, for Southern California,
which experiences high peak O3 levels, a descriptor of exposure that gives greater weight to
peak concentrations is more useful when relating plant response to O3 exposure. They also
suggest that environmental conditions may influence stomatal conductance and O3 uptake.
Therefore, summary statistics might necessitate the inclusion of other parameters that relate to
environmental factors. Finally, it is suggested that flattening out concentrations so that peaks
remain lower than 0.10 ppm might be expected to benefit the vegetation of Southern
California. Again, it should be noted that in all of the studies by Musselman et al. (1983,
1986b, 1994) peaks greatly exceed those in any of the other exposure studies.
The experiments of Hogsett et al. (1985a) were the initial studies using a newly
designed modified OTC, with an automated control system in which plants were exposed to
simulated ambient concentrations typical of the midwest. In the study, alfalfa and tall fescue
growing in pots were exposed to generator-produced O3 in OTCs using two different types of
exposure profiles (Table 5-18). Concentrations used were based on a 1978 Storage and
Retrieval of Aerometric Data (SAROAD) database for a selected midwestern site where a
substantial acreage of hay was grown. This study used the longest exposures of any of the
papers reviewed. The first exposure was a 30-day episodic profile of varying peak frequency,
concentration, and duration; a profile that was repeated every 30 days throughout the growing
season (Table 5-18; Figure 5-25). The second exposure was a daily peak profile of equivalent
peak concentration and duration each day. Daily 7-h exposures of alfalfa were from 0900 to
1600 hours (9 a.m. to 4 p.m.) for the 133-day growing season. Episodic 7-h mean
concentrations ranged from 0.064 to 0.084 ppm, with peaks of nearly 0.2 ppm occurring at
1400 to 1500 hours, whereas the profile for the mean daily peak concentrations varied from
0.074 to 0.099 ppm, with peaks ranging between 0.10 to 0.15 ppm occurring at 1400 hours.
Reduction in alfalfa growth was reported under both exposure profiles; however, response to
the episodic exposures was greater. Actual response data is not given in the paper. The
response of tall fescue was reduced only slightly over a period of 90 days when exposed to
either regime. Both alfalfa and fescue were cut three times during the exposure period. This
is the only study exposing a perennial plant, alfalfa, and a grass. The growth habit of grasses
differs from that of dicotyledonous plants because the growth of each leaf blade results from
a meristem at the base of the leaf, not from the apical meristem. Therefore, cutting or injury
to the leaf blade does not prevent its continued growth. Of the papers cited, this OTC
experiment is the only long-term study in which plants were exposed to both mid-range and
peak concentrations. The fluctuating episodic O3 pattern in the Hogsett et al. (1985b) and the
single 6-h/week exposure of the Musselman et al. (1983, 1986b) studies permit plants a brief
recovery period between exposures to peak concentrations. Also, in the above studies, plant
response to O3 exposure resulted in a reduction in growth, whereas, in the studies discussed
below, foliar injury is the plant response observed.
Tonneijck and Bugter (1991), Tonneijck (1994), and Krupa et al. (1993) were
reviewed by Krupa et al. (1995) who cited these Bel W3 studies in support of the concept
5-126
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0.20-
I
0.15-
0.10-
0.05-
o-l
A. Episodic
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
0.20-
B. Daily
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Exposure Day
Figure 5-25. Ozone exposure profiles for the 1983 season.
Source: Hogsett et al. (1985b).
5-127
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that "mid-range" concentrations (0.05 to 0.09 ppm) play a greater role than peak
concentrations in causing plant response (Figures 5-5, A, B, and D, and 5-6). Bel W-3, is a
variety of tobacco noted for its sensitivity to O3 and has been used as a sensitive monitor for
photochemical ambient air pollution for many years. Visible foliar injury is a clear and
unequivocal indication of O3 exposure. Heggestad and Middleton (1959) discovered Bel W3
and first reported on its sensitivity to O3. Heggestad and Menser (1962), Heck et al. (1969)
and Heck and Heagle (1970) all reported its value as a sensitive monitor of photochemical
ambient air pollution. Both Heck et al. (1969) and Heck and Heagle (1970) reported,
however, that there was no consistent relationship between oxidant values (O3 concentrations
measured as total oxidants) and foliar injury. They state, however, that a monitoring system
such as they describe can provide a community with estimates of the frequency of phytotoxic
levels of oxidants, of the relative severity of each episode, and of regional distribution of
phytotoxic air pollution (Heck and Heagle, 1970).
The papers of Tonneijck and Bugter (1991) report on observations made in the
Netherlands from 1984 to 1988, during which Bel W3 was used as a part of an extensive
network for monitoring the effects of ambient air pollution along with the O3-sensitive
indicator plant subterranean clover cv. Geraldton (Trifolium subterraneum).
Indicator plants grown in the greenhouse in pots were taken to 17 field locations at
weekly intervals and were exposed to ambient air for 1 week for Bel W3 tobacco and
2 weeks for clover. Foliar injury on the tobacco Bel W3 cultivar used in 1988 was greater
than that on the variety used during the years 1984 through 1987 (Figure 5-5A), although
mean O3 concentrations to which the varieties were exposed were similar (Figure 5-26, B).
The increased injury appeared to be associated with the new line of "relatively sensitive"
tobacco used in 1988 when compared with the "rather tolerant" strains used from 1984 to
1987. Exposures were reported as mean weekly O3 concentrations, 24-h means, daytime
average concentrations, number of hours >80 jig m3 (-0.04 ppm), and cumulative dose of
hourly values >120 jig m3 (-0.06 ppm). No peak concentrations were listed. The highest
effect intensity, a mean O3 concentration of 100 |ig/m3 (-0.05 to 0.06 ppm), was observed
during Week 22 of the exposures at the field site in 1988 (Figure 5-26, B). The mean
O3 concentration was the highest in Week 32.
The authors state that "foliar injury on tobacco Bel W3 was poorly related to the
ambient ozone in the Netherlands" (Figure 5-26, A, B, and C), whereas foliar injury on
subterranean clover correlated well with O3 exposure concentrations (Figure 5-26, D). Ozone
exposure indices emphasizing the importance of peak values did not correlate better with
injury than those based on mean values (Figure 5-26, E). Even though no peaks, as
previously defined above, were listed in their paper, foliar injury of tobacco was observed.
Tobacco plants appeared to be "relatively" more sensitive to O3 than did clover at the end of
the season. The main reason for using Bel W3 was to demonstrate the occurrence of
symptoms induced by O3 and "not to examine the relationship between the level of ambient
ozone and foliar injury intensity," as stated by Tonneijck and Bugter (1991). These authors
further noted that care should be taken when comparing the responses of both species because
of the difference in length of exposure and effect parameter. Even when both species of
plants were exposed to ambient air at the same location for the same length of time (7 days),
foliar injury on tobacco was not related to foliar injury on primary leaves of bean plants.
Finally, the authors state, "From these results, it can be concluded that ozone injury on
tobacco Bel W3 does not adequately indicate the concentration of ambient ozone nor is it a
good indication of the risk of ozone to other plant species or to vegetation as a
5-128
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79 80 81 82 83 84 85 86 87 88
Year
0.100
100
f 50H
-I
£ 25-
c.
0.025 0.05
Ozone (ppm)
0.075
iiiiiiiiiiiiiirniiii\
21 23 25 27 29 31 33 35 37 39 41 43
Week Number in 1988
0.075
-0.05
I
-0.025
16 18 20 22 24 26 28 30 32 34 36 38 40 42
Week Number in 1988
Figure 5-26. (A) Mean foliar injury on tobacco Bel W3 and mean ozone
concentrations for the years 1979 to 1988, (B) mean foliar injury on tobacco
Bel W3 and O3 concentrations for weekly exposures during the 1988 growing
season, (C) maximal foliar injury on tobacco Bel W3 in relation to
O3 concentrations for 1988, and (D) mean foliar injury on subterranean
clover cv. Geraldton and mean O3 concentrations for two weekly exposures
during the 1988 growing season.
Source: Tonneijck and Bugter (1991).
whole" (Tonneijck and Bugter, 1991). In other words, Tonneijck and Bugter (1991) concur
with the reports of Heck et al. (1969) and Heck and Heagle (1970), who much earlier had
reported similar views based on the results of their studies. Also, in their studies they
observed that ratios of weekly tobacco injury indices to oxidant indices at an oxidant-
monitoring site revealed no consistent relationship between weekly oxidant concentrations and
weekly plant injury. In addition, they observed that, although considerable new injury was
recorded each week of the season, the relationship between oxidant values and plant injury
was not consistent. In other words, data from Bel W3 exposures is not a good basis from
which to make extrapolations.
Tonneijck (1994) used data from the Dutch monitoring network for the years 1979
to 1983 (Figure 5-27, A) for Bel W3 and from 1982 to 1983 (Figure 5-27, B) for two bean
cultivars, the O3-sensitive "Stratego" and the O3 tolerant "Groffy", to evaluate injury-response
relationships among certain indicator plants. Various O3 exposure indices were
5-129
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T I I I I I I I I T
.005 .015 .025 .035 .045 .055 .065 .075 .085 .095 0.15
Weekly Average Ozone Concentrations (ppm) (1979-1983)
Averaged for Each Weekly Exposure Period for 40 Locations
40-
30^
B.
Stratego
Groffy
0.015 0.025 0.035 0.045 0.055 0.065
Weekly Average Ozone Concentration (ppm)
0.075
Figure 5-27. (A) Maximum foliar injury (percent of leaf area affected) on tobacco Bel W3
in relation to ozone (OJ concentrations expressed in classes of 10 fig/m3 for
1979 to 1983, and (B) maximum foliar injury (percent of leaf area affected)
on two bean cultivars in relation to O3 concentrations for 1982 to 1983.
Source: Tonneijck (1994).
5-130
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calculated from hourly O3 concentrations for all exposure periods. Data of foliar injury to
Bel W3 tobacco based on 20 to 22 weekly observations for 5 years (1979 to 1983) at
40 locations (Figure 5-27, A) were regressed against several exposure indices. Results of
correlation analysis indicated that the weekly sum of all hourly concentrations >40 |ig/m3
(0.02 ppm) has a negligibly better linear association with maximum weekly foliar injury
response than does the 24-h mean. Tonneijck (1994) does not present strong evidence in
favor or against the importance of mid-range concentrations in causing foliar injury response
due to low correlations (<0.28). The role of mid-range concentrations is difficult to
substantiate using correlation analyses because the effects of O3 on maximum foliar injury
response are not linear (Figures 5-27, B and C) and are confounded with environmental
factors. Tonneijck stated that the results of the Dutch monitoring network generally do not
support the conclusion that hourly concentrations of ambient O3 above 80 to 120 |ig/m3
(0.05 to 0.06 ppm) may be relatively more important in causing tobacco injury. Problems
with weak associations between weekly pollutant concentrations and visible foliar injury that
make the ability to discriminate among exposure indices difficult, which were reported by
Tonneijck (1994), also were experienced by Tonneijck and Bugter (1991) and Heck et al.
(1969), and Heck and Heagle (1970).
Based on his study, Tonneijck (1994) concluded that "the greatest injury to the
ozone-sensitive indicators, tobacco Bel-W3 and bean cv. Stratego, seems to occur at moderate
levels of ambient ozone." At relatively high O3 concentrations (>115 to 135 |ig/m3; -0.055
to 0.065 ppm), less injury was observed than at "moderately enhanced concentrations".
Results of the above study do not support the "concept that higher O3 concentrations should
be given more weight in terms of plant response than lower ones, since higher concentrations
do not necessarily cause greater effects." In Figure 5-27, A, it can be noted that foliar injury
on Bel W3 tobacco did not increase even when O3 concentrations neared 0.15 ppm.
However, the manner in which the data in the above study is presented makes it difficult to
determine the actual concentrations to which the plants were exposed.
In neither the Tonneijck and Bugter (1991) nor Tonneijck (1994) papers are the
actual O3 concentrations to which the plants were exposed stated, except as mean values.
Also, the terms "peak", "moderate", "moderately enhanced", and "circa" are used, but never
defined. The problems associated with attempting to make extrapolations from Bel W3 have
already been mentioned. In addition, Posthumus (1984) points out, in a paper describing the
Dutch monitoring program, that plants grown in the greenhouse may be "more vulnerable" to
ambient air pollutants than are crops grown in the field because those grown in a greenhouse
have been grown under ideal circumstances.
Krupa et al. (1993) used two tobacco cv. (the sensitive Bel W3 and the tolerant
Bel B) as differential indicators of ambient O3 pollution. When reviewing previous studies in
the introduction to their paper, Krupa et al. (1993) mention that the tobacco cultivars Bel W3
and Bel B have been used for over 25 years and indicate that other studies using Bel W3
have produced conflicting results. The aim of their present study was to further examine this
subject. Seedlings of the two cultivars grown in pots containing Fafard Mix No. 2 (screened
peat + Perlite) in CF air and fertilized every 7 days with liquid fertilizer until the day prior to
exposure were transferred to the two field sites when each set of plants reached its "true four-
leaf stage" after removing the two juvenile leaves. Exposures to ambient O3 concentrations
were made at two different sites (near Amherst, MA, and in the Green Mountains of southern
Vermont) from mid-June to August during the 9 weeks of the study (Figure 5-28, A and B).
Ambient O3 concentrations were measured continuously. Exposures occurred in an OTC with
5-131
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CF air, an OTC with NF air, and a chamberless ambient-air field plot (Table 5-18). There
were two replicates per treatment, with six plants of each cultivar in each replicate. Visual
estimates of leaf area showing O3 injury were made, beginning with the bottommost fully
expanded leaf (leaf no. 1) at the end of each weekly exposure. Ratings were given a value
from 1 to 10. A new set of plants was exposed each week. Maximum hourly average
concentrations for the 9-week period ranged from 0.06 to 0.1 ppm, with the highest
concentrations occurring during week seven.
Observations, based on foliar injury scores, indicated that injury to leaves
no. 1 and 2 on Bel W3 was much greater than corresponding leaves on Bel B. Foliar injury
on Bel W3 was much higher in the NF OTCs and chamberless ambient-air exposures than in
the filtered-air OTC exposures. Injury scores indicated that leaf no. 1 on Bel W3 was more
sensitive than leaf no. 2. Also, injury scores on leaf no. 1 were very similar in the NF OTC
and the chamberless ambient field plot. Study results indicated that, in all cases, of the
several O3 descriptors tested, the number of hours with O3 concentrations >40 ppb (N40) and
>60 ppb (N60) or the number of hours with O3 concentrations >40 ppb (SUM40) and >60
ppb (SUM60) were best predictors of O3 injury. Neither the N40 or N60 nor the SUM40 or
SUM60 performed well independently of the corresponding variable in the best regression.
The authors state that the results of the present study support the conclusions of
Menser et al. (1963), who pointed out that mature leaves were more sensitive than over-
mature and rapidly expanding younger leaves. Consequently, all subsequent analyses were
based on the responses of leaf no. 1. The authors also point out that their analysis had two
limitations: (1) the number of foliar injury observations was low (nine) on a per-site basis,
and, hence, results had to be pooled; and (2) foliar injury observations each week involved
new groups of plants, and the results on consecutive weeks were thus independent of each
other. This is the only study, of those being discussed, in which plants were grown in an
artificial medium.
Krupa et al. (1994) suggested that mid-level hourly average concentrations of
O3 (0.05 to 0.087 ppm) are more important than higher hourly average concentrations in
affecting vegetation. The key result of Krupa et al. (1994) is questioned because the CF-NF
and AA-NF (i.e., comparisons between CF and NF OTC plots and between ambient air
nonchambered and NF chambered plots) differences, as reported by the authors, were
inconsistent with earlier publications of the same NCLAN studies, which found few cases
with significant CF-NF differences (e.g., Heagle et al., 1988a; Rawlings et al., 1988a; Kress et
al., 1985; Kohut and Laurence, 1983). For three of the eight harvests, which Krupa et al.
(1994) reported as having significant CF-NF difference, Kohut and Laurence (1983) reported
a 2% yield reduction at NF for kidney bean plants at the Ithaca site in 1980; Heagle et al.
(1987a) reported 0 and 34% yield reductions at NF for well-watered and water-stressed
soybean plants, respectively, at the Raleigh, NC, site in 1983; and Kohut et al. (1987)
reported an 11% yield reduction at NF for wheat plants at the Ithaca site in 1983, which was
not significant at the 5% level. Another two harvests of clover in the 1985 Raleigh
experiment should not have been used by Krupa et al. (1994) because Heagle et al. (1989b)
reported significant chamber effects on total biomass, based on a 33% yield reduction at NF
relative to AA. Two other inconsistencies were found in Krupa et al. (1994). First, the two
clover studies conducted at Raleigh in 1984 and 1985 had six and seven harvests during each
year of the studies (Heagle et al., 1989b), not 12 and 14 as reported by Krupa et al. (1994).
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0.12
0.08
.o
<3 0.06
+->
o 0.04 H
o
0.12
E '
Q.
•S* 0.08-
c
g
'cc 0.06 -
"c
0.04-
8
0.02
A.
B.
Maximum
Median
Minimum
0.02-
— '
i i i i i i i
1 234567
I i
8 9
Week Number
\
2
I
4
I
6
I
8
Week Number
Figure 5-28. (A) Summary hourly ambient ozone (OJ concentrations during 9 weeks of
experimentation (1990) at Montague-Amherst, MA, and (B) summary hourly
ambient O3 concentrations during 9 weeks of experimentation (1990) at
Mount Equinox.
Source: Krupa et al. (1993).
5-133
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Second, the two clover studies conducted at Ithaca in 1984 and 1985 had three harvests
during each year of the studies (Kohut et al., 1988a), not six as reported by the authors.
Krupa et al. (1995) attempted in another paper to present "a cohesive view of the
dynamics of ambient O3 exposure and adverse crop response relationships, coupling the
properties of photochemical O3 production, flux of O3 from the atmosphere into crop canopies
and the crop response per se." The results from two independent approaches, (1) statistical
and (2) micrometeorological, were analyzed for understanding cause and effect relationships
of foliar injury responses of tobacco Bel W3 to the exposure dynamics of ambient O3
concentrations. Additionally, other results from two independent approaches were analyzed to
(1) establish a micrometeorological relationship between hourly ambient O3 concentrations
and their vertical flux from the atmosphere into a grassland canopy and (2) establish a
statistical approach relationship between hourly O3 concentrations in long-term, chronic
exposures and crop yield reductions. Based on the above approaches, Krupa et al. (1995)
noted that atmospheric conditions appeared to be most conducive and crop response appeared
to be explained best statistically by the cumulative frequency of hourly ambient O3
concentrations between 0.05 and 0.09 ppm. The diurnal occurrence of this concentration
range, frequently between the hours 9:00 a.m. and 4:00 p.m. in a polluted agricultural
environment, coincided with the optimal CO2 flux from the atmosphere into the crop canopy,
thus facilitating high uptake. The frequency of hourly concentration >0.90 ppm appeared to
be of little importance. The higher concentrations, generally appeared to occur when
atmospheric conditions did not facilitate optimal vertical flux into the crop canopy, therefore
uptake was low.
Krupa et al. (1995) concluded, based on their overall results, that, if the cumulative
frequency of hourly ambient O3 concentrations between 0.05 and 0.062 ppm (100 and
124 jig m3) occurred during 53% of the growing season, and the corresponding cumulative
frequency of hourly concentrations between 0.05 and 0.074 ppm occurred during 71% of the
growing season, a potential yield reduction in sensitive crops could be expected, if other
factors supporting growth, such as adequate soil moisture, are not limiting. In summary, they
concluded that these results need further verification.
High correlations can be obtained from chamber experiments because exchange
properties inside chambers are more or less constant in time (Griinhage and Jager, 1994b).
Under ambient conditions, however, exposure indices obtained from the chamber studies
frequently yield unsatisfactory results (Griinhage and Jager, 1994a). Griinhage and Jager
(1994a,b) support this view by presenting the results of O3 flux density measurements above a
permanent grassland in Germany. Two years of observations demonstrate the influence of
atmospheric conditions on O3 exposure potential (i.e., how vertical flux and stomatal
conductance change during the day). Diurnal flux densities of O3 varied during the growing
seasons of 1990 and 1991 (Griinhage et al., 1994). Vertical flux densities have to be
calculated using micrometeorological approaches. Though similar in pattern, the higher flux
densities in 1991 coincided with lower O3 concentrations. Therefore, under ambient
conditions, exposures cannot be expressed as a simple function of the concentration in the air.
Flux densities and deposition velocities of O3, as well as the biological activity of the canopy,
need to be considered when determining the effects of ambient air exposures on vegetation.
Griinhage and Jager (1994a,b) and Griinhage et al. (1994), using the information obtained
from the micrometeorological measurements of vertical flux densities of CO2 and O3 above
the native grassland, developed a mathematical model. Griinhage and Jager (1994b) fit this
mathematical model to Bel W3 tobacco data to describe a dose-response relationship for leaf
5-134
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injury. They concluded that it is possible with this model to attribute the DLA on Bel W3
tobacco to O4 flux densities. Correlations between O3 fluxes and leaf injury to tobacco are
significantly higher than those using exposure indices based on chamber studies. Griinhage
and Jager (1994b) emphasize the need for taking ambient conditions into account when
developing exposure indices to determine critical levels that will prevent injury to vegetation.
Finally, it is not possible at this time, based on a comparison of data from the
above mixed studies, to conclude whether the cumulative effects of mid-range concentrations
are of greater importance than those of peak hourly average concentrations in determining
plant response. The data are not comparable; exposure methods, concentrations and durations
used, age of plants at exposure, length of exposure, the plants exposed, and the media in
which they were grown all differ across experiments. Some exposures were in chambers in
the greenhouse, others in OTCs and others in the ambient air. Many of the exposures in the
studies supporting the importance of mid-level O3 concentrations were only 1 week in
duration. It is doubtful that an exposure duration of only 1 week and foliar response data
from a sensitive plant species like Bel W3 or from any other plant species are sufficient to
ascertain whether cumulative peaks or mid-range concentrations play a greater role in plant
growth response. It should be noted, however, that plants are not exposed just to peak O3
concentrations, therefore, response to O3 involves the cumulative effect of all concentrations
that enter the plants. The short-term exposures indicate that foliar injury can occur even in
the absence of peaks. The timing is the key to plant response. Peak and mid-range
concentrations do not occur at the same time. A plant effect is determined by which
concentrations occur when stomatal conductance is highest. Peaks are important in plant
response only where and when plants are exposed to them.
Most important of all is that the response parameters measured in the studies of
Musselman et al. (1983, 1986b, 1994) and Hogsett et al. (1985b) differ from those of
Tonneijck and Bugter (1991), Tonneijck (1994), and Krupa et al. (1993, 1994). The former
measured both foliar injury and growth reductions; all but one of the latter based their
conclusions on foliar injury alone. Although foliar injury in tobacco can result in important
economic loss to the grower, for the majority of crops, reduction in growth and yield is the
measure of importance. As stated in the previous criteria document (U.S. Environmental
Protection Agency, 1986), foliar injury in crops does not necessarily signify growth or yield
loss. Many studies can be cited to illustrate the inconsistency of relationship between foliar
injury and yield loss when foliage is not the yield component.
The studies of Musselman et al. (1983, 1986b) and Hogsett et al. (1985b) have
been cited previously (U.S. Environmental Protection Agency, 1986, 1992) as a basis for
emphasizing the importance of episodic peak exposures. In addition, the conclusions
discussed in previous sections that favored the concept that cumulative effects of hourly
O3 (>0.10 ppm) concentrations are of greater importance than seasonal mean exposures in
causing vegetation injury are based on subsequent reanalyses of the NCLAN data. The
information presented above in Section 5.5.2.5 does not alter the conclusions reached in the
retrospective statistical analyses of NCLAN (Lee et al., 1987, 1991; Tingy et al., 1989;
Lefohn and Foley, 1992) that episodic peaks are of importance in causing growth effects, nor
does it rule out the possibility that mid-range exposures also could have had an effect.
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5.5.3 Summary
The effects of O3 on individual plants and the factors that modify plant response to
O3 are complex and vary with species and environmental soil and nutrient conditions.
Because the effects of O3 and its interactions with physical and genetic factors that influence
response are complex, it is difficult to develop a measure of exposure that relates well with
plant response based on experimental data. At best, experimental evidence of the impact of
O3 on biomass production can suggest the important factors of O3 exposure that modify plant
response, which should be considered when developing an exposure index.
Considerable evidence of the primary mode of action of O3 on plants (injury to
proteins and membranes, reduction in photosynthesis, changes in allocation of carbohydrate,
and early senescence), which ultimately lead to reductions in biomass production, identifies
O3 uptake as an important factor (see Section 5.2). Ozone uptake is controlled by canopy
conductance, stomatal conductance, O3 concentration outside the leaf and gases emitted from
the leaf (see Figure 5-2). Any factor that will affect stomatal conductance (e.g., light,
temperature, humidity, soil and atmospheric chemistry and nutrients, time of day, phenology,
biological agents) will affect O3 uptake and, consequently, plant response.
The factors such as respite time, temporal variation, phenology, canopy structure,
physiological processes, environmental conditions, and soil and nutrient conditions are
important in determining the impact of O3 on crops and trees but are not well understood and
interact with concentration and duration in different fashions depending on species. Ozone
uptake integrates these factors with atmospheric conditions and relates well with plant
response, but is difficult to measure. Empirical functions to predict stomatal conductance
have been developed for particular species (e.g., Losch and Tenhunen, 1981) but have not
been used to estimate O3 uptake or used in development of exposure indices. Based on
atmospheric measurement of deposition and diurnal patterns of O3 and gas exchange in a
natural grassland ecosystem, Griinhage and Jager (1994a,b) and Griinhage et al. (1993a)
proposed an ambient O3 exposure potential for characterizing O3 uptake and related it to the
DLA of Bel W3 tobacco. Griinhage and Jager (1994a,b) proposed a weighting scheme that
preferentially weights the hourly O3 concentrations occurring during periods of optimal
vertical flux into the canopy. For the diurnal pattern of distribution at the natural grassland
site in Germany, there was a greater frequency of concentrations in the 0.05- to 0.09-ppm
range during the 0900 to 1559 period that matched the DLA of Bel W3 when atmospheric
and canopy resistance was minimal.
Further, the biochemical mechanisms, discussed in Section 5.2, describe the mode
of action of O3 on plants as the culmination of a series of physical, biochemical, and
physiological events leading to alterations in plant metabolism. Ozone-induced injury is
cumulative, resulting in net reductions in photosynthesis, changes in allocation of
carbohydrate, and early senescence, which lead to reductions in biomass production
(Section 5.2). Increasing O3 uptake will result in increasing reductions in biomass production.
The optimum exposure index that relates well with plant response should
incorporate the factors (directly or indirectly) described above; unfortunately, such an index
has not yet been identified. At this time, exposure indices that weight the hourly
O3 concentrations differentially appear to be the best candidates for relating exposure with
predicted plant response. Peak concentrations in ambient air occur primarily during daylight,
thus, these indices, by providing preferential weight to the peak concentrations, give greater
5-136
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weight to the daylight concentrations than to the nighttime concentrations (when stomatal
conductance is minimal). The timing of peak concentrations and maximum plant uptake is
critical in determining their impact on plants.
Some studies reported in the literature show that, when O3 is the primary source of
variation in response, year-to-year variations in plant response are minimized by the peak-
weighted, cumulative exposure indices. However, the study of Fuhrer et al. (1992) illustrates
some of the limitations in applying exposure indices. The study is significant for its use of
the mean O3 flux in minimizing the year-to-year variation in response when combining
replicate studies, indicating the importance of environmental conditions in quantifying the
relationship between O3 exposure and plant response.
5.6 Exposure-Response of Plant Species
5.6.1 Introduction
Determining the response of plants to O3 exposures continues to be a major
challenge. The effects of exposure usually are evaluated by exposing various plant species
under controlled experimental conditions, such as those discussed in Section 5.2, to known
concentrations and exposure periods. Plant responses are influenced not only by the
biochemical and physiological changes that may occur within the plant after O3 entry
(Section 5.3, Mode of Action, see also Figure 5-5) but also by the many factors (both internal
and external) that modify plant response (Section 5.4). Of the internal factors discussed in
Section 5.4, those that are most likely to apply under controlled experimental conditions are
the genetic makeup and age of the plant at the time of exposure. Compensatory responses
(Section 5.3.4.2) also will influence plant response. This section analyzes, summarizes, and
evaluates what is known about the response of various plant species or cultivars, either as
individuals or in populations, to O3 exposure. Species as populations will be considered only
in the case of pasture grasses, or forage mixes, which commonly occur as mixed stands. The
response of forest and trees in their natural habitats is discussed in the next section.
Emphasis will be placed on those studies conducted since the publication of the previous
criteria document 1986 (U.S. Environmental Protection Agency, 1986). Much of the
discussion of vegetation response to O3 exposure in the current document is based on the
conclusions of both the 1978 and 1986 criteria documents (U.S. Environmental Protection
Agency, 1978, 1986); therefore, to provide a basis for understanding the effects presented
below, the conclusions of the two documents are summarized.
Finally, the results of O3 exposure-response presented in this section must be
related to one or more assessment endpoints. Historically, the dollar value of lost production
was the endpoint of interest; however, other endpoints (e.g., biodiversity, habitat, aesthetics,
recreation) must be considered now, particularly as the impacts of O3 on long-lived species of
ecological importance are evaluated (Tingey et al., 1990).
5.6.2 Summary of Conclusions from the Previous Criteria
Documents
The experimental data presented in the 1978 and 1986 criteria documents dealt
with the effects of O3 primarily on agricultural crops species (U.S. Environmental Protection
Agency, 1978, 1986). The chapter on vegetation effects in the 1978 criteria document (U.S.
Environmental Protection Agency, 1978) emphasized visible injury and growth effects;
5-137
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however, the growth effects were not those that affected yield. This emphasis was dictated
by the kind of data available at the time. The document also presented data dealing with the
response of the San Bernardino forest ecosystem to O3. This information also was discussed
in the 1986 document (U.S. Environmental Protection Agency, 1986). It remains the best and
most comprehensive study of forest ecosystem responses to O3 stresses (see Section 5.7).
The 1986 document emphasized the fact that although foliar injury on vegetation is
one of the earliest and most obvious manifestations of O3 exposure, the effects of exposure
are not limited to visible injury. Foliage is the primary site of plant response to
O3 exposures. Significant secondary effects include reduced growth, both in foliage and roots.
Impacts range from reduced plant growth and decreased yield to changes in crop quality and
alterations in plant susceptibility to biotic and abiotic stresses. Also, the 1986 document
noted that O3 exerts a phytotoxic effect only if a sufficient amount reaches sensitive sites
within the leaf (see Section 5.3). Ozone injury will not occur if the rate of uptake is low
enough that the plant can detoxify or metabolize O3 or its metabolites or if the plant is able to
repair or compensate for the effects (Tingey and Taylor, 1982; U.S. Environmental Protection
Agency, 1986). Cellular disturbances that are not repaired or compensated are ultimately
expressed as visible injury to the leaf or as secondary effects that can be expressed as reduced
root growth or as reduced yield of fruits or seeds, or both. Ozone would be expected to
reduce plant growth or yield if it directly impacts the plant process (e.g., photosynthesis) that
limits plant growth or if it impacts another step to the extent that it becomes the step limiting
plant growth (U.S. Environmental Protection Agency, 1986; Tingey, 1977). Conversely, if
the process impacted is not or does not become rate-limiting, O3 will not limit plant growth.
These conditions also suggest that there are combinations of O3 concentration and exposure
duration that a plant can experience that will not result in visible injury or reduced plant
growth and yield. Indeed, numerous studies have demonstrated this fact. This information is
still pertinent today (Section 5.3)
Ozone can induce a diverse range of effects beginning with individual plants and
then proceeding to plant populations and, ultimately, communities. The effects may be
classified as either injury or damage. Injury encompasses all plant reactions, such as
reversible changes in plant metabolism (e.g., altered photosynthesis), leaf necrosis, altered
plant quality, or reduced growth that does not impair yield or the intended use or value of the
plant (Guderian, 1977). In contrast, damage or yield loss includes all effects that reduce or
impair the intended use or value of the plant. Thus, for example, visible foliar injury to
ornamental plants, detrimental responses in native species, and reductions in fruit and grain
production by agricultural species all are considered damage or yield loss. Although foliar
injury can not always be classified as damage, its occurrence indicates that phytotoxic
concentrations of O3 are present, and, therefore, studies should be conducted to assess the risk
to vegetation.
The concept of limiting values used to summarize visible foliar injury in the 1978
document also was considered valid in the 1986 document (U.S. Environmental Protection
Agency, 1978, 1986). Jacobson (1977) developed limiting values by reviewing the scientific
literature and identifying the lowest concentration and exposure duration reported to cause
visible injury to a variety of plant species. Expressed in another way, limiting values were
concentrations and durations of exposure below which visible injury did not occur.
A graphical analysis presented in both of the previous documents indicated the limit for
reduced plant performance was an exposure to 0.05 ppm for several hours per day for more
than 16 days. Decreasing the exposure period to 10 days increased the concentration required
5-138
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to cause injury to 0.1 ppm, and a short, 6-day exposure further increased the concentration to
cause injury to 0.3 ppm.
By 1986, a great deal of new information concerning the effects of O3 on the yield
of crops plants had become available, both through EPA's NCLAN and the results of research
funded by other agencies. The NCLAN project was initiated by EPA in 1980, primarily to
improve estimates of yield loss in the field and of the magnitude of crop losses caused by
O3 (Heck et al., 1982, 1991). The primary objectives were:
(1) to define the relationships between yields of major agricultural crops and
O3 exposure as required to provide data necessary for economic assessments
and the development of National Ambient Air Quality Standards;
(2) to assess the national economic consequences resulting from the exposure of
major agricultural crops to O3; and
(3) to advance understanding of the cause and effect relationships that determine
crop responses to pollutant exposures.
The cultural conditions used in the NCLAN studies approximated typical
agronomic practices. The methodology used in these studies is described in Section 5.2.
Yield loss in the 1986 document was defined as "damage", an impairment in the
intended use of the plant. This concept included reductions in aesthetic values, the
occurrence of foliar injury (changes in plant appearance), and losses in terms of weight,
number, or size of the plant part that is harvested. Yield loss also may include changes in
physical appearance, chemical composition, or the ability to withstand quality storage
(collectively termed crop quality). Losses in aesthetic values are difficult to quantify. Foliar
injury symptoms can substantially reduce the marketability of ornamental plants or crops in
which the foliage is the plant part (e.g., spinach, lettuce, cabbage) and constitute yield loss
with or without concomitant growth reductions. At that time (1986), most studies of the
relationship between yield loss and O3 concentration focused on yields as measured by weight
of the marketable organ of the plant.
The OTC studies conducted to estimate the impact of O3 on the yield of various
crop species (e.g., the NCLAN program) were grouped into two types, depending on the
experimental design and statistical methods used to a analyze the data: (1) studies that
developed predictive equations relating O3 exposure to plant response and (2) studies that
compared discrete treatment level to a control. The advantage of the regression approach is
that exposure-response models can be used to interpolate results between treatment levels
(see Section 5.2.2).
Using NCLAN data as an example of plant response, the O3 concentrations that
could be predicted to cause 10 or 30% yield loss were estimated using the Weibull function
(Table 5-19). The data in Table 5-19 are based on yield-response functions for 38 species or
cultivars developed from studies using OTCs. Review of that data indicated that 10% yield
reductions could be predicted for 58% of the species or cultivars, when 7-h seasonal mean
concentrations were below 0.05 ppm, and for 34%, when seasonal mean concentrations were
between 0.04 and 0.05 ppm, but only 18% required 7-h seasonal mean concentrations in
excess of 0.08 ppm to suffer a 10% loss in yield. Furthermore, approximately 11% of the 38
species or cultivars would be expected to have a yield reduction of 10% loss at 7-h seasonal
mean concentrations below 0.035 ppm, suggesting that these plants are very sensitive to O3.
Grain crops were apparently less sensitive than the other crops. The data also
demonstrate that the sensitivity within species may be as great as differences between
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Table 5-19. Estimates of the Parameters for Fitting the Weibull
Model Using the 7-Hour Seasonal Mean Ozone Concentrations3 b
Parameters for Weibull Model
Crop
LEGUME CROPS
Soybean, Corsoy
Soybean, Davis (81)
Soybean, Davis (CA-82)6
Soybean, Davis (PA-82)e
Soybean, Essex (81)
Soybean, Forrest (82-1)
Soybean, Williams (81)
Soybean, Williams (82-1)
Soybean, Hodgson
Bean, Kidney (FP)f
Peanut, NC-6
GRAIN CROPS
Wheat, Abe (82)
Wheat, Arthur 71 (82)
Wheat, Roland
Wheat, Vona
Wheat, Blueboy II (T)
Wheat, Coker 47-27 (T)
Wheat, Holly (T)
Wheat, Oasis (T)
Corn, PAG 397
Corn, Pioneer 3780
Corn, Coker 16 (T)
Sorghum, DeKalb-28
Barley, Poco
FIBER CROPS
Cotton, Acala SJ-2 (81-1)
Cotton, Acala SJ-2 (82-1)
Cotton, Stoneville
HORTICULTURAL
CROPS
Tomato, Murrieta (81)
Tomato, Murrieta (82)
Lettuce, Empire (T)
Spinach, America (T)
Spinach, Hybrid (T)
Spinach, Viroflay (T)
Spinach, Winter Bloom (T)
&
2,785.00
5,593.00
4,931.00
4,805.00
4,562.00
4,333.00
4,992.00
5,884.00
2,590.00
2,878.00
7,485.00
5,363.00
4,684.00
5,479.00
7,857.00
5.88
5.19
4.95
4.48
13,968.00
12,533.00
240.00
8,137.00
1.99
5,546.00
5,872.00
3,686.00
32.90
32.30
1,245.00
21.20
36.60
41.10
20.80
tf
0.133
0.128
0.12/
0.103
0.187
0.171
0.211
0.162
0.138
0.120
0.111
0.143
0.148
0.113
0.053
0.175
0.171
0.156
0.186
0.160
0.155
0.221
0.296
0.205
0.199
0.088
0.112
0.142
0.082
0.098
0.142
0.139
0.129
0.127
A
c
1.952
0.872
2.144
4.077
1.543
2.752
1.100
1.577
1.000
1.171
2.249
2.423
2.154
1.633
1.000
3.220
2.060
4.950
3.200
4.280
3.091
4.460
2.217
4.278
1.228
2.100
2.577
3.807
3.050
1.220
1.650
2.680
1.990
2.070
CF
0.022
0.025
0.019
0.019
0.014
0.017
0.014
0.017
0.017
0.019
0.025
0.023
0.023
0.023
0.022
0.030
0.030
0.030
0.030
0.015
0.015
0.020
0.016
0.020
0.018
0.012
0.026
0.012
0.012
0.043
0.024
0.024
0.024
0.024
Concentration for
Predicted Yield
Losses of:
10%d
0.048
0.038
0.048
0.059
0.048
0.076
0.039
0.045
0.032
0.033
0.046
0.059
0.056
0.039
0.028
0.088
0.064
0.099
0.093
0.095
0.075
0.133
0.108
0.121
0.044
0.032
0.047
0.079
0.040
0.053
0.046
0.043
0.048
0.049
30%d
0.082
0.071
0.081
0.081
0.099
0.118
0.093
0.088
0.066
0.063
0.073
0.095
0.094
0.067
0.041
0.127
0.107
0.127
0.135
0.126
0.111
0.175
0.186
0.161
0.096
0.055
0.075
0.108
0.059
0.075
0.082
0.082
0.080
0.080
5-140
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Table 5-19 (cont'd). Estimates of the Parameters for Fitting the
Weibull Model Using the 7-Hour Seasonal Mean Ozone Concentrations3 b
Concentration for
Predicted Yield
Parameters for Weibull Model Losses of:
Crop a o CA CFC 10%d 30%'
|0/d
HORTICULTURAL
CROPS (cont'd)
Turnip, Just Right (T)
Turnip, Pur Top W.G. (T)
Turnip, Shogoin (T)
Turnip, Tokyo Cross (T)
10.89
6.22
4.68
15.25
0.090
0.095
0.096
0.094
3.050
2.510
2.120
3.940
0.014
0.014
0.014
0.014
0.043
0.040
0.036
0.053
0.064
0.064
0.060
0.072
T)ata are from Heck et al. (1984) and are based on individual plot means unless the crop name is followed by
"(T)". The "T" indicates that the parameters were based on treatment means and the data are from Heck et al.
(1983). The parameters given in Heck et al. (1983, 1984) also contain the standard errors of the parameters.
bAll estimates of $ are in ppm. The yield is expressed as kilograms per hectare for all crops except barley—see
weight (grams per head); tomato (both years)—fresh weight (kilograms per plot); cotton—lint + seed weight
(kilograms per hectare); peanut—pod weight (kilograms per hectare). In cases where the estimatedcf parameter
is exactly 1.0, it has been bounded from below to obtain convergence in the nonlinear model fitting routine.
Parameters were estimated from data not showing the expected Weibull form. Caution should be used in
interpreting these Weibull models. Other models might better describe the behavior observed in these
experiments. For those crops whose name is followed by "(T)", the yield is expressed as grams per plant.
The ozone (O3) concentration in the charcoal-filtered (CF) chambers expressed as a 7-h seasonal mean
concentration.
dThe 7-h seasonal mean O3 concentration (parts per million) that was predicted to cause a 10 or 30% yield loss
(compared to CF air).
eCA and PA refer to constant and proportional O3 addition.
fOnly the bean data from the full plots are shown. The partial plot data are given Heck et al. (1984).
Source: U.S. Environmental Protection Agency (1986).
species. For example, at 0.04 ppm O3, estimated yield losses ranged from 2 to 15% in
soybean and from 0 to 28% in wheat. Year-to-year variations in plant response also were
observed during the studies.
Discrete treatments were used to determine yield loss in some studies. These
experiments were designed to test whether specific O3 treatments were different from the
control rather than to develop exposure-response equations, and the data were analyzed using
analyses of variance. When summarizing these studies using discrete treatment levels, as
opposed to the variable concentrations used in NCLAN, the lowest O3 concentration that
significantly reduced yield was determined from analyses done by the authors. Frequently,
the lowest concentration used in the study was the lowest concentration reported to reduce
yield; hence, it was not always possible to estimate a no-effect exposure concentration.
In general, the data indicated that O3 concentrations of 0.10 ppm (frequently the lowest
concentration used in the studies) for a few hours per day for several days to several weeks
generally caused significant yield reductions. The concentrations derived from the regression
5-141
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studies were based on a 10% yield loss, whereas, in the studies using the analysis of variance,
the 0.10-ppm concentration frequently induced mean yield losses of 10 to 50%.
A chemical protectant, EDU was used to provide estimates of yield loss. The
impact of O3 on yield was determined by comparing the yield data from plots treated with
EDU with those that were not. Studies indicated that yields were reduced by 18 to 41%
when ambient O3 concentrations exceeded 0.08 ppm during the day for 5 to 18 days over the
growing season.
In summary, the 1986 criteria document (U.S. Environmental Protection Agency,
1986) states that several general conclusions can be drawn from the various approaches used
to estimate crop loss yield.
(1) Based on the comparison of crop yield in CF and unfiltered (ambient)
exposures, data clearly indicate that O3 at ambient levels is elevated
sufficiently in several parts of the country to impair the growth and yield of
plants. Data from the chemical protectant studies support the conclusion and
extend it to other plant species.
(2) Both of the above-mentioned approaches indicate that effects occur with only
a few O3 occurrences above 0.08 ppm.
(3) The growth and yield data cited in the 1978 criteria document (U.S.
Environmental Protection Agency, 1978) indicate that several plant species
exhibited growth and yield effects when the mean O3 concentration exceeded
0.05 ppm for 4 to 6 h/day for at least 2 weeks.
(4) The data obtained from regression studies conducted to develop exposure-
response functions for estimating yield loss indicated that at least 50% of the
species and cultivars tested were predicted to exhibit a 10% yield loss at 7-h
season mean O3 concentrations of 0.05 ppm or less.
Though most of the data from the discrete treatment studies (non-NCLAN studies)
did not use concentrations low enough to support the values cited above, the magnitude of
yield losses reported at 0.10 ppm under a variety of exposure regimes indicate that, to prevent
O3 effects, a substantially lower concentration is required (U.S. Environmental Protection
Agency, 1986).
The limiting values established in 1978 were still deemed appropriate in the 1986
criteria document for ornamentals and certain vegetable crops where visible injury was still
considered the response of interest because appearance is of importance (e.g., spinach, lettuce,
cabbage) (U.S. Environmental Protection Agency, 1986). This remains the case today.
5.6.3 Information in the Published Literature Since 1986
The major question to be addressed in this section is whether the conclusions of
the 1986 criteria document summarized in the previous section, remain valid, given the results
of research published since 1988. In particular, whether the response of plants to
experimental treatments at or near concentrations of 0.05 ppm (7-h seasonal mean), which are
characteristic of ambient concentrations in many areas, can be compared to a control or to
reduced O3 treatment to establish a potential adverse effect.
The 1986 criteria document (U.S. Environmental Protection Agency, 1986) made
the following statement: "The characterization and representation of plant exposures to
O3 has been and continues to be a major problem because research has not yet clearly
identified which components of the pollutant exposure cause plant response." This is still true
5-142
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today, although some insight into the importance of peak concentrations versus long-term
means has been gained (See Section 5.5). The importance of the timing of exposure during
the growing season, the duration of peaks, the rate of increase of concentration, and the
respite periods is unresolved.
The aim of most air pollution research experiments have been designed to quantify
the relationship between pollutant exposure and agricultural crop yield. The problem is the
incorporation of the concentration, duration, frequency, age, genetic composition, and respite
time into an exposure statistic or index that may be used to predict yield loss. The correct
exposure representation is the amount of pollutant entering the plant, not the ambient
concentration to which the plant is exposed (Taylor et al., 1982; Tingey and Taylor, 1982).
Unfortunately, it is rarely possible to know the amount of pollutant taken up by the plant, so
therefore, an appropriate index of exposure must be chosen. Most indices were not developed
from a biological basis, nor were they developed using an experimental approach specifically
designed to address all key factors (Lee et al., 1991). A number of exposure indices have
been developed in an attempt for depicting plant response to O3 exposure (see Section 5.5).
Much of the data in this section is evaluated using these indices. For this reason, several
different exposure statistics are used to determine the effect of an exposure on plant response.
It should be remembered that the SUM06, which is used more than any of the other indices,
is the seasonal sum of hourly concentrations at or above 0.06 ppm (see Section 5.5).
Exposure indices calculated for each of 10 years (1982 to 1991) and two exposure
periods, June through August (3 mo) and May through September (5 mo), are presented in
Table 5-20 (modified from Tingey et al., 1991). The monitoring data, collected at nonurban
sites, show that ambient O3 is frequently at, or near, the 7-h seasonal mean that would be
expected to cause a yield loss in crops, based on the conclusions of the 1986 criteria
document. This table may be used for comparison of ambient-O3 concentrations to those used
in experiments. Although the examples here are based on 10% loss figures, losses below that
level may occur and be important. Thirty-four percent of the 38 species or cultivars under
consideration would be predicted to have a 10% yield loss at a 7-h mean concentration of
between 0.04 and 0.05 ppm, but only 19% required a 7-h mean concentration of greater than
0.08 ppm to suffer a predicted 10% loss in yield. Furthermore, 11% of the 38 species or
cultivars would be expected to have a yield reduction of 10% at a 7-h mean, or less than
0.028 to 0.035 ppm (Tables 6-17 and 6-19; U.S. Environmental Protection Agency, 1986). It
also was concluded that grain crops (with the exception of a few very sensitive cultivars)
were generally less sensitive than others, but that within-species variability in sensitivity may
be as great or greater than between species. The preceeding results are similar to those
previously obtained from Table 6-19 in the 1986 document. Lee et al. (1994a,b) have revised
Table 6-19 in U.S. Environmental Protection Agency (1986) (see Table 5-19) using
recalculated peak-weighted exposure indices (shown to be more appropriate than long-term
means for relating effects to ambient concentrations) for the 54 studies (listed in Tables 5-21
and 5-22).
In 1992, the Supplement to the Air Quality Criteria Document for Ozone and
Other Photochemical Oxidants (1986) reviewed effects of oxidant exposure on vegetation.
Considerable emphasis was placed on the appropriate exposure index for relating biological
effects of O3 on plants (U.S. Environmental Protection Agency, 1992). An analysis of the
data at that time indicated that a seasonal mean concentration (e.g., 7 or 24 h) might not be
the best expression of the exposure because it did not weight high concentrations differently
from low concentrations, and it did not account for the variable length of growing seasons or
5-143
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exposure durations. Unfortunately, it is often impossible to calculate the different possible
exposure indices (means, cumulative peak- or threshold-weighted, or continuously weighted
[sigmoid] cumulative) from information given in published papers. Thus, difficulties remain
when comparing exposure-response studies that utilize different exposure indices. However,
reported responses and concentrations of O3 can be compared to those that occur at ambient
concentrations and then to other exposure indices (Table 5-20).
5.6.3.1 Effects of Ozone on Short-Lived (Less Than One Year) Species
Plant species can be characterized by their life span. They are either short-lived
annual species or longer lived perennials and trees. Physiological processes may be related to
life span (for instance, leaf gas exchange tends to be lower in longer-lived trees than in crop
species), so the response to O3 may be different (Reich, 1987). In addition, multiple-year
exposures and carry-over effects may be of importance in long-lived species, but of no
concern in annuals. Accordingly, annuals and perennials will be discussed separately. The
response of plants to O3 also is affected by interactions with other physical, chemical, and
biological factors. Those interactions are discussed elsewhere in this document (Section 5.3).
In most cases, the research analyzed here was conducted under near-optimal conditions of
water and nutrient availability. Although deviations from these conditions may affect the
magnitude of response, it is important to understand the potential of O3 exposure and its
consequences.
Several papers (Lee et al., 1988, 1991, 1994a,b; Lefohn et al., 1988a; Lesser
et al., 1990; Tingey et al., 1991) present a reanalysis of NCLAN data and data from field
studies conducted on potato that were not part of the NCLAN project. Lee et al. (1988,
1991) examined a number of measures of O3 exposure in relation to response data collected in
the experiments. The investigators were particularly interested in examining the ability of a
seasonal mean, a cumulative exposure index, and the second-highest daily maximum
concentration (2HDM) to predict the biological response of the plant. They found that no
particular index of O3 concentration dominated as best in all studies, but that cumulative
indices that weighted high concentrations at the "grain-filling" stage of the life cycle were
better than a seasonal mean. Seasonal means did work well within a given experiment where
treatments were highly correlated. The 2HDM was consistently a poor predictor of plant
response.
In a reanalysis of NCLAN data, Lesser et al. (1990) presented composite exposure-
response functions for a number of crop species, or groups of species. Predicted yield losses
(compared to yield at an assumed background concentration of 0.025 ppm) of up to 20%
occurred at a 12-h seasonal mean of 0.06 ppm, with a loss of 10% at a 12-h mean
concentration of about 0.045 ppm.
Tingey et al. (1991) and Lee et al. (1991) went on to reanalyze the crop response
data using three measures of exposure: (1) the SUM06, (2) the 7-h seasonal mean, and
(3) the 2HDM. Their analysis included crops that account for 70% of all crop land in the
United States and 73% of the agricultural receipts. The analysis included 31 field
experiments with 12 crop species, conducted in OTCs and resulted in composite exposure-
response functions. The results of their studies and additional reanalyses done since then are
summarized in Tables 5-23 and 5-24. They concluded that to limit yield loss to 10% or less
in 50% of the cases (all experiments and crops), a SUM06 of 24.4 ppm-h (or 26.4 ppm-h,
5-144
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Table 5-20. Summary of Ozone Exposure Indices Calculated for
3- or 5-Month Growing Seasons from 1982 to 1991a
3 mo (June-August)
HDM2C
Year
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
Among
No. of
Sites"
99
102
104
117
123
121
139
171
188
199
Years
ppm
Mean
0.114
0.125
0.117
0.117
0.115
0.119
0.129
0.105
0.105
0.106
0.113
cvd
23.7%
24.9%
24.6%
24.6%
21.8%
22.9%
21.3%
23.1%
21.6%
22.0%
11.1%
M7
ppm
Mean
0.052
0.056
0.052
0.052
0.052
0.055
0.060
0.051
0.053
0.054
0.054
CV
18.7%
21.9%
18.2%
17.1%
19.1%
17.6%
17.8%
17.5%
18.3%
18.4%
10.0%
SUMOO
ppm'
Mean
82.9
86.1
84.1
84.6
85.3
86.9
97.6
86.4
85.7
87.7
87.0
h
CV
19.1%
22.1%
19.9%
18.0%
18.0%
17.3%
19.6%
19.9%
21.0%
21.3%
9.9%
SUM06
ppm-h
Mean
26.8
34.5
27.7
27.4
27.7
31.2
45.2
24.8
25.8
28.3
29.5
CV
68.8%
58.1%
58.4%
59.6%
65.0%
56.4%
46.8%
78.7%
76.2%
74.2%
42.1%
SIGMOID
ppm-h
Mean
26.3
33.0
27.4
27.4
27.7
30.4
42.9
25.8
26.6
28.9
29.4
CV
56.7%
52.3%
47.9%
47.6%
51.8%
46.8%
42.4%
59.4%
59.2%
59.5%
31.0%
5 mo (May-September)
Year
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
Among
No. of
Sites
88
87
95
114
118
116
134
158
172
190
Years
M7
ppm
SUMOO
Mean CV
0.
0.
0.
0.
0.
0.
0.
0.
048 20
051 22
048 18
048 18
048 20
050 20
054 18
047 18
0.049 19
0.
050 19
0.049 9
.6%
.1%
.0%
.4%
.3%
.3%
.7%
.6%
.8%
.8%
.8%
ppm
Mean
122.9
129.6
126.2
124.5
123.3
128.7
141.7
127.8
129.4
130.6
129.0
•h
CV
22.3%
24.4%
19.1%
19.4%
21.4%
20.4%
22.0%
22.5%
22.7%
23.6%
9.9%
SUM06
Mean
37.
44.
36.
36.
34.
42.
58.
32.
34.
36.
38.
ppm-h
3
4
7
2
9
2
0
7
6
8
7
CV
70.9%
61.9%
60.8%
63.8%
70.7%
62.0%
50.5%
87.8%
82.7%
80.7%
42.5%
SIGMOID
ppm
Mean
37.1
43.8
37.6
37.0
35.6
41.8
55.6
35.2
37.0
38.8
39.6
•h
CV
57.8%
52.7%
46.9%
50.3%
55.7%
50.3%
45.0%
64.1%
62.1%
62.9%
29.8%
aUpdated and additional years from data given in Table III of Tingey et al. (1991), where the spatial and
temporal variation in ambient O3 exposures is expressed in terms of several exposure indices.
blndicates the number of separate monitoring sites included in the analysis; fewer sites had 5 mo of
available data than had 3 mo of available data.
The 2HDM index is calculated for sites with at least 3 mo of available data. SUMOO, SUM06, M7,
SIGMOID, and 2HDM are the cumulative sum above 0.0 ppm, the cumulative sum above 0.06 ppm, the
7-h seasonal mean, the sigmoid weighted summed concentration, and the second highest daily maximum 1-h
concentration, respectively.
dCV = coefficient of variation.
Source: Tingey et al. (1991).
5-145
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Table 5-21. Comparison of Exposure-Response Curves Calculated
Using the 3-Month, 24-Hour SUM06 Values for
54 National Crop Loss Assessment Network Cases3
Species
Barley
Barley
(Linear)
(Linear)
Corn (L)
Corn (L)
Cotton
Cotton
Cotton
Cotton
Cotton
Linear)
Cotton
Linear)
Cotton
Cotton
Cotton
Kidney
Kidney
Lettuce
Peanut
Potato
Potato
(L)
(L)
(L)
(L)
(L,
(L,
Bean
Bean (L)
(T)
(L)
Sorghum
Soybean
Soybean
Soybean
Soybean
Cultivar
CM-72
CM-72
Pio
Pag
Acala
Acala
Acala
Acala
Acala
Acala
Stoneville
McNair
McNair
California
Light Red
California
Light Red
Empire
NC-6
Norchip
Norchip
Dekalb
Corsoy
Corsoy
Amsoy
Pella
Moistureb
Dry 7
Wet 8
9
10
Dry 6
Wet 9
Dry 7
Wet 7
Dry
Wet
o
J
Dry 3
Wet 4
2
2
7
6
5
5
8
2
1
1
2
Wiebull/Linwear Model
Parameters0
ABC
,741.1
,776.6
,627.4
,730.1
,465.0
,808.0
,009.8
,858.8
5.693
5. ,883
,576.1
,698.8
,811.0
,488.2
,484.3
,196.6
,402.5
,900.7
,755.6
,046.2
,652.6
,891.7
,907.2
,619.9
-4.412
15.485
92.61
94.36
92.59
71.17
83.78
78.01
-0.0011
-0.0017
94.6
165.81
117.02
27.41
44.24
54.87
100.12
93.84
79.26
178.05
57.1
65.21
75.91
174.13
2.823
4.316
2.361
1.997
1.849
1.311
2.012
2.778
1.534
3.885
2.691
5.512
2.226
1.000
1.654
2.338
1.726
5.160
2.739
1.000
RMSE
1,215
1,175
680
1,248
1,097
521
949
937
104
90
226
342
366
333
397
613
351
742
675
441
166
282
390
311
d R2e
0.12
NA
0.93
0.80
0.45
0.96
0.80
0.85
0.06
0.20
0.91
0.46
0.89
0.72
0.71
0.74
0.97
0.63
0.49
0.48
0.91
0.63
0.41
0.51
3 mo 24-h SUM06f
Values for Yield
Losses of
10% 30%
175.5
250.0
41.7
56.0
35.7
23.1
24.8
14.0
94.9
60.3
30.9
73.8
27.0
15.4
19.2
36.5
36.4
9.9
20.3
68.0
15.5
42.2
33.4
18.3
526.
250.
64.
74.
59.
42.
48.
35.
321.
204.
56.
114.
59.
21.
30.
45.
63.
33.
42.
4
0
3
3
8
5
0
5
3
0
7
4
7
0
2
5
0
5
5
114.6
31.
53.
52.
62.
4
4
1
1
5-146
-------
Table 5-21 (cont'd). Comparison of Exposure-Response Curves
Calculated Using the 3-Month, 24-Hour SUM06 Values for
54 National Crop Loss Assessment Network Cases3
Species
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Tobacco (L)
Turnip (T)
Turnip (T)
Turnip (T)
Turnip (T)
Wheat
Wheat
Cultivar
Williams
Corsoy
Corsoy
Corsoy
Corsoy
Corsoy
Corsoy
Williams
Williams
Hodgson
Davis
Davis
Davis
Davis
Davis
Davis
Young
Young
McNair
Just Right
Purple Top
Shogon
Tokyo Cross
Abe
Arthur
Wiebull/Linwear Model
Parameters0
Moistureb ABC
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
2,368.4
2,229.8
2,913.8
3,528.1
4,905.0
5,676.1
5,873.9
6,305.2
7,338.4
2,052.4
3,929.7
4,815.5
2,007.1
4,568.0
5,775.6
8,082.7
5,978.8
7,045.0
5,177.4
12.7
5.7
4.4
11.7
5,149.8
4,455.8
146.37
92.0
311.04
103.83
117.98
97.46
65.73
99.18
78.71
79.97
131.57
85.71
542.36
158.57
90.18
113.89
183.63
145.63
172.55
25.68
29.26
29.18
27.83
52.89
60.87
1.000
9.593
1.527
15.709
3.590
1.000
1.319
1.456
1.344
1.000
1.000
1.734
1.000
1.539
3.348
1.442
1.448
1.277
1.186
1.806
1.437
1.548
2.142
3.077
2.176
RMSEd
527
193
330
400
401
508
512
389
377
361
524
346
556
495
920
927
244
424
306
0.810
0.590
0.660
3.250
399
264
P/
0.27
0.16
0.38
0.55
0.80
0.81
0.89
0.87
0.94
0.78
0.64
0.87
0.04
0.61
0.55
0.71
0.93
0.93
0.81
0.96
0.92
0.81
0.78
0.90
0.92
3 mo 24-h SUM06f
Values for Yield
Losses of
10% 30%
15.4
72.8
71.3
90.0
63.0
10.3
11.9
21.1
14.8
8.4
13.9
23.4
57.1
36.8
46.0
23.9
38.8
25.0
25.9
7.4
6.1
6.8
9.7
25.5
21.6
52.2
82.6
158.4
97.2
88.5
34.8
30.1
48.8
36.5
28.5
46.9
47.3
193.4
81.2
66.3
55.7
90.1
65.0
72.3
14.5
14.3
15.0
17.2
37.8
37.9
5-147
-------
Table 5-21 (cont'd). Comparison of Exposure-Response Curves
Calculated Using the 3-Month, 24-Hour SUM06 Values for
54 National Crop Loss Assessment Network Cases3
Wiebull/Linwear Model
Parameters0
3 mo 24-h SUM06f
Values for Yield
Losses of
Species
Cultivar Moisture1"
B
C
RMSEd
R2
10%
30%
Wheat
Wheat
Wheat
Wheat
Wheat
Roland
Abe
Arthur
Vona
Vona
5,028.9
6,043.1
5,446.9
5,384.0
4,451.0
52.32
47.39
72.34
27.74
33.5
1.173
7.711
2.462
1.000
1.818
405
226
349
608
654
0.91
0.74
0.57
0.88
0.64
7.7
35.4
29.0
2.9
9.7
21.7
41.5
47.6
9.9
19.0
aSee Appendix A for abbreviations and acronyms.
bWet refers to experiments conducted under well-watered conditions, whereas dry refers to experiment
conducted under some controlled level of drought stress.
Tor those studies whose species name is followed by "Linear", a linear model was fit. A Weibull model was
fit to all other studies, and estimates of "B" parameter are in parts per million per hour. The yield is expressed
in kilograms per hectare for all crops except turnip (grams per meter per plant) and lettuce (grams per meter).
In cases where the estimated "C" parameter is exactly 1.0, the shape parameter has been bounded from below
to obtain convergence in the nonlinear-model-fitting routine. For those studies whose species name is followed
by "L", a log transformation was used to stabilize the variance. For those crops whose name is followed by
"T", the yield is expressed as either grams per plant or grams per meter.
dThe root mean square error, based on individual plot means.
TVhutiple correlation coefficient (R2) measures the proportion of total variation about the mean response
explained by the regression on individual plot means.
fThe 24-h SUM06 value (ppm-h) that was predicted to cause a 10 or 30% yield loss (compared to zero
SUM06).
Source: Based on analyses by Lee et al. (1991, 1994a,b).
based on 24 h), a 7-h seasonal mean of 0.049 ppm, or a 2HDM of 0.094 ppm would be
required. A SUM06 of about 37 ppm-h should limit yield losses to 20% in 50% of the
cases. If one standard error were added to or subtracted to account for the variability, the
metrics would be reduced to 21 ppm-h, 0.046 ppm, and 0.088 ppm or increased to
27.8 ppm-h, 0.049 ppm, and 0.10 ppm, respectively. To limit the loss to 10% or less in 75%
of the cases would require 14.2 ppm-h, 0.040 ppm, and 0.051 ppm, respectively (Table 5-23).
These values are based on studies of both well-watered and drought stressed plants.
Further analyses by Lee et al. (1991, 1994a,b) provides composite exposure-
response functions for all NCLAN studies, as well as for soybean and wheat experiments
(Table 5-22). In the analysis, they calculated the SUM06 based on 24-h/day
O3 concentrations, and the resulting exposure to prevent crops from yield loss is slightly
higher than they previously calculated (26.4 ppm-h versus 24.4 ppm-h; Table 5-23).
5-148
-------
Table 5-22. Comparison of Exposure-Response Curves Calculated
Using the 24-Hour W126 Values for 54 National Crop
Loss Assessment Network Cases3
Species
Barley
Barley
Corn (L)
Corn (L)
Cotton (L)
Cotton (L)
Cotton (L)
Cotton (L)
Cotton (L)
Cotton (L)
Cotton
Cotton
Cotton
Kidney bean
Kidney bean (L)
Lettuce (T)
Peanut (L)
Potato
Potato
Sorghum
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Cultivar
CM-72
CM-72
Pio
Pag
Acala
Acala
Acala
Acala
Acala
Acala
Stoneville
McNair
McNair
California
Light Red
California
Light Red
Empire
NC-6
Norchip
Norchip
Dekalb
Corsoy
Corsoy
Amsoy
Pella
Williams
Corsoy
Moisture1" A
Dry 8,133.2
Wet 8,927.2
9,605.0
10,686.7
Dry 6,482.8
Wet 9,817.3
Dry 7,022.7
Wet 7,927.1
Dry 310.1
Wet 393.2
3,592.1
Dry 3,700.9
Wet 4,817.6
2,484.7
2,475.2
7,197.4
6,386.0
5,867.2
5,777.9
8,049.7
2,660.3
1,895.6
1,926.1
2,602.4
2,341.8
Dry 2,229.3
WeibulF
B
1,109.6
57,439.6
92.9
94.5
89.9
66.6
81.3
74.7
174.1
582.6
94.1
174.1
113.5
28.0
44.2
54.6
97.4
96.3
113.9
205.9
58.8
63.3
79.0
161.5
138.6
88.2
C
1.000
1.000
2.594
4.190
1.949
1.603
1.540
1.070
2.189
1.000
1.582
2.430
1.410
3.706
2.353
4.921
1.905
1.000
1.299
1.963
1.455
4.032
1.977
1.000
1.000
8.632
RMSEd
1,214
1,175
650
1,253
1,075
514
948
943
104
90
223
344
360
332
401
614
370
754
675
439
169
280
390
314
533
192
24-h W126f
Values for Yield
Losses of
R2" 10% 30%
0.13
NA
0.93
0.80
0.47
0.96
0.80
0.85
0.06
0.20
0.91
0.45
0.89
0.72
0.70
0.74
0.96
0.62
0.48
0.48
0.91
0.63
0.41
0.50
0.25
0.16
116.9
6,051.9
39.0
55.2
28.3
16.4
18.8
9.1
62.3
61.4
22.7
68.9
23.0
15.3
17.0
34.6
29.9
10.1
20.1
65.4
12.5
36.2
25.3
17.0
14.6
67.9
395.8
20,487.3
62.4
73.9
53.0
35.0
41.6
28.5
108.7
207.8
49.1
113.9
54.6
21.2
28.5
44.3
56.7
34.3
51.5
121.8
28.9
49.0
46.9
57.6
49.4
78.2
5-149
-------
Table 5-22 (cont'd). Comparison of Exposure-Response Curves
Calculated Using the 24-Hour W126 Values for 54 National
Crop Loss Assessment Network Cases3
Species
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Soybean
Tobacco (L)
Turnip (T)
Turnip (T)
Turnip (T)
Turnip (T)
Wheat
Wheat
Wheat
Wheat
Cultivar
Corsoy
Corsoy
Corsoy
Corsoy
Corsoy
Williams
Williams
Hodgson
Davis
Davis
Davis
Davis
Davis
Davis
Young
Young
McNair
Just Right
Purple Top
Shogon
Tokyo Cross
Abe
Arthur
Rol
Abe
Moistureb
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
Wet
A
2,929.7
3,533.5
4,909.5
5,597.1
5,884.8
6,314.1
7,352.3
2,044.6
3,837.6
4,810.8
1,992.3
4,595.4
5,770.1
8,101.3
5,994.2
7,075.0
5,223.9
12.7
5.8
4.4
11.7
5,138.1
4,467.4
5,074.4
6,042.8
Weibuir
B
470.2
113.2
126.5
95.7
65.6
106.3
80.7
76.2
130.3
87.5
537.6
170.9
90.6
118.2
199.8
149.7
179.8
24.1
28.2
28.2
26.8
53.3
63.8
51.2
48.5
C
1.128
11.095
2.803
1.000
1.139
1.243
1.162
1.000
1.000
1.494
1.000
1.253
2.796
1.220
1.251
1.133
1.018
1.473
1.155
1.174
1.710
2.602
1.747
1.000
5.843
RMSEd
329
403
405
526
515
391
368
361
530
352
558
496
928
939
244
418
291
1.0
1
1
3
407
264
397
225
24-h W126f
Values for Yield
Losses of
R2" 10% 30%
0.39
0.54
0.80
0.80
0.88
0.87
0.95
0.78
0.63
0.86
0.03
0.61
0.54
0.70
0.93
0.93
0.83
0.96
0.92
0.82
0.78
0.89
0.92
0.91
0.75
64.0
92.4
56.7
10.1
9.1
17.4
11.6
8.0
13.7
19.4
56.6
28.4
40.5
18.7
33.1
20.5
19.7
5.2
4.0
4.1
7.2
22.4
17.6
5.4
33.0
188.6
103.1
87.6
34.1
26.6
46.4
33.2
27.2
46.5
43.9
191.7
75.1
62.7
50.8
87.7
60.2
65.3
12.0
11.6
11.7
14.7
35.8
35.4
18.3
40.6
5-150
-------
Table 5-22 (cont'd). Comparison of Exposure-Response Curves
Calculated Using the 24-Hour W126 Values for 54 National
Crop Loss Assessment Network Cases3
24-h W126f
Values for Yield
Weibuir
Species
Wheat
Wheat
Wheat
Cultivar
Arthur
Vona
Vona
Moisture15 A
5,440.0
5,300.8
4,462.7
B
76.1
25.0
32.3
C
2.100
1.000
1.517
RMSEd R2"
349 0.57
679 0.85
665 0.63
Losses of
10%
26.1
2.6
7.3
30%
46.6
8.9
16.4
aSee Appendix A for abbreviations and acronyms.
bWet refers to experiments conducted under well-watered conditions, whereas dry refers to experiments
conducted under some controlled level of drought.
°A11 estimates of "B" parameter are in parts per million per hour. The yield is expressed in kilograms per
hectare for all crops except turnip (grams per plant) and lettuce (grams per meter). In cases where the
estimated "C" parameter is exactly 1.0, the shape parameter has been bounded from below to obtain
convergence in the nonlinear-model-fitting routine. For those studies whose species name is followed by "L".
a log transformation was used to stabilize the variance. For those crops whose name is followed by "T", the
yield is expressed as either grams per plant or grams per meter.
dThe root mean square error, based on individual plot means.
TVfultiple correlation coefficient (R2) measures the proportion of total variation about the mean response
explained by the regression on individual plot means.
fThe 24-h W126 value (parts per million per hour) that was predicted to cause a 10 or 30% yield loss
(compared to zero W126).
Source: Based on analyses by Lee et al. (1991, 1994a,b).
Research since 1986 has focused largely on understanding the response of trees
and other perennials to O3 (covered in the next section) and of five crop species: (1) cotton,
(2) wheat, (3) spring rape, (4) bean, and (5) soybean. A number of the studies were
conducted as part of NCLAN, but many also were the result of research activity in Europe.
Results of these studies, as well as those species studied less intensively, are summarized in
Table 5-25. A composite exposure-response function is illustrated in Figure 5-29.
Yield losses in cotton of 13 to 19% have been reported at 12-h mean
concentrations of 0.050 or 0.044 ppm by Heagle et al. (1988a) and Temple et al. (1988b)
(Table 5-25). These are typical ambient concentrations, as listed under M7 (Table 5-20).
The same experiments showed that drought stress reduced the predicted yield loss due to O3,
but did not eliminate it.
Wheat yields have been reduced by 0 to 29%, depending on the cultivar and
exposure conditions (Adaros et al., 1991a; Fuhrer et al., 1989; Grandjean and Fuhrer, 1989;
Kohut et al., 1987; Pleijel et al., 1991) (Table 5-25). In no case was a 7-h average of greater
than 0.062 ppm required to cause the reported loss, but Slaughter et al. (1989) suggest that
hourly concentrations above 0.06 ppm during the period following anthesis may be
particularly effective in reducing yield.
5-151
-------
Table 5-23. The Exposure Levels (Using Various Indices)
Estimated To Cause at Least 10% Crop Loss in
50 and 75% of Experimental Cases3
50th PERCENTILEb
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
Cotton Data (N =
Soybean Data (N
Wheat Data (N =
Cotton Data (N =
Soybean Data (N
Wheat Data (N =
= 49;
= 39;
= 54;
= 42;
= 10;
= 10;
5)
= 13)
6)
5)e
= 15)
7)e
wet
wet
wet
wet
wet)
diy)
e
and dry)d
only)
and dry)6
only)6
SUM06
24.4
22.3
26.4
23.4
25.9
45.7
23.6
26.2
21.3
30.0
23.9
25.9
SEC SIGMOID
3.4
1.0
3.2
3.1
4.5
23.3
2.3
5.4
15.2
12.7
6.5
10.5
21.5
19.4
23.5
22.9
23.4
40.6
19.3
22.6
19.3
27.2
22.0
21.4
SE
2.0
2.3
2.4
4.7
3.2
0.1
2.3
3.6
12.7
12.8
8.0
9.4
M7
0.049
0.046
NA
NA
0.041
0.059
0.041
0.044
0.061
NA
NA
NA
SE
0.003
0.003
NA
NA
0.001
0.014
0.001
0.005
0.018
NA
NA
NA
2HDM
0.094
0.090
0.099
0.089
0.110
0.119
0.066
0.085
0.098
0.075
0.088
0.097
SE
0.006
0.010
0.011
0.008
0.042
0.017
0.032
0.013
0.059
0.012
0.008
0.028
75th PERCENTILEb
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
NCLAN Data (N
Cotton Data (N =
Soybean Data (N
Wheat Data (N =
Cotton Data (N =
Soybean Data (N
Wheat Data (N =
= 49;
= 39;
= 54;
= 42;
= 10;
= 10;
5)
= 13)
6)
5)e
= 15)
7)e
wet
wet
wet
wet
wet)
dry)
e
and dry)
only)
and dry)6
only)6
14.2
14.3
16.5
17.2
16.4
24.0
21.8
14.2
11.7
21.1
15.3
5.1
4.2
2.7
4.3
3.0
3.7
0.8
5.0
0.1
2.5
6.0
4.1
2.6
11.9
12.6
14.5
14.7
13.7
22.3
17.5
12.4
10.9
16.7
13.4
8.5
5.6
2.3
3.2
2.4
3.2
0.1
2.8
0.1
2.4
5.7
4.1
3.4
0.040
0.039
NA
NA
0.040
0.053
0.041
0.041
0.054
NA
NA
NA
0.007
0.005
NA
NA
0.001
0.022
0.001
0.006
0.032
NA
NA
NA
0.051
0.056
0.073
0.070
0.080
0.093
0.065
0.069
0.062
0.070
0.078
0.054
0.010
0.006
0.006
0.006
0.032
0.003
0.014
0.004
0.035
0.034
0.007
0.027
aSee Appendix A for abbreviations and acronyms.
bThe numbers in parentheses are the number of cases used in deriving the various exposure levels.
"Standard error (SE).
dNCLAN data refers to studies conducted as part of the NCLAN project. Wet and dry refer to watery regimes
used in the studies, wet being well-watered, and dry meaning some level of drought stress was imposed.
624-h exposure statistics reported in Lee et al. (1994b). Relative yield loss for 2HDM is relative to yield at
0.04 ppm rather than 0.00 ppm as was used in Tingey et al. (1991).
Source: Modified from Tingey et al. (1991).
Studies with spring rape in Europe have documented yield losses of 9.5 to 26.9%
at 8-h growing season average concentrations ranging from 0.03 to 0.06 ppm (Adaros et al.,
1991b,c) (Table 5-26).
The yield of beans (fresh pods) was reduced by 17% at a 7-h average of
0.045 ppm (Schenone et al., 1992) or 20% at an 8-h growing season average of 0.080 ppm
(Bender et al., 1990). In a similar study, Heck et al. (1988) found that the predicted yield of
sensitive cultivars was reduced an average of 17.3% by exposure to a 7-h growing season
5-152
-------
Table 5-24. SUM06 Levels Associated with 10 and 20% Yield Loss for
50 and 75% of the National Crop Loss Assessment Network (NCLAN)
Crop Studies3
Weibull Equations (all 54 NCLAN studies):
50th Percentileb PRYL = 1 - exp(-[SUM06/89.497]**l.84461)
75th Percentile PRYL = 1 - exp(-[SUM06/60.901]**1.72020)
Weibull Equations (all 22 NCLAN soybean studies; 15 well-watered, 7 water-stress):
50th Percentile PRYL = 1 - exp(-[SUM06/117.68]**1.46509)
75th Percentile PRYL = 1 - exp(-[SUM06/88.99]**1.47115)
Weibull Equations (15 NCLAN well-watered soybean studies):
50th Percentile PRYL = 1 - exp(-[SUM06/112.75]**1.46150)
75th Percentile PRYL = 1 - exp(-[SUM06/79.62]**l.36037)
Weibull Equations (7 NCLAN wheat studies):
50th Percentile PRYL = 1 - exp(-[SUM06/49.02]**3.52788)
75th Percentile PRYL = 1 - exp(-[SUM06/29.56]**1.29923)
SUM06 Levels Associated with 10 and 20% Yield Loss for 50 and 75% of the Crops:
All 54 NCLAN Cases
All 22 NCLAN Soybean Cases
15 Well-Watered Soybean Cases
Percent of Crops
50% 75%
Relative 10% 26.4 16.5
Yield Loss 20% 39.7 25.5
Percent of Crops
50% 75%
Relative 10% 25.3 19.3
Yield Loss 20% 42.3 32.1
Percent of Crops
50% 75%
Relative 10% 24.2 15.2
Yield Loss 20% 40.4 26.4
All Seven NCLAN Wheat Cases
Relative
Yield Loss
10%
20%
Percent of Crops
50% 75%
25.9 5.2
32.0 9.3
aSee Appendix A for abbreviations and acronyms.
b50th and 75th percentiles refer to the percentage of studies analyzed in which loss of the stated magnitude
would have been prevented.
Source: Based on analyses by Lee et al. (1994b).
5-153
-------
Table 5-25. A Summary of Studies Reporting the Effects of Ozone
on the Growth, Productivity, or Yield of Annual Plants Published Since
U.S. Environmental Protection Agency (1986)a
Species
Soybean
Soybean
Soybean
Soybean
Soybean
-------
Table 5-25 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Annual Plants
Published Since U.S. Environmental Protection Agency (1986)a
Species
Concentration
Duration
Facility0 Variable*
Effect6
Reference
en
01
01
Cotton
Cotton
Cotton
Cotton
Cotton
Bean, fresh
Bean, fresh
Bean, fresh
Bean, fresh
Bean, dry
15 to 111 ppb 12-h mean 123 days
10 to 90 ppb 12-h mean 102 days
25 to 74 ppb 12-h mean 123 days
22 to 44 ppb 12-h mean 124 days
26 to 104 ppb 7-h mean 119 days
35 to 132 ppb 7-h mean 42 days
11 to 40 ppb 12-h mean, 69 days
7 to 42 ppm-h
OTC
Leaf, stem,
and root
weight
OTC Lint weight
OTC Lint weight
OTC Lint weight
OTC Lint weight
OTC in pots Green pod
weight
OTC Pod weight
26 to 126 ppb 7-h mean 26 days and OTC in pots Pod weight
44 days, early
and late in
season
24 to 109 ppb 8-h mean 43 days 34 days, OTC Pod weight
two growing
seasons
15 to 116 ppb 12-h mean, 54 days
339 ppb highest hour
OTC Seed yield
Up to 42% reduction in leaf
and stem and 61% reduction in
root weights.
40 to 71% reduction at highest
concentration determinant
cultivars more susceptible.
Predicted loss of 26.2% at
74 ppb.
Predicted loss of 19% at
44 ppb.
Predicted loss of 11% at
53 ppb.
Significant yield reductions of
>10% in eight lines at 63 ppb
7-h mean.
15.5% reduction at 45 ppb
(39 ppm-h).
3.5 to 26% reduction in
resistant and sensitive cultivars
at 55 to 60 ppb.
20% reduction at 80 ppb.
55 to 75% reduction at 72 ppb
12-h mean, 198 highest hour.
Temple et al.
(1988c)
Temple (1990b)
Temple et al.
(1988b)
Heagle et al.
(1988a)
Heagle et al.
(1986a)
Eason and Reinert
(1991)
Schenone et al.
(1992)
Heck et al. (1988)
Bender et al.
(1990)
Temple (1991)
-------
Table 5-25 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Annual Plants
Published Since U.S. Environmental Protection Agency (1986)a
en
Oi
O)
Species
Bean, dry
Bean, dry
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Wheat, spring
Concentration15
10 to 50 ppb 7-h mean
300 ppb
14 to 46 ppb 24-h mean
21.6 to 80 and
24.6 to 93.5 ppm-h
3 to 56 ppb 7-h mean
8 to 101 and 20 to
221 ppb 8-h mean
0 to 38 ppb 8-h mean
17 to 77 ppb 7-h mean
25 to 75 ppb 8-h mean
6 to 10 ppb, 6 h/day
10 to 125 ppb,
6 h/day
Duration
86 days
3 h, two exposures
79, 92, and 79 days
in three growing
seasons
82 and 88 days in
two growing seasons
61 and 55 days in
two growing seasons
118 and 98 days in
two growing seasons
Entire growing
season
90 and 87 days in
two growing seasons
40 days
21 days
21 and 17 days
Facility0
OTC
GC
OTC
OTC
OTC
OTC
OTC
OTC
OTC
GC
GC
Variable11
Seed weight
Dry weight
Seed weight
Seed weight
Seed weight
Seed weight
Seed weight
Seed weight
Total weight
Shoot dry
weight
Top dry
weight
Effect6
26 to 42% reduction at
38 to 50 ppb.
Growth response detected
if exposure separated by
3 to 5 days.
13% reduction at 40 ppb.
48 to 54% reduction at
80 and 93.5 ppm-h.
7% reduction at 15 and
22 ppb.
10% reduction at 17 to
23 ppb.
5% reduction at 38 ppb.
9.5 to 11.6 reduction at
37 and 45 ppb.
Reductions at 75 ppb.
Decreased 35 to 60% at
101 ppb in low and high
light.
Reduced by up to 35%.
Reference
Sanders et al.
(1992)
McCool et al.
(1988)
Fuhrer et al.
(1989)
Grandjean and
Fuhrer (1989)
Pleijel et al.
(1991)
Adaros et al.
(1991a)
De Temmerman
et al. (1992)
Fuhrer et al.
(1992)
Johnsen et al.
(1988)
Mortensen
(1990b)
Mortensen
(1990c)
-------
Oi
Oi
Table 5-25 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Annual Plants
Published Since U.S. Environmental Protection Agency (1986)a
Species
Wheat, winter
Wheat, winter
Wheat, winter
Wheat, winter
Wheat, winter
Barley, spring
Barley, spring
Barley, spring
Rape, spring
Rape, spring
Concentration15
1 1 to 42 ppb
14-week mean
30 to 93 ppb
4-h mean
27 to 96 ppb
7-h mean
22 to 96 ppb
7-h mean
23 to 123 ppb
4h/day
6 to 45 ppb
7-h mean
0.6 to 27 ppb
monthly mean
0.8 to 83 ppb
8-h mean
25 to 75 ppb
8-h mean
0.8 to 83 ppb
8-h mean
Duration
109 days
39 and 40 days in
two growing seasons
5 days/week 4 h/day
36 days
65 days and 36 days
in two growing
seasons
5 days at anthesis
96 days
Growing season
97, 108, and 98 days
in three growing
seasons
31 days
89, 113, and 84 days
in three growing
seasons
Facility0
OTC
OTC
OTC
OTC
OTC
OTC
OTC
OTC in pots
OTC
OTC in pots
Variable11
Seed weight
Seed weight
Seed weight/
head
Seed weight
Seed weight
Seed weight
Seed weight
Seed weight
Premature
senescence
Seed weight
Effect6
No effect.
Exposures >60 ppb during
anthesis reduce yield.
50% reduction at 96 ppb.
33 and 22% reductions at
42 and 54 ppb, respectively.
Up to 28% reduction.
No effect.
No effect.
0 to 13% reduction at
highest.
Increased at 75 ppb.
9.4 to 16% reduction at
30 or 51 ppb.
Reference
Olszyk et al.
(1986b)
Slaughter et al.
(1989)
Amundson et al.
(1987)
Kohut et al. (1987)
Mulchi et al. (1986)
Pleijel et al. (1992)
Weigel et al. (1987)
Adaros et al.
(1991b)
Johnsen et al.
(1988)
Adaros et al.
(1991b)
-------
Table 5-25 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Annual Plants
Published Since U.S. Environmental Protection Agency (1986)a
en
Oi
00
Species
Rape, spring
Tomato
Tomato
Tomato
Moss campion
Buckhorn
16 Other species
Radish
Lettuce
Lettuce
Faba bean
Fenugreek
Concentration15
43 to 60 ppb 8-h mean
13 to 0.109 ppm
12-h mean, 79.5 ppm-h
10 to 85 ppb, 6 li/day
18 to 66 ppb 12-h mean
5 to 80 ppb, 8 h/day
5 to 80 ppb, 8 h/day
5 to 80 ppb, 8 h/day
20 or 70 ppb 24-h mean
21 to 128 ppb 7-hmean
10 to 34 ppb 7-week
mean
6 or 15 ppb 24-h mean
120 ppb, 7 h/day
Duration
89, 113, and
84 days in
three growing
seasons
75 days
12 to 21 days
11 weeks
Up to 90 days
Up to 90 days
Up to 90 days
27 days
52 days
64 days
134 days
4 weeks
Facility0
OTC in pots
OTC
GC
OTC
GC
GC
GC
GC
OTC
OTC
OTC
CC
Variable11
Seed weight
Fresh weight
Shoot dry weight
Fresh fruit
weight
Dry weight
Dry weight
Dry weight
Shoot and root
growth
Head weight
Fresh weight
Seed weight
Dry weight
Effect6
12 to 27% reduction.
17 to 54% reduction
at 0.109 ppm; no
reduction at ambient.
35 to 62% reduction.
No effect.
25% reduction at
80 ppb.
14% reduction at
50 ppb.
No effect.
36 and 45% reduction
at 70 ppb.
Significant reduction
at 83 ppb, 35% at
128 ppb.
No effect.
No effect.
No significant effect.
Reference
Adaros et al. (1991c)
Temple (1990a)
Mortensen (1992b)
Takemoto et al.
(1988c)
Mortensen and Nilsen
(1992)
Mortensen and Nilsen
(1992)
Mortensen and Nilsen
(1992)
Barnes and Pfirrman
(1992)
Temple et al. (1986)
Olszyk et al. (1986b)
Sanders et al. (1990)
Kasana (1991)
-------
Table 5-25 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Annual Plants
Published Since U.S. Environmental Protection Agency (1986)a
Species
Chickpea
Gram, black
Rice
Rice
Watermelon
Pea
en
en Green pepper
CD
Green pepper
Celery
Concentration15
120 ppb, 7 h/day
120 ppb, 7 h/day
0 to 200 ppb, 5 h/day
50 ppb 24-h mean
15 to 27 ppb 7-h mean
10 to 35 ppb 12-h mean
19 to 66 ppb 12-h mean
18 to 66 ppb 12-h mean
18 to 66 ppb 12-h mean
Duration Facility0
4 weeks CC
4 weeks CC
5 days/week OTC
15 weeks
8 weeks GC
81 days OTC
58 and 52 days in OF
two growing
seasons
77 days OTC
11 weeks OTC
11 weeks OTC
Variable11
Dry weight
Dry weight
Seed weight
Dry weight
Fresh weight
and number
(marketable)
Fresh weight
Fresh fruit
weight
Fresh fruit
weight
Shoot dy
weight
Effect6
No significant effect.
No significant effect.
12 to 21% reduction at
200 ppb.
No effect at 50 ppb.
20.8 and 21.5% reduction at
27 ppb.
Linear decrease in yield with
increasing O3.
12% reduction at
13% reduction in
66 ppb.
12% reduction at
66 ppb.
fruit weight at
66 ppb.
Reference
Kasana (1991)
Kasana (1991)
Kats et al. (1985)
Nouchi et al.
(1991)
Snyder et al.
(1991)
Runeckles et al.
(1990)
Takemoto et al.
(1988c)
Takemoto et al.
(1988c)
Takemoto et al.
(1988c)
aSee Appendix A for abbreviations and acronyms.
bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposures are SUMOO unless
otherwise specified; accumulation based on 24 h/day unless otherwise noted.
°OTC = open-top chamber with plants in ground unless specified in pots; CC = closed chamber, outside; GC = controlled environment growth chamber
or CSTR; OF = open-field fumigation.
dThe effect reported in the study that is a measure of growth, yield, or productivity.
eEffect measured at specified ozone concentration, over the range specified under concentration, or predicted (if specified) to occur based on relationships developed
in the experiment.
-------
A 100%-
90%-
80%-
o>70%-
•Jj40%-
«
CD
CC30%-
20%-
10%-
B
m
100%-
90%
80%
70%.
60% •
50%.
40%.
30%.
20%.
10%.
0% •
Crops
75th Percentile
50th Percentile
25th Percentile
10
20
30 40
24-h SUM06 (ppm-h)
"T"
50
60
Tree Seedlings
75th Percentile
50th Percentile
25th Percentile
10
~ I I [ I ~~ I""
20 30 40 50 60
24-h SUM06 (ppm-h) (adjusted to 92 days)
Figure 5-29. Box-plot distribution of biomass loss predictions from Weibull and linear
exposure-response models that relate biomass and ozone exposure as
characterized by the 24-h SUM06 statistic using data from (A) 31 crop
studies from National Crop Loss Assessment Network (NCLAN) and
(B) 26 tree seedling studies conducted at U.S. Environmental Protection
Agency's Environmental Research Laboratory in Corvallis, OR; Smoky
Mountains National Park, TN; Michigan; Ohio; and Alabama. Separate
regressions were calculated for studies with multiple harvests or cultivars,
resulting in a total of 54 individual equations from the 31 NCLAN studies
and 56 equations from the 26 seedling studies. Each equation was used to
calculate the predicted relative yield or biomass loss at 10, 20, 30, 40, 50, and
60 ppm -h, and the distributions of the resulting loss were plotted. The solid
line is the calculated Weibull fit at the 50th percentile (from Hogsett et al,
1995).
5-160
-------
cn
O)
Table 5-26. A Summary of Studies Reporting the Effects of
Ozone on the Growth, Productivity, or Yield of Perennial Crop Plants
Published Since U.S. Environmental Protection Agency (1986)a
Species
Strawberry
Timothy
Orchard grass
Kentucky blue
grass
Red grass
Tall fescue
Colonial bent grass
Rye grass
Red clover
Common plantain
Red clover
Timothy
Concentration15
18 to 66 ppb 12-h mean
10 to 55 ppb 7-h mean
10 to 55 ppb 7-h mean
10 to 55 ppb 7-h mean
10 to 55 ppb 7-h mean
10 to 55 ppb 7-h mean
10 to 55 ppb 7-h mean
62 ppb 7-h mean
6 to 59 ppb 7-h mean
70 ppb 7-h mean
19 to 62 ppb 12-h mean
19 to 62 ppb 12-h mean
Duration
11 weeks
5 weeks
5 weeks
5 weeks
5 weeks
5 weeks
5 weeks
5 weeks
5 weeks
8 weeks
83 and 91 days in
two growing seasons
83 and 91 days in
two growing seasons
Facility0
OTC
GC
GC
GC
GC
GC
GC
GC
GC
GC
OTC
OTC
Variable11
Fresh fruit
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Shoot dry
weight
Total dry
weight
Dry weight
Dry weight
Effect6
20% increase in fruit
weight at 66 ppb.
45% reduction at 55 ppb.
28% reduction at 55 ppb.
28% reduction at 55 ppb.
23% reduction at 55 ppb.
16% reduction at 55 ppb.
No effect.
No effect.
30% reduction at 59 ppb.
Reduced up to 36%
depending on growth
stage.
11% reduction at 62 ppb.
No effect.
Reference
Takemoto et al.
(1988c)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Mortensen (1992a)
Reiling and
Davison (1992c)
Kohut et al.
(1988a)
Kohut et al.
(1988a)
-------
Table 5-26 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth, Poductivity, or Yield of Perennial Crop Plants
Published Since U.S. Environmental Protection Agency (1986)a
Species
Concentration15
Ladino clover- 22 to 114 ppb 12-h mean
tall fescue pasture
Ladino clover 28 to 46 ppb 12-h mean
Alfalfa
Alfalfa
y, Alfalfa
i
8 Alfalfa
Alfalfa
Grape
14 to 98 ppb 12-h mean
20 to 53 ppb 12-h mean
18 to 66 ppb 12-h mean
10 to 109 ppb 12-h mean
60 to 80 ppb 6-h day
Not reported
Duration
Five 3- to 4-week
exposure periods.
Six 3- to 4-week
exposures in 2 years
180 and 191 days in
two growing seasons
32 days
11 weeks
11 weeks
208 and 200 days in
two growing seasons
5 days/week for
8 weeks
Two growing seasons
Facility0 Variable11
OTC Shoot dry
weight,
root dry
weight
OTC Dry weight
OTC Dry weight
OTC Dry weight
OTC Shoot dry
weight
OTC Dry weight
GH Relative
growth rate
OTC Yield
Effect6
18 to 50% reduction in shoot dry
weight (SOW) at 40 to 47 ppb clover;
25% reduction root dry weight at
40 to 47 ppb. SOW increased by up
to 50% in fescue.
Predicted yield of mix reduced 10%,
with 19% decrease in clover and
19% increase in fescue at 46 ppb.
2.4% reduction at 40 ppb, 18.3%
reduction at 66 ppb.
22% reduction at 53 ppb.
22% reduction at 36 ppb.
0 to 25% reduction at levels of
38 ppb and above.
Reduced up to 40% in Saranac.
No effects of ambient air vs. filtration.
Reference
Rebbeck et al.
(1988)
Heagle et al.
(1989b)
Temple et al. (1987)
Takemoto et al.
(1988a)
Takemoto et al.
(1988c)
Temple et al.
(1988a)
Cooley and Manning
(1988)
Musselman et al.
(1985)
aSee Appendix A for abbreviations and acronyms.
bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposures are SUMOO unless
otherwise specified; accumulation based on 24 h/day unless otherwise noted.
°OTC = open-top chamber with plants in ground unless specified in pots; GC = controlled environment growth chamber or CSTR; GH = greenhouse.
dThe effect reported in the study that is a measure of growth, yield, or productivity.
eEffect measured at specified ozone concentration, over the range specified under concentration, or predicted (if specified) to occur based on relationships developed
in the experiment.
-------
mean of 0.05 ppm, but resistant cultivars suffered only a 1.6% loss. Temple (1991) reported
reductions in dry bean yield of 44 to 73% in three cultivars grown in California and exposed
to a 12-h seasonal mean of 0.072 ppm. One other cultivar increased in yield in NF chambers
but was severely affected in higher concentration O3 treatments. Sanders et al. (1992) also
observed yield stimulation at a 7-h growing season mean of 0.025 ppm; however, significant
yield reductions were measured as O3 concentrations increased to 50 ppb (7-h seasonal mean).
Several studies have shown soybean yields to be reduced by 10 to 15% at 7- or
12-h seasonal mean concentrations of 0.05 to 0.055 ppm (Table 5-26; Heagle et al., 1986b,
1987a; Heggestad and Lesser, 1990; Miller et al., 1989b).
A number of the studies cited above and some of those in Table 5-26 were
conducted as part of NCLAN and are considered in the discussions of Tingey et al. (1991),
Lee et al. (1993), and Lesser et al. (1990), but many of the experiments (primarily those not
part of NCLAN) were not included in their analyses. Although the range of variability in
species response to O3 is apparent, these studies support, for the most part, the conclusions of
U.S. Environmental Protection Agency (1986), Tingey et al. (1991), and Lesser et al. (1990).
Table 5-24 summarizes the studies reporting the response of annual plants, particularly crops,
as growth, dry weight, or yield to O3 exposures (C x T) under experimental conditions since
the previous criteria document (U.S. Environmental Protection Agency, 1986). Based on the
results of the studies reviewed in this section, including the reanalysis of NCLAN, exposures
for a 3-mo period to O3 concentrations currently occurring in the ambient air (0.048 to 0.06
ppm, 7-h seasonal mean; see M7, Table 5-20) have been shown to cause losses of 10% or
more in the yield of the majority of major crop plants grown in the country. A number of
crop species are more sensitive, and greater losses could be expected (Tables 5-21 through 5-
25). It should be noted that a variety of methodologies has been used to generate these data.
Generally speaking, data obtained through growth chamber experiments and experiments
conducted using potted plants, in fact, are more scientifically reliable but less relevant to
ambient conditions when assessing the effects of O3 than are results from field growth plants.
5.6.4 Effects of Ozone on Long-Lived Plants
Quantifying exposure-response in the case of perennial plants (agricultural crops
such as pastures, alfalfa, and shrubs and trees) is complicated by they fact that they can
receive multi-year exposures and because the results of exposures in a previous year, or over
a number of years, may be cumulative. Reduction in growth and productivity, a result of
altered carbon allocation, may appear only after a number of years or when carbohydrate
reserves are depleted (U.S. Environmental Protection Agency, 1986; Laurence et al., 1993;
Garner, 1991; Garner et al., 1989). A further complication is that, in the case of evergreen
plants, the life span of a leaf exceeds 1 year and usually persists for several years. In such
cases, loss of a leaf or a reduction in photosynthetic performance may have a large effect on
a plant's ability to survive and grow. Physiological differences among species (rates of gas
exchange, for instance) may have a tendency to equalize exposure over a number of years,
however, as shown in Reich's (1987) analysis of crops, hardwoods, and conifers and in Pye's
analysis of tree species (1988). Unfortunately, there is little experimental data regarding the
effects of long-term O3 exposure on perennial plants, because only a few experimental studies
have extended exposures beyond a single growing season. Most of what is known regarding
the effects of O3 on mature trees is from field observations. There have been some studies
that have extended observation of growth alterations into the season following exposures and,
5-163
-------
thus, observed "carry-over effects" in several species. Hogsett et al. (1989) reported altered
bud elongation in ponderosa pine, lodgepole pine (Pinus contorta), and western hemlock
(Tsuga heterphylla), following a season of O3 exposure. Altered root regrowth in ponderosa
pine in the season following exposure that was correlated with root storage carbohydrate was
observed by Andersen et al. (1991). Most studies have used seedlings because of the
difficulty of exposing large trees. The extrapolation from seedlings to large trees and to
forest stands is not straight-forward and, most likely, will depend on the use of models
(Hogsett et al., 1995; Laurence et al., 1993; Taylor and Hanson, 1992). Correlative studies,
such as those conducted in the San Bernardino Mountains of California, indicate potentially
large impacts on ecosystems (U.S. Environmental Protection Agency, 1986). Cregg et al.
(1989), however, point out that notable differences between trees and seedlings are their
carbon allocation and use patterns. There is a significantly higher ratio of respiring to
photosynthetic tissue in mature trees. This section will address three distinct types of long-
lived plants: (1) multiple-year agricultural crops, (2) deciduous shrubs and trees, and (3)
evergreen coniferous trees.
5.6.4.1 Perennial Agricultural Crops
Cooley and Manning (1988) conducted a greenhouse study of the response of
alfalfa to O3 applied at 0.06 to 0.08 ppm for 6 h/day, 5 days/week for 8 weeks during
2 different years (to different plants). Ozone treatment reduced the growth and relative
growth rate (by about 15 to 20% for tops and 20 to 40% for roots) of plants before cutting,
when compared to a filtered-air control. The growth of roots was affected more than the
growth of tops, with a shift in the allocation pattern. In the second year of the study,
O3 exposure was continued after the plants were harvested and the impact of exposure on
regrowth was determined. In this case, they found that the relative growth rate in O3 exposed
plants was higher, perhaps because of an increased demand for carbon by the root systems of
the O3-stressed plants. It is unclear whether these plants would sustain their increased growth,
and, in fact, the authors speculate that the increased growth, in lieu of partitioning carbon to
other compounds, might alter the cold hardiness of the plants.
Ozone has been demonstrated to affect the growth of field grown alfalfa. Temple
et al. (1988a) reported a 2-year study of alfalfa in which O3 at ambient concentrations
(0.049 in 1984 and 0.042 ppm in 1985 for the seasonal 12-h means, April to October) did not
affect the growth and yield of the plants, but at 12-h seasonal means of 0.063 and 0.078 ppm,
yield was reduced by about 15 and 19%, respectively. The exposure-response functions for
the 2 years were homogeneous; there was no indication of cumulative effect of O3 exposure;
however, crown weight (an indicator of health and vigor) of exposed plants was reduced
significantly.
In a different field experiment conducted to determine the interactive effects of
O3 and simulated acid fog on stomatal conductance, photosynthesis, foliar injury, and yield of
an established stand of alfalfa, plants were exposed 12 h daily for 4 weeks (Temple et al.,
1987). Ozone was added in proportion to its concentration in the ambient air. Ambient
O3 concentrations during the experiment were 0.043 ppm. Ozone injury symptoms appeared
on the alfalfa exposed to 0.098 ppm (NF x 2.0), 1 week after the start of the regrowth period.
When exposures were at 0.081 and 0.066 ppm (NF x 1.7 and NF x 1.3), more than a week
was required for injury to appear. A 1-mo exposure of the plants at the end of the growing
season resulted in a reduction of about 2.5% in aboveground yield at a 12-h seasonal mean
concentration of 0.04 ppm. At a concentration of 0.066 ppm, the exposure resulted in a
5-164
-------
reduction in yield of approximately 18%. It should be noted that the whole plant was
exposed to ambient O3 for the growing season, only new leaves that had developed after
harvest received the 1-mo exposure. Ozone exposures could shorten the productive life of
alfalfa stands, in addition to its affecting yield.
Kohut et al. (1988a) and Heagle et al. (1989b) experimented with forage mixtures
characteristic of the northeast and southeast, respectively. In both cases, exposure to
O3 resulted in a reduction in total forage yield of about 10 to 20% at 12-h seasonal mean
O3 concentrations of 0.045 to 0.05 ppm. In both cases, the clover component of the mix was
more sensitive than the grass and was reduced in prevalence in the stand. The relevance of
these studies to competition and species composition is discussed in the section on ecosystem
response (Section 5.7).
Results of studies on perennial plants conducted since 1986 are summarized in
Table 5-26. As with single-season agricultural crops, yields of multiple-year forage crops are
reduced at concentrations at or near ambient (0.05 to 0.06 ppm for 5 weeks) in many parts of
the country.
5.6.4.2 Effects of Ozone on Deciduous Shrubs and Trees
Most of the information concerning the response of deciduous shrubs and trees to
episodes or season-long or multiple-year exposures to O3 is based on field observations. The
longevity of perennial plants and their size, in the case of trees, makes their study under
experimental conditions difficult. For this reason, there is little experimental data concerning
the response of deciduous shrubs and trees.
Trees, because of their size, are difficult to study under controlled conditions,
therefore, most experiments have used seedlings in pots or in OTCs. Most of the hardwood
experiments included in Reich's analysis (1987), for example, were exposed under laboratory
or greenhouse conditions to relatively high concentrations for short periods of time. Although
exposure durations of weeks were used, square-wave exposure regimes that do not capture
important characteristics of ambient exposure were used. In addition, in Pye (1988), the
majority of the studies were conducted in a laboratory or greenhouse. The results of a few
OTC studies are cited; however, the majority of these studies used O3 concentrations of 0.10
ppm or higher, a condition found only during peak exposures in the ambient air. Although
the studies reported in the previous criteria document (U.S. Environmental Protection Agency,
1986) (see Section 5.6.2) support the sensitivity of the seedlings of some species grown in
chambers, little information of value with regard to tree growth or biomass production in the
long-term can be extrapolated from the experiments. Since 1986, a number of studies have
been conducted documenting the sensitivity of hardwoods to O3 (Table 5-27). Some species,
such as black cherry, are very sensitive, although great variability in foliar injury was
observed among individual trees, indicating that sensitivity varies greatly within species
(Davis and Skelly, 1992a,b; Simini et al., 1992). No significant reductions in basal diameter
and height growth were observed during the 3 years of the study, although growth was
reduced during 1988 at two sites where O3 concentrations exceeded 0.12 ppm (Simini et al.,
1992), with SUM06 exposures as low as 12.9 ppm-h over 92 days (concentrations not given)
predicted to cause a 10% yield loss (Hogsett et al., 1995; Table 5-28).
Based on studies previously reviewed, the growth of some hardwood species,
particularly those of the genus Populus, may be affected by ambient concentrations of
5-165
-------
Table 5-27. A Summary of Studies Reporting the Effects of
Ozone on the Growth or Productivity of Deciduous Shrubs and Trees
Published Since U.S. Environmental Protection Agency (1986)a
en
O)
O)
Species
Almond
Almond
Almond
Plum
Plum
Pear
Apricot
Skunk bush
Black cherry
Black cherry
Red oak
Red oak
Concentration15
38 to 112 ppb 12-h mean
30 to 117 ppb 12-h mean
250 ppb, 4 h/week
44 to 111 ppb 12-h mean
30 to 117 ppb 12-h mean
30 to 117 ppb 12-h mean
30 to 117 ppb 12-h mean
10 to 75 ppb 12-h mean
16 to 67 ppb 12-h mean
40 or 80 ppb, 7 h/day,
5 days/week
18 to 87 ppm-h
15 to 69 ppb 7-h mean
16 to 67 ppb 12-h mean
Duration
153 days
3.5 mo
16 weeks in each
of two growing
seasons
191 and 213 days
3.5 mo
3.5 mo
3.5 mo
3 mo
Three growing
seasons
8 or 12 weeks
177 days
Three growing
seasons
Facility0
OTC
OTC
CC
OTC
OTC
OTC
OTC
OTC in pots
OTC
GC
OTC
OTC
Variable11
Total dry weight
Cross-sectional
area
Net growth
Number of fruit
per tree
Cross-sectional
area
Cross-sectional
area
Cross-sectional
area
Growth
Growth and leaf
dynamics
Growth
Tree canopy
Growth and leaf
dynamics
Effect6
Linear reduction in
two cultivars, no effect in
three.
6% reduction at 51 ppb.
28 and 36% reduction in
years 1 and 2.
29% fewer fruit at ambient
and above.
19% reduction at 51 ppb.
8% reduction at 51 ppb.
53% reduction at 117 ppb.
Increase in leaf weight in
ambient air; no other effect.
Leaf abscission increased
with increasing ozone.
Reduced leaf, stem, and
root dry weight, and
height at 80 ppb.
Reduced 41% at 82 ppm-h
or 69 ppb 7-h mean.
No effect.
Reference
Retzlaff et al.
(1992a)
Retzlaff et al.
(1991)
McCool and
Musselman (1990)
Retzlaff et al.
(1992b)
Retzlaff et al.
(1991)
Retzlaff et al.
(1991)
Retzlaff et al.
(1991)
Temple (1989)
Simini et al. (1992)
Davis and Skelly
(1992b)
Samuelson and
Edwards (1993)
Simini et al. (1992)
-------
cn
O)
Table 5-27 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth or Productivity of Deciduous Shrubs and Trees
Published Since U.S. Environmental Protection Agency (1986)a
Species
Red oak
Red maple
Red maple
Tulip poplar
Yellow poplar
European beech
Aspen
Aspen
Aspen
Concentration15
40 or 80 ppb, 7 h/day,
5 days/week
16 to 67 ppb 12-h mean
40 or 80 ppb, 7 h/day,
5 days/week
16 to 67 ppb 12-h mean
40 or 80 ppb, 7 h/day,
5 days/week
10 to 90 ppb weekly mean
80 ppb, 6 h/day,
3 days/week
Filtered air or 80 ppb,
6 h/day, 3 days/week
Ambient + 27, 51, or
102-ppb exposure period
mean
Duration
8 or 12 weeks
Three growing
seasons
8 or 12 weeks
Three growing
seasons
8 or 12 weeks
5 years
70 and 92 days in
two growing seasons
93 days at two sites
in Michigan
105 days
Facility0
GC
OTC
GC
OTC
GC
OTC
OTC
OTC
CC
Variable11
Growth
Growth
and leaf
dynamics
Growth
Growth
and leaf
dynamics
Growth
Growth
Stem
weight
Growth
Dry
weight
Effect6
Reduced root dry weight at 80 ppb.
No effect.
Reduced stem diameter and dry
weight at 80 ppb.
Leaf abscission increased with
increasing ozone.
Reduced leaf dry weight and stem
diameter at 80 ppb.
Reduced shoot growth and leaf
area.
No effect on tolerant clones; 46%
reduction for sensitive clones in
1 year 5% (tolerant), and 74%
(sensitive) reductions in the second
year.
18 to 26% reduction in diameter
growth.
40% reduction; 44% reduction in
early growth the following year.
Reference
Davis and Skelly
(1992b)
Simini et al. (1992)
Davis and Skelly
(1992b)
Simini et al. (1992)
Davis and Skelly
(1992b)
Billen et al. (1990)
Karnosky et al.
(1992b)
Karnosky et al.
(1992a)
Keller (1988)
-------
Table 5-27 (cont'd). A Summary of Studies Reporting the Effects of
Ozone on the Growth or Productivity of Deciduous Shrubs and Trees
Published Since U.S. Environmental Protection Agency (1986)a
en
O)
00
Species
Yellow poplar
Paper birch
Downy birch
Downy birch
Red alder
aSee Annenrlix A fn
Concentration15
0 to 200 ppb,
3 days/week
60 to 80 ppb,
5 days/week
25 to 82 ppb,
25 to 82 ppb,
25 to 82 ppb,
r abbreviations an
8h/day,
7h/day,
7h/day
7h/day
7h/day
H acrnnvms
Duration
4.5 mo
12 weeks
50 days
50 days
50 days
Facility0
GC
GH
GC
GC
GC
Variable11
Growth
Dry weight
Dry weight
Dry weight
Dry weight
Effect6
Up to a 24% reduction at
200 ppb but moderated by
pH treatment.
Decreased shoot and root
weight and leaf area.
Shoot and root dry weight
decreased linearly with ozone.
Shoot and root dry weight
decreased linearly with ozone.
Shoot and root dry weight
decreased linearly with ozone.
Reference
Jensen and Patton
(1990)
Keane and
Manning (1988)
Mortensen and
Skre (1990)
Mortensen and
Skre (1990)
Mortensen and
Skre (1990)
bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposures are SUMOO unless
otherwise specified, accumulation based on 24 h/day unless otherwise noted.
°OTC = open-top chamber with plants in ground unless specified in pots; CC = closed chamber, outside; GC = controlled environment growth chamber
or CSTR; GH = greenhouse.
dThe effect reported in the study that is a measure of growth, yield, or productivity.
eEffect measured at specified ozone concentration, over the range specified under concentration, or predicted (if specified) to occur based on relationships
developed in the experiment.
-------
Table 5-28. Exposure-Response Equations That Relate Total Biomass (Foliage,
Stem,
and Root) to 24-Hour SUM06 Exposures (C) Adjusted to 92 Days (ppm-h/year)a
Rate of
Growth
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Slow
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Fast
Slow
Fast
Fast
Fast
Habit Study Species
D
D
D
D
D
D
D
D
D
D
D
D
D
D
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
D
D
D
D
D
D
D
D
D
D
D
D
1
1
2
2
3
3
4
4
4
4
5
5
5
6
7
7
7
7
8
8
8
9
9
10
10
10
10
11
11
11
12
13
14
15
15
16
16
17
18
19
20
21
21
22
Aspen, wild
Aspen, wild
Aspen, wild
Aspen, wild
Aspen, wild
Aspen, wild
Aspen 216
Aspen 253
Aspen 259
Aspen 271
Aspen 216
Aspen 259
Aspen 271
Aspen, wild
Douglas fir
Douglas fir
Douglas fir
Douglas fir
Douglas fir
Douglas fir
Douglas fir
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Red alder
Red alder
Red alder
Red alder
Red alder
Red alder
Black cherry
Black cherry
Red maple
Tulip poplar
Tulip poplar
Tulip poplar
Location
(State)
OR
OR
OR
OR
OR
OR
MI
MI
MI
MI
MI
MI
MI
MI
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
OR
TN
TN
TN
TN
TN
TN
Exposure" Weibull Parameters
Days Year Harvests' ABC
84
84
118
118
112
112
82
82
82
82
98
98
98
98
113
113
234
234
118
118
230
111
111
113
113
234
234
118
118
230
140
84
121
113
113
118
118
112
76
140
55
75
184
81
1989
1989
1991
1991
1990
1990
1990
1990
1990
1990
1991
1991
1991
1991
1989-90
1989-90
1989-90
1989-90
1991-92
1991-92
1991-92
1989
1989
1989-90
1989-90
1989-90
1989-90
1991-92
1991-92
1991-92
1992
1991
1990
1989
1989
1991
1991
1992
1989
1992
1988
1990-91
1990-91
1992
1
2
1
2
1
2
1
1
1
1
1
1
1
1
1
2
3
4
1
2
3
1
2
1
2
3
4
1
2
3
1
1
1
1
2
1
2
1
1
1
1
1
3
1
9.9
17.7
31.0
75.6
67.8
96.9
54.5
73.1
79.1
91.3
37.4
35.2
35.7
19.0
16.8
27.9
33.3
83.5
26.7
85.9
119.1
12.8
25.8
12.9
25.7
32.1
90.1
20.2
47.1
44.5
134.6
136.0
42.4
84.4
206.8
63.5
248.8
54.1
53.7
37.1
28.5
45.8
334.1
150.1
96.3
165.2
130.0
124.9
111.0
142.1
121.1
265.5
92.7
44.9
128.6
95.9
73.1
263.1
462.7
3.8E+17
438.9
2,887.0
109.5
-0.0058
218.7
246.9
365.2
233.7
358.8
327.8
634.3
266.4
206.5
458.5
235.8
442.8
217.0
253.0
179.9
501.7
2.0E+13
274.4
79.1
176.6
387.1
46.4
623.5
50.8
1.316
1.000
3.062
5.529
6.532
1.257
1.609
1.000
1.000
8.964
1.000
1.000
4.012
1.000
1.844
1.000
5.383
1.000
57.655
(lin)
12.254
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.257
2.570
1.000
1.427
1.000
5.294
1.000
1.000
1.107
1.123
1.168
1.537
4.518
1.000
1.852
SUM06 for Loss of1
10% 30%
19.09
19.06
48.62
64.80
64.60
19.48
33.56
31.38
10.96
39.20
12.72
9.49
39.16
26.02
111.17
250.00
113.61
119.61
82.13
250.00
72.80
21.56
31.89
20.05
30.77
13.58
26.27
21.88
16.96
30.61
64.56
51.10
34.08
21.70
95.76
41.21
250.00
29.50
12.91
16.90
149.75
34.56
32.85
17.12
48.21
64.54
72.41
80.79
77.86
51.40
71.60
106.23
37.10
44.91
43.06
32.11
53.07
88.08
215.37
250.00
142.49
404.91
83.88
250.00
80.42
73.00
107.95
67.87
104.18
45.97
88.94
74.09
57.42
80.77
103.76
172.98
80.10
73.46
120.57
139.51
250.00
88.79
38.23
48.00
331.07
45.27
111.19
33.07
5-169
-------
Table 5-28 (cont'd). Exposure-Response Equations That Relate Total Biomass
(Foliage, Stem, and Root) to 24-Hour SUM06 exposures (C) Adjusted to
92 days (ppm-h/year)a
Rate of
Growth
Fast
Fast
Slow
Slow
Slow
Slow
Slow
Location
Habit Study Species (State)
E
E
D
D
E
E
E
23
23
24
24
25
25
26
Loblolly GAKR 15-91
Loblolly GAKR 15-23
Sugar maple
Sugar maple
Eastern white pine
Eastern white pine
Virginia pine
AL
AL
MI
MI
MI
MI
MI
Exposure" Weibull Parameters
Days Year Harvests0 ABC
555
555
83
180
83
180
98
1988-89
1988-89
1990-91
1990-91
1990-91
1990-91
1992
3
3
1
3
1
3
1
22.7
20.4
4.12
24.63
0.35
1.21
78.3
4,402.5
13,125.4
100.0
110.2
63.1
719.5
3,045.1
1.000
1.000
40.069
5.987
4.191
1.000
1.000
SUM06 for Loss of
10% 30%
76.89
229.24
104.79
38.68
40.90
38.74
250.00
260.30
250.00
108.03
47.42
54.72
131.16
250.00
"See Appendix A for abbreviations and acronyms.
"Duration corresponds to the length in days of the first year of exposure for Harvests 1 and 2 and to the total length of the first and
second years of exposure for Harvests 3 and 4.
'Harvest 1 occurs immediately following the end of the first year of exposure. Harvest 2 occurs in the spring following the first year of
exposure. Harvest 3 occurs immediately following the end of the second year of exposure. Harvest 4 occurs in the spring following the
second year of exposure.
dTo compare the results from seedling studies of varying exposure duration, the SUM06 value is calculated for an exposure of fixed
period of 92 days per year. For example, Study 1 Harvest 1 has an exposure duration of 84 days and a SUM06 value of 19.09 ppm-h
over 92, days which corresponds to a SUM06 value of 19.09*84/92 = 17.43 ppm-h over 84 days, at which biomass loss is 10%. The
calculation assumes that exposures can be scaled up or down in uniform fashion.
'Based on GIS, TREGRO, and ZELIG models projections. No data given in paper.
Source: Hogsett et al. (1995).
O3 (U.S. Environmental Protection Agency, 1978, 1986). In studies of the response of aspen
clones to O3 at two field sites in Michigan, Karnosky et al. (1992a,b) documented reductions
in stem weight of up to 46% in sensitive aspen clones after 70 days of exposure in OTCs to
0.08 ppm for 6 h/day, 3 days/week.
Tjoelker and Luxmoore (1991) found leaf abscission on tulip poplar (Liriodendron
tulipiferd) seedlings to be increased by exposure to a 7-h seasonal mean concentration of
0.108 ppm, resulting in a doubling of the leaf turnover rate, but this was not translated into an
effect on growth, perhaps due to the indeterminate growth habit of the plant. In such plants,
leaf production continues throughout the growing season, which may permit the tree to
maintain an optimal leaf area; however, continued leaf growth could deplete carbon or
nitrogen reserves.
Samuelson and Edwards (1993), in a study to determine if seedlings and trees
responded similarly to O3, found canopy weight of 30-year-old northern red oak, exposed in
large OTCs, to be reduced by 41% after exposure for 177 days at a 7-h seasonal mean of
0.069 ppm (87 ppm-h SUM08), compared to a subambient treatment at a 7-h seasonal mean
of 0.015 ppm (18 ppm-h SUMOO). Two-year-old seedlings were not affected by similar
exposures. Trees produced only one flush of leaves, seedlings produced as many as three.
Hogsett et al. (1995) developed exposure-response functions for aspen, red alder
(Alnus rubra), black cherry (Primus serotina), red maple (Acer rubrum\ and tulip poplar
(Table 5-28), as well as composite functions for deciduous tree seedlings (Table 5-29). Their
results suggest that, for 28 deciduous seedling cases, a SUM06 exposure of 31.5 ppm-h over
92 days with a mean concentration of approximately 0.055 ppm could result in less than a
5-170
-------
Table 5-29. SUM06 Levels Associated with 10 and 20% Total
Biomass Loss for 50 and 75% of the Seedling Studies
(The SUM06 value is adjusted to an exposure length of 92 days per year.)3
Weibull Equations (all 51 seedling studies):
50th Percentile PRYL = 1 - exp(-[SUM06/176.342]**1.34962)
75th Percentile PRYL = 1 - exp(-[SUM06/104.281]**1.46719)
Weibull Equations (27 fast-growing seedling studies):
50th Percentile PRYL = 1 - exp(-[SUM06/150.636]**1.43220)
75th Percentile PRYL = 1 - exp(-[SUM06/89.983]** 1.49261)
Weibull Equations (24 slow to moderate growing seedling studies):
50th Percentile PRYL = 1 - exp(-[SUM06/190.900]**1.49986)
75th Percentile PRYL = 1 - exp(-[SUM06/172.443]**l. 14634)
Weibull Equations (28 deciduous seedling studies):
50th Percentile PRYL = 1 - exp(-[SUM06/142.709]** 1.48845)
75th Percentile PRYL = 1 - exp(-[SUM06/87.724]**l.53324)
Weibull Equations (23 evergreen seedling studies):
50th Percentile PRYL = 1 - exp(-[SUM06/262.91 !]**!.23673)
75th Percentile PRYL = 1 - exp(-[SUM06/201.372]**1.01470)
Levels Associated with Prevention of a 10 and 20% Total Biomass Loss for 50 and 75% of the Seedlings:
All 51 Seedling Cases
Percent of Seedlings
50% 75%
Relative 10% 33.3 22.5
Biomass Loss 20% 58.0 37.5
27 Fast-Growing Seedling Cases
Percent of Seedlings
50% 75%
Relative 10% 31.3 19.4
Biomass Loss 20% 52.9 32.4
24 Slow-to-Moderate-Growth Seedling Cases
Percent of Seedlings
50% 75%
Relative 10% 42.6 24.2
Biomass Loss 20% 70.2 46.6
28 Deciduous Seedling Cases
Percent of Seedlings
Relative
Biomass Loss
10%
20%
50%
31.5
52.1
75%
20.2
33.0
5-171
-------
Table 5-29 (cont'd). SUM06 Levels Associated with 10 and 20% Total
Biomass Loss for 50 and 75% of the Seedling Studies
(The SUM06 value is adjusted to an exposure length of 92 days per year.)3
23 Evergreen Seedling Cases
Percent of Seedlings
50% 75%
Relative 10% 42.6 21.9
Biomass Loss 20% 78.2 45.9
aSee Appendix A for abbreviations and acronyms.
Hogsett et al. (1995).
10% growth (biomass) reduction in 50% of the cases. A 20% reduction in growth should
result from a SUM06 exposure of greater than 52.1 ppm-h. Comparison with Table 5-20
shows a SUM06 for 3 mo of 29.5 ppm-h at ambient concentrations, a value near that
(33.3 ppm-h) expected to prevent a 10% growth reduction in 50% of the cases (Table 5-27).
An individual year, such as 1988, might be significantly above the no-injury exposure value
(Table 5-20). By further grouping the seedlings by rate of growth (fast or slow), the
investigators were able to refine estimates of the SUM06 exposure that would protect
seedlings, based on growth strategy. Deciduous seedlings, and fast-growing species are more
sensitive than evergreen and slow-growing seedlings (Table 5-27). Seedlings utilize more of
the carbon compounds formed during photosynthesis for growth, whereas mature trees use
more for maintenance; therefore, extrapolation of exposure response from seedlings to mature
trees may lead to inaccurate assumptions.
The response of a number of fruit and nut trees to O3 has been reported (McCool
and Musselman, 1990; Retzlaff et al., 1991, 1992a,b). Almond (Prunus amygdalis Batsch)
has been identified as the most sensitive, but peach (Prunus persica\ apricot, pear, and plum
(Prunus domestica) also have been affected. Net growth of almond, the stem diameter of
peach, and the stem diameter and number of shoots produced on apricot were reduced by
4 mo (the exposure duration specified by the authors) of once-weekly exposure to 0.25 ppm
for 4 h (an exposure found only in California), a relatively small exposure cumulatively
(16 ppm-h as a SUMOO or as a SUM06) (McCool and Musselman, 1990), but one with a
high peak value. Cross-sectional area of almond, plum, apricot, and pear stems decreased
linearly with increasing O3, with a significant reduction at a 12-h seasonal mean of 0.051; dry
weight of roots, trunk, and foliage also was reduced in one variety of almond (Retzlaff et al.,
1992a).
Finally, two studies report the response of citrus and avocado to O3 (Eissenstat
et al., 1991a; Olszyk et al., 1990b). These species retain their leaves for more than 1 year,
but fit best in the deciduous category because, although evergreen, leaves are replaced more
frequently than in most evergreen species. Valencia orange trees (Citrus sinensis), exposed
during a production year to a seasonal 12-h mean of 0.04 or 0.075 ppm, had 11 and 31%
lower yields than trees grown in filtered air at 0.012 ppm and atypical concentration. During
an off-production year, yield was not affected. Growth of Ruby Red grapefruit (Citrus
paradisi) was not affected by concentrations of three times that of the ambient concentration
5-172
-------
(Eissenstat et al., 1991b). Avocado growth was reduced by 20 or 61% by exposure during
two growing seasons at 12-h seasonal mean concentrations of 0.068 and 0.096 ppm.
In summary, deciduous trees appear to be less sensitive to O3 than are most crop
plants, but there are species that are as sensitive or more so because of their genetic
composition than are crops (e.g., Populus species and perhaps black cherry; see discussion in
Section 5.4.2). Analysis of the shrub and tree data presented in Table 5-25 and discussed
above suggests that a 7-h seasonal mean exposure of approximately 0.055 ppm over a 3-mo
period would not result in injury to tree seedlings. However, the absence of multiple-year
studies, or studies using older, more mature trees, leaves unanswered the question of
long-term and cumulative effects.
5.6.4.3 Effects of Ozone on Evergreen Trees
As with hardwoods, little long-term data from controlled studies of evergreen trees
were available at the time the literature was reviewed for the previous criteria document (U.S.
Environmental Protection Agency, 1986). The 1986 document did point out, however, that
studies conducted on eastern white pine on the Cumberland Plateau in Tennessee indicated
that ambient O3 may have reduced the radial growth of sensitive individuals by as much as 30
to 50% annually over a period of 15 to 20 years (Mann et al., 1980). Also, field studies in
the San Bernardino National Forest indicated that, over a period of 30 years, O3 may have
reduced the growth in height of ponderosa pine by as much as 25%, radial growth by 37%,
and total volume of wood produced by 84% (Miller et al., 1982). Calculations of biomass in
these studies were based on apparent reductions in radial growth without standardization of
the radial growth data with respect to tree age. Since 1986, studies on the effects of O3 on
evergreen trees have focused primarily on three species or groups: (1) red spruce in the
eastern United States, (2) southern pines (loblolly and slash), and (3) western conifers
(primarily ponderosa pine). For the most part, the research has been conducted with tree
seedlings or saplings and has involved exposures lasting one to four growing seasons.
In many cases, the research has concentrated on defining the mode of action of O3 in conifers
and is discussed elsewhere in this document (Section 5.3). Results of studies with evergreen
trees are summarized in Table 5-30.
Studies of the response of red spruce to O3 exposures, regardless of whether they
have been conducted in growth chambers (Lee et al., 1990a,b; Patton et al., 1991; Taylor
et al., 1986) or in the field (Kohut et al., 1990; Laurence et al., 1993; Thornton et al., 1992)
have failed to detect effects on growth of seedlings or saplings, even after exposure to
12-h seasonal means of up to approximately 0.09 ppm (concentrations that are considerably
greater than those expected in ambient air) each year for up to 4 years. There was an
indication that total nonstructural carbohydrate content was reduced by O3, which might be an
indicator of cumulative stress (Woodbury et al., 1992). However, results of these studies
indicate red spruce is tolerant of O3, at least for exposures of a few years.
Growth of seedlings of loblolly pine (a much faster growing species than red
spruce) has been reduced by O3 under some conditions. In growth chamber experiments,
height growth was reduced after exposure to 0.10 ppm for 4 h/day, 3 days/week for 10 weeks,
but only in combination with a "control" rain treatment. The effect was not observed in trees
that received significant inputs of potential nutrients in simulated rain. Conversely, Tjoelker
and Luxmoore (1991) reported a significant reduction in the weight of current year needles
following an OTC exposure to O3 at a 7-h seasonal mean of 0.056 or 0.108 ppm, only in a
high-nitrogen treatment.
5-173
-------
Table 5-30. A Summary of Studies Reporting
Productivity of Evergreen Trees Published Since U
the Effects of Ozone on the Growth or
S. Environmental Protection Agency (1986)a
cn
Species
Avocado
Orange
Orange
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Ponderosa pine
Lodgepole pine
Jeffrey pine
Concentration15
0.010 to O.lOSppm
12-h mean
0.010 to O.lOSppm
12-h mean
0.012 to 0.075 ppm
12-h mean
0.036 to 0.051 ppm
24-h mean
0.013 to 0.095 ppm
12-h mean, 0.047 to
0.0350 ppm-h over
3 years
0.011 to 0.087 ppm
12-h mean
5, 122, or 169 ppm-h
0.067 to 0.071 ppm
7-h mean
0.067 to 0.071 ppm
7-h mean
0 to 0.0200 ppm, 4 h/day,
3 days/week
Duration
4 and 8 mo in
two growing seasons
4 and 8 mo in two
growing seasons
7 mo/season for
5 years
June to August
Three growing
seasons
Three growing
seasons
112 days
134 days
134 days
44 and 58 days in
two growing seasons
Facility0 Variable11
OTC in pots Leaf mass
OTC in pots Leaf mass
OTC Fruit weight
F Radial growth
rate
OTC Growth
OTC Leaf weight
OTC in pots Root growth
OTC in pots Leaf, stem,
and root dry
weight
OTC in pots Leaf, stem,
and root dry
weight
GC Root, stem,
and needles
dry weight
Effect6
20 and 61% reduction in leaf
mass at 86 and 108 ppb.
No effect.
"On" production year: 1 1 and
31% reduction at 40 and 75 ppb;
"off year: no effect.
No change in growth rate on
symptomatic trees.
19.5% reduction at 95 ppb.
70 and 48% loss of 1- and
2-year-old needles at 87 ppb.
43% reduction in coarse and fine
nongrowing roots; 50, 65, and
62% reduction in coarse, fine,
and new growing roots,
respectively.
20 to 33% reduction from filtered
air at 67 ppb.
No effect.
Reduced 10 to 20% ppb in
1 year.
Reference
Eissenstat et al.
(1991a)
Eissenstat et al.
(1991a)
Olszyk et al.
(1990b)
Peterson and
Arbaugh (1988)
Beyers et al. (1992)
Temple et al. (1993)
Andersen et al.
(1991)
Hogsett et al. (1989)
Hogsett et al. (1989)
Temple (1988)
-------
Table 5-30 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth or
Productivity of Evergreen Trees Published Since U.S. Environmental Protection Agency (1986)a
Species
Concentration15
Duration
Facility0
Variable11
Effect6
Reference
en
Oi
Jeffrey pine
Western hemlock
Western red cedar
Douglas fir
Giant sequoia
Red spruce
>0.10 ppm
0.067 to 0.071 ppm
7-h mean
0.067 to 0.071 ppm
7-h mean
0.067 to 0.071 ppm
7-h mean
0-0.0200 ppm, 4 h/day,
3 days/week
0.08 to 0.0166 ppm
8-h mean, 8 to
156 ppm-h
On 34 days of
1985
134 days
F Radial growth 11% reduction in symptomatic Peterson et al. (1987)
trees.
OTC in pots Leaf, stem, and 11 to 30% reduction at Hogsett et al. (1989)
root dry weight 71 ppb.
134 days OTC in pots Leaf, stem, and No effect.
root dry weight
134 days OTC in pots Leaf, stem, and No effect.
root dry weight
44 and 58 days in GC Root, stem, No effect.
two growing and needles
seasons dry weight
135 days OTC Scion growth No effect on juvenile or
mature scion growth.
Hogsett et al. (1989)
Hogsett et al. (1988)
Temple (1988)
Rebbeck et al. (1992)
Red spruce
Red spruce
Red spruce
Red spruce
0.023 to 0.087 ppm
12-h mean
0.120 ppm, 4 h/day,
twice per week
0, 0.150 ppm, 6 h/day
or 150 ppb, 6 h, plus
70 ppb 18 h/day
0.025 or 0.100 ppm,
4 h/day, 3 day/week
Two growing
seasons
4 mo
195 days
10 weeks
OTC in pots
GC
GC
GC
Dry weight
Growth
Dry weight
Growth
No effect.
No effect.
No effect.
No effect.
Kohut et al. (1990)
Taylor et al. (1986)
Patton et al. (1991)
Lee et al. (1990b)
-------
Table 5-30 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth or
Productivity of Evergreen Trees Published Since U.S. Environmental Protection Agency (1986)a
cn
O)
Species
Red spruce
Norway spruce
Norway spruce
Norway spruce
Sitka spruce
Silver fir
Fraser fir
White pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Concentration15
0.027 to 0.054 ppm
12-h mean
0.080 to 0.100 ppm,
7 to 8 h/day
0.014 to 0.070 ppm
8-h mean
0.010- to 0.090-ppm
weekly mean
0.05 to 0.170 ppm,
7 h/day, 5 days/week
0.010- to 0.090-ppm
weekly mean
0.020 to 0.100 ppm,
4 h/day, 3/week
0.020 to 0.140 ppm,
7 h/day, 3 day/week
0.021 to 0.086 ppm
7-h mean
0.021 to 0.1 17 ppm
7-h mean
0.022 to 0.094 ppm
7-h mean
0.032 to 0.108 ppm
7-h mean
0.023 to 0.090 ppm
12-h mean, 46 to 0.209
max 12-h
Duration
Three growing
seasons
100 days
5 to 6 mo in two
growing seasons
5 years
65 days
5 years
10 weeks
3.5 mo
96 days
Three growing
seasons
Three growing
seasons
18 weeks
150 days
Facility0
OTC in pots
GC
OTC in pots
OTC
GH
OTC
GC
GC
OTC in pots
OTC in pots
OTC in pots
OTC in pots
OTC in pots
Variable11 Effect6
Dry weight,
and height
Dry weight
Growth
Growth
Growth and
hardiness
Growth
Biomass
Dry weight
Dry weight
Growth
Dry weight
Dry weight
Growth
diameter, No effect.
0 to 14% reduction vs.
filtered air, five
provenances.
No effect.
Reduced lateral shoot
growth in last year.
winter No effect on growth,
reduced winter hardiness.
Increased dry matter
production.
No effect.
No effect.
18% reduction at 86 ppb;
20% reduction in foliage
at 40 or 86 ppb.
No effect on five families.
4% reduction at 30 to
38 ppm; 8% reduction at
51 to 65 ppm.
20% reduction in needles
at 108 ppm.
10% reduction at 46 ppm.
Reference
Thornton et al.
(1992)
Mortensen (1990a)
Nast et al. (1993)
Billen et al. (1990)
Lucas et al. (1988)
Billen et al. (1990)
Tseng et al. (1988)
Reich et al. (1987)
Adams et al. (1988)
Adams et al. (1990b)
Edwards et al.
(1992a)
Tjoelker and
Luxmoore (1991)
Shafer et al. (1987)
-------
Table 5-30 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth or
Productivity of Evergreen Trees Published Since U.S. Environmental Protection Agency (1986)a
en
Species
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Loblolly pine
Concentration15
0.022 to 0.092 ppm
12-h mean, 37 to
0.143 ppm 1-h max
0.007 to 0.166 ppm
12-h mean, 12-h max
248 ppm
0.007 to 0.132 ppm
12-h mean
17 to 382 ppm-h
0.021 to 0.137 ppm
12-h mean
60 to 397 ppm-h
0.020 to 0.137 ppm
12-h mean
0.050 to 0.286 ppm
max 12-h mean
0 to 0.1 50 ppm,
5 h/day, 5 days/week
0 to 0.320 ppm,
6 h/day, 4 days/week
0 to 0.120 ppm,
7 h/day, 5 days/week
0 to 0.320 ppm,
8 h/day, 4 days/week
Duration
Three
growing
seasons
245 days
Three
growing
seasons
241 days
Two
growing
seasons
6 to 12
weeks
8 weeks
12 weeks
9 weeks
Facility0 Variabled
OTC in pots Dry weight
OTC in pots Foliar weight
OTC Foliage abscission
OTC Shoot growth
OTC Needle retention
and fascicle length
GC Dry weight
GC Height and
diameter growth
GC Dry weight
GC Relative growth
rate (RGR)
Effect6
0 to 13% reduction after 3 years at
about 45 to 50 ppm 12-h seasonal
mean, depending on family.
35% reduction at 166 ppm.
Initiated above 130 to 220 ppm-h in
trees exposed to ambient or above.
Shoot length reduced 30% at 137 ppm.
Needle retention decreased in elevated
ozone — fascicle length reduced by
ozone in early flushes, increased in
later flushes.
8% reduction at 150 ppm.
20% reduction in height growth; 36%
reduction in diameter growth in three
open-pollinated families.
Top dry weight increased up to 60%;
root dry weight reduced 6%.
36% reduction in height RGR;
10% reduction in diameter RGR.
Reference
Shafer and
Heagle (1989)
Qiu et al.
(1992)
Stow et al.
(1992)
Mudano et al.
(1992)
Kress et al.
(1992)
Meier et al.
(1990)
Horton et al.
(1990)
Spence et al.
(1990)
Wiselogel
et al. (1991)
-------
Oi
00
Table 5-30 (cont'd). A Summary of Studies Reporting the Effects of Ozone on the Growth or
Productivity of Evergreen Trees Published Since U.S. Environmental Protection Agency (1986)a
Species
Loblolly pine
Slash pine
Slash pine
Slash pine
Concentration15
0.020 to 0.100 ppm, 4 h/day,
3 days/week
0.076 to 0.104 ppm 7-h mean
0.126 ppm 1-h max 122 and
155 ppm-h
200 to 1,000 ppm-h
179 to 443 ppm-h 24-h
SUMOO multiples of ambient
Duration
10 weeks
112 days
28 mo
28 mo
Facility0
GC
GC
OTC
OTC
Variable11
Dry weight
Top and root
dry weight
Litterfall
Leaf area
Effect6
No effect.
18% reduction in top dry weight
and 39% reduction in root
at 122 ppm-h.
Twice as much litterfall at
above 220 ppm-h.
dry weight
ozone
Reduced up to 33% by 443 ppm-h.
Reference
Lee et al. (1990a)
Hogsett et al.
(1985a)
Byres et al. (1992)
Dean and Johnson
(1992)
"See Appendix A for abbreviations and acronyms.
bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposures are SUMOO unless otherwise
specified, accumulation based on 24 h/day unless otherwise noted.
°OTC = open-top chamber with plants in ground unless specified in pots; GC = controlled-environment growth chamber or CSTR; GH = greenhouse; F = field.
dThe effect reported in the study that is a measure of growth, yield, or productivity.
eEffect measured at specified ozone concentration, over the range specified under concentration, or predicted (if specified) to occur based on relationships developed
in the experiment.
-------
Multiple-year OTC exposures of loblolly pine have resulted in decreased foliar
weight, partly through accelerated abscission, and decreased root surface area in the first year
following exposure to a 2.5-times-ambient O3 treatment (0.10 ppm 12-h seasonal average, 318
ppm-h) (Qiu et al., 1992). In a 2-year study, Kress et al. (1992) found that fascicle length
and number of early season needle flushes decreased linearly with increasing O3, but the
reverse was true in flushes produced later in the season. This may occur only in seedlings
that produce more than two leaf flushes per year. Foliage retention decreased with O3, and
fewer fascicles were retained on trees exposed to ambient concentrations of O3 (12-h seasonal
mean of 0.045 ppm averaged over 2 years). Shafer and Heagle (1989) exposed seedlings of
four families of loblolly pine to O3 over three growing seasons and, based on their data,
predicted growth suppressions of above ground plant parts of 0 to 19% (depending on the
sensitivity of the family) at a 12-h seasonal mean of 0.05 ppm, after 2 years; after 3 years,
suppressions of 13% were predicted in the most sensitive family. Cumulative effects of
multiple-year exposures were not apparent from the above study, but no measures of root
growth, which has been reported to be affected in other species (Andersen et al., 1991;
Edwards et al., 1992a; Temple et al., 1993), were reported. Edwards et al. (1992a) also
conducted a 3-year exposure and found a 4% reduction in whole plant biomass after
exposure to a 7-h seasonal concentration of about 0.050 ppm. An 8% reduction was
associated with a 7-h concentration of about 0.10 ppm. Growth reductions occurred in both above-
and belowground plant parts.
Many studies with loblolly pine have used multiple families with a range of
reported tolerance to O3 (Adams et al., 1988, 1990b; Kress et al., 1992; Qiu et al., 1992;
Shafer and Heagle, 1989; Wiselogel et al., 1991). These studies have demonstrated the range
of response, from tolerant to sensitive, in the species. Adams et al. (1990b) suggest that
resistance to natural stresses, such as drought, may be linked to tolerance to O3, thereby
affecting the response of the species to multiple stresses.
The response of slash pine to O3 also has been characterized. Dean and Johnson
(1992) found leaf area to be reduced by O3 in all three growing seasons studied, with an
intensification of the effect each year at an O3 exposure of about 0.03 to 0.04 ppm
(12-h seasonal means) or 77 to 216 ppm-h (SUMOO). Leaf litterfall also was increased by
O3 (Byres et al., 1992a,b). Volume increment of the trees was affected, with an increased
sensitivity to simulated acid rain in trees exposed to twice the ambient concentration. Hogsett
et al. (1985a) found reduced height (22%), diameter (25%), top (18%), and root growth (39%)
in slash pine exposed to a 7-h seasonal mean of 0.076 ppm, with a maximum concentration of
0.094 ppm. From these studies, it is clear that slash pine is relatively sensitive to O3 on an
annual basis.
Hogsett et al. (1989) report the results of exposing five western conifers to O3 at a
seasonal 7-h mean concentration of 0.067 or 0.071 ppm (SUM06 for 134 days was 49.5 and
63 ppm-h, respectively; SUMOO was 140 and 153 ppm-h, respectively). Ponderosa pine and
western hemlock had reduced needle, stem, and root dry weight after 134 days of exposure.
Douglas fir (Pseudotsuga menziesii) and western red cedar (Thuja plicata D. Don) were not
different from the CF air control, but Douglas fir showed consistent decreases in weight of
plant components. Lodgepole pine was not affected by either O3 treatment. Carry-over
effects were observed in bud elongation in the following spring in lodgepole pine, ponderosa
pine, and hemlock. Andersen et al. (1991) also observed reduced root dry weight in
ponderosa pine after exposure to SUMOO of 122 or 169 ppm-h during a 120-day growing
5-179
-------
season. In addition, they observed a reduction in the weight of newly formed roots the
following spring, possibly due to reduced levels of root starch.
In a 3-year field study, Temple et al. (1993) and Beyers et al. (1992) found that
ponderosa pine trees exposed to a 24-h seasonal mean of 0.087 ppm had a 48 and 70% loss
of 2- and 3-year-old needles, respectively. Radial stem growth and coarse root growth also
were reduced but not as severely as needle weight (due to abscission). After three seasons of
exposure, current-year needles in elevated O3 treatments had a higher photosynthetic
performance than those in filtered air. The compensation was apparently due to higher foliar
nitrogen in O3-exposed needles, a product of redistribution of nitrogen before abscission of
needles. Cumulative responses would suggest that, eventually, reductions in growth of the
trees would occur at lower concentrations of O3.
A number of field studies have been conducted in North America in which an
attempt was made to relate air quality to growth or injury of forest trees. Two field studies
have correlated radial growth with visible injury in ponderosa and Jeffrey pine in California
(Peterson and Arbaugh, 1988; Peterson et al., 1987). An 11% reduction in radial growth was
measured in symptomatic Jeffrey pine, compared to trees that did not show symptoms of
O3 injury, but no reduction could be demonstrated in ponderosa pine; however, the authors
point out that the trees they measured were not under competitive stress, which might alter
their response.
The response of evergreen trees varies widely, depending on species and genotype
within species. It is clear, however, that major forest species, such as ponderosa, loblolly,
and slash pine are sensitive to O3 (depending on length of exposure, based on seedling
studies) at or slightly above the concentrations of O3 (0.04 to 0.05 ppm) that occur over wide
areas of the United States. Furthermore, because of the long life span of these trees,
including those that have not been reported sensitive to O3, there is ample opportunity for a
long-term, cumulative effect on growth of the trees. Most of the experiments are conducted
over only 2% or less of the life expectancy of the tree; an equivalent exposure in field crop
plants would be 2 to 3 days. Consideration also must be given to the fact that most of these
trees grow as part of mixed forests, in competition with many other species. Small changes
in growth might be translated into large changes in stand dynamics, with concomitant effects
on the structure and function of the ecosystem.
5.6.5 Assessments Using Ethylene Diurea as a Protectant
A chemical protectant, EDU (7V-[2-(2-oxo-l-imidagolidinyl)ethyl]-Ar-phenylurea),
has been used to study the response of plants to O3 without attempting to control the
concentration of the pollutant during the exposure (Table 5-31) (U.S. Environmental
Protection Agency, 1986).
Disadvantages of the use of OTCs for assessing the effects of O3 on the growth of
plants include relatively high cost, the need for electrical power, and potential effects of the
chambers themselves on the growth of the plants. In many cases, no chamber effects can be
detected, and because most studies compare against a control, chamber effects would have a
minimal effect on interpretation of results. Although, the number of experiments conducted
with OTCs has led to a firm understanding of plant response to a chamber environment, the
possibility of interactions with treatment cannot be ruled out. The use of EDU is attractive
due to low cost and ease of application; however, it is essential to establish the correct dosage
for protection from O3, without direct effects of EDU on the plant, and an estimate of
5-180
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Table 5-31. Effects of Ethylene Diurea (EDU) on Ozone Responses3
Crop/Species
EDU Application
O3 Exposure
Effects of EDU
Reference
White bean Spray to runoff, 2,000 ppm
Spray to runoff, 2,000 ppm
Soil drench, 500 ppm,
0.5 L/pot
Soil drench, 500 ppm,
4 L/6 m row
Field; 34 h > 0.08 ppm
Field; hours > 0.08 ppm =
518 ppnvh
Greenhouse (charcoal-filtered)
Field; 78 h > 0.12 ppm (0.2 ppm
max)
Reduced O3 injury, 38%; delayed
defoliation; increased yield, 24%.
Reduced O3 injury, 20 to 80%; increased
yield up to 35%.
No effect on growth.
Reduced O3 injury up to 50%; retarded
maturation.
Temple and
Bisessar
(1979)
Toivonen
et al. (1982)
Brennan
et al. (1990)
Brennan
et al. (1990)
Oi
00
Corn
Cotton
Potato
Radish
Spray to runoff, 500 ppm
Spray to runoff, 500 ppm
Spray to runoff, 1.1 kg/ha,
five applications
Soil drench, 6.7 kg/ha,
four applications
Soil drench, 100 mg/L,
2 L/m of row
Soil drench, up to 800 mg/L,
100 mL/pot
Soil drench, up to 400 mg/L,
100 mL/pot
Field (no details)
Greenhouse (no details)
Field; > 0.08 ppm on 18 days
(0.138 ppm max)
Field; 282 h > 0.08 ppm
Field; 0 h > 0.1 ppm, hours >
0.05 ppm = 0.76 ppm-h
Greenhouse, < 0.025 ppm
Greenhouse, 0.075 ppm/7 h, 6
days/week, with one weekly peak
to 0.14 ppm
19% yield reduction.
Increased yield in nonfiltered air; reduced
yield in filtered air.
Reduced O3 injury, 50%; increased tuber
weight, 35%.
Reduced O3 injury; increased tuber weight,
20 to 30%.
No response to O3. Reduced growth rates at
low O3 exposures.
Increased shoot growth at <300 mg/L;
reduced shoot growth at >300 mg/L.
Reduced hypocotyl growth at all EDU
levels.
Complete protection against O3 injury
at 100 mg/L.
Heggestad
(1988)
Heggestad
(1988)
Bisessar
(1982)
Clarke et al.
(1990)
Kostka-Rick
and Manning
(1992a)
Kostka-Rick
and Manning
(1993)
Kostka-Rick
and Manning
(1993)
-------
Crop/Species
Table 5-31 (cont'd). Effects of Ethylene Diurea (EDU) on Ozone Responses3
EDU Application
O3 Exposure
Effects of EDU
Reference
Radish (cont'd)
Soil drench, 150 mg/L,
60 mL/pot
Greenhouse, 0.07 ppm/7 h,
5 days/week, with two weekly
peaks to 0.12 ppm
Reduced O3 injury, 90
to 100%; less reduction
in hypocotyl weight.
Kostka-Rick and Manning
(1992b)
Soybean
Soil drench, 500 ppm,
0.5 L/pot
Greenhouse; 0.2 ppm,
6 h/day, 2 days
Reduced O3 injury,
80 to 90%.
Brennan et al. (1987)
Soil drench, 500 ppm,
4 L/6 m row
Field; 78 h > 0.12 ppm (0.2 ppm
max)
No effect on loss of
chlorophyll; no effect
on seed weight.
Smith et al. (1987) and
Brennan et al. (1990)
Tobacco
Spray to runoff, 1 kg/ha,
seven applications
Field; > 0.08 ppm on 2 days
Increased growth, 22%.
Bisessar and Palmer
(1984)
Oi
03
Beech
Black cherry
Other woody species:
Red maple
Stem injection 1 g/L;
0.25 mL
Spray to runoff, 1,000 ppm,
seven applications per year
Spray to runoff, 500 ppm
or soil drench, 500 or
2,000 ppm, 250 mL/pot
OTC; ambient and ambient
+0.08 ppm, 8 h/day
Field; 75 h > 0.08 ppm
(over 4 years)
Up to 0.95 ppm, 3 h
No consistent effect.
Ainsworth and Ashmore
(1992)
Twofold increase in growth. Long and Davis (1991)
Reduced O3 injury.
Cathey and Heggestad
(1982)
Paper birch
White ash
Honey locust
Golden-rain
London plane
Lilac
Basswood
Reduced O3 injury.
Reduced O3 injury.
Reduced O3 injury.
Reduced O3 injury.
Reduced O3 injury.
Reduced O3 injury.
Reduced O3 injury.
aSee Appendix A for abbreviations and acronyms.
-------
the level of protection from O3 achieved (Kostka-Rick and Manning, 1992a,b, 1993).
Ethylene diurea is known to be phytotoxic, so studies under controlled O3 conditions to
establish an effective level of protection without phytotoxicity are essential before EDU can
be used as an assessment tool.
Previous studies with EDU led to the conclusion, as did experiments with OTCs,
that ambient concentrations of O3 were sufficient to reduce crop yields (U.S. Environmental
Protection Agency, 1986). If hourly O3 concentrations exceeded 0.08 ppm for 5 to 18 days
during the growing season, yields of crops might be reduced 18 to 41% (U.S. Environmental
Protection Agency, 1986).
Inspection of Table 5-31 shows that in many cases there were clear-cut reductions
in O3-induced injury and increases in yield resulting from the application of EDU. However,
the conflicting results for field-grown soybean indicated that, at the rate of EDU application
used, no beneficial effects could be demonstrated. Similarly, experiments with corn and
cotton suggest that any possible effects of O3 may have been confounded by direct effects of
EDU on growth.
A few studies using EDU have been conducted since 1986. Kostka-Rick and
Manning (1992a,b, 1993) conducted studies to determine the direct effects of EDU on
growth and to develop an understanding of dose-response to EDU itself. Their studies used
EDU and radish (Raphanus sativus) in the presence or absence of a controlled O3 fumigation
in a greenhouse and found that the chemical did suppress O3-induced reductions in
belowground plant organs; it also protected the plants from foliar injury. The EDU itself did
not cause effects on growth at a concentration of 150 mg L"1 applied as a 60-mL drench to
each plant, a dosage much lower than often has been used (e.g., Long and Davis, 1991; Smith
et al., 1987; discussed below). Kosta-Rick and Manning emphasize that it is essential to
establish the appropriate dose for the species under consideration. Armed with this
background, the investigators used EDU in a field study and found an O3-induced decrease in
the relative growth rates of sink organs of field-grown radish plants above a threshold level of
about 0.052 to 0.058 ppm (7-h daily mean), an exposure that is near ambient
O3 concentrations.
Ethylene diurea also has been used to estimate the effect of O3 on field-grown
soybean in New Jersey (Smith et al., 1987; Brennan et al., 1990). In this case, the
researchers did not establish the appropriate dose level for O3 protection, as was done by
Kostka-Rick and Manning. No differences in yield were found, and the authors concluded
that O3 does not impact soybean yield of the tested cultivars in New Jersey. However, they
did not demonstrate that EDU was an effective protectant at the concentrations used and on
the cultivars grown.
In a similar study, potato yields were measured and related to foliar injury in
EDU-treated and nontreated plots over a 4-year period (Clarke et al., 1990). The cumulative
O3 dose ranged from 45 to 110 ppm-h, depending on the year, producing a range of foliar
injury from 1 to 75%. The authors found that significant differences in yield between
EDU-treated and control plants occurred only when foliar injury on untreated plants was 75%
of leaf area. No level of protection, other than from foliar injury, could be assessed.
In a 3-year study of potted green ash, no significant effects on growth were
measured using EDU (2 years) or by comparison of filtered and NF air in OTCs (1 year)
(Elliot et al., 1987). Foliar injury was observed only late in the season of the first year in the
NF chambers.
5-183
-------
An effort by Ensing et al. (1986) to assess the impact of O3 on yield of peanut in
Ontario found that year-to-year variation was greater than that they could account for either
by correlation of O3 concentration with yield of test plots or by EDU treatment. They
conclude that a correlative approach to assessing losses due to O3 will not work.
Finally, a 4-year study of black cherry using EDU as a protectant was conducted
by Long and Davis (1991). They found significant effects with a 47% reduction in
aboveground biomass compared to EDU-treated trees. The authors do not believe the
difference was due to a stimulation in growth due to nitrogen in the EDU, but they did not
conduct studies, as recommended by Kostka-Rick and Manning, to characterize the EDU
system for black cherry.
In summary, the EDU method for assessing the impact of O3 is promising,
particularly for remote areas or as a validation tool for existing crop-loss models. The system
must be carefully characterized, however, as pointed out by many of its users.
It should be noted that, in spite of the promise shown by EDU as a field protectant
over many years, it has not been developed commercially and, until recently, was unavailable
for further experimentation.
5.6.6 Summary
Several conclusions were drawn from the various approaches used to estimate crop
yield loss. In 1986, U.S. Environmental Protection Agency (1986) established that 7-h/day
growing season mean exposures to O3 concentrations above 0.05 ppm were likely to cause
measurable yield loss in agricultural crops. At that time, few conclusions could be drawn
about the response of deciduous or evergreen trees or shrubs because of the lack of
information about the response of such plants to season-long exposures to O3 concentrations
of 0.04 to 0.06 ppm and above. However, the 1978 and 1986 criteria documents (U.S.
Environmental Protection Agency, 1986) indicate that the limiting values for foliar injury to
trees and shrubs was 0.06 to 0.10 ppm for 4 h. Since 1986, considerable research has been
conducted, and the sensitivity of many tree species has been established.
Based on research published since U.S. Environmental Protection Agency (1986), a
number of conclusions can be drawn.
(1) An analysis of 10 years of monitoring data from more than 80 to almost
200 nonurban sites in the United States established ambient 7-h growing
season average concentrations of O3 for 3 or 5 mo of 0.051 to 0.060 ppm and
0.047 to 0.054 ppm, respectively. The SUM06 exposures ranged from 24.8 to
45.2 ppm-h for 3 mo, and 32.7 to 58.0 ppm-h for 5 mo (Tingey et al., 1991).
(2) The results of OTC studies that compare yields at ambient O3 exposures with
those in filtered air and retrospective analyses of crop data summarized in this
section establish that the current ambient (0.04 to 0.05 ppm) concentrations of
O3 at some sites are sufficient to reduce the yield of major crops in the United
States. The results of research since 1978 do not invalidate the conclusions of
the U.S. Environmental Protection Agency (1978, 1986) that visible injury due
to O3 exposures reduces the market value of certain crops and ornamentals
where leaves are the product (spinach [Spinacea oleracea], petunia, geranium
[Pelargonium hotortomm], and poinsettia [Euphorbia pulcherrima] for
5-184
-------
instance), and that such injury occurs at O3 concentrations (0.04 to 0.10 ppm)
that presently occur in the United States.
(3) A growing season SUM06 exposure of 26.4 ppnvh, corresponding to a 7-h
growing season mean of 0.049 ppm and a 2HDM of 0.094 ppm may prevent a
10% loss in 50% of the 54 experimental cases analyzed by Tingey et al.
(1991) and Lee et al. (1994a,b). A 12-h growing season mean of 0.045 should
restrict yield losses to 10% in major crop species (Lesser et al., 1990).
(4) Concentrations of O3 and SUM06 exposures, depending on duration, that occur
at present in the United States are sufficient to affect the growth of a number
of trees species. Given the fact that multiple-year exposures may cause a
cumulative effect on the growth of some trees (Simini et al., 1992; Temple et
al., 1992), it is likely that a number of species currently are being impacted,
even at ambient exposures (0.04 to 0.05 ppm).
(5) Exposure-response functions for 51 cases of seedling response to O3 (Hogsett
et al., 1995), including 11 species representing deciduous and evergreen
growth habits, suggest that a SUM06 exposure for 5 mo of 31.5 ppnvh would
protect hardwoods from a 10% growth loss in 50% of the cases studied.
A SUM06 exposure of 42.6 ppm-h should provide the same level of
protection for evergreen seedlings. It should be noted that these conclusions
do not take into the account the possibility of effects on growth in subsequent
years, an important consideration in the case of long-lived species.
(6) Studies of the response of trees to O3 have established that, in some cases
poplars (Populus) and black cherry, for instance, trees are as sensitive to O3 as
are annual plants, in spite of the fact that trees are longer lived and have lower
rates of gas exchange, and, therefore, a lower uptake of O3.
(7) The use of the chemical protectant, EDU is of value to establish O3-related
losses in crop yield and tree growth, providing care is exercised in establishing
the appropriate dosage of the compound to protect the plants without affecting
growth. Ethylene diurea cannot be used to predict the response of plants at
concentrations greater than those that exist in ambient air.
5.7 Effects of Ozone on Natural Ecosystems
5.7.1 Introduction
Ozone is a regionally distributed phytotoxic air pollutant capable of changing the
chemical environment of forests. It is the only gaseous air pollutant capable of exposing a
large region without a leaving a permanent trace of its presence. Ozone molecules are
ephemeral. They decompose rapidly to oxygen and free radicals and leave no residuals;
therefore, O3-caused stresses are frequently difficult to determine (Taylor and Norby, 1985;
Garner, 1991).
Ozone stresses can be acute, chronic, or both. Trees may experience O3 exposures
for minutes, hours, a few days, or weeks. In addition, exposures usually occur more than
once during a growing season. During an episode, O3 trajectories may cover very large areas.
Concentrations can increase as the air trajectories move across the country and pass over new
sources of O3 (Wolff et al., 1977a,b,c, 1980; Wolff and Lioy, 1980). Acute episodic
exposures (short-term high concentrations) may be experienced several times in a year.
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During chronic exposures, low concentrations may be experienced continuously for a major
portion of the life of a plant. Forest trees, shrubs, and other perennial plants must cope with
the cumulative effects of several acute episodes; chronic, long-term exposures; or both. Trees
may respond rapidly; for example, the needles of sensitive eastern white pine exhibit visible
injury symptoms within days after exposure to high O3 concentrations (Garner, 1991). In
most instances, however, responses are subtle and not observable for many years because
trees adapt and respond to cumulative stresses by differential growth, which is the result of
altered carbon allocation (Waring and Schlesinger, 1985). Trees usually can recover when the
stresses are removed, depending on the length of exposure.
Ozone concentrations and the effects, past and present, of exposure to O3 on
ecosystems in the San Bernardino Mountains and the Sierra Nevada Mountains of California
and in the Appalachians Mountains of the eastern United States are presented in the pages
that follow. The final section relates known ecosystem responses to stress and presents
possible reasons why the effects on the ecosystem components in the two regions resulted in
different responses. How plants respond to O3 exposures and may compensate for stresses
has been pointed out in the section on mode of action (Section 5.3). The importance of
genetic variability in plant response and plant competition, as well as the multiple biological
and physical factors that may modify plant response and, in some cases, cause stress, have
been discussed in factors that modify plant response (Section 5.4). The discussion regarding
modifying factors is of particular importance in understanding ecosystem response to stresses
because they are much more likely to be encountered by plants growing in their natural
habitats. Figure 5-30 outlines how plant response can lead to ecosystem response.
The responses to a variety of O3 concentrations and exposure durations of various
species of deciduous trees and shrubs (Table 5-27) and evergreen trees (Table 5-30) under
experimental conditions have been presented in the previous section. The studies cited in the
tables in the previous section, whether conducted in chambers, greenhouses, or OTCs, suggest
that all sensitive plants will respond within hours to O3 concentrations above 0.06 ppm. In
general, depending on the length of exposure, the number and height of peaks, and the
sensitivity of the vegetation, data from the field supports this contention. This section places
the response of the individual trees, shrubs, and other perennial plants in the ecosystem
context. The responses of forest ecosystems to pollutant exposure have received more study
than unmanaged ecosystems of other biomes (grasslands, shrublands, or deserts), therefore,
the following discussion relies mainly on forest ecosystems for examples.
5.7.2 Ecosystem Characteristics
Ecosystems are composed of populations of "self-supporting" and "self-
maintaining" living plants, animals, and microorganisms (producers, consumers, and
decomposers) interacting with one another and with the nonliving chemical and physical
environment within which they exist (Odum, 1989; U.S. Environmental Protection Agency,
1993). Ecosystems respond to stresses through their constituent organisms. The response of
plant species and populations to environmental perturbations depends on their genetic
constitution (genotype), their life cycles, and the microhabitats in which they are growing.
Stresses such as the changes in the physical and chemical environment of plant populations
apply new and additional selection pressures on individual organisms (Treshow, 1980). The
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Reduced
Carbohydrate
Production
Carbohydrate I
Allocation J\
V \
I Mycorrhizae Formation J
Figure 5-30. Effects of ozone (OJ on plant function and growth. Reduced carbohydrate
production decreases allocation and resources needed for plant growth
processes. Individual plant responses must be propagated hierarchically
through the more integrative levels of population and community to produce
an ecosystem response. Solid black arrows indicate the effects of O3
absorption; stippled arrows indicate affects on plant functions. Double
border indicates site of response; darkened border indicates site of impact.
changes that occur within plant communities reflect these new and different pressures.
A common response in a community under stress is the elimination of the more sensitive
populations and an increase in abundance of species that tolerate or are favored by the stress
(Woodwell, 1970; Guderian et al., 1985).
Ecosystems usually have definable limits within which the integrated functions of
energy flow, nutrient cycling, and water flux are maintained (Odum, 1993). Their boundaries,
and the organisms that live within them, are determined by the environmental conditions of
that particular habitat, area, or region. Structurally complex communities, they are held in an
oscillating steady state by the operation of a particular combination of biotic and abiotic
factors. They may be large or small (e.g., fallen logs, forests, grasslands, meadows, old
uncultivated fields, ponds, lakes or rivers, estuaries, oceans, the earth) (Odum, 1971).
Together, the environment, the organisms, and the physiological processes resulting from their
interactions form the life-support systems that are essential for the existence of any species on
earth, including man (Odum, 1993).
Human existence on this planet is dependent on ecological systems and processes.
Natural ecosystems traditionally are spoken of in terms of their structure and functions.
Ecosystem structure includes the species (richness and abundance) and their mass and
arrangement in an ecosystem. This is termed an ecosystem's standing stock—nature's free
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"goods" (Westman, 1977; U.S. Environmental Protection Agency, 1978, 1986, 1993). Society
reaps two kinds of benefits from the structural aspects of an ecosystem: (1) products with
market value such as fish, minerals, forest products and pharmaceuticals, and genetic
resources of valuable species (e.g., plants for crops and timber and animals for
domestication); and (2) the use and appreciation of ecosystems for recreation, aesthetic
enjoyment, and study (Westman, 1977; U.S. Environmental Protection Agency, 1978, 1986,
1993).
More difficult to comprehend, but of equal or greater importance are the functional
aspects of an ecosystem. Ecosystem functions are characterized by the way in which
components interact. They are the dynamics of ecosystems—nature's free "services". The
benefits imparted to society include absorption and breakdown of pollutants, cycling of
nutrients, binding of soil, degradation of organic waste, maintenance of a balance of gases in
the air, regulation of radiation balance, climate, and the fixation of solar energy. These, in
short, are the functions that maintain clean air pure water, a green earth, and a balance of
creatures, the functions that enable humans to obtain the food, fiber, energy, and other
materials for survival (Westman, 1977). The majority of the free services are performed by
the microorganisms that constitute as many as half of all living creatures on the earth but are
seldom recognized.
The term "ecological risk" highlights the importance of ecosystems to human
existence. Ecosystems change dramatically throughout time, have no optimal condition, and
are only healthy when compared to some desired state specified by humans (Lackey, 1994).
The importance of ecosystems to human existence is presented in more detail in the nitrogen
oxides (NOX) criteria document (U.S. Environmental Protection Agency, 1993).
5.7.3 Effects of Exposure to Ozone on Natural Ecosystems
5.7.3.1 The San Bernardino Forest Ecosystem—Before 1986
The mixed-conifer forest ecosystem in the San Bernardino Mountains of Southern
California is one of the most thoroughly studied ecosystems in the United States. Chronic
O3 exposures over a period of 50 or more years has resulted in major changes in the San
Bernardino National Forest ecosystem. The primary effect was on the more susceptible
members of the forest community, individuals of ponderosa and Jeffrey pine, such that they
were no longer able to compete effectively for essential nutrients, water, light, and space. As
a consequence of altered competitive conditions in the community, there was a decline in the
sensitive species, permitting the enhanced growth of more tolerant species (Miller et al., 1982;
U.S. Environmental Protection Agency, 1978, 1986). The results of the studies of the San
Bernardino Forest ecosystem were reported in both the 1978 and 1986 criteria documents
(U.S. Environmental Protection Agency, 1978, 1986). The information summarized below is
from these two documents.
An inventory of the forest was begun in 1968 and conducted through 1972 to
determine the results of more than 30 years of exposure to O3. Based on that inventory and
accompanying studies, the conclusions reached are presented in Table 5-32. Data from the
inventory indicated that, during 5 mo/year from 1968 through 1972, trees were exposed to
O3 concentrations greater than 0.08 ppm for more than 1,300 h. Concentrations rarely fell
below 0.05 ppm at night near the crest of the mountain slope (elevation approximately
5,500 ft [Miller, 1973]). The importance of altitude in plant response was discussed in the
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Table 5-32. San Bernardino Forest—Status 1972
1. Ponderosa and Jeffrey pine suffered the most injury. Mortality of one population of ponderosa pine
(n = 160) was 8% between 1969 and 1971 (p = 0.01); in a second population (n = 40), mortality was
10% between 1968 and 1972. White fir populations suffered slight damage, with scattered individual
trees showing severe symptoms. Sugar pine, incense cedar, and black oak exhibited only slight foliar
injury from oxidant exposure.
2. A substantial shift occurred in ponderosa pines from the "slight injury" category in 1969 to the
"moderate injury" category in 1971, indicating that there was continuing oxidant stress and that the
selective death of ponderosa pines was occurring.
3. Suppression of photosynthesis in seedlings was observed (Miller et al., 1969). In ponderosa pine
saplings, needles shortened by exposure to oxidants returned to normal length when the seedlings were
moved to O3-free air from 1968 to 1973 (Miller and Elderman, 1977).
4. Bark beetles were judged to be responsible for the death of weakened trees in the majority of cases.
Elimination of ponderosa pine from the mixed-conifer forest was postulated to occur in the future if the
rate of bark beetle attack were to continue unabated (Cobb and Stark, 1970).
5. Aerial portions of O3-injured pine trees showed a decrease in vigor that was associated with
deterioration of the feeder root system (Parmeter et al., 1962).
6. Seed production was decreased in injured pines. Ordinarily, trees 25 to 50 in. diameter at breast height
produce the most cones, but they were also the most sensitive to oxidants (Luck, 1980).
7. Under-story plant species sensitive to oxidant pollution may already have been removed by air pollution
stress at the time of these early studies (Miller and Elderman, 1977).
Source: U.S. Environmental Protection Agency (1986).
1986 criteria document (U.S. Environmental Protection Agency, 1986) and also is discussed
in Chapter 4 of this document. The monthly averages of the daily maxima of total oxidant
concentrations for the 5 years of the study are given in Figure 5-31. The highest single daily
maximum oxidant concentration of 0.58 ppm occurred in June 1970 between 4:00 and
9:00 p.m., PST (Miller, 1973).
The survey cited above indicated the need for further information. To more
accurately determine the effects of the 30 years of exposure to O3 of the San Bernardino
Forest ecosystem, an interdisciplinary research team designed a study to answer the following
questions: how do organisms and biological processes of the conifer forest respond to
different levels of chronic oxidant exposure? and how can these responses be interpreted
within an ecosystem context?
Included in the study plan were the following ecosystem processes: carbon
(energy) flow (the movement of CO2 into the plants, its incorporation into carbohydrates, and
then its partitioning among consumers, decomposers, litter, and soil); the movement of water
in the soil-plant-atmosphere continuum; mineral nutrient flow through the green plant, litter,
and soil-water compartments; and the shift in diversity patterns in time and space, as
represented by changes in age, structure, and density in the composition of tree species in
communities.
The major abiotic components studied were water (precipitation), temperature,
light, mineral nutrients (soil substrate), and oxidant pollution. The biotic components studied
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U.HU —
0.35 -
0.30 -
1 o-25 -
&
^ 0.20 -
1
1° 0.15-
0.10 -
0.05 -
0.00 -
-
n
1-1
j-
Total Oxidant (ppm) ^^^™
Hours Exceeding 0.10 ppm i i
p, "
[
-
-i
1
MJJASO AMJJASON AMJJASO MJJASO MJJAS
1968 1969
— ID
-14
1
0
-10 d
.?
— 8 g>
-6 o
-4
-2
-0
1970 1971 1972
Years and Months
Figure 5-31. Total oxidant concentrations at Rim Forest (5,640 ft) in Southern California
during May through September, 1968 through 1972. Values of total oxidant
are averages of daily maxima for a month. The number of hours in which
total oxidant exceeded 0.10 ppm also was recorded for the 5-year period.
Source: Miller (1973).
included producers (an assortment of tree species and lichens), consumers (wildlife, insects,
and disease organisms), and decomposers, (populations of saprophytic fungi responsible for
the decay of leaf and woody litter) (U.S. Environmental Protection Agency, 1978, 1986).
During the period of the study, 1973 to 1978, average 24-h O3 concentrations
ranged from a background of 0.03 to 0.04 ppm in the eastern part of the San Bernardino
Mountains to a maximum of 0.10 to 0.12 ppm in the western part during May through
September. Hourly average concentrations for 1975 (measured by ultraviolet [UV]) indicated
that O3 buildup began around 10 a.m. and reached a maximum at all six monitoring stations
in all months (May through September) at around 4 p.m. For example, at the Rim Forest-Sky
station, where the highest concentrations usually were recorded, the 1-mo average of hourly
values ranged from 0.07 to 0.10 ppm at 10 a.m. and from 0.15 to 0.22 at 4 p.m. The highest
concentrations occurred in June, July, and August, and the lowest were observed in
September. The total number of hours with concentrations of 0.08 ppm or more during June
through September was never less than 1,300 h per season during the first 7 years (1968
5-190
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through 1974) of the study (Miller and Elderman, 1977). In addition to total oxidant, PAN
and NO2 concentrations were measured. Peroxyacetyl nitrate injury symptoms could not be
distinguished from O3 symptoms on herb-layer plant species while NO2 remained at nontoxic
concentrations (Miller et al., 1982; U.S. Environmental Protection Agency, 1978, 1986).
The study indicated that the major changes in the ecosystem began with injury to
ponderosa and Jeffrey pine. Ponderosa pine was the most sensitive of the trees to O3, with
Jeffrey pine, white fir, California black oak (Quercus kelloggii), incense cedar (Calocedrus
decurrens), and sugar pine (Pinus lambertiana) following in decreasing order of sensitivity.
Foliar injury on sensitive ponderosa and Jeffrey pine was observed when the 24-h average
O3 concentrations were 0.05 to 0.06 ppm (Miller et al., 1982). Foliar injury, premature
senescence, and needle fall decreased the photosynthetic performance of stressed pines and
reduced the production of carbohydrates needed for use in growth and reproduction by the
trees. Nutrient availability to the trees also was reduced by the trees retention of smaller
amounts of green foliage (Miller et al., 1982). Decreased carbohydrate resulted in a decrease
in radial growth and height of stressed trees (McBride et al., 1975; Miller and Elderman,
1977).
A reduction in available carbohydrate also influenced tree reproduction. Injured
ponderosa and Jeffrey pines older than 130 years produced significantly fewer cones per tree
than uninjured trees of the same age (Luck, 1980). Tree-ring analysis indicated declines in
ring-width indices for many trees. Stand thinning, however, reversed the trend (Miller et al.,
1982).
Summarized, the responses of individual conifers sensitive to O3 include visible
foliar injury; premature needle senescence; reduced photosynthesis; reduced carbohydrate
production and allocation; reduced plant vigor; and reduced growth or reproduction, or both
(Miller et al., 1982).
The ecosystem components most directly affected by O3 exposure were tree
species, the fungal microflora of conifer needles, and the foliose lichens growing on tree bark.
Injury to or changes in the functioning of other living ecosystem components affected, either
directly or indirectly, the processes of carbon (energy) flow, mineral nutrient cycling, water
movement, and changed vegetational community patterns (Miller et al., 1982). Early
senescence and abscission resulted in accumulation of pine needles into a thick layer under
the stands of O3 injured trees and changed decomposition patterns, which changed
successional patterns of the fungal microflora as well. Altering the taxonomic diversity and
population density of the microflora that normally develop on needles while they are on the
tree influenced the relationship of the microflora with the decomposer community. Change in
the type of fungi on needles weakened the decomposer community and slowed the rate of
decomposition (Bruhn, 1980). Nutrient availability was influenced by the carbon and mineral
nutrients accumulated in the heavy litter and thick needle layer under stands with the most
severe needle injury and defoliation.
A comparison of species of lichens found on conifers during the years 1976 to
1979 with collections from the early 1900s indicated a 50% reduction in species in the more
recent period. Marked morphological deterioration of the common species Hypogymnia
enteromorpha was documented in areas of high oxidant concentrations (Sigal and Nash,
1983).
Biotic interactions associated with predators, pathogens, and symbionts were
influenced by changes in the energy available to the trees. The decrease in vigor and lack of
ability to recover from O3 injury associated with reduced carbohydrates made the ponderosa
5-191
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pines more susceptible to attack by predators and pathogens (Stark and Cobb, 1969).
Dahlsten and Rowney (1980) have pointed out that oxidant-weakened pines can be killed by
fewer western pine beetles than are required to kill healthier trees. In stands with a high
proportion of O3-injured trees, a given population of western pine beetles therefore could kill
more trees. James et al. (1980a,b) observed that the root rot fungus, Heterobasidium
annosum, increased more rapidly because freshly cut stumps and roots of weakened trees
were more vulnerable to attack (U.S. Environmental Protection Agency, 1986).
Changes in the plant populations that alter communities and forest stands also can
affect the animal populations. Production of fewer cones, seeds, and fruits reduces the food
available to small vertebrates living in the ecosystem (U.S. Environmental Protection Agency,
1978). The continuum of ecosystem responses associated with increasing pollutant stress
(presented in Table 5-33) are reflected in the response of the San Bernardino mixed forest
ecosystem (Garner et al., 1989; U.S. Environmental Protection Agency, 1986). The influence
of pollutants on the processes of carbon production and allocation are presented in continuum
Stage II, Table 5-33.
Table 5-33. Ecosystem Response to Pollutant Stress
Continuum of Vegetation Responses
Continuum of Ecosystem Responses
0
I
II
III
Anthropogenic pollutants insignificant.
Pollutant concentrations low; no measurable
physiological response.
Pollutant concentrations injurious to sensitive
species:
(1) Reduced photosynthesis, altered carbon
allocation, and reduced growth and
vigor;
(2) Reduced reproduction;
(3) Predisposition to entomological or
microbiological stress.
Severe pollution stress. Large plants of
sensitive species die. Forest layers are peeled
off; first trees and tall shrubs, then, under the
most severe conditions, short shrubs and
herbs.
Unaffected; systems pristine.
Ecosystem functions unaffected; pollutants
transferred from atmosphere to organic or
available nutrient compartments.
Altered species composition; populations of
sensitive species decline; some individuals are
lost. Their effectiveness as functional
ecosystem members diminishes; they could be
lost from the system. Ecosystem reverts to an
earlier stage.
(1) Simplification, basic ecosystem structure
changes, becomes dominated by weedy
species not previously present.
(2) Reduced stability and productivity; loss
of capability for repairing itself. Runoff
increases and nutrient loss and erosion
accelerates; a barren zone results.
Ecosystem collapses.
Source: Garner et al. (1989); adapted from Bormann (1985); Kozlowski (1985); Smith (1974).
5.7.3.2 The San Bernardino Forest Ecosystem—Since 1986
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Monitoring of O3 trends in the South Coast Air Basin of Southern California, the
source of pollutants transported to the mixed-conifer forests of the San Bernardino Mountains,
resulted in the conclusion that the air quality had improved substantially between 1976 and
1984.
Between 1976 and 1991 the weather-adjusted O3 data for the May through October
"smog season" indicates that the number of Basin days exceeding 0.12 ppm, 1-h average,
have declined at an average annual rate of 2.27 days/year, whereas the number of days with
episodes greater than 0.2 ppm, 1-h average, have declined at an average annual rate of
4.70 days/year over the same period. The total days per year with concentrations greater than
0.12 ppm was as high as 159 in 1978, with the lowest number being 105 days in 1990
(Davidson, 1993). The 1974 to 1988 trends of the May through October hourly average and
the average of monthly maximum O3 concentrations for Lake Gregory, a forested area in the
western section of the San Bernardino Mountains, also have shown a gradual decline (Miller
et al., 1989a). Similarly, for the same period, there was an improvement shown in the injury
index used to describe chronic injury to the crowns of ponderosa and Jeffrey pines in 13 of
15 plots located on the gradient of decreasing O3 exposure in the San Bernardino Mountains
(Miller et al., 1989a). The two exceptions were plots located at the highest exposure end of
the gradient. The basal area increase of ponderosa pines was generally less than competing
species at 12 of the 13 plots evaluated. The total basal area for each species as a percent of
the total basal area for all species indicates that ponderosa and Jeffrey pines in plots with
slight to severe crown injury lost basal area in relation to competing species that are more
tolerant to O3, namely, white fir, incense cedar, sugar pine, and California black oak
(Figure 5-32).
In effect, stand development had been reversed (i.e., the development of the
normal fire climax mixture dominated by fire-tolerant ponderosa and Jeffrey pines was
altered). The accumulation in the understory of a greater number of stems of more
O3-tolerant species resulted in the formation of a fuel ladder that jeopardized the remaining
overstory trees in the event of a catastrophic fire. The O3-tolerant species, because of thinner
bark and branches growing close to the ground, are inherently more susceptible to fire injury.
The important question for the future at that time was whether the declining O3 exposure
eventually would allow ponderosa and Jeffrey pine to resume dominance in basal area.
The possible interactive effects of nitrogen and O3 on the forests of the San
Bernardino Mountains has come under consideration more recently. For some time, there has
been a concern that O3 is not the only pollutant in the photochemical mixture that may be
causing lasting changes in the mixed-conifer forest ecosystem. A multidisciplinary study to
investigate the possibility of the combined impacts on ecosystem processes from chronic
O3 injury and both wet and dry deposition of acidic nitrogen compounds has been under way
since 1991 at Barton Flats in the San Bernardino Mountains. The database includes frequent
measurements of stomatal conductance in relation to weather and O3 exposure.
The NOX criteria document (U.S. Environmental Protection Agency, 1993)
explored the possible effects of increased nitrogen on litter content and decomposition. That
discussion is presented here.
Increases in the nitrogen litter content and in litter decomposition rates and an
alteration in nitrogen cycling have been observed in the more highly polluted areas when
compared with moderately polluted and low-polluted areas of the San Bernardino Mountains
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w —
80 -
60 -
40 -
20 -
n
G % of Total 88
CampPaivika • *ofTotal74
Sky Forest
Breezy Point
1
Dogwood
IlLi.
Schne
rl
ider Creek
ill.
J
PP 1C SP BO PPWF 1C SP BO LO PPWF 1C SP BODW PP JP WF SP BOQC CP PPWF 1C SP BO
w —
80 -
60 -
40 -
20 -
n
D %ofTota!88BA
U.C. • % of Total 74 BA
Center
n. ,
Camp Angelus r
GreenValley Creek
. fh.,1
(B)
Barton Flats
II ,
1.
PP BO
w —
80 -
60 -
40 -
20 -
n -
D % of Total 88
• % of Total 74
Camp Osceola
n
„ n
Holcomb Valley Heart Bar (C)
rln
Bluff Lake
1
i
PP JP WF BO
JP WF BO
JP WF
JP WF
Figure 5-32. Total basal area for each species as a percent of the total basal area for all
species in 1974 and 1988 on (A) plots with severe to moderate damage,
(B) plots with slight damage, and (C) plots with very slight damage or no
visible symptoms. PP = Ponderosa pine, 1C = Incense cedar, SP = Sugar
pine, BO = Black oak, WF = White fir, LD = Libocedrus decurrens, DW =
Dogwood, QC = Quercus chrysolepis, CP = Coulter pine, and JP = Jeffrey
pine.
Source: Miller et al. (1991).
5-194
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(Fenn and Dunn, 1989). A pollutant concentration gradient was observed to exist, with 24-h
O3 concentrations at the high sites in the west averaging 0.1 ppm or more, moderate sites
ranging from 0.06 to 0.08 ppm, and low sites in the east averaging 0.05 ppm or less (Fenn,
1991). Nitrogen and sulfur compounds also occur in the pollutant mixture to which the
mountains downwind of the Los Angeles Basin are exposed (Bytnerowicz et al., 1987a,b;
Solomon et al., 1992). A nitrogen deposition gradient from west to east parallels the
decreasing O3 gradient. Deposition of nitrogen exceeds that of sulfur (Fenn and
Bytnerowicz, 1993). Annual average FDSTO3 concentrations in 1986 ranged from 1.2 ppb near
the Southern California coast to 2.7 ppb in the San Gabriel Mountains (Solomon et al., 1992).
The litter layers under trees severely injured by O3 are deeper than those under
trees less severely injured (Fenn and Dunn, 1989). A comparison study of decomposition
rates of the undecomposed surface layer of needle litter indicates that litter in the more
polluted areas in the west decomposed at a significantly (p = 0.01) faster rate than did litter
from moderate to low pollution levels (Fenn and Dunn, 1989; Fenn, 1991). Nitrogen content
of litter was greatest at the high pollution sites and was positively correlated with the litter
decomposition rate. The higher nitrogen and lower calcium contents of the litter suggest that
litter in the western plots originated from younger needles than those at the less polluted sites,
possibly due to O3-induced needle abscission. Fungal diversity was also greater in the litter
from the western San Bernardino Mountains (Fenn and Dunn, 1989).
When the factors associated with enhanced litter decomposition were investigated,
it was found that nitrogen concentrations of soil, foliage, and litter of ponderosa and Jeffrey
pine were greater in the plots where pollution concentrations were high than in moderately
polluted or low-pollution sites. This was also true for sugar pine and for incense cedar, two
O3-tolerant species. The rate of litter decomposition for sugar pine, incense cedar, and
Ponderosa pine species was greatest at the high-pollution sites. Therefore, the increased rate
of litter decomposition in the high-pollution plots does not appear to be related to
O3 sensitivity or premature needle abscission, but, instead, it is associated with higher levels
of nitrogen in the soils (Fenn, 1991). Foliage and litter nitrogen is higher in high-pollution
sites when compared with moderate- or low-pollution sites.
At the present time, data dealing with the response of trees or other vegetation to
the combined stresses of O3 exposure above ground and nitrate deposition through the soil are
sparse. Tjoelker and Luxmoore (1991), however, have assessed the effects of soil nitrogen
availability and chronic O3 stress on carbon and nutrient economy in 1-year-old seedlings of
loblolly pine and yellow poplar. Elevated O3 concentrations altered biomass partitioning to
needles of the current year. Ozone concentrations of 0.108 ppm reduced the biomass of
current-year needles in loblolly pine seedlings grown at the highest (172 |ig/g) nitrogen
supply by 20%, but not those grown with a low (59 |ig/g) supply of nitrogen. The interaction
between O3 and nitrogen suggests that plants grown with a high nitrogen supply are more
sensitive to chronic O3 stress in terms of biomass reduction (Tjoelker and Luxmoore, 1991).
Similar results in the growth of domestic radish were obtained by Pell et al. (1990). Brewer
et al. (1961) and Harkov and Brennan (1980) observed increased foliar injury when plants
were grown with an adequate nitrogen supply (U.S. Environmental Protection Agency, 1986).
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5.7.3.3 The Sierra Nevada Mountains
The continued presence over the years of O3 concentrations injurious to trees in the
San Bernardino Mountain forests and the knowledge that O3 is a regionally dispersed gaseous
air pollutant led to concern that other forests in California, and possibly other western states
as well, were being exposed to injurious concentrations. Summary statistics for the 1980 to
1988 growing season (May through October), using data from O3-monitoring sites in or near
Western forests, substantiated the concern. Growing season (May through October) means,
percentiles and percent occurrence of hourly O3 concentrations above 0.06, 0.08, 0.10, and
0.120 ppm for all O3 sites near Western forests are presented in Table 5-34 (Bohm, 1992).
The lowest O3 concentrations with little hourly variation were experienced at sites far from
urban or point sources. Sites on the fringe of urbanized centers or valleys, on the other hand,
experienced patterns with some variation in hourly concentrations; the higher concentrations
usually occurred during the late afternoon. Forests located on the rims of valleys with large
urban areas experienced O3 concentrations >0.10 ppm. Yosemite and Sequoia National Parks,
which receive pollutants transported from highly urbanized areas, had 24-h means ranging
from 0.036 to 0.085 ppm on 75% of summer days, whereas Lake Gregory had a growing
season mean of 0.073 ppm. During 49% of the summer days, means of diurnal patterns
ranged from 0.085 to 0.100 ppm, decreasing with altitude and distance from the source
(Bohm, 1992). The San Bernardino National Forest was exposed to O3 levels >0.10 ppm
during all seasons. Ozone concentrations tended to decrease with altitude and distance from
the source.
There is little evidence of O3 injury in forests in the western United States outside
of California, even near urban sites. Growing season means near forests ranged between
0.012 and 0.022 ppm in Washington, between 0.028 and 0.037 ppm in Utah, and between
0.032 and 0.058 ppm in Colorado (Table 5-34; Bohm, 1992; Bohm et al., 1995).
The Sierra Nevada, the largest forested area in the world documented to have
visible injury from high O3 exposures, is an area approximately 300 miles long (Peterson and
Arbaugh, 1992). Since 1991, there has been an annual survey of the amount of crown injury
by O3 to the same trees in approximately 33 sample plots located in the Sierra Nevada.
These include Tahoe, Eldorado, Stanislaus, Yosemite, Sierra, Sequoia, and San Bernardino
National Forests and Yosemite and Sequoia-Kings Canyon National Parks.
Dominant tree species in the area are ponderosa and Jeffrey pine, white fir, sugar
pine, incense cedar, Douglas fir, and California black oak, and the giant sequoia
(Sequoiadendron giganteum) is locally common (Peterson and Arbaugh, 1992).
Foliar O3 injury to ponderosa and Jeffrey pine was first documented in the Sierra
Nevada Mountains of California in the early 1970s (Miller and Millecan, 1971). Monitoring
of visible injury to ponderosa pine on national forest land in the western Sierra Nevada,
however, was not begun until 1975 (Duriscoe and Stolte, 1989). Results of the monitoring in
the Sierra and Sequoia National Forests showed that there was an increase in chlorotic mottle
of pines in the plots from approximately 20% in 1977 to approximately 55% in 1988, and an
increase in severity of injury was observed as well.
In general, the results of this study document the regional nature of the
O3 pollution problem originating primarily from the San Jaoquin Valley Air Basin, as well as
from the San Francisco Bay Air Basin further to the west. Oxidant air pollution is
transported southward in the San Jaoquin Valley Air Basin until it reaches the southern
boundary of the air basin, the Tehachipi Mountains. Because of this barrier, polluted air
5-196
-------
en
CD
Table 5-34. Growing Season (May Through
Sites in or Near Forests
(Percentiles and means were generated using the
October) Summary Statistics for Ozone Monitoring
for the Period 1980 through 1988
entire data set [1980 through 1988; May through October].)
Siteb
Aptos, CA
Ash Mountain, CA (AIRS)
Ash Mountain, CA (NFS)
Azusa, CA
Banning, CA
Bishop, CA
Burbank, CA
Camp Mather, CA
Carmel Valley, CA
Fresno County, CA
Lake Gregory, CA
Lassen NP, CA
Kaweah, CA (AIRS)
Kaweah, CA (NFS)
Mammoth Lakes, CA
Monterey, CA
Ojao, CA
Pasadena, CA
Pinnacles NM, CA
Redwood NP, CA
San Bernardino, CA
Santa Barbara, CA
Santa Barbara County, CA
Santa Monica Mountains, CA
Scotts Valley, CA
South Lake Tahoe, CA
Ventura County, CA
Wawona Valley, CA
Elevation
(m)
78
526
610
185
722
1,260
170
1,432
131
1,723
1,397
1,788
1,901
1,890
2,395
23
233
255
355
233
320
25
12
191
171
1,907
1,600
1,280
Percent
Data
Capture
100
50
57
93
98
84
95
33
86
85
93
36
35
58
92
86
87
89
66
49
80
96
96
55
79
88
83
66
Percentiles (ppb)
5
0
20
20
0
10
0
0
22
10
20
10
17
10
21
20
10
10
0
10
8
0
0
0
0
0
10
0
9
10
10
30
30
0
10
10
0
26
10
20
20
21
20
30
30
10
10
0
16
10
0
10
10
2
0
20
10
15
25
10
50
47
0
20
20
0
36
20
30
40
28
40
41
40
20
20
10
26
15
0
20
20
10
10
20
20
27
50
20
60
61
20
40
30
20
46
30
40
60
36
60
56
50
30
40
20
41
22
30
30
30
30
20
40
40
42
Mean ± SDC
25.1 ± 15
64.1 ± 26
62.9 ± 24
43.3 ± 56
49.6 ± 35
31.5 ± 16
36.3 ± 45
47.5 ± 16
28.4 ± 14
44.9 ± 17
72.5 ± 49
37.8 ± 14
59.7 ± 26
56.3 ± 21
46.6 ± 16
27.3 ± 12
42.3 ± 26
47.8 ± 58
42.8 ± 22
22.0 ± 0.09
50.2 ± 57
32.2 ± 19
31.5 ± 20
39.6 ± 35
22.4 ± 18
37.8 ± 17
36.2 ± 22
44.0 ± 23
75
30
80
80
70
70
40
50
59
40
60
100
46
80
71
60
30
60
70
58
28
80
40
40
59
30
50
50
61
90
40
100
93
130
100
50
100
70
50
70
140
58
90
83
70
40
80
130
72
34
140
60
60
86
50
60
60
76
95
50
110
100
160
120
60
130
76
50
80
170
64
100
90
70
50
90
170
80
39
170
60
70
110
50
60
70
83
Percent
>60
3
64
59
28
35
7
25
24
4
26
55
9
57
44
30
1
30
30
22
0
35
11
13
25
5
18
18
26
Hours"
>80 >100 >120
0
36
29
22
19
0
18
3
1
5
37
0
32
15
5
0
12
24
5
0
28
2
2
13
1
1
5
7
0
12
8
17
11
0
12
0
0
0
26
0
8
2
0
0
3
18
1
0
21
0
1
7
0
0
1
1
0
2
1
12
6
0
8
0
0
0
18
0
1
0
0
0
1
14
0
0
15
0
0
4
0
0
0
0
-------
Table 5-34 (cont'd). Growing Season (May Through October) Summary Statistics for Ozone Monitoring
Sites in or Near Forests for the Period 1980 through 1988
(Percentiles and means were generated using the entire data set [1980 through 1988; May through October].)
Siteb
Yreka, CA
Clackamas County, OR
Columbia County, OR
Crook County, OR
Eugene, OR
Marion County, OR
Medford, OR
Cedar River, WA
King County, WA
Olympic NP, WA (DOE)
Olympic NP, WA (NFS)
^ Pack Forest, WA
A Pierce County, WA
60
6
4
2
2
3
3
5
7
3
0
0
8
2
0
2
20
7
12
8
13
0
10
2
8
12
10
11
4
>80 >100 >120
0
1
0
0
1
1
1
2
1
0
0
3
0
0
0
0
0
1
0
1
0
1
0
1
1
1
2
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
-------
Table 5-34 (cont'd). Growing Season (May Through October) Summary Statistics for Ozone Monitoring
Sites in or Near Forests for the Period 1980 through 1988
(Percentiles and means were generated using the entire data set [1980 through 1988; May through October].)
Oi
1
CD
CD
Siteb
Colordao MM, CO
Denver, CO
Great Sand Dunes, CO
Larimer Country, CO
Rocky Mountains NP, CO
Arches NP, UT
Bountiful, UT
Logan, UT
Ogden, UT
Provo, UT
Salt Lake, UT
Albuquerque, NM
Yellowstone NP, WY
Elevation
(m)
1,750
1,591
2,487
1,522
2,743
1,567
1,335
1,382
1,314
1,402
1,305
1,585
2,484
Percent
Data
Capture
30
96
54
90
49
32
87
45
97
72
87
89
58
Percentiles (ppb)
5
30
0
24
1
25
28
8
8
0
2
2
1
15
10
32
2
27
4
31
31
14
12
1
5
4
5
19
25
37
7
33
14
38
36
25
20
9
14
11
15
27
50
42
19
39
27
46
43
38
32
30
29
28
29
36
Mean ± SDC
44.1 ± 14
21.9 ± 18
38.4 ± 0.09
27.9 ± 18
46.0 ± 12
42.8 ± 0.09
38.3 ± 20
32.5 ± 15
29.8 ± 22
32.1 ±22
30.4 ± 22
29.8 ± 19
35.4 ± 12
75
48
33
44
40
54
49
49
45
46
49
45
43
44
90
54
47
49
52
60
54
62
52
58
62
59
55
51
95
57
55
52
59
65
58
72
58
65
68
70
61
55
>60
2
3
1
5
10
4
12
4
8
12
10
6
2
Percent Hoursa
>80
0
1
0
0
1
0
3
0
1
2
3
1
0
>100
0
0
0
0
0
0
1
0
0
0
1
0
0
>120
0
0
0
0
0
0
0
0
0
0
0
0
0
"Percent hours are normalized to represent the average occurrence of ozone levels during May through October. Percent data capture = number of valid
hours/4,416 x 100, where 4,416 is the total number of hours during the period May through October.
bSite abbreviations: NFS = National Park Service, NM = National Monument, DOE = Department of Energy.
°SD = Standard deviation.
Source: Modified from Bohm (1992).
-------
masses circulate back northward. This circulation cell causes higher O3 levels to be adverted
to the southernmost sites, the Sequoia National Forest and the Sequoia-Kings Canyon
National Park. Mean hourly average concentrations in the Sierra Nevada during 1987 ranged
from 0.018 to 0.076 ppm, with annual hourly maxima of 0.11 to 0.17 ppm. An O3 exposure
gradient with highest concentrations in the south and lowest in the north was observed.
Associated with the gradient, injury is most severe at the southern end of the range and least
severe in the north (Peterson et al., 1991).
The studies cited above reported visible O3 injury only to the trees in the Sierra
Nevada forests. To evaluate growth changes in O3-stressed ponderosa and Jeffrey pine,
Peterson and his coworkers, beginning in 1985, conducted the largest investigation of regional
tree growth in the western United States (Peterson et al., 1987; Peterson and Arbaugh, 1988,
1992; Peterson et al., 1991). Using cores to determine whether growth reductions had
occurred, they randomly sampled both trees with visible O3 injury symptoms and
asymptomatic trees. Major decreases in growth occurred for both symptomatic and
asymptomatic trees during the 1950s and 1960s. The percentage of trees exhibiting growth
decreases at any given site never exceeded 25% in a given decade (Peterson et al., 1991).
The mean annual radial increment of trees with symptoms of O3 injury was 11% less than
trees at sites without O3 injury. Trees larger than 40 cm in diameter and trees older than 100
years showed greater decreases in growth than did smaller and younger trees. Differences in
growth between injured and uninjured trees were prominent after 1965 (Peterson et al., 1987).
The region-wide survey (Peterson et al., 1991) of ponderosa pine provides a useful
backdrop for reporting a number of other studies or surveys in the Sierra Nevada that were
more narrowly focused. Another tree ring analysis and crown injury study concentrated on
Jeffrey pines in Sequoia-Kings Canyon National Park (Peterson et al., 1989). This study
suggested that decreases of radial growth of large, dominant Jeffrey pines growing on thin
soils with low moisture holding capacity and direct exposure to upslope transport of
O3 amounted to as much as 11% in recent years when compared with similar trees without
symptoms.
Both a network of permanent plots established in 1980 and cruise surveys have
been employed in Sequoia-Kings Canyon and Yosemite National Parks to determine the
spatial distribution and temporal changes of injury to ponderosa and Jeffrey pine within the
parks (Duriscoe and Stolte, 1989). In Sequoia-Kings Canyon, O3 injury to individual trees
and the mean number of trees injured in each plot increased from 47% for 1980 to 1982 to
79% for 1984 to 1985. Foliar injury was the most common response among the 28 plots
studied. Ozone injury tends to decrease with the increasing elevation of plots. The
O3 concentrations associated with the highest levels of tree injury in the Marble Fork drainage
of the Kaweah River, at approximately 1,800 m elevation, are hourly averages peaking
frequently at 80 to 100 ppb but seldom exceeding 120 ppb.
During a cruise survey in 1986 (Duriscoe and Stolte, 1989) to identify the partial
distribution of injury, there were 3,120 ponderosa or Jeffrey pines evaluated for O3 injury in
Sequoia-Kings Canyon and Yosemite National Parks. Approximately one-third of this
number were found to have some level of chlorotic mottle. At Sequoia-Kings Canyon,
symptomatic trees comprised 39% of the sample (574 of 1,470), and, at Yosemite, they
comprised 29% (479 of 1,650). Ponderosa pines generally were injured more severely than
Jeffrey pines.
5-200
-------
In Sequoia-Kings Canyon, observations at field plots showed that giant sequoia
seedlings developed O3 injury symptoms at both ambient O3 concentrations and 1.5 x ambient
O3 (0.08- to 0.1-ppm hourly peaks) in OTCs during the 8 to 10 weeks following germination
(Miller et al., 1994). Field-plot observations of seedling health and mortality in natural giant
sequoia groves over a 4-year period showed that seedling numbers were reduced drastically
from drought and other abiotic factors. Any variable, such as O3, that could stress seedlings
sufficiently to reduce root growth immediately after germination could increase vulnerability
to late summer drought. Significant differences in light-compensation point, net assimilation
at light saturation, and dark respiration were found between seedlings in CF air treatments
and 1.5 x ambient O3 treatments (0.08- to 0.1-ppm hourly peaks) (Grulke et al., 1989). One
interpretation of these results is that O3 could be a new selection pressure during the
regeneration phase of giant sequoia, possibly reducing genetic diversity.
The Lake Tahoe Basin is located at the northern end of the Sierra Nevada (near
Eldorado National Forest) (Peterson et al., 1991). Because it is an air basin unto itself, the air
quality situation is distinct from other Sierra Nevada sites. Ozone injury was first reported
for the area in the late 1970s. In 1987, a survey of 24 randomly selected plots in the basin
included a total of 360 trees, of which 105 (29.2%) had some level of foliar injury (Pedersen,
1989).
The radial growth response of big cone Douglas firs (Pseudotsuga macrocarpd) to
long-term O3 exposure was studied throughout the range of these firs in the San Bernardino
Mountains of Southern California. Big cone Douglas fir is found in the mountain ranges of
Southern California and northern Baja California, Mexico. In the San Bernardino Mountains,
the species grows in canyons and on dry slopes at elevations from 700 to 2,200 m and, in
association with canyon live oak (Quercus chrysolepis), throughout the chaparral and lower
elevation mixed-forest communities. Big cone Douglas fir is usually rated as less sensitive
than ponderosa or Jeffrey pine; however, injury symptoms resulting from elevated O3
exposures have been seen (Peterson et al., 1995).
Dendroecological analyses indicate that growth rates have decreased considerably
since 1950 (Peterson et al., 1995). Differences in basal area indices for 1913 to 1950 were
compared with those for 1951 to 1988 to determine whether there were growth changes
associated with increased air pollution during the latter period. More than 80% of all trees
had reduced growth. Trees growing in regions of high O3 exposure had the largest growth
decreases, with approximately 30% of those growing under these conditions having reductions
greater than 50%, and 60% having reductions greater than 20%. Fewer than 10% of the trees
in any O3 exposure area had growth increases greater than 25%. Based on their study, the
authors conclude that, although O3 does not have the same level of impact on these trees as it
does on ponderosa and Jeffrey pine, reduced needle retention and lower recent growth rates
could indicate increased O3 stress (or O3 stress mediated by climate) in big cone Douglas fir.
Long-term monitoring of this species could provide an early warning of additional injury
caused by air pollution in forest ecosystems of Southern California (Peterson et al., 1995).
Site Variables Affecting Ozone Response in the California Ecosystems
Structural changes in forest stands are highly related to their position or site on the
landscape. Site variables can be defined at regional and local levels. For example, the
regional level is defined in California by the location of forested mountain slopes and
summits in relation to polluted urban air basins. In both the Sierra Nevada and the
San Bernardino Mountains in California the greatest tree injury is found on ridges that
5-201
-------
overlook the polluted air basins. The polluted air masses are transported up-slope or
up-cany on in terrain that is usually sunlit in the afternoon and early evening, thus the thermal
convection on warm slopes is a major means by which O3 and associated pollutants are
delivered to the first forested ridges. Both vertical mixing and horizontal diffusion into
cleaner air results in a distinct gradient of decreasing O3 concentration in more distant forest
stands. Two such gradients have been described in the San Bernardino Mountains (Miller
et al., 1986). Along the longer, west-to-east orientation axis of the mountain range, 24-h
average O3 concentrations for the highest summer months ranged from 0.09 to 0.140 ppm
nearest the polluted South Coast Air Basin to 0.04 to 0.05 ppm at a downwind distance of
35 to 40 km. In the more narrow, south-to-north direction, the same concentration gradient is
seen over a much shorter distance of 5 to 8 km because of a more rapid transition to the
warm desert influence, which causes mixing and dilution (Miller et al., 1972). Accordingly,
O3 injury to sensitive vegetation ranges from severe to none over these distances.
In the Sierra Nevada Mountains, a gradient of decreasing injury is observed from
west to east and south to north (Peterson and Arbaugh, 1992). But the worst level of chronic
injury is generally much less than observed in the San Bernardino Mountains.
With respect to localized site variables, there is evidence from repeated surveys in
Sequoia-Kings Canyon National Parks that the percent of trees injured and the severity of
foliar injury both increased with decreasing elevation in the 1,500- to 2,500-m zone on
generally west-facing slopes adjacent to the polluted San Joaquin Valley Air Basin (Stolte
et al., 1992). In Sequoia-Kings Canyon National Parks, radial growth reductions in Jeffrey
pine with foliar injury by O3 were documented only for large, dominant trees growing on
shallow soils (Peterson et al., 1987). Soil moisture availability is generally lower on such
sites. One hypothesis for explaining radial growth decline on these sites and not on more
favorable sites with greater moisture-holding capacity is that O3 defoliation in favorable
moisture years and water stress in dry years integrate sequentially to suppress growth.
In the San Bernardino Mountains, radial growth of ponderosa and Jeffrey pines in
plots along the decreasing O3 gradient was not well correlated with level of chronic injury but
was better correlated with soil-moisture-holding capacity. Within a single plot with relatively
uniform moisture availability there was a good correlation between increased radial growth
and a decreasing level of chronic O3 visible injury to crowns.
5.7.3.4 The Appalachian Mountains—Before 1986
Oxidant-induced injury on vegetation in the Applachian Mountains has been
observed for many years but has not produced the same ecosystem responses as vegetational
injury in the San Bernardino Mountains. Results of studies in the eastern United States were
reported in the 1986 criteria document and are summarized in the following passages (U.S.
Environmental Protection Agency, 1986). Needle blight of eastern white pine was first
reported in the early 1900s, but it was not known until 1963 that the needle blight was the
result of acute and chronic O3 exposure (Berry and Ripperton, 1963). In the 1950s, the U.S.
Forest Service studied the decline of eastern white pine in an area covering several hundred
square miles on the Cumberland Plateau in Tennessee and concluded that atmospheric
constituents were the causes of this decline (Berry and Hepting, 1964; Garner et al., 1989;
Garner, 1991).
Growth reductions in trees growing on the Cumberland Plateau of eastern
Tennessee were studied by Mann et al. (1980) and McLaughlin et al. (1982). A steady
growth decline in annual-ring increment was observed during the years 1962 through 1979.
5-202
-------
Reductions of 70% in average annual growth and of 90% in average bole growth were
observed in sensitive trees, when compared to the growth of tolerant and intermediate trees.
Tolerant trees, when compared to trees of intermediate sensitivity, consistently showed a
higher growth rate (from 5 to 15%) than did intermediate trees for the 1960 to 1968 interval,
similar growth rate from 1969 through 1975, and a reduction in growth (5 to 15%) for the
period 1976 through 1979. The decline was attributed to chronic O3, which frequently
exceeded 1-h average concentrations of 0.08 ppm. Maximum 1-h concentrations ranged from
0.12 to 0.30 ppm for the years 1975 to 1979 (U.S Environmental Protection Agency, 1986).
McLaughlin et al. (1982) observed that the decline in vigor and the reduction in
growth in trees and the production of carbohydrates (carbon flow) were associated with the
following sequence of events and conditions: premature senescence of mature needles at the
end of the growing season; reduced carbohydrate storage capacity in the fall and reduced
resupply capacity in the spring to support new needle growth; increased reliance of new
needles on self-support during growth; shorter new needles, resulting in lower gross
photosynthetic productivity; and higher retention of current photosynthate (carbohydrate) by
foliage, resulting in reduced availability for transport for external use, including repair of
chronically stressed tissues of older needles (U.S. Environmental Protection Agency, 1986).
Despite the early field observations of Berry (1961) and Berry and Ripperton
(1963), no concerted effort was made to determine the effects of O3 on vegetation in the
Appalachian Mountains until the 1970s, when, between April 1975 and March 1976, Skelly
and his coworkers began monitoring total oxidant concentrations and recording associated
injury to eastern white pine in three rural Virginia sites. Injury was observed in the Jefferson
and George Washington National Forests and throughout the Blue Ridge Mountains, including
areas in the Shenandoah National Park and along the Blue Ridge Parkway in Virginia and
North Carolina (Hayes and Skelly, 1977; Skelly et al., 1984). Taylor and Norby (1985), in
their analysis of the 4-year monitoring data of Skelly et al. (1984), point out that there were
an average of five episodes (any day with a 1-h mean O3 concentration >0.08 ppm) during the
growing season in this area. Episodes lasted from 1 to 3 days.
In studies conducted in the Blue Ridge Mountains of Virginia, Benoit et al. (1982)
used annual-ring increments to evaluate the possible effects of oxidant air pollution on the
long-term growth on eastern white pine of reproducing age. Reductions in overall growth of
eastern white pine trees classified as tolerant, intermediate, and sensitive to O3 exposure were
observed. Comparison of growth from 1974 to 1978 with that for 1955 to 1959 indicated
decreases of 26, 37, and 51% for tolerant, intermediate, and sensitive trees, respectively. No
significant changes in seasonal precipitation had occurred during the 1955 to 1963 period or
the 1963 to 1978 period; therefore, the significant reduction in radial growth was assumed by
the authors to be the result of cumulative O3 stress and reduced photosynthetic performance
due to oxidant injury. Monitoring of O3 indicated monthly average concentrations of 0.05 to
0.07 ppm on a recurring basis, with episodic 1-h peaks frequently in excess of 0.12 ppm for
the latter time period (Benoit et al., 1982; U.S. Environmental Protection Agency, 1986).
Duchelle et al. (1982), monitoring in the same area, reported peak hourly averages >0.08 ppm
for the months of April through September in 1979 and 1980. As early as 1979, Skelly
(1980) concluded that the most sensitive eastern white pines were injured so severely by
oxidant exposure that they probably were being removed from the population. It was
estimated that, of the population, 22% were tolerant, 67% were intermediate, and 11% were
sensitive.
5-203
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In the previous O3 document (U.S. Environmental Protection Agency, 1986),
Duchelle et al. (1982, 1983) reported that exposing native tree seedlings and herbaceous
vegetation in the Big Meadows area of the Shenandoah National Park in the Blue Ridge
Mountains of Virginia to ambient O3 reduced both the growth of the native trees other than
eastern white pine and the productivity of the native herbaceous vegetation found growing in
forested areas. Comparison of growth of seedlings in open plots or OTCs with CF air
revealed that growth was suppressed in wild-type seedlings of tulip poplar, green ash, sweet
gum (Liquidambar stymciflud), black locust (Robinia pseudoacacia), eastern hemlock (Tsuga
canadensis), Table Mountain pine (Pinus pungens\ Virginia pine (Pinus virginiana\ and
pitch pine, usually without visible foliar injury symptoms. Open-top chambers were operated
continuously from May 9 until October 9 during 1979 and from April 24 until September 15
in 1980 (U.S. Environmental Protection Agency, 1986). Common milkweed and common
blackberry (Rubus allegheniensis) were two species of native vegetation that exhibited visible
injury symptoms (Duchelle and Skelly, 1981). Monthly 8-h average O3 concentrations ranged
from 0.035 to 0.065 ppm, and peak hourly concentrations from 0.08 to 0.13 ppm (Skelly et
al., 1984; U.S. Environmental Protection Agency, 1986). Common milkweed and common
blackberry represented natural vegetation sensitive to O3 exposure (Duchelle and Skelly, 1981;
U.S. Environmental Protection Agency, 1986).
Forest ecosystems at high altitudes experience higher total exposures because of
the prolonged duration of elevated O3 at high altitudes (see Section 5.4; Wolff et al., 1987;
Winner et al., 1989; U.S. Environmental Protection Agency, 1986). Although daily maximum
and mid-day O3 concentrations are similar at different altitudes, the dosage increases with
height. Ozone is depleted rapidly at night near the earth's surface below the nocturnal
inversion layer; however, mountainous sites above the nocturnal inversion layer do not
experience this depletion. Therefore, the total exposure to O3 in mountainous areas can be
much higher than that in nearby valleys (Berry, 1964; Garner et al., 1989). Maximum
O3 concentrations observed at elevated mountain sites often occur at night; in addition, higher
elevations are often exposed to sustained or multiple peak concentrations of O3 within a given
24-h period. High morning concentrations occur at a time when stomatal conductance is high
and photosynthetic activity is greatest. The cumulative effects of O3 uptake, therefore, could
be severe. These considerations need to be taken into account when assessing the exposure-
response relationships of forest ecosystems at high altitudes (Wolff et al., 1987; Garner et al.,
1989; Garner, 1991).
The field observations cited above indicate that oxidant-induced injury to
vegetation has been occurring in the Appalachian Mountains for many years. By the time
intensive studies were begun in Pocahontas County, WV, in 1957, to determine the cause of
"emergence tipburn", many people living in the area had been reporting casual observations of
the phenomenon for over 20 years. Emergence tipburn, also known as needle blight, of
eastern white pine was observed first in the early 1900s, however it was not shown to be the
result of acute or chronic O3 exposure until 1963 (Berry and Ripperton, 1963).
Although vegetation injury resulting from O3 exposure had been observed in New
Jersey in the 1940s, its cause was not recognized until 1960 (Daines et al., 1960). Ozone was
first recognized as a causal factor of foliar injury when Heggestad and Middleton (1959)
reported that weatherfleck of tobacco was the result of O3 exposures. Concentrations of 0.38,
0.43, and 0.5 ppm were measured at Beltsville by newly developed Mast meters during 1958.
(The concentrations cited are approximately 0.1 ppm higher than those measured more
recently. Calibration of the then new Mast meters was sometimes a problem [Garner, 1991]).
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Regular oxidant monitoring stations were first established east of the Mississippi
River in 1962. Valid oxidant data, however, was not available until 1964, and then only for
the cities of Chicago, Cincinnati, St. Louis, Philadelphia, Washington, DC, and Denver
(National Air Pollution Control Administration, 1968). Maximum oxidant concentrations
recorded between 1964 and 1967 indicated that Cincinnati had 10 days >0.15 ppm;
Philadelphia, 60 days >0.06 and 13 days >0.15 ppm; and Washington, DC, 65 days >0.10
ppm and 7 days >0.15 ppm (U.S. Environmental Protection Agency, 1986). Berry and
Ripperton (1963) reported the presence of oxidant concentrations above 0.10 ppm during 1961
and 1962 in West Virginia and in North Carolina as far east as Raleigh. These data indicate
that O3 concentrations sufficient to injure vegetation regularly were present from the Midwest
to the east coast (Garner et al., 1989; Garner, 1991).
In retrospect, it is apparent that O3 episodes in the eastern United States have not
been unusual. Taylor and Norby (1985) analyzed the 4-year monitoring data of Skelly et al.
(1984) and concluded that episodes in which the 1-h O3 concentration was >0.08 ppm were
experienced, on average, five times during the growing season. Episodes when peak
O3 concentrations exceeded 0.10 ppm in the southern Appalachian Mountains were recorded
during 1975 (Hayes and Skelly, 1977) and 1979 through 1982 (Skelly, 1980). Injury to
eastern white pine at three rural sites in Virginia from July 1 to 5, 1975, was associated with
a high pressure over the Great Lakes and a low, Hurricane Amy, off the Atlantic coast. Air
parcels bearing O3 moved in from the Northeast and Midwest into Virginia. The episode
dissipated when the cold from the Midwest moved across Virginia into the Atlantic Ocean
(Hayes and Skelly, 1977). More recent O3 episodes in the same area have been associated
with meteorological phenomena similar to the one mentioned above (Skelly et al., 1984;
Garner et al., 1989).
Ozone episodes for the eastern United States also were recorded during 1976 and
1977. Typical episodes were associated with high-pressure systems that originated in Canada,
moved southeastward into the Midwest, and then eastward to the Atlantic coast. For example,
an episode covering most of a 20-state area occurred April 12 to 23, 1976. During this
episode, O3 concentrations in excess of 0.08 ppm occurred simultaneously from the Midwest
to the Atlantic coast and into the northeastern United States. Ozone trajectories extended
from Ohio to New Jersey (Wolff et al., 1977a,b,c; Garner, 1991). Additional studies
indicated that two other episodes exhibiting trajectories similar to the one described above
took place in August 1976. These episodes included an area extending from West Virginia
across Virginia in the south and north to Maine. Maximum concentrations measured in the
trajectories during the two August episodes were 0.20 ppm (Wolff et al., 1980; Garner, 1991).
In 1977, there were three episodes: (1) July 12 to 21, (2) July 21 to 24, and
(3) July 26 to 30 (Wolff et al., 1980). The first episode, unlike the ones the previous year,
originated in the Texas-Louisiana area. Air parcels traveled northeastward to the lower
Midwest and then to the Atlantic coast, extending an "ozone river" from the gulf coast of
Texas to Louisiana to the northeast Atlantic coast, exposing the entire area to concentrations
averaging 0.12 to 0.13 ppm. The second and third episodes, like the 1976 episodes,
originated in Canada. Because the southern part of the first episode persisted at the time the
second and third episodes began, O3 from the south was pulled into the Midwest, and the
region from the Texas gulf coast eastward to the Atlantic coast continued to be exposed to the
high concentrations. These episodes simultaneously exposed nearly two-thirds of the United
States (Wolff and Lioy, 1980; Garner, 1991).
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Long-range transport of O3 need not begin in Canada, the Midwest or Texas.
Fankhauser (1976) reported the transport of O3 in a giant loop stretching from New York
City, Philadelphia, Baltimore, and Washington, DC, west through Virginia and Ohio and back
to Wheeling, WV, to the Pittsburgh, PA, area. This path continued for 4 to 5 days in
September, 1972. Earlier, in May 1972, a stagnant high and a slow-moving low transported
air parcels from the Chicago and Pittsburgh areas to Miami, FL (Garner et al., 1989; Garner,
1991).
The foregoing discussion not only depicts the episodic nature of O3 exposures, but
also points out the fact that the major portion of the United States east of the Mississippi
River has been exposed frequently to phytotoxic O3 concentrations. Taylor and Norby (1985)
estimate the probability is 80% that any given O3 episode in the Shenandoah forest will
persist for at least 3 days. This information concerning the effects of O3 exposure is
summarized from the 1986 criteria document (U.S. Environmental Protection Agency, 1986).
5.7.3.5 The Appalachian Mountains and the Eastern United States—Since 1986
Changes in growth, decline, and mortality of certain tree species have been
reported for high-elevation forest ecosystems from Maine, New Hampshire, Vermont, and
New York, south to North Carolina and Tennessee. Studies indicate that the decrease in
growth of forest trees began during the late 1950s or early 1960s (Adams et al., 1985; Benoit
et al., 1982; Johnson et al., 1984; Phipps and Whiton, 1988; Garner et al., 1989; Garner,
1991). The extent of decrease in growth and of dieback and mortality, and the factors that
precipitated them, are subject to controversy (Garner, 1991; Garner et al., 1989; Taylor and
Norby, 1985). Many hypotheses, including O3 exposure, have been advanced as possible
causes. The problem, as pointed out by Woodman and Cowling (1987), is establishing
causation. Rigorous proof is needed, but only circumstantial evidence is available. Because
the growth reductions began so many years ago, long-term historical data regarding forest
structure and composition is lacking (Garner, 1991; Garner et al., 1989). An additional factor
that makes causation difficult to determine is that mature ecosystems are not completely
stable, but maintain themselves in an oscillating steady state (Kozlowski, 1985). No long-
term studies of the effects of tree decline and mortality on ecosystems similar to those dealing
with the exposure and response of the San Bernardino mixed-forest ecosystem in California
have been made in the East.
Surveys made in 1982, but mentioned only briefly in the previous criteria
document (U.S. Environmental Protection Agency, 1986) give quantitative evidence of a
marked dieback and large reductions in basal area and in density of red spruce in the
high-elevation forests of New York, Vermont, and New Hampshire (Johnson and Siccama,
1983). Red spruce is the most characteristic species of subalpine forests that occupy the
higher peaks and ridges of the Appalachian Mountains from Maine to North Carolina and
Tennessee. A co-dominant species in the North is balsam fir (Abies balsamea), whereas
Fraser fir, a closely related species, is co-dominant in the South (Adams et al., 1985).
A detailed description of the red spruce decline in the eastern United States and possible
causes and studies conducted to determine the causes can be found in Eager and Adams
(1992). In the summary chapter of that text, Johnson et al. (1992) write that they "are in a
position to state and support with field and laboratory data that regional scale air pollution has
played a significant role in the decline of red spruce in the eastern United States." Ozone
usually is considered the only regional air pollutant. In this instance, however, the authors
are referring to NOX and SOX, the precursors of acidic deposition. Studies evaluating the
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direct effects of O3 on red spruce have found little evidence for a significant effect
(McLaughlin and Kohut, 1992). Recent studies evaluating the responses of red spruce and
loblolly pine to acidic precipitation and O3 indicate that high-elevation red spruce forests
could be impacted by acidic deposition enhancing soil acidification, mobilization of aluminum
ions (A13+), and reducing the availability of important base cations (Edwards et al., 1995).
In the Southeast, the decline and mortality of Fraser fir in the Great Smoky
Mountains National Park, and, in North Carolina, the Plott Balsam Mountains and the Black
Mountains, which include Mt. Mitchell, have been attributed to infestation by the balsam
wooly adelgid (Hain and Arthur, 1985). The west-facing slope of Mt. Mitchell showed the
greatest injury. During a 20-year experimental study of Fraser fir growing in the Smoky
Mountains National Park, balsam wooly adelgids killed almost all of the canopy trees and
reduced the basal area in two plots established in the 1960s. Red spruce basal area in these
plots remained about the same for the same period. The report does not mention whether
atmospheric pollutants were monitored, nor does it discuss possible pollutant-pathogen
interaction or possible predisposition (Busing et al., 1988).
Other studies on Mt. Mitchell, however, do not attribute the death of Fraser fir
solely to the balsam wooly adelgid, but suggest that atmospheric deposition and multiple
pollutant stresses also had a role in tree mortality. These studies cite exposure to gaseous air
pollutants, particularly O3, and cloud-water deposition of acidic substances among possible
stresses that have increased host susceptibility to attack by the balsam wooly adelgid (Hain
and Arthur, 1985; Aneja et al., 1992). Ozone levels for the area have ranged from 0.01 to
0.150 ppm, with the highest concentrations occurring early in the summer (Aneja et al.,
1992).
Other than the studies of tree death in the specific regions cited above, the studies
in the Appalachian Mountains have been field surveys made to identify possible O3-related
foliar injury symptoms on native vegetation and experimental exposures to verify the
symptoms and to determine O3 response of individual forest tree species and other native
vegetation, usually using OTCs. Unfortunately, some of the studies exposing individual forest
tree species cannot be used because the concentrations at which exposure occurred are given
as ambient plus 1, plus 1.5, or plus 2, etc. The actual ambient concentration at the time of
exposure is never mentioned in the paper. A few studies use an index, again without stating
the O3 concentration and duration of exposure from which the index was derived. These
papers are of little scientific value in this discussion because the actual concentrations and
duration of exposures at which vegetational injury occurred cannot be determined.
Data from the Forest Inventory Analysis timber inventory taken between 1972 and
1982, revealed that the annual growth rate of most southern yellow pines (loblolly, pitch,
shortleaf, and slash) under 16 in. in diameter had declined by 30 to 50% throughout the
Piedmont and mountain areas of the Southeast since measurements were made during the
survey of 1957 to 1966 (Sheffield et al., 1985). Ozone has been suggested as a possible
cause; however, verification of growth effects on mature trees has been lacking (McLaughlin
and Downing, 1995).
Additional studies of the forest condition were conducted by the United States
Forest Service. Millers et al. (1989) reviewed the information on tree mortality that has
occurred in the eastern hardwood forest during the last century to determine whether a
relationship exists between the patterns of mortality and the patterns of atmospheric pollution.
The authors suggest "that the apparent increase in the decline and mortality of many
hardwood species during the last few decades may be due to intensification of reporting and
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to the maturation of the forest itself." Most of the mortality observed was attributed to
abiotic and biotic stress factors such as weather, silviculture, and injury by insects and
diseases. Although there is evidence of injury to hardwoods from point-source pollutants
such as smelters and to eastern white pine from O3, there is no conclusive evidence of an
association between patterns of hardwood mortality and regional atmospheric pollution
(Millers et al., 1989). Millers et al. (1989) point out, however, that historical data on
atmospheric deposition are not readily available to compare with historical data on mortality.
Twardus et al. (1993) describe forest conditions in twenty states within the
Northeastern United States. Information on forest health in this report was obtained from the
Cooperative Forest Health Program, from the Forest Inventory and Analysis Surveys
conducted by the U.S. Department of Agriculture Forest Service between 1971 and 1993, and
from the Northern Forest Health Monitoring Program. They state that "there continues to be
no evidence of large, regional-scale declines in forest ecosystem health as determined by
observation of visible crown indicators on trees, e.g., crown dieback, crown density, and
foliage transparency." Symptoms of exposure to O3 were noted on sensitive plants on 10 of
98 plots where bioindicator plants were located.
Recently, McLaughlin and Downing (1995) completed a 5-year study of the
interactive effects of ambient O3 and climate on the growth of mature loblolly pines. Ozone,
temperature, and moisture stress often correlate well with each other in the southeastern
United States because hot, dry years often are associated with air stagnation systems that
result in regional O3 episodes. Tree growth rates, as measured by annual circumference
increase per tree for two drier upland sites (16 trees) and a wetter more fertile stand near a
stream bottom (18 trees), were compared. Short-term changes in stem circumference of 24 to
34 mature trees were measured at 138 intervals during five growing seasons (May through
October) using a sensitive dendrometer band system. During the period of the study, widely
variable temperature, rainfall, and O3-exposure conditions and growth rates that varied by
75% across the years were observed. Growth rates were consistently influenced by 3-day
average O3 exposures >40 ppm during the period from 0900 to 2000 hours (9:00 a.m. to
8:00 p.m.). McLaughlin and Downing (1995) stated that their model, which combined
5 years of growth data, suggested that the high-frequency effects of the 0.30 ppm-h increase
in mean daily O3 exposure in the most polluted year (1988), when compared to the cleanest
year (1989), would reduce stem growth by approximately 7% in a relatively moist year and
by almost 30% in a moderately dry year. They conclude that both episodic and chronic
alterations of stem growth in mature trees are associated with ambient levels of O3. Episodic
reductions are related directly to O3 exposure, whereas chronic alterations reflect the
interaction of O3 exposures and climatic stresses.
The surveys described below, specifically those made in the Shenandoah National
Park, indicate that the injury to native vegetation reported by Hayes and Skelly (1977), Skelly
(1980), Benoit et al. (1982), and Duchelle et al. (1982) continues to occur. This is cause for
concern because the 48 national parks, including the Great Smoky Mountain and Shenandoah
National Parks, are designated as Class I areas under the amended Clean Air Act (U.S. Code,
1991). Air pollution effects on resources in Class I areas constitute an unacceptable adverse
impact if such effects diminish the national significance of the area, impair the quality of the
visitor experience, or impair the structure and functioning of the ecosystem (Fox et al., 1989;
Chappelka et al., 1992). Factors considered in determining if an effect is unacceptable
include the frequency, magnitude, duration, location, and reversibility of the impact.
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In a survey of eastern white pine stands in the southern Appalachians, 50 white
pines were examined for foliar symptoms (chlorotic mottle) believed to be caused by O3 at
each of 201 sites distributed on a 24 x 24-km grid across the natural range of the species in
South Carolina, Tennessee, Virginia, North Carolina, Kentucky, and Georgia (Anderson et al.,
1988). The survey was conducted from September through November 1985. The percentage
of stands with at least one symptomatic tree was highest in Kentucky (77%), followed by
Tennessee (31%), and lowest in Georgia (10%). The mean percentage of symptomatic trees
per plot for all six states was 27%. The mean volume difference of 48 pairs of symptomatic
and nonsymptomatic trees was 49% less for symptomatic trees. Elevation and percent slope
were not correlated with occurrence of symptomatic trees, but most symptomatic trees were
found on southwest-facing slopes. Plantations had a higher percentage of symptomatic trees
than did natural stands. Ozone exposure concentrations were not reported, but it may be
possible to make estimates of exposure using data from the nearest O3 monitoring sites.
Shenandoah and Great Smoky Mountains National Parks are contained within the
survey area investigated by Anderson et al. (1988). Winner et al. (1989) surveyed 7 to
10 individuals of five native species at 24 sites in Shenandoah National Park. These species
included tulip poplar, wild grape (Vitis sp.), black locust, virgin's bower (Clematis
virginiana), and milkweed. Visible foliar injury due to O3 was most prevalent on milkweed
species (up to 70%), whereas the remaining species had injury approaching 20%. In each
case, the level of foliar injury increased with the elevation of the sites. The summer monthly
24-h mean O3 concentrations at Blacksburg, Rocky Knob, Salt Pond, and Big Meadows did
not exceed 0.06 ppm, and foliar injury still was observed.
Another survey made during August to September, 1991, in the Shenandoah
National Park included black cherry, yellow poplar, and white ash; and, in the Great Smoky
Mountains National Park, black cherry, sassafras (Sassafras albidum), and yellow poplar
(Chappelka et al., 1992). Black cherry exhibited symptoms in both parks. In the former, the
percentage of leaves injured ranged from 18 to 40, whereas, in the latter, the range was 8 to
29% in 1991. Black cherry at Cove Mountain in the Great Smoky Mountains National Park
exhibited the highest percentage of symptomatic trees (97%). This site also had the highest
number of hours exceeding 0.08 ppm. The majority of occurrences of concentrations
exceeding 0.08 ppm occurred during evening hours. Chappelka et al. (1992) suggest that
some of the variability in foliar injury response of hardwood species to O3 in the Shenandoah
and Great Smoky Mountains National Parks is due to elevation and microsite conditions,
including proximity to streams.
During surveys made in the summers of 1987 through 1990, a total of 95 different
plant species, approximately 6% of those growing in Smoky Mountain National Park,
exhibited possible foliar injury symptoms attributable to O3 exposures (Neufeld et al., 1992).
Plant species exhibiting foliar injury varied from herbaceous herbs, a grass and a fern, to
woody deciduous angiosperms and nine species of evergreens, of which six were conifers.
Species exhibiting field symptoms included the native trees (black cherry; sycamore; tulip
poplar; black locust; sweet gum; eastern hemlock; and Virginia, Table Mountain, and pitch
pines) and herbaceous plants, such as virgin's bower, wild grape, and tall milkweed, all plants
previously reported by Duchelle and Skelly (1981) and listed in the previous criteria
document (U.S. Environmental Protection Agency, 1986) as being sensitive to O3 exposures.
Ozone concentrations during the period of the surveys did not exceed 0.12 ppm. The
observation was made that plants growing at the highest elevations experienced higher
maximum and higher minimum concentrations and were exposed to 50% more O3.
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To verify the foliar injury observed in the field as being due to O3, 39 species,
28 of them with field injury symptoms, had been fumigated experimentally in OTCs at the
time of publication. Exposures resulted in injury symptoms on 25 of the 28 species that
exhibited injury in the field (Neufeld et al., 1992).
Surveys also were made in a Class I areas in New Hampshire and Vermont during
the years 1988 to 1990 (Manning et al. 1991; Lefohn and Manning, 1995). Ozone injury was
extensive on vegetation growing in open-top and ambient air experimental plots in both states
in 1988, when O3 concentrations were unusually high. The incidence and intensity of O3
injury symptoms were considerably less in 1989, whereas, in 1990, injury symptoms were
evident on all plants. Based on the studies, it was determined that black cherry, milkweed,
white ash, white pine, and two species of blackberry were all reliable biological indicators of
ambient O3 exposure (Manning et al., 1991).
The above surveys indicated that although there has been evidence of widespread
injury to native trees and other vegetation from exposure to O3, the amount of injury has not
been great enough for it to be transferred from the tree level to the stand level. Undoubtedly,
there has been selection for and removal of the most sensitive tree species of eastern white
pine, for example. However, the numbers of sensitive individuals in a stand have not been
great enough to make a visible impact on the forest. Simulations suggest that, in forests with
mixed species of uneven-aged stands, long-term responses are likely to be shifts in species
composition rather than widespread degradation (Taylor and Norby, 1985; U.S. Environmental
Protection Agency, 1986).
5.7.3.6 Rhizosphere and Mycorrhizal-Plant Interactions
The importance of the below-ground ecosystem largely has been overlooked when
evaluating ecological responses to oxidant exposure. Although the soil system is part of the
larger terrestrial ecosystem, it is a system that operates independently and, therefore, is itself
an ecosystem (Richards, 1987). Although above-ground components of the terrestrial
ecosystem are dominated by producers, the below-ground system is composed primarily of
consumers. Thus, the below-ground system is dependent on the above-ground system for
inputs of energy-containing substrates. Bacteria, fungi, protozoa, nematodes, microarthropods,
earthworms, and enchytraeids all serve various functions in maintaining biological, physical
and chemical characteristics of soil, and all are dependent on plant residues for their
maintenance. Although the uniqueness of the below-ground ecosystem needs to be
recognized, the interdependence between the above- and below-ground systems cannot be
over emphasized.
Mycorrhizal fungi are an integral part of the below-ground ecosystem of terrestrial
plant communities and are of great importance for vegetational growth. The 1986 criteria
document (U.S. Environmental Protection Agency, 1986) discussed mycorrhizae-plant
interactions and their importance in some detail. Mycorrhizae are formed on the roots of the
vast majority of terrestrial plants and contribute substantially to ecosystem function (Allen,
1991; Harley and Smith, 1983). Fungi invade the roots of terrestrial plants and transform
them into mycorrhizae or "fungus roots". The fungus and the host plant live together in an
association beneficial to both organisms. Most terrestrial plants cannot adequately take up
soil nutrients and water and achieve optimum growth and reproduction without mycorrhizae
(Hacskaylo, 1973; Ho and Trappe, 1984; Allen, 1991). Mycorrhizal fungi increase the
solubility of minerals, improve the uptake of nutrients for host plants, protect their roots
against pathogens, produce plant growth hormones, and transport carbohydrate from one plant
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to another (Hacskaylo, 1973). In exchange, the roots of the host plant provide the fungi with
simple sugars (Hacskaylo, 1973; Krupa and Fries, 1971). The fungus-plant root relationship
is particularly beneficial to plants growing on nutrient-poor soils.
Ozone stress reduces photosynthesis and growth, and roots often are more affected
than shoots (Figure 5-33; Winner and Atkinson, 1986; McCool and Menge, 1984; Blum and
Tingey, 1977; Manning et al., 1971b; Tingey and Blum, 1973; Hogsett et al., 1985a; Tingey
et al., 1976b; Spence et al., 1990; McLaughlin et al., 1982). It has been shown to affect both
leaf senescence and root production in plants, thereby disrupting carbon availability for
maintenance of the below-ground system (Gorissen et al., 1991b; Andersen and Rygiewicz,
1991), and to alter mycorrhizal colonization and compatibility (Stroo et al., 1988; Reich et al.,
1986a; Simmons and Kelly, 1989).
Leaf
Biomass
Photosynthetic
Rate
/
" K \
Root
Biomass
Nutrient N
Uptake )
Initial
Allocation
State
Environmental
Stress
Carbon
Reduce
Carbon Supply
Low Light
New
Allocation
State
Reduce
Nitrogen/Water Supply
Drought
Low Soil Fertility
Leaf
Biomass
Root
Biomass
Carbon1
Figure 5-33. Impact of a reduced supply of carbon to the shoot, or water and nitrogen to
the roots, on subsequent allocation of carbon.
Source: Winner and Atkinson (1986).
Mycorrhizae are sensitive to the capacity of the plant to translocate carbohydrate
compounds to the roots. Studies have shown that simple sugars provided by plant roots are
utilized readily by mycorrhizae and enhance fungal inoculation (McCool and Menge, 1984;
Hacskaylo, 1973). Ozone has the capability of disrupting the association between the
mycorrhizal fungi and host plants by inhibiting photosynthesis and reducing the amount of
sugars available for transfer from the shoot to the roots (see Figure 5-3). Reduction in the
roots of available sugars can reduce mycorrhizal formation and root growth as well (Andersen
et al., 1991). Berry (1961) examined the roots of eastern white pine injured by O3 and
observed that healthy trees had almost twice the percentage of living feeder roots as trees
with O3 injury. In the San Bernardino Forest in California, Parmeter et al. (1962) observed
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that the feeder roots system of ponderosa pine exposed to O3 showed marked deterioration
(U.S. Environmental Protection Agency, 1986).
Some studies of the effects of O3 on tree species that include the investigation of
the effects on ectomycorrhizal associations and have been discussed in a series of articles
(Shafer and Schoeneberger, 1991). Selected studies are summarized in Table 5-35. The
understanding of oxidant effects on root symbioses has not changed substantially since 1986
(U.S. Environmental Protection Agency, 1986); however, the understanding of the importance
of symbiotic organisms in ecosystem function has improved. The basic hypothesis on
mechanisms remains the same (i.e., effects are mediated through host carbohydrate
metabolism) because oxidants do not penetrate the soil more than a few centimeters. Most of
the research has been conducted on individual plant species, usually as seedlings, in
controlled environments. Although the role of mycorrhizae in community structure has been
recognized, it has not specifically been addressed experimentally.
Other studies have refined the understanding of oxidant stress effects on roots.
In Douglas fir, root/soil respiration was reduced significantly during the first 1 to 2 weeks
after exposure to O3 or SO2, followed by a recovery period that resulted in similar total
respiratory release between treatments and controls (Gorissen and van Veen, 1988; Gorissen
et al., 1991a). Total allocation to roots did not appear to be reduced, but O3 apparently
reduced translocation to roots in that respiration of 14C was suppressed. Edwards (1991)
found that root and soil respiration were reduced in loblolly pine seedlings exposed to
O3 levels ranging from 0.07 to 0.11 ppm (7-h mean) compared to seedlings exposed to levels
below ambient (0.02 to 0.04 ppm). Nouchi et al. (1991) found that O3 at 0.1 ppm reduced
root respiration by 16% in domestic rice (Oryza. saliva) after 1 week of exposure. However,
exposure to 3 to 7 weeks of 0.1 ppm O3 resulted in elevated levels of root respiration.
The effects of O3 on carbohydrate allocation to roots and subsequent shifts in
biomass allocation have been examined (Cooley and Manning, 1987; Kostka-Rick and
Manning, 1992a; Karnosky et al., 1992b; De Temmerman et al., 1992; Qui et al., 1992;
Sharpe et al., 1989; Gorissen and van Veen, 1988; Gorissen et al., 1991a; Spence et al.,
1990). Gorissen et al. (1991b) also studied the effects of O3 exposure on Douglas fir
inoculated with the fungi Rhizopogon vinicolor and Lactarius rufus and watered with
ammonium sulfate. The investigators found greater needle retention of 14C-labeled
compounds in the new needles of O3-treated plants, and a trend towards fewer 14C-labeled
substrates recovered in roots and root/soil fractions. Short-term transport of nC-labeled
substrates were followed throughout loblolly pine (Spence et al., 1990). A 45% reduction in
transport of photosynthates to roots occurred in O3-treated plants compared to controls.
Collectively, the studies have shown a general trend of diversion of carbohydrate from roots
and retention in the photosynthetically active portions of plants. A reduction in allocation to
roots can be associated with a change in the availability of carbohydrate for maintenance of
root symbioses.
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Table 5-35. Interactions of Ozone and Forest Tree Ectomycorrhizae3
Host Plant
Mycorrhizae
Exposure Conditions Effect of O3 on Mycorrhiza
Reference
Oi
^
CO
Loblolly pine
Scots pine
White pine
Norway spruce
Paper birch
Red oak
Pisolithus tinctorius
Not stated
Not stated
Not stated
Ten species
Pisolithus tinctorius
Six species
Four species
Pisolithus tinctorius
Not stated
OTC, field
OTC, field, 3 years
CEC
CSTR
Open air, field, 3 years
CEC
Open air, field, 3 years
CEC
CEC
CEC and OTC
Reduced root infection
Reduced root infection
No effect
Reduced root infection
No significant effects
Reduced root infection
No significant effects
No consistent effects
No effects
Significant increase
Adams and O'Neill (1991)
Edwards and Kelly (1992)
Mahoney et al. (1985)
Meier et al. (1990)
Shaw et al. (1992)
Stroo et al. (1988)
Shaw et al. (1992)
Blaschke and Weiss (1990)
Keane and Manning (1988)
Reich et al. (1985)
aSee Appendix A for abbreviations and acronyms.
-------
The effects of O3 on mycorrhizal colonization have varied depending on the
experimental conditions and the species used. Stroo et al. (1988) studied the effects of O3 on
mycorrhizal infection in eastern white pine seedlings grown for 4 mo in several soils. Results
varied by soil type and nitrogen availability; however, in several soils, the number of
mycorrhizal short roots increased slightly at low O3 levels and decreased significantly at
higher O3 concentrations. Reich et al. (1986a) found similar results in eastern white pine and
red oak and concluded that O3 may stimulate mycorrhizal infection at low O3 concentrations.
Simmons and Kelly (1989) observed a trend of greater mycorrhizal short roots in loblolly
pine seedlings exposed to subambient O3 treatment than those exposed to ambient or twice
ambient O3 levels, but the results were not statistically significant. In another study with two
families of loblolly pine, Adams and O'Neill (1991) found that mycorrhizal colonization
tended to increase with O3 during the first 6 weeks of exposure and decrease with O3 after 12
weeks of exposure. Meier et al. (1990) found a decrease in ectomycorrhizal root tips and
percentage of feeder roots in loblolly pine seedlings. Keane and Manning (1988) found
significant interactions among O3, soil type, and pH; however, the direct effects of O3 were
difficult to elucidate. Collectively, these results suggest that O3 does impact colonization of
roots by mycorrhizal fungi; however, the results illustrate the variability in response due to
such factors as soil condition, duration of experiment, and timing of measurements.
Altered root carbohydrate allocation resulting from O3 exposure can affect host-
fungus compatibility (Edwards and Kelly, 1992; Simmons and Kelly, 1989). Combined
effects of O3, rainfall acidity, and soil magnesium status on growth and ectomycorrhizal
colonization of loblolly pine has been studied (Simmons and Kelly, 1989). Although
variation was high, there was a trend towards altered species composition and reduced
mycorrhizal infection in O3-treated seedlings. Edwards and Kelly (1992) found high
variability in morphotype (morphologically different) frequency in response to O3 treatments
in loblolly pine and noted changes in morphotype frequency over the 3-year study that
suggested fungal succession had occurred. Fungal succession and the effects of oxidant stress
on normal success!onal patterns are poorly understood. Shaw et al. (1992), using an open-
field exposure system, found no differences in morphotype frequency or fruit-body succession
in response to O3 treatments.
The availability of current photosynthate for root growth is reduced under
O3 stress, and maintenance of below-ground processes dependent on roots for their carbon
substrates may be affected. Mycorrhizae alter the size, quality, and retention time of carbon-
pools below ground. As noted in the previous section, a 45% reduction in transport of
photosynthates to roots occurred in O3-treated loblolly pine (Spence et al., 1990). Ozone
reduces concentrations of root carbohydrates (Jensen, 1981; Tingey et al., 1976b; Meier et al.,
1990; Andersen et al., 1991). Starch in roots was reduced significantly in ponderosa pine by
the end of one growing season of O3 exposure (Tingey et al., 1976b). Reductions in coarse
and fine root starch concentrations persisted over the winter in O3-treated ponderosa pine and
were lower during shoot flush in subsequent years (Andersen et al., 1991). In this study,
lower starch concentrations in O3-treated seedlings were associated with suppressed growth of
new roots. The consequences of a reduction in carbon allocation below ground include
reduced substrate availability for soil flora and fauna; altered soil physical characteristics,
such as total organic matter and aggregation; and altered soil chemical characteristics
including cation exchange capacity.
Premature leaf senescence has been observed in plants exposed to O3 stress
(U.S. Environmental Protection Agency, 1986). Premature senescence affects the
5-214
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belowground ecosystem by reducing canopy photosynthesis and carbon availability for
transport to the belowground system and by increasing leaf litter inputs to the forest floor
(Miller, 1984; Fenn and Dunn, 1989). The result is increased flux of nutrients, especially
nitrogen, below ground, due to oxidant exposure.
The increased flux of nitrogen due to premature needle senescence in
oxidant-exposed plants may act to disrupt the nutrient flow of the ecosystem. Allocation of
carbon resources throughout a plant is based on a priority scheme that is driven by carbon
and nutrient availability (Waring and Schlesinger, 1985). When soil nutrient levels are high,
allocation to the shoot is favored over the roots (Figure 5-32). By shifting carbon allocation
to organs in this fashion, plants can adjust to shifts in resource availability in their
environment. Oxidant stress alters typical allocation schemes and, in the process, may impair
the plant's ability to cope with drought or other stresses. In addition, reductions in allocation
to roots can alter root-system size, architecture, and spatial arrangement, which, in turn, can
influence populations of soil organisms.
Bacteria and fungi are particularly important in nutrient cycles and act to
immobilize nitrogen, carbon, phosphorus, and other nutrients in the biomass. The turnover of
these nutrient pools is relatively short because bacterial and fungal predators act to release
these nutrients. The majority of plant-available nitrogen during the growing season comes
from these predatory interactions in the soil (Kuikman et al., 1990; Ingham et al., 1985),
emphasizing their importance in the maintenance of terrestrial ecosystems. Currently, there
are no data available on the effect of O3 on soil fauna.
In summary, mycorrhizal fungi are essential for optimal plant growth. Mycorrhizal
fungi increase the solubility of minerals, improve the uptake of nutrients for the host plants,
and protect plant roots against pathogens. In turn, the plant roots furnish the fungi with
simple sugars that readily are utilized by the fungi and enhance their ability to form
mycorrhizae. Mycorrhizae are sensitive to the capacity of the plant to translocate these
carbohydrates to the roots. Ozone, by inhibiting photosynthesis, reduces the production of
sugars available for transport to the roots. Reduction of sugars in the roots can reduce
formation of mycorrhizae and root and tree growth as well.
5.7.4 Ecosystem Response to Stress
5.7.4.1 Introduction
Mature forest ecosystems are seldom stable. They are complex, dynamic
communities of living and dead trees interacting among themselves; with populations of
native forest floor plants; and with an array of microorganisms, insect pests, and
environmental, human, and other factors to continuously shape and reshape the community
over time (Manion and Lachance, 1992). Forest communities are held in steady state by the
operation of a particular combination of biotic and abiotic factors. Stresses that alter or
remove any of the factors can alter the community and change the ecosystem (Kozlowski,
1980; Garner et al., 1989).
Growth of new trees and other vegetation requires the expenditure of energy in the
form of carbon compounds. Plants accumulate, store, and use carbon compounds to build
their structure and to maintain their physiological processes. Carbon dioxide absorbed from
the atmosphere is combined in plant leaves with water from the soil to produce the carbon
compounds (sugars) that provide the energy utilized by trees for growth and maintenance
(Figure 5-34; Waring and Schlesinger, 1985). Patterns of carbon allocation to roots, stems,
5-215
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and leaves directly influence growth rate. The strategy for carbon allocation changes during
the life of a plant, as well as with different environmental conditions (Figure 5-33; Winner
and Atkinson, 1986). Mature trees have a higher ratio of respiration to photosynthetic tissue
(Cregg et al., 1989). Even small changes in photosynthesis or carbon allocation can
profoundly alter the structure of a forest (Waring and Schlesinger, 1985). Impairment of the
process of photosynthesis shifts carbon allocation from growth and maintenance to repair and
increased respiration and can result in resource imbalances. The significant changes observed
in the San Bernardino Forest ecosystem were possible outcomes of the combined influences
of O3 on carbon, water, and nutrient allocation (McLaughlin, 1994).
Intense competition among plants for light, water, nutrients, and space, along with
recurrent natural climatic (temperature) and biological (herbivory, disease, or pathogen)
stresses, can alter the species composition of communities by eliminating those individuals
sensitive to specific stresses, a common response in communities under stress (Woodwell,
1970; Guderian, 1985). Individual organisms within a population vary in their ability to
withstand the stress of environmental changes. The range of variability within which these
organisms can exist and function determines the ability of the population to survive. Those
organisms able to cope with stresses survive and reproduce. Competition among different
species results in succession (community change over time) and ultimately produces
ecosystems composed of populations of plant species that have a capacity to tolerate the
stresses (Kozlowski, 1980). Pollutant stresses, such as those caused by exposure to O3, are
superimposed on the naturally occurring competitional stresses mentioned above (see also
Section 5.4). Communities, due to the interaction of their populations, respond to pollutant
stresses differently from individuals (U.S. Environmental Protection Agency, 1993). Air
pollutants are known to alter the diversity and structure of plant communities (Guderian et al.,
1985). The extent of change that may occur in a community depends on the condition and
type of community, as well as on the pollutant exposure.
The plant processes of photosynthesis, nutrient uptake, respiration, translocation,
carbon allocation, and growth are directly related to the two essential ecosystem functions of
energy flow and nutrient cycling. Altering the above processes can alter energy flow and
nutrient cycling and impact ecosystems (Smith, 1992). Response of forest ecosystems to
stress are growth-
related processes that begin within individual trees and progress to increasing levels of
integration and complexity (Figure 5-35; McLaughlin, 1994). Cytological and biochemical
changes within a tree can impact physiological functions and alter the tree's growth and
productivity. Plants acclimate to changing environmental stresses through both short- and
long-term physiological responses, as well as through structural and morphological
modifications (Dickson and Isebrands, 1991). When there are many sensitive individuals, the
forest structure is changed. As indicated above, response begins with the interaction of the
individual and its environment, progresses to the population and its environment, and then to
the biological community and its environment (Billings, 1978).
In unpolluted atmospheres, the number of species in an ecosystem usually
increases during succession. Productivity, biomass, community height, and structural
complexity increase in the early stages of development. Severe stresses, on the other hand,
divert energy from growth and reproduction to maintenance and repair and alter succession
(Waring and Schlesinger, 1985). In addition, biomass accumulation and production decrease,
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1
Construction
Respiration 2
Carbon
Gain
^Carbon
Pool
Distribution^~*Synthesis
en
^J
.Photosynthetic
System
.Reproductive.
System
c
o
I
"a.
to
o
cc
Storage (in Roots, Stems, or Leaves)
CO,
CO,
.Support and
Conductive System's
"Root System
SCO,
CO
I
"(6
CO,
Figure 5-34. Carbon uptake through photosynthesis is made available to a general pool of carbohydrates used in construction and
maintenance of various tissues. Carbohydrates may be shifted from one category to another, depending on
environmental conditions.
Source: Waring and Schlesinger (1985).
-------
Oi
^
00
Cytological and
Biochemical Changes
Enzyme activity
Membrane permeability
Organelle integrity
Osmotic potential
Physiological
Function
Photosynthesis
Transpiration
Respiration
Stomatal function
Resource allocation
Growth
Defense
Reproduction
Root uptake
Tree
Growth
Amount
Timing
Quality
Distribution
Resilience
Forest
Productivity
Growth
Competition
Succession
Mortality
Reproduction
Figure 5-35. Organizational levels at which air pollutants have been shown to affect the growth-related process of forest trees.
Source: McLaughlin (1994).
-------
Table 5-36. Interaction of Air Pollution and Temperate Forest
Ecosystems Under Conditions of Intermediate Air Contaminant Load
Forest Soil and Vegetation:
Activity and Response
Ecosystem Consequence
and Impact
1. Forest tree reproduction, alteration, or inhibition
2. Forest nutrient cycling, alteration
a. Reduced litter decomposition
b. Increased plant and soil leaching and soil
weathering
c. Disturbance of microbial symbioses
3. Forest metabolism
a. Decreased photosynthesis
b. Increased respiration
c. Altered carbon allocation
4. Forest stress, alteration
a. Phytophagous insects, increased
or decreased activity
b. Microbial pathogens, increased
or decreased activity
c. Foliar damage increased by direct
air pollution influence
1. Altered species composition
2. Reduced growth, less biomass
3. Reduced growth, less biomass
4. Altered ecosystem stress:
increased or decreased
insect infestations;
increased or decreased
disease epidemics;
reduced growth, less
biomass, altered species
composition
Source: Smith (1990).
and structural complexity, biodiversity, environmental modification, and nutrient control are
reduced (Bormann, 1985). With maturity, energy utilization in ecosystems shifts from
production to maintenance (Odum, 1993) (see Figure 5-34). When catastrophic disturbances
or injury, whether from natural (e.g., fire, flood, windstorm) or anthropogenic stresses (e.g.,
O3), alter the species composition (biodiversity) of a forest sufficiently to disrupt food chains
and to modify rates of energy flow and nutrient cycling, succession reverts to an earlier, less
complex stage. The effects of stresses on ecosystems, unless the effects are catastrophic
disturbances, are frequently difficult to determine (Kozlowski, 1985; Garner et al., 1989). In
a mature forest, a mild disturbance becomes part of the oscillating steady state of the forest
community or ecosystem. Responses to catastrophic disturbances, however, as a rule, are
readily observable and measurable (Garner, 1994). How changes in plant processes attributed
to O3 exposure affect forest ecosystems is discussed in the following text.
5.7.4.2 Forest Ecosystems
The primary responses of a forest ecosystem to sustained exposure of O3 are
reduced growth and biomass production (Table 5-36; Smith, 1990). Exposure to O3 inhibits
photosynthesis and decreases carbohydrate production and allocation, and, as has been
5-219
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discussed previously, decreased allocation to the roots interferes with mycorrhizae formation
and nutrient uptake (Figure 5-33). The resulting loss in vigor affects the ability of trees to
compete for resources and makes them more susceptible to a variety of stresses (Table 5-36;
see also Sections 5.3, 5.6.4.2, 5.6.4.3, and 5.7.3.1). Responses of seedlings under
experimental conditions indicate that reductions in growth occur at O3 concentrations of
0.06 ppm or greater (Table 5-30). Cregg et al. (1989) state that information on seedling
response must be used with caution. The environments in which seedlings and trees grow are
substantially different due to differences in rooting depth and canopy structure. Trees have
the potential to significantly alter their environments through shading, whereas seedlings do
not. In the San Bernardino Forest, mortality of canopy trees leads to replacement by trees
(white fir, incense cedar, sugar pine, and black oak) more tolerant to O3 and reduced
ecosystem structure. Reduction in structure altered nutrient cycling and energy flow and
affected the functioning of other ecosystem components (see Section 5.7.3.1). Ozone
concentrations capable of causing injury to forest trees and affecting forest processes continue
to occur both in the West and the East. Although reports have described the presence of
sensitive species in other U.S. forests; only the San Bernardino Forest has been severely
impacted by exposure to O3. Why this is the case is impossible to answer definitively
because of the absence of data. Evidence obtained from many studies of a variety of
ecosystems over the years indicates that ecosystems, in response to pollution or other
disturbances, follow definite patterns that are similar even in different ecosystems (Woodwell,
1970). It is possible, therefore, to predict broadly the basic biotic responses to the
disturbance of an ecosystem. These responses are reduction in standing crop (trees),
inhibition of growth or reduction in productivity, differential kill (removal of sensitive
organisms at the species and subspecies level), food chain disruption, successional setback,
and changes in nutrient cycling (U.S. Environmental Protection Agency, 1978).
The effects of the stresses associated with O3 exposure that have developed over
the years in the San Bernardino Forest ecosystem are similar to those listed in the previous
paragraph.
The extent of injury that an ecosystem will experience from O3 exposure is
determined by the severity and extent of individual response. Leaf injury, as has been stated
previously, is usually the first visible indication of O3 exposure. Structural effects develop
when physiological processes within individual plants are disrupted severely (see Table 5-37
and Figure 5-35). With ecosystem responses such as those seen in the San Bernardino Forest,
four levels of biological organization beginning with the individual organism are altered (see
Table 5-37; Sigal and Suter, 1987). Taylor and Norby (1985) discuss the possible effects on
ecosystems at the individual population and community levels. Alteration of functional
properties (ecosystems functions) results in structural dysfunction. Stresses, whose primary
effects occur at the molecular or cellular physiology level in the individual, must be scaled
progressively up through more integrative levels of organ physiology (e.g., leaf, branch, root)
to whole plant physiology, stand dynamics, and then to the landscape level to produce
ecosystem effects (Figure 5-36; Table 5-37). Particularly, this is true if the stress is of
low-level because only a small fraction of stresses at the molecular and cellular level become
disturbances at the tree, stand, or landscape level. The processes of energy flow and nutrient
cycling must be altered if ecosystems are to be affected. Insect defoliation, for example, may
reduce severely the growth of one or several branches, whereas the growth of the tree appears
not to be affected (Hinckley et al., 1992).
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Table 5-37. Properties of Ecological Systems Susceptible
to Ozone at Four Levels of Biological Organization
Level of Organization
Properties
Structural Properties
Functional Properties
Organism
Population
Community
Ecosystem
Leaf area and distribution
Biomass and allometry
Age and size structure
Population density
Genetic composition
Spatial distribution
Dispersion (spatial pattern)
Species composition
(diversity)
Trophic levels and food
webs
Physical structure (leaf-area
index)
Biomass
Element pools
Soil properties
Photosynthesis, respiration
Nutrient uptake and release
Carbon allocation
Natality (reproduction,
mortality)
Competition
Productivity
Redundancy and resilience
Succession (the integration
of all species processes
such as competition and
predation)
Ecosystem productivity
Nutrient cycling
Hydrologic cycling
Energy flow
Source: Adapted from Sigal and Suter (1987).
Variability and compensation are two properties important in determining the effect
a stress at one hierarchial level will have on a higher level of organization (see Sections 5.3
and 5.4). Variability in individual response to stress can be the result of each individual
being genetically different (See Section 5.4). Individual trees do not respond equally to
O3 exposure. Ponderosa, Jeffrey, and eastern white pine all have been observed to have
sensitive, intermediate, and tolerant varieties based on the degree of response. Variability in
exposure-response also can be influenced by the movement of O3 from the leaf surface
through the stomata to the metabolic site of action in the leaf interior (Taylor and Hanson,
1992). The stomatal conductance also influences this action.
Variation in age and stage of growth of the organism also can determine response
to O3 exposure (see Section 5.3). Variability in response between seedlings, saplings, and
canopy black cherry trees at a site in north-central Pennsylvania was observed by
Fredericksen et al. (1994). Physiological, phenological, and morphological differences among
seedlings, saplings, and canopy trees were associated with altered O3 uptake and differential
response. Leaves at different crown positions of larger trees exhibited differences in leaf
physiology and O3 uptake. Seedling uptake of O3 and apparent sensitivity per unit leaf area
was greater, based on foliar injury symptoms; however, the relative
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\l Reactlo
Level ofs
Organization
Leaf
(cm2)
Branch
(cm2)
Tree
(m2)
Stand
(ha)
nTlme
Minute
•—
Day
•-^
Year
— E*
— ^>
^ — •
& !
JA »
^S |
I^j
^
Decade
2
3
-4
+-5
^8
ta
v^
V
—
Century
10
11
12
13
L
^ 11
~ ' '
16
Injury Symptom
Needle necrosis
and abscission
Branch length,
bifurcation ratio,
and ring-width
growth altered
Reduction in
diameter and death
of tree
Decreases in
stand productivity,
increases in mortality
and alterations in
regeneration patterns
Key Changes in Processes
Reduced carbon assimilation
because of reduced radiation
Reduced carbon available for foliage
replacement and branch growth/
export Synergistic interaction
between mistletoe and tephra
deposition
Reduced carbon available for
height, crown, and stem growth
Influence of crown class on initial
impact and subsequent recovery
Interaction between stand
composition and recovery
For a given level, the dot associated with a line begins with a process (e.g., photosynthesis for #1 under leaf) and
ends with the associated structure (e.g., the needle).
Evaluating
Impacts Within a Level of Organization
Leaf Level Carbon exchange- 1
Carbon pools-2
Needle number and size-3
Needle retention/abscission-4
Branch Level Carbon allocation-5
Branch growth-6
Branch morphology-7
Branch vigor-8
Branch retention-9
Tree Level Height and diameter growth-1 0
Crown shape and size-1 1
Tree vigor-1 2
Mortality-13
Stand Level Productivity- 14
Mortality-15
Species composltlon-16
Evaluating Interactions Between Different Levels of Organization
The diagonal arrow indicates the interaction between any two levels of organization.
The types of interaction are due to the properties of variability and compensation.
A - Refers to the interaction between the leaf and branch levels, where, for example,
variability at the branch level determines leaf quantity, and compensation at the leaf
level in photosynthesis may compensate for the reduction in foliage amount.
B - Refers to the interaction between the branch and the tree, where variability in branches
determines Initial Interception, branch vigor, and branch location In the crown;
compensation may be related to increased radiation reaching lower branches.
C - Refers to the interaction between the tree and the stand. Both genetic and
environmental variability, inter- and intraspecific compensations, and tree historical
and competitive synergisms are involved.
Figure 5-36. Effects of environmental stress on forest trees are presented on a hierarchial
scale for the leaf, branch, tree, and stand levels of organization. The
evaluation of impacts within a level of organization are indicated by
horizontal arrows. The evaluation of interactions between different levels of
organization are indicated by diagonal arrows.
Source: Hinckley et al. (1992).
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exposure of seedlings to O3 was reduced by an indeterminate growth habit because the
majority of their leaves were produced after shoot growth had ceased for sapling and canopy
trees. Therefore, their relative uptake was reduced on a whole-crown basis over the growing
season and cumulative exposure. Lower crown leaves of saplings and canopy trees appear to
be more sensitive to O3 than upper crown leaves, despite lower uptake, which possibly is due
to low availability of photosynthate for anti-oxidant defense and repair of injured leaf cell
membranes. Shade leaf morphological characteristics also may play a significant role. The
above study describes the interaction of multiple factors that determine O3 uptake and
potential response and illustrates the complexity involved in scaling responses from controlled
studies of open-grown seedlings to larger forest trees (Fredericksen et al., 1994).
Compensation in response to stress involves the capacity of the individual to adapt
to the stress. Some plants compensate physiologically by detoxifying the O3 entering the
leaves. Other plants compensate by altering the root-shoot ratio. They reallocate
carbohydrates to the source of injury in the leaves instead of to the roots, as do uninjured
trees (see Figure 5-33 and Section 5.1.3). At the stand level, the slower growth of some trees
may be compensated for by the relatively faster growth of others that are experiencing
reduced competition so that the overall growth of the stand is not affected (Hinckley et al.,
1992). These properties, when taken together, will determine the extent and the rate at which
stress at one hierarchical level will impact the next highest level. A framework of
hierarchical scales (Figure 5-36) was developed by Hinckley et al. (1992) to provide a means
by which the effects of the eruption of Mount St. Helens on forest trees could be followed
and understood. This framework is also applicable for use when considering O3 effects and
can be used to explain the difference between the response of the San Bernardino Forest
ecosystem and the forests in the eastern United States. As pointed out above, variability and
compensation determine the severity of the response of the individual.
Variability and compensation also occur at the population level, all populations do
not respond equally (Taylor and Pitelka, 1992). Plant populations can respond in four
different ways: (1) no response, the individuals are resistant to the stress; (2) mortality of all
individuals and local extinction of the extremely sensitive population (the most severe
response); (3) physiological accommodation, growth, and reproductive success of individuals
are unaffected because the stress is accommodated physiologically; and (4) differential
response, members of the population respond differentially, with some individuals exhibiting
better growth and reproductive success due to genetically determined traits (Taylor and
Pitelka, 1992). Differential response results in the progressive elimination over several
generations of the sensitive individuals and a shift in the genetic structure of the population
toward greater resistance (microevolution). Physiological accommodation or microevolution,
with only the latter affecting biodiversity, are the most likely responses for exposure to
chronic stress (i.e., stresses that are of intermediate-to-low intensity and of prolonged
duration). The primary effect of O3 on the more susceptible members of the plant community
is that the plants can no longer compete effectively for essential nutrients, water, light, and
space, hence are eliminated. The extent of change that can occur in a community depends on
the condition and type of community, as well as the exposure (Garner, 1994). Forest stands
differ greatly in age, species composition, stability, and capacity to recover from disturbance.
For this reason, data dealing with the responses of one forest type may not be applicable to
another forest type (Kozlowski, 1980).
In the eastern United States, ecosystem reduction in structure and diversity has
never reached the proportions seen in the San Bernardino Mountains. Visible tree decline has
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been observed only in the southern Appalachian Mountains, particularly Mt. Mitchell, and on
Camel's Hump, VT. The actual cause of decline and mortality of trees in these areas is a
matter of question.
Among the hypotheses suggested for the absence of major changes in the eastern
forests is a difference in the O3 exposures experienced by the eastern forests when compared
with the San Bernardino Forest, a region noted for high O3 levels. Lefohn et al. (1994)
characterized and compared O3 concentrations measured from 1988 to 1992 at Bearden Knob
and Parsons, located in a remote forested region of north-central West Virginia, with other
sites in the region. It was observed that 1988, when compared with 1992, was a year with
very high O3 exposures. At almost all sites in 1992, few hourly concentrations were
>0.10 ppm, whereas in 1988, several sites had 100 or more average concentrations
>0.10 ppm. These concentrations were found at both high- and low-elevation sites. In 1992,
Bearden Knob, a high-elevation site, experienced a flat diurnal pattern, whereas Parsons, the
nearby low-elevation site, experienced a varying diurnal pattern, an indication that O3 was
being scavenged. Horton Station, a high-elevation site in southwestern Virginia, in 1992,
experienced 25 episodes with hourly average concentrations near 0.05 ppm for 8 h or longer,
18 episodes with hourly average concentrations near 0.06 ppm, and three episodes with
concentrations at or near 0.07 ppm. For the same period, Bearden Knob experienced 31
episodes of 8 h or longer for average hourly concentrations near 0.05 ppm, 13 episodes at or
near 0.06 ppm, and 3 episodes at or near 0.07 ppm.
Maximum hourly average concentrations from April to October during 1988 were
0.145 ppm at or near Horton Station, compared with the 0.29 ppm received by the San
Bernardino National Forest. Horton Station was exposed to 2,758 hourly concentrations
between 0.05 ppm and 0.087 ppm, whereas the San Bernardino site received 2,027 h. The
latter site had more concentrations above 0.10 ppm; therefore, it received fewer exposures
between 0.05 and 0.087 ppm. It was suggested that the extreme growth reduction and injury
that has been observed in the San Bernardino area over the years, when compared with the
absence of such injury in the Horton Station area, could be attributed solely to the higher
number of hourly average concentrations exceeding 0.10 ppm at the former site (Lefohn et al.,
1994). Factors not considered were differences in sensitivity, stand composition, and the
ability to compensate for the stress, as well as site variables.
These factors definitely apply in the Appalachian Mountains and, to a degree, in
the Sierra Nevada, where the sensitive individuals and composition of the forests vary from
the San Bernardino Mountains. The forests of the Appalachian Mountains are known to be
more biologically diverse than western forests. Only in the San Bernardino Forest did the
removal of sensitive trees reach the population level. Population dynamics impact the
ecosystem functions of energy flow and nutrient cycling.
Eastern white pine responses to O3 exposures were classified into three sensitivity
levels ([1] sensitive, [2] intermediate, and [3] tolerant) by both McLaughlin et al. (1982) and
Benoit et al. (1982). Black cherry also has been observed to have three sensitivity levels.
None of these trees can be termed canopy dominants. In addition to conifers, the forest
canopy includes varieties of oaks that are not as sensitive to O3 exposures. Species removal,
therefore, has not affected the eastern forests as did removal of ponderosa and Jeffrey pine
from the San Bernardino Forest. Taylor and Norby (1985) have pointed out that the nature of
community dynamics, particularly in mixed species, and stands with trees of uneven age play
important roles in forest response. Shifts in species composition are more likely responses to
stresses such as O3 than to community degradation. The removal of the codominant
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American chestnut (Castanea dentata) in the first half of this century caused no major change
in the tree species relationships in the Appalachian forests. The effects of O3 exposure also
will probably not cause major change.
The previous O3 document (U.S. Environmental Protection Agency, 1986)
concluded that none of the tree species shown to be injured by O3 play a dominant role in the
Blue Ridge Mountain ecosystem. Therefore, the removal of any of these species probably
would not have the impact that the decline and death of ponderosa and Jeffrey pine have had
on the San Bernardino Forest ecosystem. This same conclusion applies today.
5.7.5 Summary
Ecosystems are composed of populations of "self-supporting" and "self-
maintaining" living plants, animals, and microorganisms (producers, consumers, and
decomposers) interacting with one another and with the nonliving chemical and physical
environment within which they exist (Odum, 1989; U.S. Environmental Protection Agency,
1993). Mature ecosystems are seldom stable. Structurally complex communities, they are
held in an oscillating steady state by the operation of a particular combination of biotic and
abiotic factors, and they must respond and adapt continually to changing environments
(Kozlowski, 1985).
Ecosystem response to stress begins with individuals (Figures 5-34, 5-35, and
5-36). Growth of trees and other vegetation requires the expenditure of energy in the form of
carbon compounds. Carbon compounds are accumulated, stored, and used by plants to build
their structure and maintain their physiological processes (Figure 5-34). Carbon dioxide
absorbed from the atmosphere, combined with water from the soil in plant leaves during
photosynthesis, provides the energy in the form of carbon compounds (sugars) utilized by
trees for growth and maintenance (Figure 5-34; Waring and Schlesinger, 1985). Patterns of
carbon allocation to roots, stems, and leaves directly influence growth rate. The strategy for
carbon allocation may change during the life of a plant, as well as with different
environmental conditions (Figure 5-33; Winner and Atkinson, 1986). Trees acclimate to
changing environmental stresses through both short-term and long-term physiological
responses and structural and morphological modifications (Dickson and Isebrands, 1991).
Even small changes in photosynthesis or carbon allocation can alter profoundly the structure
of a forest (Waring and Schlesinger, 1985). Impairment of the processes of photosynthesis
shifts carbon allocation from growth and maintenance to repair, increases respiration, and can
result in resource imbalances. The significant changes observed in the San Bernardino Forest
ecosystem were a possible outcome of the combined influences of O3 on carbon, water, and
nutrient allocation (McLaughlin, 1994).
Mycorrhizae are an extremely important, but unheralded, component of all
ecosystems. The majority of plants depend on them for the uptake of mineral nutrients from
the soil. Their absence from the roots of plants has been shown to have a detrimental impact
on plant growth. Decreased carbohydrate production and reduced allocation to the roots due
to O3 exposure affect the formation of mycorrhizae and impact plant growth. Exposure to O3,
therefore, affects plant growth both above and below ground.
Intense competition among plants for light, water, nutrients, and space, along with
recurrent natural climatic (temperature) and biological (herbivory, disease, pathogens) stresses,
can alter the species composition of communities by eliminating those individuals sensitive to
specific stresses, which is a common response in communities under stress (Woodwell, 1970;
5-225
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Guderian, 1985). Those organisms able to cope with stresses survive and reproduce. The
effects of stresses on ecosystems, unless the effects are catastrophic disturbances, are
frequently difficult to determine (Kozlowski, 1985; Garner et al., 1989). In a mature forest, a
mild disturbance becomes part of the oscillating steady state of the forest community or
ecosystem. Responses to catastrophic disturbances, however, as a rule, are readily observable
and measurable and return ecosystems to a less complex stage (Garner, 1994).
Ecosystem responses are hierarchical. The extent of injury that an ecosystem can
experience from exposure to O3 will be determined by the severity of the effect on individual
members of a population. Stresses, whose primary effects occur at the molecular or cellular
physiology level of an individual, must be propagated progressively through the more
integrative levels, from the leaf, branch, or root, to whole plant physiology, to stand
dynamics, and, ultimately, to the ecosystem (see Figures 5-35 and 5-36). Only a small
fraction of the stresses at the molecular, cellular, or leaf level leads to disturbances at the tree,
stand, or ecosystem level. Variability in response to stress at both the individual and the
population level and the ability to compensate for the stress determine the hierarchical extent
of the response.
The mixed-conifer forest ecosystem in the San Bernardino Mountains of Southern
California is one of the most thoroughly studied ecosystems in the United States. The
changes observed in the mixed-conifer forest ecosystem exemplify those expected in a
severely disturbed ecosystem. Chronic O3 exposures over a period of 50 or more years
resulted in major changes in the San Bernardino National Forest ecosystem by influencing
forest processes. The primary effect was on the more susceptible members of the forest
community, individuals of ponderosa and Jeffrey pine, in that they were no longer able to
produce the energy required to compete effectively for essential nutrients, water, light, and
space. As a consequence of altered competitive conditions in the community, there was a
decline in the sensitive species, permitting the enhanced growth of more tolerant species
(Miller et al., 1982; U.S. Environmental Protection Agency, 1978, 1986). Changes in the
function of other ecosystems components directly or indirectly affected the processes of
carbon (energy) flow, mineral-nutrient cycling, and water movement and changed community
patterns. Biotic interactions associated with predators, pathogens, and symbionts were
influenced by changes in available energy. The results of the studies of the San Bernardino
Forest ecosystem were reported in both the 1978 and 1986 criteria documents (U.S
Environmental Protection Agency, 1978, 1986). The more recent data from the San
Bernardino Forest and from other ecosystems in California indicate that O3 concentrations
capable of injuring forest vegetation continue to occur, but at lower concentrations and with
shorter durations. Therefore, vegetational injury has not been as great.
There is some indication from new data that O3 may not have been the only stress
encountered by the San Bernardino Forest ecosystem. Nitrate deposition gradients similar to
those measured for O3 suggest that possible soil-mediated exposures to nitrate could have
been and continue to be combined with the foliage-mediated O3 exposures as an additional
stress. Research in this area is continuing.
Ozone concentrations capable of causing injury to trees in the Sierra Nevada
Mountains have been occurring for many years. Injury to sensitive trees, however, has never
reached the same proportions as in the San Bernardino Forest. Differences in forest stand
composition (fewer conifers, more hardwoods), ability to compensate for stress, and site
dynamics undoubtedly play roles in the forest response.
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The forests of the Appalachian Mountains have been episodically exposed to
O3 concentrations capable of causing vegetational injury for many years. Visible injury to
foliage of eastern white pine and reduction in growth have been associated with the exposures
to concentrations >0.06 ppm lasting for several days. Black cherry also has been shown to be
sensitive to O3 exposures. Surveys of various regions, including the Smoky Mountain and
Shenandoah National Parks, indicate that visible injury to a variety of different types of
vegetation is continuing to occur. Neither eastern white pine nor black cherry are dominant
canopy trees. Removal of sensitive individuals and the absence of changes in the population
of these species have not resulted in any visible change in the forest ecosystems along the
Appalachian Mountains, possibly because no changes in the ecosystem functions of energy
flow or nutrient cycling have occurred. Decline and dieback of trees on Mt. Mitchell and
Camel's Hump cannot be related solely to O3 injury. Ongoing research is attempting to better
understand the effects of O3 exposure on individual plants and the effect, if any, on the
ecosystems to which the plants belong.
5.8 Effects of Ozone on Agriculture, Forestry, and
Ecosystems: Economics
5.8.1 Introduction
Evidence from the plant science literature cited in the 1986 O3 Criteria Document
(U.S. Environmental Protection Agency, 1986) and in the present document is unambiguous
with respect to the adverse effects of tropospheric O3 on some types of vegetation. For
example, findings from EPA's multiyear NCLAN program provide rigorous corroboration of
at least a decade of previous research that showed that O3 at ambient levels caused physical
damage to important species. Specifically, NCLAN established that ambient O3 levels
resulted in statistically significant reductions in yields for these crops. Literature reviewed in
Section 5.6 of this document assesses the state of natural science findings regarding O3 effects
on crops, forests, and other types of vegetation in more detail.
Information on the benefits and costs of alternative policy options or states of the
world (such as changes in air pollution) is of use to decision makers in a variety of settings.
For example, economic information provides one means by which to choose from alternative
policies or public investments. The role of cost-benefit analysis in federal rule making or
standard setting was enhanced by President Reagan's Executive Order 12291 (February 19,
1981), which required that such calculations be performed on any rule or regulation
promulgated by the federal government. President Clinton's Executive Order 12886 (October
4, 1993) reconfirmed the importance of economic information in the federal regulatory
process. These executive orders provided the stimulus for a large increase in the use of
economic analysis in evaluating federal actions, including environmental policies. Although
the Clean Air Act and its amendments do not allow the use of cost-benefit analysis in the
standard-setting process for primary (human health) effects, economic information has been
introduced into the discussion of secondary or welfare effects. A number of economic studies
addressing vegetation and other welfare effects have been performed in the last decade.
Assessments of the economic consequences of O3 on vegetation reflect the state of
natural science information on each vegetation category. The natural science evidence
concerning effects of O3 on individual tree species or plant communities is less secure than
for agricultural crops (see Section 5.6). As a result, most economic assessments focus on
5-227
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agricultural crops. The economics literature on effects of O3 and other air pollutants on forest
productivity is very sparse; the few assessments are confined to evaluations of assumed or
hypothetical changes in output (e.g., board feet of lumber). The economic effects of O3 on
plant communities or ecosystems have not been measured in any systematic fashion.
This section reviews economic assessments across these vegetation categories. The
discussion of economic valuation of ecosystem effects is limited to conceptual and
methodological issues in performing such assessments, given the absence of empirical
analyses in this category.
5.8.2 Agriculture
In view of the importance of U.S. agriculture to both domestic and world
consumption of food and fiber, reductions in crop yields could adversely affect human
welfare. The plausibility of this premise resulted in numerous attempts to assess, in monetary
terms, the losses from ambient O3 or the benefits of O3 control to agriculture. Fourteen
assessments of the economic effects of O3 on agriculture were reviewed in the 1986 document
(U.S. Environmental Protection Agency, 1986). Since the preparation of the 1986 document,
there have been at least nine other studies published in the peer review literature that provide
estimates of the economic consequences of O3 on agriculture.
The 1986 document highlighted key issues in judging the validity of economic
assessments that are applicable to post-1986 studies (i.e., how well the biological, aerometric,
and economic inputs used in the assessment conform to specific criteria). First, the evidence
on crop response to O3 should reflect how crop yields will respond under actual field
conditions. Second, the air quality data used to frame current or hypothetical effects of O3 on
crops should represent actual exposures sustained by crops at individual sites or production
areas. Finally, the assessment methodology into which such data are entered should capture
the economic behavior of producers and consumers as they adjust to changes in crop yields
and prices that may accompany changes in O3 air quality; should reflect accurately
institutional considerations, such as regulatory programs and income support policies (e.g.,
provisions of federal "Farm Bill" legislation), that may result in market distortions; and use
measures of well-being that are consistent with principles of welfare economics.
5.8.2.1 Review of Key Studies from the 1986 Document
Assessments of O3 damages to agricultural crops reported in the 1986 document
displayed a range of procedures for calculating economic losses, from simple monetary
calculation procedures to more complex assessment methodologies that conform to some or
all of the economic criteria above. As noted in the 1986 document, the simple procedures
calculate monetary effects by multiplying predicted changes in yield or production resulting
from exposure to O3 by an assumed constant crop price. By failing to recognize possible
crop price changes arising from yield changes and not accounting for potential producer
responses, such assessments are flawed, except for highly restricted situations such as
localized pollutant events. Conversely, some assessments provide estimates of the economic
consequences of O3 and other air pollutants that reflect producer-consumer decision-making
processes, associated market adjustments, and some measure of distributional consequences
between affected parties. The distinctions between studies based on naive or simple models
and those based on correct procedures is important at the regional and national levels, because
the simple procedures may be biased and lead to potentially incorrect policy decisions.
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Most (9 of 14) of the economic assessments reviewed in the 1986 document
focused on O3 effects in specific regions, primarily California and the Corn Belt (Illinois,
Indiana, Iowa, Ohio, and Missouri). There have been a number of additional regional
assessments since the 1986 document; most are non-peer-reviewed reports arising from
consulting or contract research. This regional emphasis in the earlier literature may be
attributed to the relative abundance of data on crop response and air quality for selected
regions, as well as the importance of some agricultural regions, such as California, in the
national agricultural economy. Most of the recent state or regional assessments are
commissioned by state public utility commissioners or similar regulatory agencies and use
variants of the simple "price times yield" approach, where yields are calculated from response
functions arising from the NCLAN data. Although perhaps of use to public utility
commissioners concerned with effects from single power plants or other localized sources,
these studies generally contribute little to the assessment of pollution effects at the national
level. (Most local or regional studies abstract from physical and economic interdependences
between regions, which limits their utility in evaluating secondary National Ambient Air
Quality Standards [NAAQS].)
National studies that account for economic linkages between groups and regions
can overcome some limitations of regional analyses. A proper accounting of these linkages,
however, requires additional data and more complex models and frequently poses more
difficult analytical problems. Thus, detailed national assessments tend to be more costly to
perform. As a result, there are fewer assessments of pollution effects at the national level
than at the regional level.
Two national studies reported in the 1986 document were judged to be "adequate"
in terms of the three critical areas of data inputs. Together, they provided a reasonably
comprehensive estimate of the economic consequences of changes in ambient air O3 levels on
agriculture. Because of their central role in the 1986 document, these two studies are
reported in Table 5-38 and are reviewed briefly below.
In the first of these studies, Kopp et al. (1985 [cited as 1984 in the earlier
document but subsequently published as a journal article in 1985]) measured the national
economic effects of changes in ambient O3 levels on the production of corn, soybeans, cotton,
wheat, and peanuts. In addition to accounting for price effects on producers and consumers,
the assessment methodology used is notable in that it placed emphasis on developing
producer-level responses to O3-induced yield changes (from NCLAN data available at the
time) in 200 production regions. The results of the Kopp et al. study indicated that a
reduction in O3 from 1978 regional ambient levels to a seasonal 7-h average of approximately
0.04 ppm would result in a $1.2 billion net benefit in 1978 dollars. Conversely, an increase
in O3 to an assumed ambient concentration of 0.08 ppm (seasonal 7-h average) across all
regions produced a net loss of approximately $3.0 billion.
The second study, by Adams et al. (1986a), was a component of the NCLAN
program. The results were derived from an economic model of the U.S. agricultural sector
that includes individual farm models for 63 production regions integrated with national supply
and demand relationships for a range of crop and livestock activities. Using NCLAN data,
the analysis examined yield changes for six major crops (corn, soybeans, wheat, cotton,
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Table 5-38. Recent Studies of the Economic Effects of Ozone and Other Pollutants on Agriculture3
Model Features
Study Region
Garcia et al. Illinois
(1986)
Adams et al. U.S.
(1986a)d
Kopp et al. U.S.
(1985)d
Shortle et al. U.S.
(1988)
Adams et al. U.S.
(1986b)
Kopp and U.S.
Krupnick (1987)
01
^j Adams et al. U.S.
O (1989)
Adams and Rowe U.S.
(1990)
Pollutant and Concentration
Ozone, 10% increase from
46.5 ppbb
Ozone, 25% reduction from 1980
level for each state"
Ozone, universal reduction from
53 to 40 ppbb
Ozone, universal reduction from
53 to 49 ppb"
Acid deposition, 50% reduction in
wet acidic deposition
Ozone, 10% reduction from annual
levels (1986 to 1990) for rural
areas. Includes adjustments for
1985 Farm Bill.
Ozone, seasonal standard of 50 ppb
with 95% compliance0; includes
adjustments for 1985 Farm Bill.
Increased UV-B radiation and
associated increase of tropospheric
O3 (of 16%)
Price Output
Changes Substitutions
No Yes
Yes Yes
Yes Yes
Yes No
Yes Yes
Yes Yes
Yes Yes
Yes Yes
Input Quality
Substitutions Changes
Yes No
Yes No
Yes No
No Yes
Yes No
Yes No
Yes No
Yes No
Results (Annual 1980
Crops
Corn, soybeans
Corn, soybeans,
cotton, wheat,
sorghum, barley
Corn, soybean, wheat,
cotton, peanuts
Soybeans
Soybeans
Corn, cotton,
soybeans, wheat
Corn, soybeans,
cotton, wheat,
sorghum, rice, hay,
barley
Soybeans (for UV-B)
and all crops in
Adams et al. (1989)
for tropospheric O3
Consumer
Benefits
None
$1,160 x 106
Not reported
$880 x 106
$172 x 106
NA
$905 x 106
NA
U.S. Dollars)
Producer
Benefits
$226 x 106
$550 x 106
Not reported
$-90 x 106
$-30 x 106
NA
$769 x 106
NA
Total Benefits
(Costs)
$226 x 106
$1,700 x 106
$1,300 x 106
$790 x 106
$142 x 106
$2,500 x 106
(sum of
discounted
values at 5%,
1986 to 1990)
$1,674 x 106
-830 x 106
(for the
increase in
tropospheric
O3 only)
"All studies except Garcia et al. (1986) use NCLAN data to generate yield changes due to ozone; see Appendix A for abbreviations and acronyms.
'Seven-hour growing season geometric mean. Given a log-normal distribution of air pollution events, a 7-h seasonal ozone level of 40 ppb is approximately equal to an hourly standard of 80 ppb,
not to be exceeded more than once a year Heck et al. (1982).
'Seven and 12-h growing season geometric mean. Analysis includes both fixed roll-backs (e.g., 25%) and seasonal standards (with variable compliance rates).
dReported in the previous criteria document (U.S. Environmental Protection Agency, 1986).
-------
sorghum, and barley) that together account for over 75% of U.S. crop acreage. The estimated
annual benefits (in 1980 dollars) from O3 adjustments are substantial, but make up a relatively
small percentage of total agricultural output (about 4%). Specifically, in this analysis, a 25%
reduction in O3 from 1980 ambient levels resulted in benefits of $1.7 billion. A 25% increase
in O3 resulted in an annual loss (negative benefit) of $2.4 billion. When adjusted for
differences in years and crop coverages, these estimates are close to the Kopp and Krupnick
(1987) benefit estimates.
The Kopp et al. (1985) and Adams et al. (1986a) studies indicated that ambient
levels of O3 were imposing substantial economic costs on agriculture. However, both Kopp et
al. (1985) and Adams et al. (1986a) were judged to suffer from several sources of uncertainty.
These include the issue of exposure dynamics (7-h/day exposures from the NCLAN
experiments versus longer exposure periods, such as 12-h exposures) and the lack of
environmental interactions, particularly O3-moisture stress interactions, in many of the
response experiments. Also, the O3 data in both studies are based on a limited set of the
monitoring sites in the AIRS system, mainly sites in urban and suburban areas. Although the
spatial interpolation process used for obtaining O3 concentration data (Kriging) resulted in a
fairly close correspondence between predicted and actual O3 levels at selected validation
points, validation for rural sites was limited (Lefohn et al., 1987a). The economic models,
with their large number of variables and parameters and the underlying data used to derive
these values, also were noted as potential sources of uncertainty, including the effects on
economic estimates of market-distorting factors such as the federal farm programs. Concern
over farm programs stems from the evidence that reductions in O3 will increase yields and
hence total production of some crops. If the crop is covered (eligible for deficiency
payments) under the provisions of the farm program, then the total costs to the government
(of the farm program) may increase as a result of reduced O3 (McGartland, 1987). Thus, the
benefits of the O3 reduction may not be as great as estimated.
The 1986 criteria document concluded that these possible improvements in future
assessments were not likely to alter greatly the range of agricultural benefit estimates for
several reasons. First, the studies covered about 75 to 80% of U.S. agricultural crops
(by value). For inclusion of the other 20% to change the estimates significantly would
require that their sensitivities to O3 be much greater than for the crops included to date.
Second, model sensitivity analyses reported in past studies indicate that changes in plant
exposure-response relationships must be substantial to translate into major changes in
economic estimates. For example, it was believed unlikely that use of different exposure
measures or inclusion of interaction effects would alter greatly the magnitude of the economic
estimates. Third, it was believed that there were likely to be countervailing effects that would
mitigate against large swings in the estimates (e.g., longer exposure periods may predict
greater yield losses), but O3-water stress tends to dampen or reduce the yield estimates.
Finally, the document noted that potential improvements in economic estimates are
policy-relevant only to the extent that they alter the relationship between total benefits and
total costs of that policy. The possible exception to this generally optimistic assessment of
the robustness of the estimates was inclusion of market-distorting factors (i.e., farm
programs), an issue that is addressed in some of the post-1986 assessments reviewed below.
5.8.2.2 A Review of Post-1986 Assessments
The previous criteria document (U.S. Environmental Protection Agency, 1986)
concluded that the O3 assessments of economic benefits to agriculture by Kopp et al. (1985)
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and Adams et al. (1986a) provided the most defensible evidence in the literature at that time
of the general magnitude of such effects. These two studies, in combination with the
underlying NCLAN data on yield effects, were judged to be the most comprehensive
information available on which to evaluate the economic impact of O3 on crops.
Seven national assessments performed since the last criteria document are reported
in Table 5-38. Of these, all use defensible economic approaches to quantify dollar effects,
where "defensible" is measured in terms of conforming to the criteria cited earlier.
An evaluation of these studies in terms of the adequacy of critical plant science, aerometric,
and economic data is presented in the table, along with estimates of benefits or damages
associated with changes in O3.
The concluding statements in the 1986 document are a benchwork against which to
judge these seven national studies published since the last document. Most of the
contemporary studies build on either Kopp et al. (1985) or Adams et al. (1986a); indeed, the
motivation of some of the more recent studies is to test whether the problems noted above
(such as exclusion of farm programs) are sufficient to alter the original estimates in a
meaningful manner. A relevant question is whether these new studies provided any
"surprises" in terms of magnitude of economic effects. These studies are summarized in
Table 5-38.
In discussing these latest evaluations, there are several points that relate to the
comparability of the evaluations with those of Kopp et al. (1985) and Adams et al. (1986a).
First, all studies use NCLAN response data to generate yield effects (for inclusion in the
respective economic models). In most cases, data used in the post-1986 assessments reflect
improvements of earlier NCLAN data. Second, these studies may be characterized as second
generation assessments. They build on the first generation of studies reported in the 1986
document by refining selected aspects of those earlier studies, including interactions with
other stresses; use of aerometric data and assumptions that, in some cases, more closely
follow the seasonal and regional characteristics of O3 exposure (Adams et al., 1989); and
effects of O3 on quality of commodities (Shortle et al., 1988). Several of the studies use
updated versions of the economic models in Adams et al. (1986a) and Kopp et al. (1985).
In addition, some of the studies model the effects of government programs to judge the
potential consequences of such distortions on economic estimates (Kopp and Krupnick, 1987;
Adams et al., 1989). Third, there are differences in underlying aerometric assumptions; some
studies include both O3 and other environmental stresses (e.g., acid deposition, ultraviolet-B
[UV-B], radiation); others reflect O3 data for more recent time periods. Because ambient
O3 levels vary across years, the choice of year will influence the yield estimates and
ultimately the economic estimates.
Common themes or findings from these (and earlier) O3 and other air pollution
studies have been summarized in two recent synthesis papers (Adams and Crocker, 1989;
Segerson, 1991). The results of the post-1986 assessments in Table 5-38 and the recent
synthesis papers corroborate the general findings of the 1986 document. Specifically, the
agricultural effects of tropospheric O3 at ambient levels impose economic costs to society
(or conversely, that reductions in ambient O3 result in societal benefits). The magnitude of
the economic costs reported in the more recent studies is similar to the estimates in Kopp
et al. (1985) and Adams et al. (1986a). Such a similarity is not surprising, given the points
noted above concerning use of similar data and economic models.
One important recent finding pertains to farm programs. In each case, the
inclusion of farm programs in the economic models resulted in modest changes (reductions)
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in the economic benefits of O3 control (due to increased farm program costs). As Segerson
notes, however, it is not clear that these increased costs should be charged against the
potential benefits of an O3 regulatory standard but rather as an additional cost associated with
the inefficiencies of the federal farm program. Even with the inclusion of farm programs and
other elements, the general magnitude of further effects reported in the 1986 criteria
document are reduced only by approximately 20%.
In addition to including farm programs, there are a couple of other notable
additions to the assessment literature. One study (Adams et al., 1989) attempts to analyze
economic benefits under a regulatory alternative involving a seasonal (crop growing season)
O3 exposure index measured as a 12-h mean, instead of hourly levels or percent changes from
ambient reported in earlier studies. Specifically, a seasonal average of 50 ppb O3 (measured
as a 12-h seasonal average), with a 95% compliance level, is reported in Adams et al. (1989).
The result (of a $1.7-billion benefit) is similar to the assumed 25% reduction across all
regions reported by Adams et al. (1986a). At least one study also has combined
environmental stresses (e.g., O3, UV-B, radiation) in preforming economic assessments.
Adams and Rowe (1990), using the same model as Adams et al. (1986a, 1989), report that a
15% depletion of stratospheric O3 (which results in a 13% increase in tropospheric O3) caused
an economic loss of approximately $0.8 billion attributed to the tropospheric O3 increase.
5.8.2.3 Limitations and Future Research Issues
The recent literature (post-1986) on economic effects of O3 on agriculture supports
the general conclusions drawn in the 1986 document. That is, ambient levels of O3 are
imposing economic costs on producers and consumers. As in earlier economic assessments,
the validity of this finding is conditional on the quality of the supporting agronomic and
aerometric data. In addition, there are at least three issues that are not addressed in the extant
literature on the topic. First, the existing assessments do not consider the external costs of
changes in agricultural production arising from changes in O3 exposures (Sergerson, 1991).
These costs are important if changes in O3 result in changes in crop mixes or production
practices, which in turn result in changes in soil erosion, fertilizer and pesticide runoff, or
other agricultural externalities. For example, if reductions in O3 increase the relative
profitability of a crop that uses higher levels of chemical inputs, then some increase in
chemical effluent may result. Given that some assessments suggest that such changes in
crop mixes and production practices are likely to accompany O3 changes, these costs/benefits
need to be addressed.
A second issue not directly assessed in the current literature is the relationship
between climate change and tropospheric O3 effects. This relationship is important if global
warming is expected to increase tropospheric O3 levels. In addition, research indicates that
global climate change will lead to a relocation of crops (Adams et al., 1990d). This
relocation may change the vulnerability of crop species to O3, given the spatial distribution of
O3 across the United States (i.e., increased crop production in areas of relatively low ambient
O3, such as the Pacific Northwest, implies lower O3 damage).
A third issue involves the institutional setting in which agricultural production
occurs. Several recent studies have assessed O3 effects in the presence of federal farm
programs. However, the United States and most industrialized economies are moving away
from price supports, production quotas, and import restrictions, the traditional form of
government intervention in agriculture. At the same time that these market distortions are
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being removed, there is increasing government regulation of agricultural production practices
to reduce agricultural externalities. Future assessments of O3 effects may need to pay less
attention to farm program effects and instead include other institutional features of U.S.
agriculture.
5.8.3 Forests (Tree Species)
The plant science literature on O3 and other air pollutant effects on tree species is
evolving rapidly as a result of recent research initiatives by EPA and other agencies. The
long-term nature of air pollution effects on perennial species creates challenges to plant
scientists in sorting out the specific effects of individual stresses from among the many
potential explanatory factors, such as O3 (Skelly, 1989), and in measuring impacts of direct
economic value, such as reductions in board-feet of lumber produced per unit of time.
To date, most natural science literature on forest species reports O3 effects in terms
of foliar injury or similar measures (Taylor and Hanson, 1992; Davis and Skelly, 1992b;
Simini et al., 1992; Freer-Smith and Taylor, 1992). This emphasis on foliar effects (rather
than on marketable yield) is similar to the state of science for agricultural crops prior to 1975.
Such visible foliar effects information is of limited use in economic assessments. The
exception is in measuring the economic value of aesthetic changes in a forest stock (see
Crocker, 1985).
The lack of usable data concerning changes in marketed output, such as board-feet
of lumber (or even changes in growth rates), has limited the number of economic assessments
of O3 effects on forests. The few studies that attempt to measure economic losses arising
from O3 or other pollutants circumvent the lack of plant science data by assuming various
arbitrary reductions in forest species growth or harvest rates (Callaway et al., 1985; Haynes
and Adams, 1992; Adams, 1986; Crocker and Forster, 1985). These studies are summarized
in Table 5-39.
Although the economic estimates reported in Table 5-39 are comparable to those
reported for agricultural crops (e.g., $1.5 billion for eastern Canada, $1.7 billion for eastern
U.S. forests), the lack of defensible natural science data makes these studies suggestive, at
best, of possible economic consequences of forest (tree species) effects of O3 or other
environmental stresses. In addition, the economic methodology used in the assessments
varies, from simple price-times-quantity calculations (e.g., Crocker, 1980) to the use of large,
econometric-based representations of the U.S. timber market (Haynes and Adams, 1992).
With appropriate data, the Timber Assessment Market Model methodology laid out by Haynes
and Adams holds promise for assessing the economic consequences of O3 when requisite
natural science data become available.
In summary, the plant science literature shows that O3 adversely influences the
physiological performance of tree species; the limited economic literature also demonstrates
that changes in growth have economic consequences. However, the natural science and
economic literature on the topic is not yet mature enough to conclude unambiguously that
ambient O3 is imposing economic costs. The output from ongoing natural science research on
this topic will be important to the understanding of this potentially important class of effects.
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Study
Table 5-39. Studies of the Economic Effects of Ozone and
Other Pollutants on Forests
Pollutant/Coverage
Response and Air Quality
Data
Economic Model
Annual Damages
or Benefits of
Control
(billions of
dollars)
Callaway
et al.
(1985)
Crocker
(1980)
All pollutants. Forest
products (hardwood
and softwood) in the
eastern United States.
Acid deposition.
Forest products and
forest ecosystem
service flows for
eastern United States.
Assumes three arbitrary
growth reductions (10, 15,
and 20%) for hardwood
and softwood tree species.
Assumes a 5% reduction
in products due to acid
deposition: assumes a
pristine background pH of
approximately 5.2
Spatial equilibrium
models of softwood
and hardwood
stumpage and forest
products industries
in the United States.
Naive; assumed
changes in output
multiplied by
average value of
those goods or
services.
-270 to 563
damage in 1984
dollars for
assumed
reductions in
growth levels
-1,750 damage in
1978 dollars from
current levels of
acid deposition
Crocker Acid deposition.
and Forest products and
Forster forest ecosystem
(1985) services for eastern
Canada.
Assumes 5% reduction in
forest productivity for all
eastern Canadian forests
receiving >10 kg/ha/year
sulphate deposition.
Naive; assumed
changes in output
multiplied by
average value of
goods or services.
-1,500 damage in
1981 Canadian
dollars from
current levels of
acid deposition
Haynes Air pollutants,
and including acid
Adams precipitation. Losses
(1992) estimated for eastern
U.S softwoods.
None; paper demonstrates
a methodology for
assessing economic
effects of yield (growth
and inventory) reductions
due to any course.
Assumes losses from 6 to
21% for softwoods.
Econometric model
of U.S. timber sector
(Timber Assessment
Market Model).
-1,500 to -7,200
in 1986 dollars
5.8.4 Valuing Ecosystem Service Flows
5.8.4.1 Background
Over the last 30 years, economists have developed a variety of techniques for
assessing the value of nonmarket goods and services (recently surveyed by Braden and
Kolstad [1991] and Smith [1993]). "Nonmarket" refers to those goods and services not
priced and traded in markets. Although most applications are to natural resources and
environmental assets, the concepts extend to a range of goods not usually traded in markets.
Early applications focused primarily on commodities used directly by the consumer, such as
outdoor recreation. Within the last decade, attention has shifted to estimating nonuse
(or passive) values, such as what individuals are willing to pay to insure the existence of
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species or unique natural settings. The values elicited with these techniques are being used in
an increasing array of settings; however, their use is not without controversy.
Valuing complex ecological functions and the associated range of ecosystem
service flows is relatively uncharted territory and raises a number of conceptual and practical
issues. Some difficulties in valuing ecosystem services lie in the inability of ecologists to
unambiguously define and measure ecosystem performance and endpoints (see Section 5.7).
Other problems arise from the inability of economic science to measure adequately the
consequences of long-term and complex phenomenon. A related problem is the difference in
disciplinary perspectives between ecologists and economists. As a result, the current state-
of-the-art for valuing ecosystem service flows is inadequate for benefit-cost assessments used
in environmental regulatory processes. Improvement in valuation of ecosystem service flows
will require increased interdisciplinary cooperation and research between ecologists and
economists.
5.8.4.2 Nonmarket Valuation: Implications for Ecosystem Service Flows
Nonmarket valuation techniques consist of two basic types: (1) indirect
approaches rely on observed behavior to infer values, and (2) direct approaches use a variety
of survey-based techniques to directly elicit preferences for nonmarket goods and services.
Both sets of techniques share a common foundation in welfare economics, where measures of
willingness-to-pay (WTP) and willingness-to-accept (WTA) compensation are taken as the
basic data for individual benefits and costs.
Indirect approaches, sometimes referred to as revealed preference approaches, rely
on observed behavior to infer values. Examples include the travel-cost method, where the
relationship between visits to a recreational site and travel expenditures to reach the site (the
"price" of the site) is used to infer the value of the site, and the hedonic pricing method,
which attempts to infer the value of environmental attributes (e.g., clean air) by comparing
the value of a market good (such as residential housing) across neighborhoods with varying
levels of air quality. Travel-cost methods encompass a variety of models ranging from the
simple, single-site, travel-cost model, to regional and generalized models that incorporate
quality indices and account for substitution across sites. Hedonic pricing methods encompass
both land price (real estate) and wage models, which account for variations in prices or wages
due to environmental attributes (e.g., air and water quality, noise, aesthetics, environmental
hazards). The indirect approaches can measure only use values. Recent summaries of the
indirect approaches can be found in Braden and Kolstad (1991), Mendelsohn and Markstrom
(1988), Peterson et al. (1992), and Smith (1989, 1993).
Direct approaches to nonmarket valuation are survey-based techniques to directly
elicit preferences. The hypothetical nature of these experiments requires that markets (private
goods or political) be "constructed" to convey a set of changes to be valued. Although there
are a number of variants on these constructed markets, the most common is the contingent
valuation method (CVM).
Contingent valuation method can be viewed as a highly structured conversation
(Smith, 1993) that provides respondents with background information concerning the available
choices and specific increments or decrements in one or more environmental goods. Values
are elicited directly in the form of statements of maximum WTP or minimum WTA
compensation for the hypothetical changes in environmental goods. This method can be
applied to both use and nonuse values. The flexibility of constructing hypothetical markets
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accounts for much of the popularity of the technique. However, measurement of nonuse
value has been the subject of considerable debate (Federal Register, 1993; McFadden, 1994).
There are numerous methodological issues associated with application of CVM,
including the specification of the hypothetical environmental change, the elicitation format for
asking valuation questions, the appropriate welfare measure to be elicited (i.e., WTP or
WTA), and various types of response biases. Randall (1991) argues that, because of the
importance of nonuse values, CVM is likely to be the primary tool for measuring the
environmental benefits of biodiversity. Recent summaries of CVM can be found in Mitchell
and Carson (1989) and Carson (1991).
5.8.4.3 Challenges in Linking Valuation Techniques to Ecosystem Service Flows
The need for and interest in values of nonmarket goods and services have arisen
independently of concerns regarding ecosystem management and sustainability.
As environmental planning and management change to accommodate new issues, the need for
de novo valuation studies may increase (e.g., standard Resources Planning Act [1974] values
may be poor indicators of the economic benefits and costs produced by forest quality changes
under alternative air pollution regimes). The process of developing a tractable framework for
ecosystem management may require that valuation studies also co-evolve to aid critical
management decisions. For example, explicitly linking valuation techniques to physical
resource functions through bioeconomic models, remains an important research area (Adams
et al., 1990c). Linking valuation measures, from both market and nonmarket studies, to
indices of biological diversity is a fundamental challenge.
Ecologists have a traditional skepticism of attempts to assign monetary values to
ecosystem functioning, due both to the inherent limitations of benefit-cost analysis and to the
inadequacy of quantitative information about ecological and social factors (Westman, 1977;
Higgs, 1987). Attempts to monetize environmental benefits also are seen as having an
inherent "quantitative bias"; poorly understood ecological functions are neglected, whereas
traditional commodities (e.g., outdoor recreation) receive full attention (Foy, 1990).
A further question is whether total economic value really captures total value.
Economists make no claim that all values are being considered, only total economic value. A
related question is whether complex ecological functions can be accurately expressed in
monetary terms? Although the CVM has been applied to an impressive array of nonmarket
goods, precise valuation of ecosystem services with CVM will require a precisely defined
commodity. As researchers move from valuing single environmental endpoints or services to
addressing more complex "bundles" of endpoints and services, it will be become more
difficult to define the commodity in a CVM survey. This may prevent unambiguous
estimation of such values.
5.8.4.4 Valuing Ecosystem Service Flows: Summary
Economists have a variety of valuation techniques to help guide policy choices
concerning the effects of air pollution or other environmental change on environmental assets.
Applying these techniques to ecosystem management issues and valuing the full range of
ecosystem service flows is a new and, as yet, unresolved challenge. Many scholars, in both
ecology and economics, are inherently skeptical of any economic valuation of the full
complex of ecosystem services and, hence, turn toward other value indicators. The identified
research agenda for valuing ecosystem service flows crosses traditional disciplinary
boundaries (Russell, 1993). Interdisciplinary dialogue, cooperation, and the development of a
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shared language are necessary for successfully designing future valuation experiments
concerning ecosystem service flows and for determining the proper role for such valuation.
5.8.5 Summary
The 1986 criteria document (U.S. Environmental Protection Agency, 1986)
contained a review of assessments of the economic consequences of O3 on U.S. agriculture.
This section has evaluated selected post-1986 literature on the same topic. In addition, the
review has been expanded to include potential economic effects on forests and ecosystems.
Based on economic assessments and physical science data available at the time, the
previous criteria document concluded that O3 at ambient levels was imposing economic costs
on society. The review of more recent (post-1986) literature on agriculture corroborates that
earlier conclusion. Specifically, the recent literature, using the full set of NCLAN data and
addressing some deficiencies in the pre-1986 assessments, confirms the findings of substantial
economic losses from ambient O3 concentrations.
The exact level of these economic effects is a function of cropping patterns,
O3 concentrations (both ambient and episodic), and the spatial and temporal characteristics of
projected or observed O3 levels. The current economic assessments represent improvements
in the scientific understanding of O3 effects on agriculture. However, the assessments of
economic effects initially incident on the agricultural sector remain incomplete.
Only a few assessments consider the economic effects of O3 on forest trees and on
urban trees, shrubs, and ornamentals. These studies assess the economic effects of
hypothetical changes resulting from O3 or other stressors on forest productivity and aesthetics
and are best viewed as measures of the potential effect of O3 on these receptors.
Improvements linking O3 effects data to productivity and aesthetic effects will improve the
utility of such economic analyses.
The economic effects of O3 on ecosystems have not been addressed in the
published literature. There is, however, an emerging interest in applying economic concepts
and methods to the management of ecosystems. Economic techniques for valuing nonmarket
goods and services hold the potential to value some ecosystem goods and services.
Ecological research also is addressing the challenging conceptual and practical issues in
understanding and managing ecosystem functions. Increased dialogue between the disciplines
is needed before empirical analyses of the economic consequences of ecosystem management
are feasible.
In summary, the state of science concerning O3 economic effects on agricultural
crops is sufficient to conclude that O3 imposes costs on society. Conclusions regarding
effects on forests and ecosystems must await the acquisition of additional data and possible
refinements in ecological and economic methods.
5.9 Summary and Conclusions for Vegetation and
Ecosystem Effects
5.9.1 Introduction
Review of the post-1986 literature has not altered the conclusions of the 1986
O3 criteria document (U.S. Environmental Protection Agency, 1986) or its supplement (U.S.
Environmental Protection Agency, 1992). In the 1986 criteria document, several general
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conclusions were drawn from various experimental approaches: (1) current ambient
O3 concentrations (>0.04 ppm) in many areas of the country were sufficient to impair growth
and yield of plants, (2) effects occur with only a few hourly occurrences above 0.08 ppm,
(3) data cited in the 1978 O3 criteria document (U.S. Environmental Protection Agency, 1978)
indicate growth and yield effects for some species when the mean O3 concentration exceeded
0.05 ppm for 4 to 6 h/day for at least 2 weeks, and (4) regression analyses of NCLAN data to
develop exposure-response functions for yield loss indicate that at least 50% of the crops
studied will exhibit a 10% yield loss at 7-h seasonal mean O3 concentrations of 0.05 ppm or
less. These conclusions remain valid today. The 1992 supplement reviewed the literature on
the appropriate exposure index for expressing O3 effects on vegetation, including evaluation
of the roles of exposure duration and peak concentrations and the 7- and 12-h mean
concentrations, and compared many possible exposure indices to summarize seasonal
exposures related to yield loss. It was concluded that, in light of research that indicated the
influential roles of episodic, peak concentrations and the duration of the exposure, the 7- or
12-h seasonal mean is not an appropriate index because it treats equally all concentrations and
fails to consider exposure duration. Instead, the supplement (U.S. Environmental Protection
Agency, 1992) recommended use of indices that cumulate all hourly concentrations during the
growing season and preferentially weight the higher concentrations. Since 1988, a few
experimental studies have addressed directly the roles of individual exposure components in
order to develop a more appropriate exposure index. Also, however, results from several
retrospective statistical analyses of NCLAN data have increased scientific confidence in the
use of the peak-weighted, cumulative indices.
The post-1986 literature includes additional analyses of the NCLAN database and
of several European crop-yield-loss studies that substantiate the O3 effects observed in this
country. Although there has been little increase in the information about the response of
mature trees individually or in stands, new studies of forest tree seedlings have substantiated
pre-1986 reports concerning the sensitivity of a number of species as seedlings. Seedling
growth response of several species is altered at the O3 concentrations (>0.08 ppm)
experienced for hours to days in many areas of the United States. Studies of the effects of O3
on mature trees in their natural habitats are limited. Literature on the roles played by various
biotic and abiotic environmental factors in plant response to O3 indicates the need for more
research concerning the response of plants in natural ecosystems, where the interaction of
species of various genotypes with a multitude of environmental influences dictates the
eventual response of the species or community in question.
The species is the level of biological complexity for which the understanding of O3
response is greatest. The focus of research for developing quantitative relationships between
O3 exposure and biological effects has emphasized the response of individual species for three
reasons. First, single species studies are achievable experimentally, including ease of
developing adequate experimental design and exposure technology. Second, in many
instances, the plants are grown in monoculture (e.g., most crop plants, ornamentals, fruit and
nut species, plantation forests), and the interspecific competition and plant diversity, which
typify natural communities, are not issues. The environmental influences of a plant's growing
environment (e.g., drought) that modify the exposure-response relationship can be observed
more readily. Third, in systems that are comprised of a multitude of species (e.g., mixed
forest stands, pastures, grasslands), it is important to understand the response of the individual
components so that behavior of the system may be analyzed systematically. The underlying
assumption is that understanding how a forest stand responds to O3 requires knowledge of the
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response of sensitive individuals of each species within that stand as a starting point. The
interactions that typify the population and the community are subject to O3 effects as well and
may manifest themselves as a measurable effect some time later as a result of these
interactions.
The potential for using individual plant (species) responses to an environmental
stress (such as O3 exposure) to predict population and community response may be limited
(Woodward, 1992). Propagation of stress responses from a tissue or organ to the whole plant,
the population, the community, or the ecosystem level can be influenced by interactions
between plants and by feedback mechanisms at the different levels. Important components of
such feedback are the mechanisms of homeostasis that involve injury repair (at the metabolic
level) or various types of compensation (Tingey and Taylor, 1982). Compensation, which
may occur at all levels of organization, from the subcellular to the ecosystem, invokes
processes that counteract the detrimental effects of the stress. At the ecosystem level, an
effect on the growth rate of a sensitive species may not be translated into a comparable effect
on the growth rate of a population of the species, because of changes in the intensity of
competition within a community (Woodward, 1992).
Currently, most of the knowledge of O3 concerns effects on individual plants or
their parts. Although some information exists on effects at the population level with some
agricultural crops, little is known about how, and to what extent, effects may be propagated
through the different hierarchical levels within natural and forest ecosystems.
5.9.2 Methodologies
Most of the currently available information dealing with the effects of O3 exposure
on crops and tree seedlings is the result of experimental fumigation studies. The type of
fumigation study determines the applicability of the data. Ozone-fumigation, plant-response
studies require fumigation of well-characterized vegetation to varying regimes. Variation in
regimes may be achieved by controlled fumigation, chemical/mechanical fumigation
exclusion, or natural O3 gradients. Controlled fumigation systems are designed to maintain a
modified gaseous atmosphere around a plant for a specified period of exposure in order to
monitor plant responses to that modified atmosphere. All fumigation systems share some
features in common, namely, general plant growth conditions (light, temperature, humidity,
CO2, and soil moisture) must be met, and differential concentrations of O3 generated either
artificially or naturally must be supplied to the vegetation and maintained during the exposure
period. Exposure systems have been established in controlled environments, greenhouses, and
the field. Controlled fumigation systems may range from cuvettes that enclose leaves or
branches to a series of tubes with calibrated orifices spatially distributed over a field to emit
gaseous pollutants to a plant canopy. Systems that exclude O3 by mechanical or chemical
means have been used, as have natural gradients.
Open-top chambers represent the best technology for determination of crop yield to
O3 at the present time. Concentration and duration of the gaseous exposures are well
controlled and plants are grown under near-field-culture conditions; however, plot size is
small when compared with a field, microclimate may influence plant sensitivity to O3, and air
quality after passage through the charcoal filter has not been widely characterized. Caution
should be used when extrapolating results to field conditions. Exclusion methods, particularly
those using chemicals such as EDU, are the least disruptive of ambient culture conditions in
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the field; therefore, these approaches most closely estimate "real" crop losses to O3.
However, the mechanism by which EDU protects plants is unknown.
5.9.3 Species Response/Mode of Action
The mode of action of O3 on plant species described in the 1986 criteria document
(U.S. Environmental Protection Agency, 1986) still holds true. The plant leaf is the site of
O3 action, and the critical effect is on the plant's carbon budget (the amount of carbohydrate
produced). Inhibition of photosynthesis limits carbohydrate production and allocation
resulting in reduced biomass, growth, and yield and increases susceptibility to abiotic and
biotic stresses.
Ozone exerts a phytotoxic effect only if a sufficient amount reaches the sensitive
cellular sites within the leaf. To do this, it must diffuse from the atmosphere into the leaf
through the stomata, which exert control on O3 uptake. Ozone effects will not occur if the
rate of O3 uptake is low enough that the plant can detoxify or metabolize O3 or its
metabolites, or if the plant is able to repair or compensate for the effects. Cellular
disturbances that are not repaired or compensated are expressed ultimately as visible injury to
the leaf or effects on growth, yield, or both (Tingey and Taylor, 1982; U.S. Environmental
Protection Agency, 1986). The effects of O3 exposures on plants are cumulative. The level
of O3 concentration and length and number of exposures determine the extent of plant effects.
Annual plant responses are determined by the number of exposures during a single growing
season. For trees and other perennial plants the effects are determined by multiple exposures
over a number of years.
Ozone is expected to reduce growth or yield only if it directly impacts the plant
process that is limiting to plant growth (e.g., carbon produced), or it impacts another step
sufficiently so that it becomes the step limiting plant growth (e.g., allocation of carbohydrates
to roots and nutrient uptake becomes limiting to plant growth) (Tingey, 1977). Conversely,
O3 will not limit plant growth if the process impacted by O3 is not growth limiting. This
implies that not all effects of O3 exposures on plants are reflected in growth or yield
reductions. These conditions also suggest that there are combinations of O3 concentration and
exposure duration that the plant can experience that may not result in visible injury or
reduced plant growth and yield (U.S. Environmental Protection Agency, 1986). However,
subtle physiological effects that may not result in immediate growth reductions may result in
increased plant susceptibility to other environmental factors (e.g., drought, fungal pathogens,
insects, at these concentrations) and competition.
Studies since 1986 corroborate this understanding, adding information on the effect
of O3 on photosynthetic capacity, respiration, leaf dynamics, and the detoxification and
compensatory processes. In particular, exposure to O3 concentrations at or near current
ambient levels (0.04 to 0.06 ppm) (see Section 5.6; Table 5-18), depending on their duration,
can affect photosynthesis, but exposures of longer duration are necessary to produce growth
responses, taking days to weeks, rather than hours, as in earlier studies with high
concentrations (0.25 ppm or greater). The loss of leaves prematurely as a result of
O3 exposure has been observed in several species and is particularly important in coniferous
trees. However, the mechanism of premature senescence is not understood. Both reduced
photosynthetic capacity and reduced leaf area due to O3-induced leaf loss contribute to the
reduction in carbohydrate production by plants. In addition to leaf loss, reports of stimulation
of production of new leaves and higher photosynthetic capacity of new leaves represent
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compensation processes that operate in some species of trees. More information is needed to
understand O3 uptake at the canopy level and how plants integrate the effects of O3. Some
quantitative understanding of these processes is needed to be able to predict long-term effects
of O3 on tree species. Unfortunately, there is little experimental evidence to date regarding
effects of long-term O3 exposure on perennial plants. Few experimental studies of tree
seedlings have extended exposures beyond one season, and only in a limited number of
studies have observations of growth effects been extended into the following year, thus
observing "carry-over" effects. These carry-over effects are significant to long-lived species
such as trees because they affect the elongation of new spring shoots or root growth in the
year following exposure to O3. In at least one instance, this has been correlated with reduced
storage carbohydrate in roots. Reduction in growth and productivity, a result of altered
carbohydrate production and allocation, may appear only after a number of years or when
carbohydrate reserves in the tree are severely depleted. To enable prediction of long-term
effects of O3 exposure in ecosystems, species response as a function of interactions with other
species and the effects of abiotic and biotic environmental factors on these interactions both
must be known.
5.9.3.1 Exposure Dynamics
The uptake of O3 from the atmosphere is a complex process involving absorption
of O3 primarily through the leaves. Plant uptake is influenced by temporal and seasonal
variation of exposures. Plant response is influenced by canopy structure, stomatal
conductance, respite time between exposures, phenology, and environmental conditions
(e.g., soil moisture and nutrient content). Studies both prior to and after the 1996 criteria
document, indicate that the components of exposure (i.e., peak concentrations >0.10 ppm,
frequency of occurrence, duration, temporal distribution of hourly O3 concentrations during a
growing season) play influential roles in plant response. Greater yield reductions in both
annual and perennial crop species (e.g., bush beans and alfalfa) and greater biomass
reductions in tree seedlings (e.g., ponderosa pine and aspen) have resulted from experimental
episodic peak exposures than from equivalent exposures with either daily peak occurrences or
nondiurnal, continuously elevated exposures. In addition to the temporal distribution of
concentration, the distribution of O3 exposure during the growing season, as related to plant
phenology, is also important. Some phenotypic stages of growth (e.g., the time of pod-fill in
beans and the period of starch storage in perennial species) are more sensitive to O3 than are
others. Thus, effects of early-season versus late-season exposure will vary depending both on
the phenology of the plant species and the growth response measured. Another key to plant
response is the timing of the exposure. Ozone uptake is greatest when stomatal conductance
is highest; therefore, the greatest potential effect for O3 exposures to produce an effect on
plants occurs at that time. Neither peak nor mid-range concentrations occur at the same time.
Plant effects are determined by which concentrations occur when stomatal conductance is
highest. Associated with stomatal conductance is atmospheric turbulence; O3 concentrations
must reach leaf surfaces if they are to be taken up by a plant.
In most crop-exposure studies, in particular, those included in the NCLAN
database, the exposure treatments used in developing response functions have been based on
O3 concentrations at the experimental site. Few studies have been designed specifically to
study the effect of varying the types of exposure regimes on crop and tree seedling responses.
Research results enable only the prioritization of components of the exposure in terms of their
degree of influence on growth alterations. For example, peak or higher concentrations are
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more effective than lower concentrations in altering growth when those peaks occur in the
daytime when stomatal conductance is high. Episodic occurrences of high concentrations
during daylight hours are more injurious according to experimental chamber studies by
Musselman et al. (1983, 1986b, 1994) than are either the daily occurrences of the same peak
value with the regime having the same total exposure value as the episodic regime, or
regimes having no episodic occurrence of peaks and no rise and fall diurnal pattern to daily
concentrations (i.e., "flat", but relatively moderate to high concentrations) and having the
same total exposure value over a growing season as the episodic regime. The concentrations
used in these chamber studies were all >0.10 ppm, exposures seldom experienced outside of
California. Because of the variation in species' growth/yield response as a function of
exposure dynamics (i.e., concentration, distribution, duration), it is important to have an
exposure index that is biologically based (i.e., a measure of ambient O3 concentration that is
related to the measured biological effects).
5.9.3.2 Age and Size
The role of age and size in modifying tree response to O3 is the single largest
uncertainty in quantifying O3 effects on tree species. To date, most of the biological effects
data and all of the exposure-response functions for trees have been developed with seedlings
and saplings. The implicit assumption is that seedling response is a good indicator of large-
tree response. However, gas-exchange and water-use differences with tree size and age
presumably would affect O3 uptake and thus O3 exposure response. Indeed, published reports
indicate that O3 sensitivity is related to the gas-exchange characteristics of the current life
stage. Recent data indicate that, for some species (e.g., giant sequoia), seedling growth is
affected more by O3 than is growth in large trees, whereas, for other species (e.g., red oak),
seedling growth is less affected than is growth in large trees. These observations of
differences in O3 growth response between seedlings and large trees follow the differences in
leaf conductance with age for each of these two species.
Another factor related to tree and size is the occurrence of "carry-over effects"
(i.e., the impact of O3 on growth responses in the season following exposure). For example,
reductions in root growth and starch concentration and in shoot elongation in the year
following exposure have been reported for ponderosa pine and aspen. Carry-over effects are
significant in determining long-term growth response in long-lived species exposed year after
year to both O3 and changing environments.
5.9.4 Factors That Modify Plant Response to Ozone
Plant response to O3 exposure is modified by factors within and external to the
plant species; cultivars and individuals within populations display variable response to O3.
The plant's response and the variation of that response is dictated by genetics and the plant's
present and past environmental milieu. The environment includes biotic and abiotic factors of
the species' growing environment, the temporal pattern of exposure concentrations, and the
plant's phenotypic stage during exposure.
5.9.4.1 Genetics
The response of an individual plant within a species and at any age is affected
both by its genetic makeup and the environment in which it is growing. The specific genes
controlling O3 response and involved in mechanisms of O3 tolerance are largely unknown;
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however, control of stomatal conductance and internal biochemical defense systems are
among the most commonly postulated tolerance mechanisms. Ozone tolerance is generally
thought to be controlled by multiple genes. The implications of genetic variation for
managed and natural ecosystems are several-fold. First, the potential for natural selection for
O3 tolerance and associated loss of sensitive genotypes is regional in nature, unlike
point-source pollution impacts that occur mainly on plant populations in the vicinity of the
source. However, the intensity of O3 selection is generally thought to be quite low, 0.3 or
less (Taylor and Pitelka, 1992), across most U.S. areas. Second, although it is known that
individual plants within a species vary in their O3 tolerance, the physiological costs to tolerant
plants in terms of carbohydrate assimilation (energy production) and allocation are not known.
Tolerance mechanisms based on reduced stomatal conductivity in the presence of
O3 presumably would reduce the growth of tolerant plants. Similarly, tolerance mechanisms
based on the productivity of antioxidant compounds would shunt plant resources away from
growth to the production of the defense compounds. Third, exposure-response equations and
yield-loss equations developed for a single or small number of cultivars, genotypes, families
or populations may not represent adequately the response of the species as a whole. As a
corollary to this, the sensitivity of responder genotypes can not be determined by measuring
effects just in relation to mean O3 concentrations.
5.9.4.2 Environmental Factors
Plant response to O3 exposure can be modified by a number of biotic and abiotic
factors in the plants' past and present growing environment. Understanding and, if possible,
quantifying these modifications will reduce uncertainty in the estimates of species' exposure
responses. Also important is an understanding of how exposure to O3 can modify a plant's
ability to integrate the effects of its environment. For example, exposure to O3 has been
shown to reduce a tree's ability to withstand winter injury due to freezing temperatures and
also to increase the success of pest infestations.
Biotic factors in a plant's environment include pests, pathogens, and plants of the
same or competing species. Although only a limited number of plant-insect systems have
been studied, some insect pests appear to have a preference for and to grow better when
feeding on plants that have been affected by O3 exposure, but there is no evidence to suggest
that O3 may trigger pest outbreaks in plants. Because the effects of O3 on the vast majority
of plant-insect systems are unknown, quantitative assessment of such interactions on crops
and natural vegetation is impossible. At best, it reasonably may be concluded that some
insect pest problems will increase as a result of increased ambient O3 levels. Indeed, this
phenomenon was observed in the San Bernardino Forest study where injured ponderosa pines
experienced an increase in bark beetle infestations at higher O3 exposures.
Plant-pathogen interactions also appear to be affected by O3. The suggestion that
O3 exposure tends to diminish diseases caused by obligate pathogens and to favor those
diseases caused by facultative pathogens (Dowding, 1988) generally is supported by the
limited evidence currently available. This suggests that continued exposure to O3 may lead to
a change in the overall pattern of the incidence and severity of specific plant diseases
affecting crops and forest trees.
Abiotic environmental factors include, among other physical and chemical
elements, solar radiation, wind/atmospheric turbulence, and air and soil moisture and
temperature. Collectively, abiotic factors greatly affect plant growth because of their
influence on the processes of photosynthesis, respiration, and transpiration. For agricultural
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crops, water availability may be the most important of these interactions with O3. There is
consistent evidence that severe drought conditions tend to reduce the direct adverse effects of
O3 on growth and yield, and that ready soil water availability tends to increase the
susceptibility of plants to O3 injury. However, a lack of water should not be viewed as a
potentially protective condition, because of the adverse effects of drought per se. Unlike the
situation with annual crops, a limited amount of evidence suggests that prolonged exposure of
perennial trees to O3 may lead to greater water-use efficiency, which, in turn, would better
enable the exposed trees to survive drought conditions.
The numerous chemical components in a plant's environment, including soil
nutrients, agricultural chemicals, and other air pollutants, also potentially influence the plant's
response to O3 exposure. The nature of these interactions is largely unknown. Although
many studies have been conducted on the effects of O3 on plants in conjunction with other
gaseous air pollutants such as SO2 and NO2, the data obtained in several of these studies is of
academic interest only because of the unrealistic exposure scenarios used.
Because increased tropospheric O3 is a component of global climate change, which
is of growing concern within world communities, data on the interactions of O3 with
increased levels of CO2 and UV-B radiation, elevated temperatures, and drought are beginning
to appear. Initial data suggest that increased CO2 levels may ameliorate the effects of O3, but
conclusive generalizations about the outcome of this interaction are not yet possible. Studies
investigating the interaction of O3 with UV-B exposure reveal no significant changes in O3
effect on the growth and yield of soybean due to UV-B levels, although there are significant
effects of O3.
Although a number of studies have examined the interactions of O3 with specific
environmental factors, no quantitative database exists from which the effects of O3 on species
can be extrapolated across environments. The role of different growing environments in a
species' O3 exposure response and the effect of O3 exposure on a species' ability to integrate
its' environment remain uncertain.
5.9.5 Effects-Based Air Quality Exposure Indices
A measurement is needed that relates ambient O3 exposures with the degree of
plant response. The effects of O3 on individual plants and the factors that modify plant
response to O3, however, as indicated in the previous sections, are complex and vary with
species, environmental conditions, and soil and nutrient conditions. Due to the complexities
of the processes associated with uptake and O3 interactions with external physical and internal
genetic factors that influence plant response, the development of exposure indices that
characterize plant exposure and response in a quantifiable manner has been and continues to
be a major problem.
Plant uptake of O3 (either rate of uptake or cumulative seasonal uptake) is a critical
factor in determining plant response. Ozone uptake is controlled by canopy conductance,
stomatal conductance, O3 concentration external to the leaf and gases emitted from the leaf
through the stomata. Any factor that affects stomatal conductance (e.g., light, temperature,
humidity, atmospheric chemistry, soil and nutrients, time of day, phenology, biological
agents) will affect O3 uptake and, consequently, plant response. Empirical functions for
predicting stomatal conductance have been developed for particular species (Losch and
Tenhunen, 1981) but have not been used in development of exposure indices.
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The mode of action of O3 on plants, as presented in Section 5.2, is a culmination
of a series of biochemical and physiological processes that lead to alterations in plant
metabolism. Ozone-induced injury is cumulative, the result of net reduction in
photosynthesis, changes in carbohydrate allocation, and early leaf senescence, which lead to
reduction in biomass formation and reduction in yield. Increasing O3 uptake results in
increasing reduction in biomass production and yield.
The optimum exposure index that relates well with plant response should
incorporate, directly or indirectly, the factors described above; unfortunately, such an index
has not yet been identified. Exposure indices that weight the hourly O3 concentration
differentially appear to be the best candidates for relating exposure with predicted plant
response. Peak concentrations occur primarily during daylight hours, thus indices that provide
differential weight to the peak concentrations give greater weight to daylight concentrations,
when stomatal conductance is usually greatest, than to nighttime concentrations, when
conductance is minimal. Peak concentrations do not occur throughout the day; therefore, the
timing of the exposure is important in determining plant response.
Evidence from the Musselman et al. (1983, 1986b, 1994) and Hogsett et al.
(1985b) experimental chamber studies that applied two or more different exposure regimes
support the view that daytime peak concentrations and respite time are important in eliciting
plant responses. Ozone effects on plants exposed to two (or more) regimes having equal total
exposure were greater for exposures experiencing the higher peak concentrations, respite time
of 2 to 6 days, or peak concentrations during period of maximum leaf expansion. This
conclusion is consistent with the mode of action of O3 on plants and with the conclusions in
the previous EPA criteria document (U.S. Environmental Protection Agency, 1986) and its
supplement (U.S. Environmental Protection Agency, 1992).
No studies have been designed specifically to evaluate the adequacy of the peak-
weighted, cumulative indices. Consequently, it is not possible to discriminate among the
various peak-weighted, cumulative indices based on experimental data. Functional weighting
approaches, including allometric, sigmoid, or threshold weighting, have been suggested and,
in earlier retrospective studies, compared, but there is no evidence to favor one approach over
the other on the basis of statistical fits to the data. Generally, the peak-weighted, cumulative
indices relate well with plant response and order the treatment means in monotonically
decreasing fashion with increasing exposure, based on studies that apply two or more types of
exposure regimes and when combining data from replicate studies of the same species.
Peak-weighted, cumulative indices appear to have major advantages over the mean
(e.g., 7-h seasonal mean), peak indices (e.g., 2HDM), and the index that cumulates all hourly
average concentrations (i.e., SUMOO). Crop yield loss and biomass reduction are estimated
better using the peak-weighted, cumulative indices than the 2HDM index; when duration of
exposure is taken into consideration, peak-weighted, cumulative indices perform better than
the seasonal mean indices. In addition, results have been published to indicate that the
SUMOO index does not relate adequately exposure with biological effects because the index
focuses on the lower hourly average concentrations.
The greater importance of cumulative peak concentrations (>0.10 ppm) when
compared with cumulative mid-range concentrations (0.50 to 0.09 ppm) in eliciting plant
response has been questioned. The data supporting the two viewpoints are not comparable
because the response parameters used in these studies were different. Musselman et al.
(1983, 1986b) and Hogsett et al. (1985b), whose studies have been cited as a basis for
emphasizing the importance of cumulative peaks, measured both foliar injury and growth
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reductions and were based on exposures in open-top or greenhouse chambers to
concentrations higher than those usually encountered in the ambient air outside of California.
The biological evidence for supporting the importance of mid-range concentrations is based
on ambient air field exposures using plants sensitive to O3 in which exposures, seldom if ever,
exceeded 100 ppb. The conclusions of Krupa et al. (1993, 1994, 1995), Tonneijck and Bugter
(1991), and Tonneijck (1994) must be interpreted with caution because they are based on data
from Bel W3 tobacco and other O3-sensitive indicator plants. Tonneijck and Bugter (1991)
concluded that O3 effects varied with species and climatic condition; therefore, O3 injury on
Bel W3 tobacco was not an adequate indication of ambient condition, nor was it an adequate
indicator to determine the risk of O3 to other plant species or to vegetation as a whole.
It should be obvious that plants take up all O3 concentrations present in the atmosphere, not
just O3 peaks. Cumulative effects result from all O3 concentrations that enter the plant.
Plants can not respond to peaks if there are none in the ambient air. When peaks occur at the
time of greatest stomatal conductance, the effect of mid-range concentrations will not be
observable.
When predicting the effects of O3 on vegetation under ambient conditions using
experimental exposure-response models, the types of exposure regimes used in the
experiments should be taken into consideration. For example, NCLAN experiments contained
peak hourly average concentrations in their regimes. Any exposure index based on the
NCLAN experiments should take into consideration the presence of these peak concentrations.
By doing so, the situation may be avoided where two sites that experience two distinct
distributions of high hourly average concentrations but have the same value of cumulation
(e.g., same SUM06 or W126 value) exhibit differing biological effects.
The concentration level for a cumulative, peak-weighted index was determined
from the best available biological response data (i.e., the crop yield responses from NCLAN).
The concentration level selected to prevent a particular yield loss will have associated with it
any uncertainty inherent in the methodology employed in NCLAN studies, in particular, the
modified ambient exposures of NCLAN protocol typified by a relatively large number of
episodic occurrences of high concentrations. The episodic occurrence of high concentrations
is typical of many, but not all, agricultural areas in the United States. Some regions of the
country may have different exposure regimes, typified by the lack of a large number of high
concentration occurrences but still having a high cumulative, weighted exposure index value.
The particular concentration level determined to protect 50% of the crops studied from a 10%
yield loss based on NCLAN data may over- or underestimate the yield loss from a different
regime type. Lefohn and Foley (1992) and Musselman et al. (1994) have suggested that a
multi-component index, combining a cumulative, weighted index and the number of
occurrences of concentrations >0.10 ppm would capture more adequately both the plant
exposure response and the air quality at the site, thus overcoming some of the uncertainty
associated with selection of a concentration level from the NCLAN crop response data.
Other experimental approaches have been employed to demonstrate effects of
ambient O3 exposure (e.g., chemical protectants [EDU]) but are of limited value in
determining an exposure index. The ambient exposure approach addresses one of the
shortcomings of the NCLAN methodology, but the experimental designs can not provide a
range of O3 treatments necessary for statistical robustness, quantifying the effect of ozone on
yields, and the results cannot be extrapolated beyond the site and year of the exposure study.
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5.9.6 Exposure Response of Plant Species
5.9.6.1 Introduction
The Clean Air Act seeks to protect public welfare resources, including plants and
natural ecosystems, from adverse effects of criteria pollutants, including tropospheric O3.
"Adverse effect" has been interpreted in the 1986 criteria document (U.S. Environmental
Protection Agency, 1986) and its supplement (U.S. Environmental Protection Agency, 1992)
to be equated with yield loss and impairment in the intended use of the plant. In the instance
of crop species, for example, an adverse effect of O3 is agronomic yield loss. Foliar injury
also can be an adverse effect, especially when decreasing marketability of foliar crops (e.g.,
spinach, lettuce, cabbage) or reduced aesthetic value of ornamentals. These effects constitute
yield loss with or without concomitant growth reductions. With tree species grown for
timber, paper, or pulp, biomass loss (and therefore loss of forest productivity) can be
quantified as being an adverse effect.
Diverse experimental procedures, ranging from field exposures without chambers
to field exposures with OTCs to exposures in chambers under highly controlled laboratory
conditions, have been used to study O3 effects on crops and trees seedlings. In general, the
highly controlled laboratory experiments are most useful for investigating specific responses
and for providing a scientific basis for interpreting and extrapolating results. Such
experiments are very important in increasing the understanding of the biological effects of air
pollutants. To accurately assess the economic impacts of O3 on crop yield or ecological
impact of altered carbon partitioning in tree species, however, requires exposure methodology
that provides a range of O3 treatments sufficient for quantifying effects (i.e., exposure-
response functions) and also provides growing conditions that closely match those in the
plants' natural growing environment. Because the OTC methodology provides control over
O3 exposure treatments and still allows some replication of field conditions, as well as permits
replication of studies from year to year, this has been the primary methodology used for
developing the empirical database of O3 effects on crop and seedling tree species during the
last 15 years. Many of the studies reviewed in this document, as well as those in the 1986 O3
criteria document (U.S. Environmental Protection Agency, 1986) utilized the OTC
methodology, including the NCLAN studies (see Section 5.6.2) that were initiated by EPA in
1980 primarily to improve estimates of yield loss in the field and the magnitude of crop
losses resulting from O3 exposure. The NCLAN studies used numbers of treatments sufficient
to permit robust statistical designs and the development of exposure-response functions. It is
the largest database available for establishing a quantitative relationship between O3 exposure
and crop yield. Studies of tree seedlings also have been conducted utilizing OTCs as a means
of exposing seedlings to a range of treatments, replicate treatments, and approximate field
conditions. The exposure-response function for each species permits estimations and
generalizations of biological response to O3, unlike the multiple comparison approach.
There has been debate concerning the experimental designs, particularly the
number, types of regimes, and exposure concentrations used in the NCLAN studies. The
O3 exposures utilized by the NCLAN program have been described as artificial regimes that
do not mimic actual conditions. The exposure treatments were "modified ambient" (i.e.,
treatments were achieved by addition of some amount of O3 above the ambient
concentration). Another criticism of NCLAN studies was the alteration of the environment by
the OTCs to the degree that exposure-response functions obtained using this methodology can
not be extrapolated to ambient environments. A study by Heagle and co-workers (1989a) of
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OTCs suggests that, although departures from field conditions can occur, "they allow control
of pollutant concentrations with dynamics that compare closly to exposure dynamics in
ambient air." For NCLAN studies, although it was noted that OTCs decreased mean wind
velocity, altered light profiles, and eliminated the vertical gradient in O3 concentration (less
near the ground) that usually occurs in the canopy of plants grown in the ambient air,
chamber effects were found not to enhance consistently the treatment differences or plant
responses to O3. Despite the criticisms of the NCLAN studies, there is no other database that
matches it. Approximately, 90% of the available O3 dose-yield response data comes from
these studies (Heagle et al., 1989a).
5.9.6.2 Predicted Crop Yield Losses
The NCLAN studied the major agronomic crop species, including corn, soybean,
wheat, cotton, bean, and alfalfa, as well as several other regionally important species;
collectively, the species studied account for 70% of all cropland in the United States and for
73% of the nations's agricultural receipts. To predict crop yield loss due to O3 exposure, two
approaches to developing a composite exposure-response function for all crops from the
NCLAN database were taken. The first approach predicted crop yield losses of up to 20% at
a 12-h seasonal mean of 0.06 ppm and a 10% loss at a 12-h seasonal mean of 0.045 ppm.
The second approach calculated separate regressions for studies with multiple harvests or
cultivars, resulting in a total of 54 individual equations from the 31 NCLAN studies (average
study duration of 74 days) and 12 crop species using three different exposure indices, and
concluded that 50% of the crops would experience 10% yield loss at a 3-mo SUM06
concentration of 26.4 ppm-h (Table 5-22), a 7-h seasonal mean of 0.049 ppm, or a 2HDM of
0.094 ppm. (These are averaged yield losses for all species; losses for many of the crops
would be higher at these concentrations.) The box-plot distribution of yield loss for the
compiled studies, expressed as a SUM06, is shown in Figure 5-23A.
Results reported for European crop studies support the NCLAN analyses results.
For example, in the European studies, wheat yields were reduced by up to 29%, depending on
the O3 exposure level and cultivars used, but in no instance did the exposure level exceed a
0.062 ppm 7-h seasonal mean. Spring rape yields were reduced by 9 to 26% at 8-h seasonal
means of 0.03 to 0.06 ppm. Seasonal 7-h means of 0.045 ppm reduced bean yield by 17%.
Perennial crop exposure response, unlike annual crops, is complicated by the fact
that such crops receive multiple-year exposures, and the effects of such exposures may be
cumulative. Yields of multiple-year forage crops (e.g., alfalfa and forage mixtures), as with
yields of single-season crops, are reduced at O3 concentrations at or near ambient (0.04 to
0.06 ppm, 7- and 12-h mean) in many parts of the growing areas for these crops. The
question of cumulative effects in perennial crops has been addressed only in one instance
(a 2-year alfalfa study in Southern California), and, in this study, there was no indication of
carryover effects from year to year.
5.9.6.3 Predicted Biomass Changes in Trees
Trees, depending on species and genotype, exhibit a wide range of responses to O3
exposure. Ozone exposures alter gas exchange, early senescence and needle retention on
conifers, carbohydrate allocation, root growth, total biomass production, and reproduction.
The alteration by O3 of photosynthetic performance and needle retention shifts carbon
allocation priorities and changes growth. In particular, root growth in tree seedlings is often
reduced, whereas shoot growth is maintained. Root growth reductions can decrease
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mycorrhizal formation and water and nutrient uptake in seedlings and impede seedling
establishment. Changes in carbon budgets due to O3 exposures also can affect long-term
changes in tree growth. Small changes (even less than 1 to 2% biomass loss per year) that
may not be detectable statistically may be translated into large changes during the life span of
the tree and may result in changes in stand dynamics when sufficient trees are affected, with
concomitant effects on the structure and function of the ecosystem. The implication of these
effects on long-lived species is significant. However, most of the experiments have been
conducted on seedlings for 1 to 3 seasons, only 2% or less of the life span of the tree.
Seedlings and mature trees have different carbon allocation use patterns. Mature trees have a
significantly higher ratio of respiring to photosynthetic tissue. Carbohydrate reserves also
differ between trees and seedlings. Extrapolation of information from seedlings to mature
trees must be done with caution because the environments in which trees and seedlings grow
differ substantially due to differences in rooting depth and canopy structures.
5.9.7 Effects of Ozone on Natural Ecosystems
Ozone is the only regionally distributed phytotoxic pollutant capable of changing
the chemical environment of forests without leaving a permanent trace of its presence. Ozone
molecules are ephemeral, decompose rapidly to oxygen and free radicals, and leave no
residuals; therefore, stresses resulting from exposure to O3 are frequently difficult to
determine (Taylor and Norby, 1985).
Ozone exposures are episodic. Ozone may be transported for long distances and
may cover very large areas during an episode. Concentrations can increase as O3 trajectories
move across the country and pass over new sources (Wolff et al., 1977a,b,c, 1980; Wolff and
Lioy, 1980). Forest trees, shrubs, and other perennial plants often must cope with the
cumulative effects of several acute or chronic episodes. Exposures may last for minutes,
hours, days, or weeks. Trees may respond rapidly as, for example, when needles of eastern
white pine exhibit visible injury symptoms within days after exposure to high (>0.08 ppm) O3
concentrations (Garner, 1991). In most instances, however, responses are more subtle and not
observable for many years because trees compensate, adapt, and respond to cumulative stress
by differential growth, the result of altered carbon allocation (Waring and Schlesinger, 1985).
Ecosystems are complex, dynamic communities composed of populations of living
plants, animals, and microorganisms (producers, consumers, and decomposers). Because they
must continually respond and adapt to changing environments, mature ecosystems are seldom
stable (Kozlowski, 1985). They are held in an oscillating steady state by the operation of a
particular combination of biotic and abiotic factors. Ecosystems can change dramatically
throughout time, have no optimal condition, and are only healthy when compared to some
desired state specified by humans (Lackey, 1994). Ecosystem functions maintain clean air,
pure water, a green earth, and a balance of organisms. These functions enable humans to
obtain food, fiber, energy, and other material needs for survival (Westman, 1977).
Ozone concentrations capable of causing injury to forest ecosystems (0.06 ppm or
higher of varying durations; see Section 5.7.3) continue to occur in the San Bernardino and
the Sierra Nevada Mountains and in the Appalachian Mountains from Georgia to Maine.
Visible injury to forest trees and other sensitive vegetation in these areas has been observed.
The impact that an ecosystem can experience from exposure to O3 will be
determined by the severity of the effect on individual members of a population. Stresses,
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whose primary effects occur at the molecular or cellular physiology level of an individual,
must be propagated progressively through the more integrative levels, from the leaf, branch,
or root, to whole plant physiology and stand dynamics, and, ultimately, to the ecosystem
(see Section 5.7.4; Hinckley et al., 1992; Figure 5-36). Variability and compensation in
response to stress at both the individual and the population levels determine the hierarchical
extent of the response. Other factors, in addition to compensation and variability in response
to stress, that affect response in individuals and populations include the location of a site and
environmental factors, such as air and soil moisture and temperature and genetic composition
of the individuals of a population. Responses at the population level must alter the ecosystem
functions of energy flow, water movement, and nutrient cycling to produce an ecosystem
impact.
The primary responses of a forest ecosystem to sustained O3 exposure are reduced
growth and biomass production (Section 5.7.4; Figure 5-34; Table 5-36; Smith, 1990).
In mature trees, most of the carbohydrate produced is utilized in maintenance (Figure 5-34).
Exposure to O3 inhibits photosynthesis and decreases carbohydrate production and allocation,
and, as has been stated previously, decreases allocation to the roots and interferes with
mycorrhizal formation and nutrient uptake. The resulting loss in vigor affects the ability of
trees to compete for resources and makes them more susceptible to a variety of stresses
(Section 5.7.4; Table 5-36; see also Sections 5.3 and 5.7.3.1). In the San Bernardino Forest,
the only available study dealing with the effects of O3 exposure on forest ecosystems, the
sensitive canopy trees, ponderosa and Jeffrey pine, no longer were able to compete effectively
for essential nutrients, water, light, and space. Altered competitive conditions in the plant
community, resulting from a decrease in the most sensitive species, permitted the enhanced
growth of more tolerant species, white fir, incense cedar, sugar pine, and black oak (Miller et
al., 1982; U.S. Environmental Protection Agency, 1978, 1986). Although the primary effect
was on the more susceptible members of the forest community, changes in the function of
other ecosystem components directly or indirectly affected the processes of carbon (energy)
flow, mineral-nutrient cycling, and water movement, leading to changes in community
patterns. Changes in available energy influenced biotic interactions associated with predators,
pathogens, and symbionts (mycorrhizae).
The forests of the Appalachian Mountains have been episodically exposed to
O3 concentrations capable of vegetational injury for many years. Visible injury to foliage and
reduction in growth of sensitive eastern white pine has been associated with peak hourly
concentrations ranging from 0.08 to 0.13 ppm. Black cherry, also has been shown to be
sensitive to O3 exposures. Surveys of various regions of the Appalachian Mountains,
including the Smoky Mountain and Shenandoah National Parks, indicate that visible injury to
a variety of different types of vegetation continues to occur. Neither eastern white pine nor
black cherry are canopy trees. Removal of sensitive individuals and the absence of
population changes of these species have not resulted in any visible change in the forest
ecosystems along the Appalachian Mountains, possibly because, as stated earlier
(Section 5.7.4; Figure 5-36), "only a small fraction of the stresses at the molecular, cellular,
or leaf level become disturbances at the stand or ecosystem level" (Hinckley et al., 1992).
Decline and dieback of trees on Mt. Mitchell and Camel's Hump cannot be related solely to
O3 injury. Ongoing research is attempting to understand better the effects of O3 exposure on
vegetation in these areas and the effect, if any, on the ecosystems to which they belong.
Injury to sensitive trees in the Sierra Nevada also appear to be in the same
category as stated above. Injury to individuals has not been propagated to the population
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level and has not altered ecosystem functions; therefore, no changes have taken place in the
ecosystems in those mountains.
The previous O3 document (U.S. Environmental Protection Agency, 1986)
concluded that "none of the plant species shown to be injured by O3 plays a dominant role in
the Blue Ridge Mountain ecosystem. Therefore, the removal of any of these species would
probably not have an impact that the decline and death of ponderosa and Jeffrey pine have
had on the San Bernardino Forest ecosystem." This same conclusion applies today.
5.9.8 Economic Assessments
Based on economic assessments and scientific data available at the time, the
previous criteria document (U.S. Environmental Protection Agency, 1986) concluded that
O3 at ambient levels was imposing economic costs on society. The review of more recent
(post-1986) literature on agriculture corroborates that earlier conclusion. Specifically, the
recent literature, using the full set of NCLAN data and addressing some deficiencies in the
pre-1986 assessments, confirms the finding of economic losses from ambient
O3 concentrations.
The exact level of these economic effects is a function of cropping patterns,
O3 concentrations (both ambient and episodic), and the spatial and temporal characteristics of
projected or observed O3 levels. The current economic assessments represent improvements
in the scientific understanding of O3 effects on agriculture. However, the assessments of
economic effects initially incident on the agricultural sector remain incomplete.
Only a few assessments consider the economic effects of O3 on forest trees and on
urban trees, shrubs, and ornamentals. These studies assess the economic effects of
hypothetical changes resulting from O3 or other stressors on forest productivity and aesthetics
and are best viewed as measures of the potential effect of O3 on these receptors.
Improvements linking O3 effects data to productivity and aesthetic effects will improve the
utility of such economic analyses.
The effects of O3 on ecosystems have not been addressed in the published
literature. There is, however, an emerging interest in applying economic concepts and
methods to the management of ecosystems. Ecological research also is addressing the
challenging conceptual and practical issues in understanding and managing ecosystem
functions. Economic research continues to develop, refine, and apply techniques for valuing
market and nonmarket products and services that will be of help in estimating the economic
effects of O3 on ecosystems. Increased dialogue between the disciplines is needed before
empirical analyses of the economic consequences of ecosystem management are feasible.
In summary, the state of science concerning O3 economic effects on agricultural
crops is sufficient to conclude that O3 imposes costs on society.
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5.10 Effects of Ozone on Materials
5.10.1 Introduction
Photochemical oxidants are capable of reacting with a number of man-made and
natural materials. Nearly all materials-damage research on photochemical oxidants has
focused on economically important or abundant materials that are susceptible to oxidant
damage. These include elastomers (natural rubber and certain synthetic polymers), textile
fibers and dyes, and, to a lesser extent, paints. Recent research has been conducted on
culturally important materials, such as artists' paints and pigments. It has been shown that
oxidants harden and embrittle elastomers, causing cracking and loss in physical integrity.
Oxidant exposure weakens certain textile fibers (i.e., reduces the breaking strength and
increases the rate of wear) and changes the color of some dyes. The effects of oxidants on
paints are not defined well, but they may be similar to some of the effects on elastomers;
damage from other gaseous pollutants, such as SO2, and from natural damaging agents, such
as sunlight, moisture, oxygen, and temperature fluctuations, tend to overshadow the role of
ambient O3 in causing paint damage.
The literature selected for review in this section includes research previously
reported in the 1978 and 1986 criteria documents (U.S. Environmental Protection Agency,
1978, 1986) and a limited number of other references published before and after 1986.
Because little recent work has been reported on the effects of ozone on materials, reference to
older studies is necessary for completeness. This assessment of the effects on materials
includes a review of the mechanisms of damage and protection; it also presents dose-response
information from laboratory and field studies and evaluates previously reported economic
assessments.
5.10.2 Mechanisms of Ozone Attack and Antiozonant Protection
5.10.2.1 Elastomers
Most elastomeric materials found in the marketplace are composed of unsaturated,
long-chain organic molecules (i.e., the molecules contain carbon-carbon double bonds).
Natural rubber and synthetic polymers and copolymers of butadiene, isoprene, and styrene
account for the bulk of elastomer production for products such as automobile tires (Mueller
and Stickney, 1970). These types of compounds are particularly susceptible to O3 attack.
In contrast, synthetic elastomers with saturated chemical structures, such as butyl rubber,
polymers of silicones, ethylene, propylene, hypalon, and polyurethanes, have an inherent
resistance to O3 damage, but higher cost and limiting physical and chemical properties have
constrained their use in outdoor environments.
Ozone is thought to attack elastomers by adding a chain of three oxygen atoms
directly across the double bond, forming a five-membered ring structure (Mueller and
Stickney, 1970). This structure quickly rearranges (via Criegee ozonolysis) to form a
zwitterion and an aldehyde (see Figure 5-37). The aldehyde-zwitterion pair can be formed on
either side of the point of chain scission. Subsequent reactions of the zwitterion lead to a
permanently oxidized elastomer. Ozone damage in the form of cracking is a surface
phenomenon. It is greatly accelerated by mechanical stress, which produces fresh surface
area at crack boundaries. At very high concentrations and high mechanical stress, O3 damage
can result in a large number of surface microcracks that produce a frosted appearance and
mechanical weakening (Crabtree and Malm, 1956). At pollutant
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c
H
C=C
H H
O
/ \
R O O
C—C —C
H H H
ROD
— C—C—C—
H H
H
R
C
H
C —O-O + OC
H H
Figure 5-37. Postulated mechanism for damage to elastomers by ozone.
Source: Mueller and Stickney (1970).
concentrations normally encountered outdoors (and in many indoor environments), the
elastomer hardens or becomes brittle and cracked, which results in loss of physical integrity.
According to Fisher (1957), work at the Rock Island Arsenal by R. F. Shaw,
Z. T. Ossefa, and W. J. Tonkey in 1954 led to the development of effective antioxidant
additives to protect elastomers from O3 degradation. Subsequently, antiozonants generally
were incorporated into elastomeric formulations during mixing, and their protection was
effective, even when elastomers were stretched or flexed (Fisher, 1957; Mueller and Stickney,
1970).
Several theories (Andries and Diem, 1974) have been advanced to explain the
mechanism of antiozonant protection. The two best supported theories are (1) the scavenger
theory and (2) the protective film theory. The scavenger theory suggests that the antiozonant
diffuses to the surface, where it reacts with the O3 at a faster rate than with the carbon-carbon
double bonds of the rubber, thereby protecting the rubber sacrificially. The protective film
theory also includes diffusion to the surface, but assumes that the resulting layer is less
reactive with O3 than is the rubber and, thus, constitutes a protective layer.
The work of Razumovskii and Batashova (1970) on the mechanism of protective
action by the antiozonant TV-phenyl-jV'-isopropyl-^-phenylenediamine (PIPP) is most
consistent with the scavenger mechanism. These investigators showed that O3 reacts
preferentially with PIPP at a ratio of three O3 molecules to one PIPP molecule.
Andries et al. (1979), using carbon-black-loaded natural rubber compounds, with
and without antiozonants, attempted to distinguish among possible mechanisms with
attenuated total reflectance spectroscopy and scanning electron microscopy. Their
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experiments indicated that a combination of the scavenger and protective film mechanisms
best explains antiozonant protection. Examination of the surface of the rubber samples with
antiozonant showed that only ozonized antioxidant, not ozonized rubber, was present. This
layer of ozonized antioxidant functioned as a relatively nonreactive film over the surface,
preventing the O3 from reaching and reacting with the rubber below.
Lattimer et al. (1984) conducted a series of experiments on cross-linked rubber
(c/'s-polyisoprene and c/'s-polybutadiene) containing N,N'-di-(l-methylheptyl)-/?-
phenylenediamine antiozonant. They concluded that, although a number of O3-rubber
reactions and mechanisms are possible, these reactions do not become significant until the
antiozonant is nearly completely consumed (i.e., the antiozonant preferentially reacts with the
O3). They concluded that the "scavenger-protective film mechanism" is primarily responsible
for antiozonant protection.
In addition to reactive antiozonants, paraffinic and microcrystalline waxes are used
to protect the elastomers in rubber products such as tires. The wax migrates to the surface of
the rubber and forms a barrier against O3 attack. Dimauro et al. (1979) studied the ability of
18 waxes to protect rubber against degradation from O3. Dimauro found that no wax by itself
provided an optimal level of protection; blending with a reactive antiozonant was required.
The paraffinic waxes protected best at lower exposure temperatures, and the microcrystalline
waxes were more effective at higher temperatures. Wax blends, which combine the best
effects of each type of wax, offered the best protection over a wide range of temperature
(Lake and Mente, 1992). It was found, however, that wax alone can be detrimental to
dynamic O3 resistance. Wax can induce localized stresses in the rubber that can lead to
premature rubber failure under dynamic testing conditions.
5.10.2.2 Textile Fibers and Dyes
Cellulose-based, acrylic, and nylon fibers are affected by O3 (Zeronian et al.,
1971); however, it is difficult to distinguish O3-induced damage from oxidation by molecular
oxygen. Reduction in breaking strength and an increased rate of wear are the types of
damage most commonly observed. As stated by Bogaty et al. (1952), however, for most uses
of textile fibers, the action of O3 is less important in affecting product lifetime than are
physical abrasion, biological degradation, soiling, fashion, and other factors. Furthermore,
most textiles are used and spend most of their life indoors, where O3 concentrations are
usually less than outdoor O3 concentrations (Yocom et al., 1986). Accordingly, the economic
significance of O3 damage to textile fibers is relatively low, and the differences in the
mechanisms of attack are not important.
Many textile dyes react with O3. Figure 5-38 illustrates the reaction of Disperse
Blue No. 3 with O3 and with NOX (Haylock and Rush, 1976). Ozone attacked the quinoid
portion of the molecule, completely rupturing the ring system chromophore and oxidizing the
dye to phthalic acid, which is colorless. Matsui et al. (1988) investigated the reactions of
O3 with aromatic azo compounds. Ozone was found to attack both the aromatic rings and the
more electron-rich nitrogen atoms. Both the direct attack on the azo dye structure and the
production of daughter products alter the original dye color.
The reactions between various dyestuffs and O3 are influenced by the chemical
nature of the fiber to which the dye is applied and the manner in which the dye is applied.
Additional factors include the presence of protective agents; effects of temperature, air
moisture, and other pollutants; and even the degree of strain of the base fiber caused by
folding or creasing. In a study of O3 fading of anthraquinone dyes on nylon, Haylock and
5-255
-------
O NH
Nitrogen
Oxides
9 OH
Disperse Blue No. 3
Figure 5-38. Reaction of anthraquinone dyes with ozone and with nitrogen oxides.
Source: Hay lock and Rush (1976).
Rush (1976, 1978) found that fiber properties such as cross-section shape, draw ratio, and the
degree of steam heat setting had significant effects on the rate and severity of O3 damage,
even for chemically identical systems. Moore et al. (1984) found that the rate of O3 fading of
acid and disperse dyes on polyamide fibers appeared to be a function of the rate of dye
migration to the surface of the fibers. Thus, using dyes that diffuse slowly
(high-molecular-weight dyes) improved resistance to O3 fading. Given this complexity and
sensitivity for both dye and fiber type, it is not possible to relate a specific mechanism of
damage to a broad class of damage situations.
5.10.2.3 Paint
The mechanisms of architectural paint and coil coating damage caused by O3 have
not been well defined. Damage is probably related to oxidation of the organic binders that
hold the pigment and form the protective seal over the surface. Damage is likely to be
similar to that of elastomers; that is, embrittlement and cracking as the result of chain scission
and cross-linking. The data available on O3 damage to architectural paints, however, come
primarily from studies of surface erosion caused by gaseous pollutants, and the suspected
O3 damage patterns (embrittlement and cracking) are not quantified. Because the polymeric
structure of dried paint film is significantly different from that of an elastomer under
elongation stress, direct comparisons should be made with great caution.
5-256
-------
In a series of experiments (Shaver et al., 1983; Grosjean et al., 1987, 1988a,b,
1989) the direct attack of O3 on artists' pigments and paints was investigated. Ozone was
found to react with alizarin pigments, indigos, curcumin, and triphenylmethane colorants. The
exact mechanism and site of the attack (e.g., carbon-carbon unsaturated bonds, aromatic rings,
or carbon-nitrogen bonds) and subsequent reactions with the daughter products depended on
the initial structure of the pigment. Often the products of these reactions were colorless or of
a noticeably different color than the original pigments, resulting in fading or color changes.
5.10.3 Exposure-Response Data
Laboratory exposure-response studies are criticized for their reliance on artificial
environments that do not contain all the critical variables encountered under ambient
conditions. Scientists realize the limitations of laboratory tests; no model could simulate
conditions identical to an ambient environment. Nevertheless, many laboratory tests have
represented the outdoor environment to some extent, and the findings from these tests have
been used in conjunction with field tests to estimate the nature and amount of damage to
materials. Controlled field tests have the advantage of being carried out under real exposure
conditions, but, because of the highly variable nature of real exposure conditions, data
interpretation is difficult.
5.10.3.1 Elastomer Cracking
Table 5-40 presents an overview of the available laboratory and field studies of the
effects of O3 on elastomers. Hofmann and Miller (1969) demonstrated correlations between
laboratory tests and the actual service use of passenger vehicle tires in the Los Angeles area.
Basically, three laboratory test methods were used: (1) indoor and outdoor belt flex,
(2) indoor and outdoor wheel, and (3) stress relaxation. The investigators found that the
behavior of rubber exposed to O3 under laboratory conditions correlated well with the service
behavior of tires in localities where atmospheric O3 concentrations were high.
Bradley and Haagen-Smit (1951) evaluated a natural rubber (NR) formulation for
susceptibility to O3 cracking. Strips were strained approximately 100% by bending and then
exposed in a small chamber to 20,000 ppm of O3; these specimens cracked almost
instantaneously and broke completely within 1 s. When these NR formulations were exposed
to lower concentrations of O3 (approximately 0.02 to 0.46 ppm), time periods of about 5 min
to over an hour were required for cracks to develop.
Meyer and Sommer (1957) exposed thin polybutadiene specimens to constant load,
ambient room air, and O3. Specimens exposed in the summer to average O3 concentrations of
about 0.048 ppm broke after 150 to 250 h. In the fall, at average O3 concentrations of
0.042 ppm, specimens failed after exposures of 400 to 500 h. In the winter, at average
O3 concentrations of 0.024 ppm, failures occurred between 500 and 700 h. These data show
the strong dependence of breakage on O3 dose over the average time of exposure at which
failure occurred (average C x T).
Edwards and Storey (1959) presented data demonstrating the O3 resistance of two
styrene-butadiene rubber (SBR) compounds (Polysar S and Polysar Krylene). Both
compounds were exposed with and without different levels of antiozonant protection to
0.25 ± 0.05 ppm of O3 at 120 °F (49 °C) under 100% strain (twice the original sample
length). Without antiozonants, a linear relationship was found between O3 dose (ppm-h) and
5-257
-------
Table 5-40. Laboratory and Field Studies on Effects of Ozone on Elastomers3
03
Conditions
Laboratory/
field
Laboratory
Field
Laboratory
Laboratory
Laboratory
Material/
Product Pollutant
Automotive Ozone
tires
Ambient air
Vulcanized Ozone
rubber strips
Rubber tires Ambient air
and various
polymers
SBR: Plysar S Ozone
and Plysar
Krylene, with
and without
antiozonants
White sidewall Ozone
tire specimens
Polyisoprene Ozone
Concentration, Environmental Dose,
(ppm) Exposure Variables (ppm-h)
0.25 to 0.5 NA Tires under stress —
0.04 >1 year Los Angeles >350
(annual environment;
average) actual service use
0.02 to 0.46, 3 to 65 min Physical stress -0.02 to 0.03
20,000
0.023 to 150 to 700 h Physical stress 9 to 20
0.048 and ambient
environment
0.25 19 to 51 h 120 °F, 4.75 to 12.75
100% strain
0.05 to 0.5 250 to 1,000 h 10 and 20% 20 to 500
strain
0 to 1.8 2h 22 °C Up to 3.6
Effects
Cracking of white
side wall.
Positive
correlation
between laboratory
and ambient air
tests.
Surface cracking.
Time of cracking.
Percent
antiozonant was
related
to cracking depth
rate.
Mean cracking
rates were
determined for
different stress and
O3 levels.
Cracking and
stress relaxation.
Comment
Purpose was to correlate lab
and field tests. Exposure
time, detailed pollutant
measurements, and statistical
analyses were not reported.
Test was designed to establish
dose/response curves on
O3-sensitive rubber for use as
an analytical method.
Cracking occurred over a
broad range of values and was
related to stress.
Demonstrated dose/response
linear relationship for O3 on
unprotected rubber.
Detailed data not available to
verify author's statement that
2 to 5 years of ambient
conditions were required for
O3 cracks to penetrate cord
depth.
Rate of attack rapid and
proportional to
O3 concentration.
Reference
Hofmann and
Miller (1969)
Bradley and
Haagen-Smit
(1951)
Meyer and
Sommer (1957)
Edwards and
Storey (1959)
Haynie et al.
(1976)
Razumovskii
et al. (1988)
-------
Table 5-40 (cont'd). Laboratory and Field Studies on Effects of Ozone on Elastomers3
Oi
k
Oi
CD
Material/
Conditions Product Pollutant
Laboratory Ten different NR, Ozone
SBR, and CR
formulations with
and without
protection
Laboratory Natural rubber, Ozone
epoxidised rubber,
and copolymers
Laboratory Several NR/SBR Ozone
blends, with and
without protection
Laboratory Tire cords Ozone
(66 nylon; Dacron
polyester; Kevlar
aramid)
"See Appendix A for abbreviations and acronyms.
Concentration Environmental Dose
(ppm) Exposure Variables (ppm-h)
0.5 Up to 300 h 30 °C Up to 50
0.05 to 1,000 To 16 h -20 to 70 °C, 0 to 240
10 to 100% strain
0.05 to 0.15 ~3 to 16 h Sunlight, humidity -0.15 to 2.4
0 to 1.5 Oto48h UV light; heat Up to 72
(100 °C); RH
(20 to 90%); NO2
Effects
Time to 10 to 20%
relaxation.
Time to first cracking.
Interply adhesion
affected at 0.05 ppm and
above.
RFL adhesion loss
occurred primarily during
6-h exposure to high RH
and 0.2 ppm O3.
Comment
Both formulation and
protection affected
relaxation.
Temperature
dependence of
antiozonant protection.
Both waxes and
antiozonants needed for
protection against
sunlight plus O3.
Synergism between O3
and RH; RFL
deterioration occurred
at surface.
Reference
Ganslandt and
Svensson
(1980)
Lake and
Mente (1992)
Davies (1979)
Wenghoefer
(1974)
-------
cracking depth. Increasing the amount of antiozonants significantly reduced the rate of
cracking for both rubber compounds in a dose-related manner.
Haynie et al. (1976) conducted a chamber study to evaluate the effects of various
pollutants, including O3, on several materials. In one part of the study, white sidewall
specimens from a top-quality, steel-belted radial tire were exposed (strained at 10 and 20%)
for 250, 500, and 1,000 h to O3 concentrations of 0.082 ppm (160 |ig/m3) and 0.5 ppm
(1,000 |ig/m3). The O3 level was found to be statistically significant in the rate of cracking of
this rubber; however, cracking rates were not directly proportional to O3 concentrations for
these two levels. Using the mean cracking rate calculated after long-term (1,000-h) exposure
to conditions representative of the primary air quality standard for O3 and the annual average
standard for NO2, Haynie et al. (1976) concluded that it would take a minimum of 2.5 years
for a crack to penetrate to the cord depth. For this particular premium tire, therefore, sidewall
failure from O3 damage does not appear to be the cause of reduced tire life. Tread wear,
rather than sidewall failure, probably determines the life of a typical rubber tire.
Razumovskii et al. (1988) studied the decrease in stress (stress relaxation) of
polyisoprene vulcanizates in an exposure chamber at 22 °C at five O3 concentrations ranging
from O3- free to 3,450 |ig/m3 (1.76 ppm). Stress relaxation resulting from the growth of
surface cracks caused irreversible changes in the dimension of the elastomer and decreased
tensile strength. Figure 5-39 presents the rate of change of stress as a function of time for
various O3 concentrations. The rate of stress reduction was proportional to O3 concentration,
with virtually no change for the O3-free samples and progressively more rapid relaxation as
O3 levels increased. Razumovskii et al. (1988) concluded that O3 absorption, attack of the
C=C bonds, cracking, and the resulting stress relaxation were fast processes for unprotected
elastomers.
Ganslandt and Svensson (1980) tested 10 different mixtures of three rubber
compounds, NR, SBR, and CR, with the isoelastic force method. The O3 protection afforded
each rubber formulation is summarized in Table 5-41. The samples at 50% elongation were
exposed to O3 concentrations of 0.5 ppm at 30 °C. The time to 10 and 20% relaxation of the
isoelastic force in the rubber test samples was used to gauge the O3 resistance of the
formulation. Compounds GL 2073 B, SS 202, and SS 200 C showed greatest resistance to
the effects of O3, and those formulations that were unprotected (GL 2073 D, SS 200 B,
SS 202 A, SS 203) and the formulations protected only by paraffin wax (GL 2073 G)
demonstrated the least resistance to O3 attack. The testing showed great variety in the kinds
of visible cracking effects as a result of the exposure. The compounds with no protection
often showed a large number of small cracks over the entire surface of the material, but those
compounds protected by a combination of wax and antiozonant or by wax alone sometimes
showed only a single crack, which grew rapidly. These effects are demonstrated in Figure 5-
40. Compounds SS 202 B (Figure 5-40A) and SS 200 C (Figure 5-40B), both protected with
wax and antiozonant, showed fairly good resistance when gauged by the 10 and 20% stress
relaxation tests but failed after approximately 50 and 58 h of exposure, respectively. On the
other hand, compounds SS 203 and SS 200 B, both unprotected, exhibited small surface
cracking and outlasted some of the protected compounds. Moreover, protection with wax and
antiozonant may afford long-term protection, but when one crack appears, it can grow rapidly
and cut off the test piece, as shown in Figure 5-40b.
5-260
-------
15 30
45 60 75
Time (min)
90 105 120
Figure 5-39. Relative decrease in stress (Ap) with time as a function of ozone
concentration for polyisoprene vulcanizate.
Source: Razumovskii et al. (1988).
Table 5-41. Protection of Tested Rubber Materials3
Protected
Rubber Formulation
GL 2073 (NR)
SS 200 (NR)
SS 202 (SBR)
SS 203 (CR)
Mixtures
B, C
D
G
A, C
B
A
B
Unprotected
X
X
X
X
Wax
X
X
X
X
Antiozonant
X
X
X
aSee Appendix A for abbreviations and acronyms.
Source: Ganslandt and Svensson (1980).
5-261
-------
o
o
s\
4
£
O
1
-------
Lake and Mente (1992) exposed natural rubber, epoxidised rubber, and two
acrylonitrile-butadiene copolymers with chemical antioxidants, waxes, or a combination of
antioxidants and waxes to a variety of O3 concentrations and temperatures in environmental
testing enclosures. Ozone concentrations ranged from 0.05 ppm to 1,000 ppm with
temperatures from -20 to 70 °C. Samples were kept under constant strain between 10 and
100%. Antiozonant chemicals in the concentration range from 2 to 20 p.h.r. (parts per
hundred of rubber by weight) were tested, and wax/antiozonant combinations at 6 p.h.r. wax
and 3 p.h.r. antiozonant also were tested. Lake and Mente found that O3 protection was most
effective at higher temperatures, when diffusion of the antiozonant and wax to the surface of
the elastomers was most rapid. This relationship is fortunate because ambient
O3 concentrations correlate well with higher temperatures. Antiozonants became generally
less effective as temperatures dropped; however, dialkyl paraphenylenediamine provided
reasonable protection for natural rubber to -17 °C.
Davies (1979) reported on the effects of O3 and other environmental factors on
interply adhesion of natural and synthetic rubber compounds. Excellent adhesion of plies is
essential to the proper manufacturing of tires. The rubber strips must make interlocking
contact at the joint boundary, or the strength of the tire will be inadequate. Ozone attack on
synthetic poly isoprene and polybutadiene produces a surface layer of ozonides. With NR,
the film consists of ozonides and carbonyl groups (Andries and Diem, 1974; Andries et al.,
1979). The results of the Davies (1979) tests indicated that, before curing, the adhesion of
SBR compounds is unaffected by exposure to O3 concentrations of 0.15 ppm, but the
adhesion of the NR/SBR blend decreases by approximately 30%. Large reductions (on the
order of 70%) in adhesion between plies were noted with the NR compounds; even exposure
for a few hours at 0.05 ppm reduced adhesion considerably. The adhesion tests on cured NR,
SBR, and isoprene rubber (IR) compounds after exposure to various levels of O3 and
humidity are summarized in Table 5-42. The adhesion of the SBR compound is superior to
that of the other two compounds, which were affected greatly by increased RH.
Table 5-42. Effect of Ozone and Humidity on Interply Adhesiona'b
Compound
NR
IR
SBR
Initial
Adhesion
5
5
5
0.15 ppm O3
(294 |ig/m3),
30% RH
2 to 3
4 to 5
4 to 5
Final Adhesion0
0.25 ppm O3
(490 |ig/m3),
30% RH
1
2 to 1
3 to 4
0.15 ppm O3
(294 |ig/m3),
60% RH
1
1
3 to 4
a Adhesion is rated from 1 (bad) to 5 (excellent), based on visual scale standardized by the authors.
bSee Appendix A for abbreviations and acronyms.
°A11 exposures were 16 h in duration.
Source: Adapted from Davies (1979).
5-263
-------
Wenghoefer (1974) studied the effects of O3 on adhesion of tire cords dipped in
resorcinal-formaldehyde latex (RFL). Many fibers and dip formulations were studied to
determine their sensitivity to O3, humidity, NO2, UV light, and heat. Wenghoefer exposed
these materials at a constant temperature of 100 °F (37.8 °C) to O3 levels that varied between
0 and 1.5 ppm (0 and 2,940 |ig/m3) and to RH levels ranging from 20 to 90%. Adhesion
deteriorated from changes in surface properties of the RFL-dipped cords as a result of
exposure to O3, humidity, UV light, and heat. The adhesion losses from O3 and the combined
effects of O3 and humidity were most notable in the first 6 h of exposure. The detrimental
effects of heat, NO2, and the synergistic interaction of NO2 and humidity were much less
pronounced.
5.10.3.2 Dye Fading
Color fading of certain textile dyes has been attributed to the effects of ambient
O3. Although NO2 was originally identified as the pollutant most important to color fading,
the effects of O3 were noted by Salvin and Walker (1955). The primary products affected
were permanent-press garments (polyester and cotton) and nylon carpeting. Table 5-43
summarizes studies on the effects of O3 on dyes. By using a combination of laboratory
chamber studies and outdoor exposures, Salvin and Walker (1955) demonstrated that O3 was
responsible for dye fading observed on drapery fabrics. Blue anthraquinone dyes and certain
red anthraquinone dyes were markedly bleached after exposure to just 0.1 ppm of O3. Azo
red and yellow dyestuffs and diphenylamine yellow dyes were shown to be resistant to fading
at these concentrations, also confirming the results of the field study. The use of known
antiozonants, such as diphenyl-ethylenediamine and diallyl phthalate, in combination with
disperse blue dyes, was effective against O3 fading, thus providing additional evidence of the
effects of O3 on dyed fabrics.
Ajax et al. (1967) summarized the results of a study of 69 dye-fabric combinations
that were exposed outdoors in light-free cabinets at 11 sites. These sites were Sarasota, FL;
Phoenix, AZ; Cincinnati, OH; and four urban-rural combinations: (1) Chicago and Argonne,
IL; (2) Washington, DC, and Poolesville, MD; (3) Los Angeles and Santa Paula, CA; and (4)
Tacoma and Purdy, WA. Among those fabrics exhibiting a high degree of fading at both
urban and rural sites in the first 6 mo, fading was much greater at the urban sites than at the
rural sites. The samples exposed in Phoenix, Sarasota, and Purdy showed the lowest amount
of fading, which indicated that humidity and temperature are not, by themselves, the primary
factors in fading. The highest fading rates occurred in samples exposed in Los Angeles,
Chicago, and Washington, DC. In addition, there was a marked seasonal variation in the test
results, with greater fading during the spring and summer seasons. Generally, the results
correspond with seasonal peaks in O3 concentrations.
Ajax et al. (1967) also exposed the fabrics to irradiated and nonirradiated auto
exhaust, with and without SO2, for 9 h/day for 6 consecutive days. From the results of this
chamber study, the investigators noted that "photochemically produced by-products of
automobile exhaust are a prime cause of fading compared to fading caused by nonirradiated
auto exhaust or by clean air with sulfur dioxide added." In the presence of SO2, however, a
more than additive effect was seen in the dye-fading tests for both chamber and field studies.
Although the conclusions of Ajax and co-workers concerning O3 itself are easily substantiated
in the research literature, the O3 levels measured in their test chamber are questionable. The
daily 9-h average O3 concentrations (measured by neutral-potassium
5-264
-------
Table 5-43. Laboratory and Field Studies of the Effects of Ozone on Dye Fading3
en
M
O)
Oi
Dye
Blue and red
Disperse
Direct, fiber
reactive vat,
sulfur, azo
Disperse
Disperse, basic
Disperse, acid
Direct
Premetolized, acid
Direct red 1
Reactive red 2
Sulfur green 2
Azoicb red
Direct red 1
Acid red 151
Acid yellow 65
Acid violet 1
Basic red 14
Basic yellow 1 1
Acid orange 45
Disperse blue 3
Disperse blue 3
Disperse blue 3
Disperse blue 27
Disperse blue 27
AATCC O3 ribbon
Fabric
Drapery
Cellulose acetate
Cotton
Polyester
Orion
Nylon taffeta
Viscose
Wool
Cotton
Cotton
Cotton
Cotton
Rayon
Wool
Wool
Wool
Acrylic
Acrylic
Nylon
Nylon
Cellulose
Acetate
Acetate
Polyester
Acetate
Concentration Environmental
(ppm) Exposure Variables Effects
0. 1 — — Both dyes were markedly
bleached. No fading
occurred when antioxidants
were added.
Laboratory 54 h Light-proof cabinets, Photochemical agents
0.02 to 0.55; 3 mo 11 rural and urban caused more fading than
field exposure sites nonradiated samples.
concentrations Urban locations produced
not reported more fading, and
temperature and humidity
are not the primary causes
of fading.
0.05 12 weeks Temperature = 55 °F, Induced fading at both
0.5 90 °F levels, but at a nonlinear
RH = 50%, 90% rate. Both temperature and
humidity increased fading
rate, and RH was more
important. Eight of the
tested fabric-dye
combinations faded
measurably in response to
O3. Only trace amounts of
fading occurred in the
remaining fabrics.
Comments
Insufficient data for
dose-response
determinations. This
study followed a field
study showing that
oxidants other than
NOX caused fading.
Both laboratory and
field measurements.
Reported laboratory
O3 concentrations
questionable. SO2
was also present in
laboratory exposures.
Insufficient data to
show detailed dose-
response relationships.
Although samples
were measured
throughout the
exposure, only the
12-week data were
presented.
Reference
Salvin and Walker
(1955)
Ajax et al. (1967)
Beloin (1973)
-------
Table 5-43 (cont'd). Laboratory and Field Studies of the Effects of Ozone on Dye Fading3
Dye
Olive I and II
Disperse blue
Fabric
Nylon fibers
Nylon fibers
Concentration
(ppm)
0.2
0.9
Exposure
1 to >6 h
Environmental
Variables
RH = 70 to 90%
Temperature = 40 °C
Effects
Visible fading in
Olive I after 16 h at
Comments
Both RH and O3
concentration affected
Reference
Haylock and Rush
(1976)
3 and 7
70% RH; same effect
after 4 h at 90% RH.
Linear increase in
fading at 0.9 ppm O3.
Disperse blue dye in Nylon 6 yarn
Ql an avocado green
|sj mixture
O)
O) 2 Disperse dyes and Nylon 6 and Nylon 66
2 acid dyes carpet
Disperse blue 3 Nylon 6 yarn
0.5
0.2
3 mo to 3 years
2 to 120 h
RH = 85%
Temperature = 40 °C
28 homes in different parts
of the country
RH = 65%, 85%, and 90%
Temperature = 40 °C
fading and in a nearly
linear fashion. Sleeve
form was more
susceptible than skein
form. Haylock and Rush
(1976) found that:
(1) increased fiber draw
ratio reduced fading;
(2) increased heat-setting
temperature increased
fading; and increased
fiber surface area
increased fading.
Fading was closely Insufficient data for dose- Huevel et al. (1978)
correlated with fiber response relationship
surface area (diameter), determinations.
Geographic and
seasonal variation in
fading.
Nearly linear increase
in fading with time.
RH had a major
influence on fading
rate.
Field study.
This study focused more
on mechanisms of O3
fading than on dose-
response relationships.
Nipe (1981)
Kamath et al. (1983)
Disperse, basic
Disperse
Direct vat, sulfur,
fiber reactive
Disperse
Disperse, acid
Direct
Acid, mordant
Acrylic
Cellulose acetate
Cotton
Polyester
Nylon
Viscose rayon
Wool
— 2 years in 3-mo Light-proof cabinets, Two-thirds of samples Field study.
blocks eight rural and urban sites exhibited substantial
fading, O3 was
significant for
eight fabric/dye
combinations.
Beloin (1972)
-------
Table 5-43 (cont'd). Laboratory and Field Studies of the Effects of Ozone on Dye Fading3
Dye
Disperse blue 3
Acid blue 25
Acid blue 40
Acid blue 45
Acid blue 80
Acid blue 127
Royal blue
Red
Plum
"See Appendix A for
""Coupling component
01
O)
Concentration
Fabric (ppm) Exposure
Nylon 6 yarn 0.2 0 to 96 h
Nylon 66 yarn
Drapery fabric 0.5 and 1.0 250 to 1,000 h
Rayon acetate
Rayon acetate
Cotton duck
abbreviations and acronyms.
2, azoic diazo component 32.
Environmental
Variables Effects Comments
RH = 85% Fading proceeded Study of mechanisms
Temperature = 40 °C consistent with of O3 fading, follow-
diffusion of dye to fiber on the Kamath et al.
surface. (1983).
50 and 90% RH, NO2 O3 was not a Laboratory study.
and SO2. statistically significant
cause of fading.
Reference
Moore et al. (1984)
Haynie et al. (1976)
-------
iodide and a Mast instrument) were identical for UV-irradiated and nonirradiated exhaust
(0.02 ppm); irradiated exhaust plus SO2 produced 0.55 ppm of O3.
Beloin (1972, 1973) investigated the effects of air pollution on various dyed
textiles by conducting field and controlled-environment laboratory studies. For the field
study, a wide range of dyed fabric was exposed in light-tight cabinets at the same four urban-
rural combined sites used in the Ajax studies. The study was carried out over a 2-year
period, in eight consecutive 3-mo, seasonal exposure periods. Color-change data and air
pollution and weather measurements were analyzed to identify the factors that caused fading.
About two-thirds of the fabrics studied showed appreciable fading. Most of these fabrics
faded significantly more at urban sites than at rural sites. The small amount of fading
evidenced by the samples exposed at extreme temperatures or humidity indicated that these
factors, by themselves, have no effect on fading. The samples also showed some seasonal
variations in fading. In areas of high oxidant concentration, maximum fading occurred
primarily in summer and fall. Fabrics exposed in Chicago, where SO2 concentrations are
higher in the winter, showed greater fading during this season.
The results of the outdoor fading study were used in a multiple regression analysis.
The analysis focused on 25 fabric dye samples, 23 of which showed SO2 to be a significant
variable. Ozone was also a significant contributor to the fading of eight dyed fabrics, as was
NO2 to the fading of seven dyed fabrics. The dominance of SO2 as a factor in fading may
have been complicated by soiling.
Beloin's laboratory study was designed to assess the effects of air pollutants,
temperature, and RH on the colorfastness of 30 samples selected from those exposed during
the field study. Fabric samples were exposed to two concentrations of O3: 0.05 and
0.50 ppm. The laboratory studies demonstrated that high O3 levels produced more significant
fading in more fabric samples than did low levels. Visible fading did occur in about one-
third of the sensitive fabrics (cellulose acetate, viscose, and cotton muslin with red and blue
dyes) exposed to O3 concentrations of 0.05 ppm. These levels are similar to those frequently
found in metropolitan areas. The laboratory study also demonstrated that high RH (90%) is a
significant factor in promoting and accelerating O3-induced fading.
Haynie et al. (1976) and Upham et al. (1976) reported on the degree of fading of
three different drapery fabrics exposed in a laboratory chamber to combinations of high and
low O3 concentrations (0.5 and 0.1 ppm, respectively), high and low RH (90 and 50%,
respectively), and high and low concentrations of NO2 and SO2. The three commercially
obtained fabrics selected for this study were royal blue and red rayon-acetates and a plum
cotton duck. The samples were exposed in the chamber for periods of 250, 500, and 1,000 h;
the degree of fading was measured with a color difference meter. The fading of the plum-
colored material was related statistically to RH and the NO2 concentration. For the red and
blue fabrics, only RH appeared to be a significant factor. The effects of concentrations of O3
on the amount of fading of these dyes were not statistically significant, even after exposure
for 1,000 h to 0.5 ppm, levels much higher than typical ambient exposures.
Haylock and Rush (1976, 1978) studied the fading of anthraquinone dyes on nylon
fibers. In the first test, nylon carpet yarn dyed with Olive I (0.081% Celliton Pink RF,
0.465% Celliton Yellow GR, 0.069% Celliton Blue FFRN) and Olive II (0.082% Latyl Cerise
Y, 0.444% Celliton Yellow GA, 0.143% Cellanthrene Blue CR) was exposed to varying
levels of temperature, RH, and O3. Material dyed with Olive I and exposed at 70% RH, 40
°C (104 °F), and 0.2 ppm of O3 showed visible fading after 16 h of exposure. At 90% RH,
similar fading occurred in less than 4 h. Under the same RH and temperature conditions,
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increasing the O3 concentration from 0.2 to 0.9 ppm resulted in a corresponding increase in
fading. Samples in knitted sleeve form demonstrated much greater susceptibility to O3 attack
than samples in skein form.
Using Disperse Blue 3 and 7 dyes exposed to constant conditions of 40 °C
(104 °F), 90% RH, and 0.2 ppm of O3, Haylock and Rush (1976) investigated the effect on
fading of changing the fiber cross section, the fiber-draw ratio, and the method of setting the
nylon fibers with steam heat. They found that increasing the surface area of the fibers
resulted in an increased fading rate. Increasing the fiber draw ratio reduced dye fading, and
increasing the heat-setting temperature decreased resistance to fading in disperse dyes.
The effect of high temperature and high humidity for induction of O3 fading in
nylon was confirmed further by the additional work of Haylock and Rush (1978). Their
studies showed a good correlation between accelerated O3 fading in the laboratory and in
outdoor, in-service exposure, during which temperature and humidity extremes were common.
Control samples exposed indoors, however, where temperatures and humidities were lower,
did not exhibit nearly the same magnitude of fading as the laboratory samples.
Huevel et al. (1978) investigated the importance of the physical nature of Nylon
6 yarns on the O3 fading behavior of a disperse blue dye. Samples of Nylon 6 yarns dyed
avocado green with a dye mixture including Disperse Blue 3 were exposed in a laboratory
cabinet to 0.5 ppm of O3 at 40 °C and an RH of 85%. Huevel et al. found that the
microfibril diameter and specific surface area of the fiber were the fiber characteristics most
closely related to O3 fading, thus confirming suspicions expressed earlier by Salvin (1969).
Nipe (1981) summarized the results of a 3-year study to establish the relationship
between in-service fading of carpets in a home versus O3 fading as determined by the
American Association of Textile Chemists and Colorists (AATCC) Standard Test Method
129, "Colorfastness to Ozone in the Atmosphere Under High Humidities." (Measurements
also were taken to compare the fading caused by NOX.) The test carpets were made of Nylon
6 and 66 dyed with two disperse and two acid dye formulas. Test samples from the homes of
28 participants were returned every 3 mo for the 3-year period. The exposure sites selected
for this long-term study represented variations in home heating and cooling, utilities, climate,
and geographical locations. The carpet samples were placed in areas as close as possible to
the kitchen but away from exposure to sunlight or any traffic. No measurements of O3
concentrations were collected; however, an O3-sensitive sample strip was included with each
carpet sample. Analysis of the sample strip enabled the researchers to determine the relative
O3 exposure of each carpet sample.
Geographical location appeared to have a significant effect on fading. Test
samples from sites in the Southeast and Northeast showed far more O3 fading than did those
in the West and Far West. Test samples in homes with air conditioning exhibited less fading
during the summer than those without air conditioning. In all samples, much greater fading
was caused by O3 during July, August, and September than in January, February, and March.
Typically, O3 levels indoors are higher during the summer, when doors and windows are more
likely to be open, thus allowing a greater exchange between inside and outside air. The
results of the study of in-service interior carpet exposures were compared with the results of
AATCC Test 129. In a sample that performs satisfactorily through 1.08 cycles of
O3 exposure in AATCC Test 129, there is a 98% probability against in-service fading over a
1-year period. A sample that performs satisfactorily through only 0.6 cycles of O3 testing has
only a 90% probability of satisfactory performance after 1 year of in-service exposure.
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Kamath et al. (1983) studied the effect of atmospheric O3 dye fading on nylon
fibers. Prior studies had postulated that O3 does not penetrate into the fiber to destroy the
dye, but instead attacks the dye at the surface of the fiber. Dye then diffuses outward from
the fiber interior because of the concentration gradient set up as the surface dye is destroyed.
Using microspectrophotometry to test this postulated mechanism, Kamath et al. (1983) studied
the diffusion and destruction of C.I. Disperse Blue Dye 3 on Nylon 6 continuous filament
yarn measuring about 45 jim in diameter. With this method, the investigators were able to
generate a dye distribution profile across the cross section of the fiber and to determine the
diffusion coefficient of a dye in the fiber. The fibers were exposed in a controlled
environment to O3 concentrations of 0.2 ppm for 2 to 120 h at a temperature of 40 °C and
RH levels of 90, 85, and 65%. The results of these laboratory studies indicated that RH has a
significant positive effect on fading, that destruction of the dye begins near the surface of the
fiber in the early stages of exposure, and that O3 penetration into the fiber may be an
important mechanism in O3 fading. The dependence of fading rates on humidity was substan-
tial. Even slight rises in humidity from 85 to 90% caused a significant increase in the extent
of fading. At 65% RH, the fading rate drops dramatically. This effect was attributed to the
breakage of hydrogen bonds in the presence of water, which leads to a more open structure
with high segmented mobility; this condition is more favorable to diffusion of O3 and disperse
dyes.
A follow-on study by Moore et al. (1984) used the Kamath et al. (1983) approach
with a variety of dyes, yarns, and treatments. Moore and coworkers used untreated,
phenol-treated, and steam-treated Nylon 6 and Nylon 66 continuous filament yarns, with six
disperse blue and acid blue dyes. Molecular weights of the dyes ranged from MW = 296
(Disperse Blue 3) to MW = 872 (Acid Blue 127). Dyed filaments were exposed to 0.2 ppm
O3 at 40 °C and 90% RH for various periods up to 96 h. For Nylon 6, steam-treated fibers
faded more quickly than untreated fibers, whereas phenol-treated fibers faded less quickly. In
Nylon 66, both treatments increased the rate of dye loss. The authors attributed this effect, at
least in part, to the change in morphology of the treated fibers. Faster fading was attributed
to higher diffusion rates of the dye in the fiber. They also observed that
low-molecular-weight dyes faded faster than high-molecular-weight dyes, again suggesting the
dye mobility within the fiber (rate of diffusion of the dye molecules to the surface of fiber)
played a significant role in the fading process. Cross-sectional analysis of the exposed fibers
showed that most of the dye loss appeared to occur due to reactions at the fiber surface, and
that penetration of O3 into the fiber did not seem to be significant.
Salvin (1969) reported that O3 and, to a lesser extent, NO2 caused dye fading of
cotton-polyester/permanent-press fabrics. As summarized by Dorset (1972), O3 was found to
be the major fading agent, with NOX also capable of causing fading, although to a lesser
extent. Remedial measures to avoid this problem include selecting dyes more resistant to
reaction with O3 and NO2, avoiding the use of magnesium chloride (MgCl2) catalyst in the
permanent-press process, and using different surfactants and softeners. The use of MgCl2 as a
catalyst makes O3-sensitive dyes more sensitive to O3 (Dorset, 1972). When the catalyst is
zinc nitrate, dyes are more washfast and resistant to O3 fading. The use of a zinc nitrate
catalyst appears generally to have eliminated the problem of the prefading of dyes in
permanent-press fabrics from O3 exposure.
Much of the research reported on dye fading is qualitative in nature. Earlier
studies relied on comparisons among various geographical locations and seasonal variations,
with little attention given to actual concentration and exposure characterizations. For several
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of the initial field investigations reported here, neither O3 nor oxidant concentrations were
given; rather, notations such as high versus low or urban versus rural were the only
description of oxidant levels. The few laboratory studies employed, at most, only two
concentrations of O3, making it nearly impossible to derive meaningful exposure-response
relationships. Comparisons among studies are difficult owing to the various dye and fabric
combinations tested. Also, the importance of RH on O3 fading rate confounds comparisons
among many of the studies that did not use the same RH percentages. Despite these
shortcomings, the current body of research clearly demonstrates a strong relationship between
dye fading and O3 exposure. A definitive study to develop exposure-response functions that
covers a broad spectrum of fabric/dye combinations, O3 exposures, humidities, and
temperatures has not been undertaken, although the available literature establishes the likely
significant variables for such a study.
5.10.3.3 Fiber Damage
Sunlight, heat, alternate wetting and drying, and microorganisms are causative
factors in the weathering and deterioration of fabrics exposed outdoors. The influence of
O3 at normal ambient levels is generally small by comparison. Table 5-44 summarizes the
experiments of the effects of O3 on textile fibers.
Bogaty et al. (1952), as part of a program aimed at segregating some of the
elements that cause weathering, carried out experiments to study the possible role of O3 in the
deterioration of cotton textiles. These investigators exposed samples of duck and print cloth
to air containing 0.02 and 0.06 ppm of O3. Samples were exposed both dry and wet and
tested for 50 days. The wet samples were water-saturated once per week, and moisture was
added regularly so that the moisture content of the cloth was never less than 50%. Similar
fabric samples were exposed to similar O3 concentrations with no moisture added, and another
control group was wetted similarly but exposed to clean (O3-free) air. After exposure to O3,
the wetted samples showed a loss in breaking strength of approximately 20%. The wet print
control cloth showed a loss in breaking strength of only half this amount. The study showed
that low levels of O3 degrade cotton fabrics if they are sufficiently moist. Bogaty and co-
workers surmised that an estimated 500 to 600 days of natural exposure might be required to
reach a stage of degradation similar to that caused by a 50-day exposure to O3 alone.
Because unprotected fabrics typically reach a much more advanced state of decay after such
long exposures to weathering, Bogaty and co-workers concluded that the effect of O3 is
slighter than that of other agents. Although not noted by Bogaty and co-workers, the O3 and
increased moisture may have caused the formation of H2O2, which could account for the loss
in breaking strength.
Morris (1966) also studied the effects of O3 on cotton. Samples were exposed in
the absence of light to 0.5 ppm of O3 (more than four times the NAAQS of 0.12 ppm) for
50 days in a chamber maintained at 70 °F (21 °C) and 72% RH. No appreciable effect on
breaking strength was found. Apparently, the moisture content of the cotton was not high
enough to produce the degradation that Bogaty et al. (1952) measured in wet cotton samples,
even though the concentration of O3 was considerably higher.
The laboratory study of Kerr et al. (1969) examined the effects of the periodic
washing of dyed cotton fabrics exposed to O3 and the amount of fading and degradation of
moist, dyed fabrics exposed to O3. They exposed samples of print cloth, dyed with C.I. Vat
Blue 29, in a chamber to a continuous supply of purified air containing O3 concentration
levels of 1 ± 0.1 ppm. The samples were exposed at room temperature (25 °C) in the
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Table 5-44. Laboratory and Field Studies of the Effects of Ozone on Fibers3
Fiber
Cotton
Cotton
Cotton
Modacrylic,
Acrylic,
Nylon 66,
Polyester
Nylon
Concentration
(ppm)
0.02 and 0.06
0.5
1.0
0.2
0.03
Exposure
50 days
50 days
60 days
7 days
Up to 445 days
Environmental
Variables
Cloth, both wet and dry
21 °C, 72% RH
25 °C, periodic washing or
wetting
48 °C, 39% RH,
atificial sunlight, wetting
Exposed in industrial warehouse
Effects
Cyexposed wetted samples had 20% loss of breaking
strength.
No loss of breaking strength.
Washed O3-exposed fabrics had 1 8% loss of breaking
strength.
No effect on modacrylic and polyester. Slightly reduced
breaking strength in acrylic and nylon.
Loss of dyeability.
References
Bogaty et al. (1952)
Morris (1966)
Kerr et al. (1969)
Zeronian et al. (1971)
Makansi (1986)
"See Appendix A for abbreviations and acronyms.
Oi
-------
absence of light, and a shallow container of water was kept on the chamber floor to increase
the humidity. Samples were withdrawn from the chamber after 12, 24, 36, 48, and 60 days.
After an exposure period of 60 days, which included either 20 washing or 20 soaking
treatments, the change in strength of control fabrics was not significant. By comparison, the
fabrics exposed to O3 changed significantly; the loss in strength of the washed fabrics was
18%, and that of the soaked fabrics, 9%. Fading was also evident in the fabrics exposed to
O3 but not in the control samples. Differences in the amount of fading between the washed
and soaked samples were evident, but the reason for the differences was not. Kerr et al.
concluded that washing in hot, soapy water may have affected properties of the dye.
In laboratory studies, Zeronian et al. (1971) simultaneously exposed modacrylic
(dynel), acrylic (orlon), Nylon 66, and polyester (dacron) fabrics to artificial sunlight (xenon
arc) and CF air contaminated with 0.2 ppm of O3 at 48 °C (118 °F) and 39% RH. During
exposure, the fabric samples were sprayed with water for 18 min every 2 h. Ozone damage
was measured by comparing these samples with fabrics exposed to the same environmental
conditions without O3. After exposure for 7 days, Zeronian and co-workers found that O3 did
not affect the modacrylic and polyester fibers. The exposure did seem to affect the acrylic
and nylon fibers slightly by reducing breaking strength. The degree of difference, however,
in the change of fabric properties between those exposed to light and air and those exposed to
light and air containing 0.2 ppm of O3 was not significant.
Ageing of nylon yarns causes a reduction in the dyeability of the yarn. Ageing is
caused by the reaction of amine end groups in the filament skin with O3 and other pollutants
(NOX, SO2, etc.). This phenomenon is well known within the textile trade, and procedures
such as minimizing time from yarn production to yarn dyeing are in place to reduce problems
of ageing. Makansi (1986) investigated the relationship between yarn ageing, as defined by
reduction in dyeability, and pollutant levels in yarn storage warehouses. Makansi assessed the
yarn dyeability with Acid Blue 45 and Acid Blue 122 dyes of exposed test fiber versus
unexposed control samples. Gaseous pollutant concentrations in the warehouse were
estimated either using nearby air quality station data or measured twice weekly during the
tests with commercial sampling tubes (Draeger™ Tubes). Yarn samples were exposed for up
to 1 year of ageing. Makansi found that dyeability decreased proportionally with the
O3 exposure during storage. Dyeability, as weight of dye absorbed for Acid Blue 45,
decreased over 75% for Nylon 66 stored in the warehouse at an average concentration of 0.03
ppm O3. It was not possible to statistically isolate the effects of O3 exposure from other
pollutant exposures for the samples in these tests; thus other factors besides O3 may have
contributed to the loss in dyeability. Makansi suggested that yarns should be dyed as quickly
as possible after manufacture or should be stored in airtight wrappings to prevent ageing.
In general, the contribution of O3 to degradation of fabrics has not been quantified
well. Bogaty et al. (1952) concluded that the effects of other factors (sunlight, heat, wetting
and drying, and microorganisms) far outweighed the effects of O3 on cotton duck and print
cloth. The work by Morris (1966) and Kerr et al. (1969) does point to the synergistic effect
of moisture and O3 as an important ingredient in material degradation, possibly caused by the
formation of a more potent oxidizing agent. Finally, the work of Zeronian et al. (1971) also
indicates little if any effect of O3 on synthetic fibers. Thus, it appears that O3 has little if any
effect on textiles, fibers, and synthetic cloth exposed outdoors. Because most fabrics are used
primarily indoors, where they are partially shielded from O3 exposure, O3 damage to textile
fibers is considered an insignificant problem. This was a finding of Murray et al. (1986) in a
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study of material damage and costs in the Los Angeles area, an area with relatively high
ambient O3 concentrations.
5.10.3.4 Paint Damage
A paint surface may suffer several types of damage (including cracking, peeling,
erosion, and discoloration) that affect its usefulness. Of these, erosion (i.e., wearing away of
the paint surface) is the type of damage most often studied with respect to the impact of
gaseous pollutants on architectural and coil-coating finishes. (Coil coatings are industrial,
continuous-dip process finishes typically applied to sheet metal.) Studies of paint cracking
and peeling have focused on the effects of moisture and have not dealt with the possible
influence of ambient pollutants on these types of finishes.
Several damage functions for O3-induced erosion of paint have been reported in the
literature. Such reports are based either on accelerated chamber studies or on long-term
outdoor exposure studies. Unfortunately, all studies to date have shortcomings that render
their results questionable in regard to actual exposures. Damage to a paint surface is the
cumulative effect of the conditions to which the surface is exposed, including various
combinations of temperature, moisture, sunlight, and pollution level. No exposure study to
date has been able to match all factors exactly to separate the impact of O3 from the other
factors. Table 5-45 summarizes the studies of the effect of O3 on architectural and industrial
paint and coating systems.
In a laboratory chamber exposure study, Haynie et al. (1976) exposed oil-based
house paint, latex house paint, vinyl coil coating, and acrylic coil coating to 0.5- and
0.05-ppm concentrations of SO2, NO2, and O3 in various combinations. Statistically
significant effects of O3-caused damage were observed on the vinyl and the acrylic coil
coatings: a positive interaction between O3 and RH on the vinyl coil coating and a positive
direct O3 effect on the erosion rate of the acrylic coil coating. The rate of erosion was low,
however, and both vinyl and acrylic coil coatings were shown to be very durable. A linear
regression for the acrylic coil coating data gives
Erosion rate = 0.159 + 0.000714 O3, (5-2)
where erosion rate is in micrometers per year and O3 is in micrograms per cubic meter.
Although the O3 effect on this coating was found to be statistically significant, it
has no practical significance because the erosion rate is so slow; at 0.12 ppm of O3, the
erosion rate is 0.33 jam/year. At an average annual O3 level of 0.05 ppm, this regression
predicts that a 20-|im-thick coating would last over 80 years.
In a comprehensive study by Campbell et al. (1974), panels painted with different
exterior paints (automotive refmish, latex coating, coil coating, industrial maintenance
coating, and oil-based house paint) were exposed to air pollutants in an environmental
chamber under accelerated weathering conditions. The panels were exposed to low
(0.1 ppm) and high (1.0 ppm) concentrations of O3 and SO2. After exposure, the panels were
examined by measuring erosion, gloss, surface roughness, tensile strength, attenuated total
reflectance (ATR), and the surface effects that were revealed by scanning electron microscopy
and infrared examination. The panels were examined after 0, 400, 700, and 1,000 h of
chamber exposure (considered as equivalent to 0, 200, 350, and 500 days of exposure,
respectively).
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Table 5-45. Laboratory and Field Studies of the Effects of Ozone on
Architectural/Industrial Paints and Coatings3
Paint/Coating Type
Latex house paint
Oil house paint
Vinyl coil coating
Acrylic coil coating
Concentration Environmental
Substrate (ppm) Exposure Variables Effects Comments Reference
Aluminum 0.05 and 0.5 To 1,000 h Chamber exposures with SO2, Very slow erosion of coil
panels NO2, and O3; 50 and 90% RH; coatings.
13 and 35 °C; and artificial
dew and sunlight cycles.
Haynie et al. (1976)
Automotive refmish
Latex
Coil coating
Industrial maintenance
coating
Oil house paint
Latex house paint
Ol Oil house paint
01
Stainless 0.1 and 1.0 To 1,000 h
steel panels
Chamber study with SO2, 70 to Although 1 ppm O3
100% RH, 50 to 65 °C, and
artificial dew and sunlight
cycles.
produced significant
changes in finishes,
0.1 ppm O3 did not produce
statistically increased
erosion.
To 24 mo
Stainless 0.006 to 0.055 3 to 30 mo
steel
Field studies in four sites, rural Erosion greater in urban
to industrial. areas.
Campbell et al. (1974)
Field study.
Effects of O3 not
independently statistically
significant.
No environmental
measurements conducted.
Nine sites around St. Louis. Mansfeld (1980)
"See Appendix A for abbreviations and acronyms.
-------
In general, exposures to 1 ppm of O3 produced greater increases in erosion rates
than did clean air. Concentrations of this magnitude, however, do not represent typical
ambient exposure levels of O3. At the more representative level of 0.1 ppm, O3 did not
produce statistically significant increases in erosion rates. The various finishes produced a
variety of changes for the other measures. Some finishes lost gloss or showed changes in
ATR, but O3 exposure did not produce consistent changes over the suite of finishes examined.
In conjunction with Campbell's chamber studies, field measurements were made of
the erosion of paint from test panels exposed to outdoor environments consisting of a clean,
rural atmosphere (Leeds, ND); a moderately polluted atmosphere (Valparaiso, IN); a heavily
polluted (SO2) atmosphere (Chicago); and a high-oxidant, moderately polluted atmosphere
(Los Angeles). The results of this study showed that paint erosion was much greater in the
polluted areas than in relatively clean, rural areas. The highest erosion rates were observed
for the coil coating and oil-based house paints at the Chicago and Los Angeles exposure sites.
Because meteorology and air quality were not measured at the exposure sites, correlation of
film damage with the environmental parameters was not possible. The study does suggest
that SO2 exerts an adverse effect on exterior paints with calcium carbonate as an extender
pigment. The coil coating and oil house paints were formulated with calcium carbonate.
Oxidants were probably reacting with the organic binder of the coil coating and oil house
paints, although no mechanism for this reaction was developed from this exposure study.
In an outdoor exposure test of the effects of air pollutants on materials, Mansfeld
(1980) exposed latex and oil-based house paints, as well as galvanized steel, weathering steel,
stressed aluminum, silver, marble, and nylon, at nine test sites in St. Louis. In conjunction
with the material exposures, measurements of meteorological parameters, O3, NOX, total
hydrocarbons, total sulfur, SO2, and hydrogen sulfide were made.
Haynie and Spence (1984) analyzed Mansfeld's (1980) St. Louis data, accounting
for covariances among the pollutant and meteorological variables. They analyzed the paint
damage data and found significant correlations of O3 flux with time, temperature, and NO2
flux for the experimental period. Although Haynie and Spence expected O3 to attack the
binder in latex paint, multiple regression analysis showed little dependence of paint erosion
on O3 flux. They speculate that the effects of O3 are masked by the covariance of O3 with
temperature and NOX.
5.10.3.5 Cultural Properties Damage
Ozone-induced degradation of cultural properties (e.g., fine arts paintings)
contributes to the deterioration and, ultimately, to the loss of these unique objects. Many
cultural properties are expected to last indefinitely, and irreversible damage, even at a slow
rate, is considered unacceptable by curators and the art community.
A significant series of tests of the effects of O3 on a variety of artist's pigments
and dyes was reported by Shaver et al. (1983), Grosjean et al. (1987), Whitmore et al. (1987),
Grosjean et al. (1988a,b), Whitmore and Cass (1988), Grosjean et al. (1989), Cass et al.
(1991), and Grosjean et al. (1993). The experiments are summarized in Table 5-46. The
doses of O3 applied during these tests were the equivalent of less than 10 years exposure in a
typical air conditioned indoor environment. Many pigments, notably traditional organic
pigments such as indigo, were found to be very sensitive to O3 exposure. Many of the
affected pigments underwent significant color changes on exposure to O3, and some were
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Table 5-46. Laboratory Studies of the Effects of Ozone on Artists' Pigments and Dyes3
Oi
Pigment Types Substrate Concentration
17 Artists' Paper 0.4 ppm
watercolor
pigments
Alizarin, Silica gel 0.4 ppm
Alizarin crimson, cellulose 0.4 ppm
anthraquinone — —
Teflon 10 ppm
16 Traditional Paper 0.4 ppm
organic colorants
Indigo, Teflon 10 ppm
dibromoindigo,
thioindigo,
tetrachlorothio-
indigo
Curcumin Cellulose, 0.4 ppm
watercolor 0.4 ppm
Paper, silica gel
— —
Teflon 10 ppm
Exposure
95 days
95 days
95 days
—
18-80 h
12 weeks
4 days
95 days
95 days
—
4 days
Environmental
Variables Effects
23 °C
47% RH
22 °C
50% RH
—
24 °C
<40% RH
23 °C
50% RH
24 °C
5%RH
25 °C
50% RH
—
24 °C
<20% RH
Alizarin-based
watercolors were
very sensitive;
other pigments
showed lesser
degrees of fading.
Each pigment
tested faded on all
substrates.
Eleven colorants
were reactive with
O3, three were
possibly reactive.
All indigo,
dibromoindigo
consumed.
Thioindigo and
tetrachlorothioin-
digo were much
less reactive and
still retained much
color.
Faded rapidly on
all substrates,
producing colorless
products.
Comments
Also
investigated
fading on
Japanese wood-
block print.
Presented
possible reaction
mechanisms and
products.
Reference
Shaver et al
(1983)
Grosjean et
(1987)
al.
Whitmore et al.
Presented
possible reaction
mechanisms.
Somewhat
slower fading on
watercolor
paper.
(1987)
Grosjean et
(1988a)
Grosjean et
(1988b)
al.
al.
-------
Table 5-46 (cont'd). Laboratory Studies of the Effects of Ozone on Artists' Pigments and Dyes3
Pigment Types Substrate Concentration Exposure
Traditional Paper, silk cloth 0.4 ppm 12 weeks
Japanese colorants
and dyes
Triphenylmethane Teflon 10 ppm 4 days
colorants
Alizarin crimson Watercolor paper 0.4 ppm 7 days
Oi
isj Various artists' Watercolor paper Mixture 12 weeks
O^J colorants Cellulose 0.2 ppm O3
0.01 ppm PAN
0.08 ppm NO2
Environmental
Variables Effects
22 °C Several organic
50% RH and one inorganic
pigment faded
significantly.
24 °C Found that, although
<20% RH some are not
affected, those
colorants with
unsaturated C-C
bonds may fade.
22 °C Severe fading.
50% RH
16 to 26 °C 11 colorants,
46 to 83% RH negligible changes;
12 colorants,
small changes;
3 colorants,
modest changes;
9 colorants,
substantial changes.
Comments
Also investigated
fading on ca. 1810
Japanese
woodblock print.
Presented possible
reaction
mechanisms.
Framed sample
behind glass
exhibited virtually
no fading.
Reference
Whitmore and
Cass (1988)
Grosjean et
(1989)
Cass et al.
(1991)
Grosjean et
(1993)
al.
al.
"See Appendix A for abbreviations and acronyms.
-------
virtually completely consumed, producing colorless reaction products. Cass et al. (1991)
noted that O3 damage to artwork is proportional to the O3 exposure (C x T). Because
artworks are intended to have long service lives and their appearance is important, fading is
generally considered to be unacceptable, and even low concentrations for long periods of time
can lead to noticeable fading. Grosjean et al. (1987) suggest that formulations of substitute
pigments be developed with O3 sensitivity in mind.
Druzik et al. (1990) investigated the indoor/outdoor O3 concentration ratios at
11 museums, art galleries, and historical houses in the Los Angeles area. They found that the
indoor/outdoor ratio of 8-h average O3 concentrations ranged from 0.10 to 0.87. The ratio
was strongly dependent on the type of building ventilation. Buildings with high air-exchange
rates (about two to three air changes per hour) had the highest indoor/outdoor ratios. Low
exchange rate buildings (ca. less than one air change per hour) and buildings with air
conditioning systems had significantly lower indoor/outdoor O3 concentration ratios.
De Santis et al. (1992) investigated concentrations of SO2, HNO3, HNO2, and O3 as
well as particulate sulfate, nitrate, and ammonium in the Galleria degli Uffizi in Florence for
a 5-day period. Although the museum was equipped with an air conditioning system,
O3 concentrations in the galleries correlated strongly with outdoor O3 concentrations. Indoor
hourly average O3 concentrations ranged from 0.019 to 0.030 ppm. To reduce concentrations
in the galleries, they suggested that the Uffizi's air handling system be upgraded to include
filtration and modified to include less make-up air. Cass et al. (1991) and Grosjean et al.
(1993) suggest that museums design and maintain air conditioning and air filtration systems to
control the concentrations of oxidants in order to protect their collections. Cass et al. (1991)
note that framing behind glass is an effective means of protecting oxidant sensitive pigments.
Grosjean and Parmar (1991) found that activated carbon and Purafil (4% potassium
permanganate on neutral activated alumina) could be used to reduce O3 and oxidant
concentrations in museum display cases.
5.10.4 Economics
5.10.4.1 Introduction
Damage to materials from O3 usually is expressed in terms of one or both of the
following two general classes of costs to producers and consumers: (1) O3-accelerated
replacement and repair costs, as when the service life or aesthetics of a material are impaired,
and (2) increased avoidance costs, as when certain industries (e.g., tires, plastics, paints, dyes,
and fabrics) are obligated to incur expenditures for antiozonant research and development,
substitute processes and materials, additives and formulations, product packaging, advertising,
etc., in order to offset sales losses that otherwise would occur.
In theory, the approach selected should depend on the observed behavior of the
producers and consumers of the materials in question, and the type of damage to which they
are reacting. In practice, the empirical estimates of O3 damage to materials are far from
reliable.
5.10.4.2 Methods of Cost Classification and Estimation
Computation of accelerated replacement is probably the most widely applied
method of estimating the costs of materials damage to air pollutants. In this approach, a
materials damage function is developed to show the increase in physical damage for an
increase in the dose of the pollutant. Then a cost schedule is constructed to show how
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maintenance or replacement schedules are influenced by the pollutant level. Hershaft et al.
(1978) note, however, that this method usually assumes existing inventories and does not take
into account substitutions of materials with more (or less) resistance to pollution. As a result,
this method tends to overestimate the cost of damage from pollutant increases and to
underestimate the net savings realized from pollutant reductions.
A second approach considers avoidance costs. This refers to practices such as
adopting alternative production processes and materials. Some industries add antiozonants to
their products or change the chemical formulation of their output. All of these measures
mitigate the impact of O3 on the service life or aesthetics of the products in question.
Moreover, these measures also require research, development, and implementation
expenditures. As such, estimation of these costs is conceptually and empirically difficult,
since the opportunity to use different materials changes in response to the level of
O3 concentration.
A number of factors complicate the use of both the replacement and the avoidance
methodologies. Data on key variables generally are missing or merely assumed. Lessening
the reliability of the final cost estimates are deficiencies in knowledge of the physical damage
functions; the quantities and types of materials exposed to O3 indoors, outdoors, and in
respective regions of the country; the actual expenditures incurred for increased replacement,
maintenance, and avoidance that can be directly attributed to O3; the threshold O3 damage
levels that prompt mitigating action; and the range of substitution strategies that can be used
to ameliorate degradation. On the last point, few attempts have been made to identify current
technology practices and potential innovations. The variety of rubber compounds, paint
mixtures, and fabric dyes reflects the number of proprietary formulations, and each
formulation presumably has a different response to O3 exposure.
An additional complication is that repair, replacement, and substitution are
frequently dominated by factors unrelated to O3 concentrations. This can lead to spurious
correlations if studies are accepted uncritically. For example, tire replacement may be high in
a given region of the country because of high O3 levels associated with automotive exhaust.
Alternatively, tire replacement may be high simply because the total miles of automotive use
per year are higher in that region than in the nation as a whole.
5.10.4.3 Aggregate Cost Estimates
The important caveats identified in the preceding discussion qualify the empirical
data presented in this and following sections. Table 5-47 summarizes reports of highly
aggregated estimates of oxidant damage of all materials. Unfortunately, there are no known
recognized studies that are more recent than those reported in the table. For purposes of
gross comparison only, where possible, the figures are expressed in 1984 currency equivalents
along with 1970 currency equivalents, the base data for most of the reference studies. The
figures do not, however, represent 1984 supply-demand relationships, production technologies,
or O3 concentrations. It must be emphasized that the costs cited in 1984 currency equivalents
therefore cannot be considered true 1984 costs. Because the data in Table 5-47 are reported
to four significant figures, the accuracy of this information is exaggerated.
Salmon (1970) was among the first to attempt to estimate the annual cost of air
pollution damage to materials. His computation included the dollar value of annual materials
production, a weighted average economic life of each material included in his study, a
weighted average factor for the percentage of the material exposed to air pollution, and a
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Table 5-47. Summary of Damage Costs to Materials by Oxidants
(in millions of 1970 and 1984 dollars)3
Materials Costs
Study Elastomers/Plastics Fabric/Dye All
Barrett and Waddell
(1973)
Mueller and
Stickney (1970)
Salmon (1970)
Salvin (1970)
Waddell (1974)
Yocom and
Grappone (1976)
Freeman (1979)
ND
500.0
(1,500)
295.2
(915)
ND
ND
ND
ND
(260)
ND
358.4
(1,111)
83.5
(259)
ND
ND
ND
(3,878)
ND
653.6
(2,026)
ND
900.0
(2,790)
572.0
(1,773)
505.0
(1,566)
aND = No data; investigator(s) did not develop estimates in this category. 1984 dollars are listed parenthetically.
factor for increased labor to treat damaged materials. Cost was defined as the value of the
material multiplied by the difference between the rate of material deterioration in a polluted
urban versus an unpolluted rural environment. All data, except for annual production levels
of materials, were assumed.
If it is assumed that O3 affected all of the fibers, plastics, and rubber in the study
by Salmon, then annual damage costs attributed to O3 would have been $2.026 billion
(1984$). Salmon did not consider O3-related damage to paint, since the dominant paint-
damaging mechanisms are soiling and gaseous SO2. His costs refer to maintenance and
replacement only, and do not allow for materials protection, substitution, etc.
In discussing other limitations of his study, Salmon cautioned that his estimates
were of potential loss, not of actual observed loss. Despite this and other qualifications that
lessen the usefulness of the figures derived, the Salmon study has been cited extensively and
used quantitatively in a number of the subsequent studies cited here.
For example, the materials estimate by Barrett and Waddell (1973) is based
primarily on the work of Salmon (1970). Barrett and Waddell supplemented this by drawing
on Mueller and Stickney (1970) for damage costs on elastomers and on Salvin (1970) for
damage costs related to dye fading. Combining some of these numbers, Barrett and Waddell
stated that materials damage costs attributable to oxidants alone were $3.878 billion (1984$).
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Freeman (1979) reviewed earlier studies that categorized the cost of damage to
materials. Using the work of Waddell (1974) and Salvin (1970), Freeman calculated that the
materials damage costs attributable to oxidants and NOX were $2.031 billion (1984$). Of this
total, roughly 46% was damage to textiles and dyes (from Salvin, 1970), whereas the
remaining 54% was damage to elastomers (from Mueller and Stickney, 1970). Freeman then
assumed a 20% reduction in oxidant levels since 1970 and concluded that the monetary
benefits of controlling oxidants, oxidant precursors, and NOX were between $170 and
$510 million (1984$). Freeman computed that the savings attributable to oxidant controls
alone were $128 to $383 million (1984$).
Waddell (1974) likewise depended primarily on existing studies to calculate the
national cost of air pollution in 1970. Waddell used Salmon (1970), Salvin (1970), Mueller
and Stickney (1970), and Spence and Haynie (1972) to derive an estimate of $6.820 billion
(1984$) as the total gross annual damage for materials losses in 1970 resulting from air
pollution. The component attributable to O3 and oxidants alone was $2.790 billion (1984$),
within a wide range of $1.550 to $4.030 billion (1984$).
Yocom and Grappone (1976), in work for the Electric Power Research Institute,
estimated that the cost of air pollution damage to materials was about $6.820 billion (1984$)
in 1970. Of this total, O3 was estimated to be responsible for $1.773 billion (1984$), or some
26% of the total.
Because of the reliance of the later studies on the questionable data and unverified
assumptions contained in the earlier ones, the results compared here are of extremely limited
usefulness for cost-benefit purposes. Updated research, using current economic evaluation
approaches, should be undertaken to determine the costs of O3-induced damage.
5.10.5 Summary and Conclusions
More than four decades of research show that O3 damages certain materials. The
materials most studied in O3 research are elastomers and textile fibers and dyes. The amount
of damage to actual in-use materials and the economic consequences of that damage are
poorly characterized.
Natural rubber and synthetic polymers of butadiene, isoprene, and styrene, used in
products like automobile tires and protective outdoor electrical coverings, account for most of
the elastomer production in the United States. The action of O3 on these compounds is well
known, and dose-response relationships have been established and corroborated by several
studies. These relationships, however, must be correlated with adequate exposure information
based on product use. For these and other economically important materials, protective
measures have been formulated to reduce the rate of oxidative damage. When antioxidants
and other protective measures are incorporated in elastomer production, the dose rate for
cracking is reduced considerably, although the extent of reduction differs widely according to
the material and the type and number of protective measures used.
The effects of O3 on dyes have been known for nearly four decades. In 1955,
Salvin and Walker exposed certain red and blue anthraquinone dyes to a 0.1-ppm
concentration of O3 and noted fading, which until that time was thought to be caused by NO2.
Subsequent work confirmed the fading action of O3 and the importance of RH in the
absorption and reaction of O3 in vulnerable dyes. Both the type of dye and the material in
which it is incorporated are important factors in resistance of a fabric to O3. Researchers
found no effects from O3 on royal blue rayon-acetate, red rayon-acetate, or plum cotton.
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On the other hand, anthraquinone dyes on nylon fibers were sensitive to fading from O3.
Field studies and laboratory work showed a positive association between O3 levels and dye
fading of nylon materials. At present, the available research is insufficient to quantify the
amount of damaged material attributable to O3 alone.
The degradation of fibers from exposure to O3 is poorly characterized. In general,
most synthetic fibers like modacrylic and polyester are relatively resistant, whereas cotton,
nylon, and acrylic fibers have greater but varying sensitivities to the gas. Ozone reduces the
breaking strength of these fibers, and the degree of reduction depends on the amount of
moisture present. The limited research in this area indicates that O3 in ambient air may have
a minimal effect on textile fibers, but additional research is needed to verify this conclusion.
The effects of O3 on paint are small in comparison with those of other factors.
Past studies have shown that, of various architectural and commercial paints, only vinyl and
acrylic coil coatings are affected, and that this impact has a negligible effect on the useful life
of the material coated. Preliminary results of current studies have indicated a statistically
significant effect of O3 and RH on latex house paint, but the final results of those studies are
needed before conclusions can be drawn.
A number of artists' pigments and dyes have been found to be sensitive to O3 and
other oxidants. Many organic pigments in particular are subject to fading or other color
changes when exposed to O3. Although most, but not all, modern fine arts paints are
O3 resistant, many older works of art are at risk of permanent damage because of O3-induced
fading. Museums and private collectors should take steps to ensure that susceptible artwork
is protected from O3 exposure.
For a number of important reasons, the estimates of economic damage to materials
are problematic. Most of the available studies are outdated in that the O3 concentrations,
technologies, and supply-demand relationships that prevailed when the studies were conducted
are no longer relevant. Additionally, little was (and is) known about the physical damage
functions, and cost estimates were simplified to the point of not properly recognizing many of
the scientific complexities of the impact of O3. Assumptions about exposure to O3 generally
ignored the difference between outdoor and indoor concentrations. Also, analysts have had
difficulty separating O3 damage from other factors affecting materials maintenance and
replacement schedules. For the most part, the studies of economic cost have not had the
resources to marshal factual observations on how materials manufacturers have altered their
technologies, materials, and methods in response to O3. Rather, the analysts have had to rely
on assumptions in this regard, most of which remain unverified.
It is apparent that a great deal of work remains to be done in developing
quantitative estimates of materials damage from photochemical oxidant exposures. This is not
meant to deprecate the years of research reported in this document, for much has been gained
in refining the initial methodologies used for assessing damage. The current state of
knowledge still can be summarized by the following from Yocom et al. (1985):
"We have learned that some costs may be difficult to quantify either
because they are minimal or because they are overshadowed by other
factors, such as wear or obsolescence. We have learned that damage
functions are complex and are influenced by the presence of other
pollutants and by weather. We have learned that more accurate
estimates of materials in place may be obtained using selective
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sampling and extrapolation. And we have learned that a mere cost-
accounting of damage does not present a true estimate of economic cost
if it does not account for the welfare effects induced by shifts in the
supply-demand relationship."
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References
Abeles, F. B.; Morgan, P. W.; Saltveit, M. E., Jr. (1992) Ethylene in plant biology. 2nd ed. San Diego, CA:
Academic Press, Inc.
Adams, R. M. (1986) Agriculture, forestry, and related benefits of air pollution control: a review and some
observations. Am. J. Agric. Econ. 68: 464-472.
Adams, R. M.; Crocker, T. D. (1989) The agricultural economics of environmental change: some lessons from
air pollution. J. Environ. Manage. 28: 295-307.
Adams, M. B.; O'Neill, E. G. (1991) Effects of ozone and acidic deposition on carbon allocation and
mycorrhizal colonization of Pinus taeda L. seedlings. For. Sci. 37: 5-16.
Adams, R. M.; Rowe, R. D. (1990) The economic effects of stratospheric ozone depletion on U.S. agriculture: a
preliminary assessment. J. Environ. Manage. 30: 321-335.
Adams, H. S.; Stephenson, S. L.; Biasing, T. J.; Duvick, D. N. (1985) Growth-trend declines of spruce and fir in
mid-Appalachian subalpine forests. Environ. Exp. Bot. 25: 315-325.
Adams, R. M.; Hamilton, S. A.; McCarl, B. A. (1986a) The benefits of pollution control: the case of ozone and
U.S. agriculture. Am. J. Agric. Econ. 68: 886-893.
Adams, R. M.; Callaway, J. M.; McCarl, B. A. (1986b) Pollution, agriculture and social welfare: the case of acid
deposition. Can. J. Agric. Econ. 34: 3-19.
Adams, M. B.; Kelly, J. M.; Edwards, N. T. (1988) Growth of Pinus taeda L. seedlings varies with family and
ozone exposure level. Water Air Soil Pollut. 38: 137-150.
Adams, R. M.; Glyer, J. D.; Johnson, S. L.; McCarl, B. A. (1989) A reassessment of the economic effects of
ozone on U.S. agriculture. JAPCA 39: 960-968.
Adams, M. B.; Edwards, N. T.; Taylor, G. E., Jr.; Skaggs, B. L. (1990a) Whole-plant 14C-photosynthate
allocation in Pinus taeda: seasonal patterns at ambient and elevated ozone levels. Can. J. For. Res.
20: 152-158.
Adams, M. B.; Kelly, J. M.; Taylor, G. E., Jr.; Edwards, N. T. (1990b) Growth of five families of Pinus taeda
L. during three years of ozone exposure. New Phytol. 116: 689-694.
Adams, R. M.; Klingeman, P. C.; Li, H. W. (1990c) A bioeconomic analysis of water allocations and fish habitat
enhancements, John Day Basin, Oregon. Corvallis, OR: Oregon State University; U.S. Geological
Survey grant no. 14-68-0001-G1479.
Adams, R. M.; Rosenzweig, C.; Peart, R. M.; Ritchie, J. T.; McCarl, B. A.; Glyer, J. D.; Curry, R. B.; Jones, J.
W.; Boote, K. J.; Allen, L. H., Jr. (1990d) Global climate change and U.S. agriculture. Nature
(London) 345: 219-224.
Adaros, G.; Weigel, H. J.; Jager, H.-J. (1991a) Die Wirkung von Ozon auf Wachstums- und Ertragsparameter
zweier Sommerweizensorten (Triticum aestivum L.) [Impact of ozone on growth and yield
parameters of two spring wheat cultivars (Triticum aestivum L.)]. Z. Pflanzenkr. Pflanzenschutz 98:
113-124.
Adaros, G.; Weigel, H. J.; Jager, H. J. (1991b) Single and interactive effects of low levels of O3, SO2 and NO2
on the growth and yield of spring rape. Environ. Pollut. 72: 269-286.
5-285
-------
Adaros, G.; Weigel, H. J.; Jager, H. J. (1991c) Concurrent exposure to SO2 and/or NO2 alters growth and yield
responses of wheat and barley to low concentrations of O3. New Phytol. 118: 581-591.
Adedipe, N. O.; Hofstra, G.; Ormrod, D. P. (1972) Effects of sulfur nutrition on phytotoxicity and growth
responses of bean plants to ozone. Can. J. Bot. 50: 1789-1793.
Adomait, E. J.; Ensing, J.; Hofstra, G. (1987) A dose-response function for the impact of O3 on Ontario-grown
white bean and an estimate of economic loss. Can. J. Plant Sci. 67: 131-136.
Ainsworth, N.; Ashmore, M. R. (1992) Assessment of ozone effects on beech (Fagus sylvatica) by injection of a
protectant chemical. In: Freer-Smith, P. H., ed. Acidic deposition, its nature and impacts.
Atmospheric pollution and forests: papers presented at an international conference; September 1990;
Glasgow, United Kingdom. For. Ecol. Manage. 51: 129-136.
Ajax, R. L.; Conlee, C. J.; Upham, J. B. (1967) The effects of air pollution on the fading of dyed fabrics. J. Air
Pollut. Control Assoc. 17: 220-224.
Albaugh, T. J.; Mowry, F. L.; Kress, L. W. (1992) A field chamber for testing air pollution effects on mature
trees. J. Environ. Qual. 21: 476-485.
Allen, L. H., Jr. (1990) Plant responses to rising carbon dioxide and potential interactions with air pollutants.
J. Environ. Qual. 19: 15-34.
Allen, M. F. (1991) The ecology of mycorrhizae. New York, NY: Cambridge University Press.
Allen, O. B.; Marie, B. A.; Ormrod, D. P. (1987) Relative efficiency of factorial designs for estimating response
surfaces with reference to gaseous pollutant mixtures. J. Environ. Qual. 16: 316-320.
Alscher, R. G.; Amthor, J. S. (1988) The physiology of free-radical scavenging: maintenance and repair
processes. In: Schulte-Hostede, S.; Darrall, N. M.; Blank, L. W.; Wellburn, A. R., eds. Air pollution
and plant metabolism. London, United Kingdom: Elsevier Applied Science; pp. 94-115.
Alscher, R. G.; Amundson, R. G.; Gumming, J. R.; Fellows, S.; Fincher, J.; Rubin, G.; vanLeuken, P.;
Weinstein, L. H. (1989) Seasonal changes in the pigments, carbohydrates and growth of red spruce
as affected by ozone. New Phytol. 113: 211-223.
Amiro, B. D.; Gillespie, T. J. (1985) Leaf conductance response of Phaseolus vulgaris to ozone flux density.
Atmos. Environ. 19: 807-810.
Amiro, B. D.; Gillespie, T. J.; Thurtell, G. W. (1984) Injury response of Phaseolus vulgaris to ozone flux
density. Atmos. Environ. 18: 1207-1215.
Amthor, J. S. (1988) Growth and maintenance respiration in leaves of bean (Phaseolus vulgaris L.) exposed to
ozone in open-top chambers in the field. New Phytol. 110: 319-325.
Amthor, J. S.; Gumming, J. R. (1988) Low levels of ozone increase bean leaf maintenance respiration. Can. J.
Bot. 66: 724-726.
Amundson, R. G.; Raba, R. M.; Schoettle, A. W.; Reich, P. B. (1986) Response of soybean to low
concentrations of ozone: II. effects on growth, biomass allocation, and flowering. J. Environ. Qual.
15: 161-167.
Amundson, R. G.; Kohut, R. J.; Schoettle, A. W.; Raba, R. M.; Reich, P. B. (1987) Correlative reductions in
whole-plant photosynthesis and yield of winter wheat caused by ozone. Phytopathology 77: 75-79.
5-286
-------
Amundson, R. G.; Alscher, R. G.; Fellows, S.; Rubin, G.; Fincher, I; Van Leuken, P.; Weinstein, L. H. (1991)
Seasonal changes in the pigments, carbohydrates and growth of red spruce as affected by exposure
to ozone for two growing seasons. New Phytol. 118: 127-137.
Andersen, C. P.; Rygiewicz, P. T. (1991) Stress interactions and mycorrhizal plant response: understanding
carbon allocation priorities. Environ. Pollut. 73: 217-244.
Andersen, C. P.; Rygiewicz, P. T. (1995) Effect of ozone on temporal allocation of carbon in mycorrhizal of
Pinus ponderosa seedlings. New Phytol. 131: 471-480.
Andersen, C. P.; Hogsett, W. E.; Wessling, R.; Plocher, M. (1991) Ozone decreases spring root growth and root
carbohydrate content in ponderosa pine the year following exposure. Can. J. For. Res.
21: 1288-1291.
Anderson, R. L.; Brown, H. D.; Chevone, B. L; McCartney, T. C. (1988) Occurence of air pollution symptoms
(needle tip necrosis and chlorotic mottling) on eastern white pine in the southern Appalachian
Mountains. Plant Dis. 72: 130-132.
Anderson, J. V.; Chevone, B. L; Hess, J. L. (1992) Seasonal variation in the antioxidant system of eastern white
pine needles: evidence for thermal dependence. Plant Physiol. 98: 501-508.
Andries, J. C.; Diem, H. E. (1974) A study of ozone attack on elastomer surfaces by attenuated total reflectance
spectroscopy. J. Polym. Sci. Polym. Lett. Ed. 12: 281-286.
Andries, J. C.; Rhee, C. K.; Smith, R. W.; Ross, D. B.; Diem, H. E. (1979) A surface study of ozone attack and
antiozonant protection of carbon black loaded natural rubber compounds. Rubber Chem. Technol.
52: 823-837.
Aneja, V. P.; Yoder, G. T.; Arya, S. P. (1992) Ozone in the urban southeastern United States. Environ. Pollut.
75: 39-44.
Ashmore, M. R. (1984) Effects of ozone on vegetation in the United Kingdom. In: Grennfelt, P., ed. Proceedings
of the international workshop on the evaluation of the effects of photochemical oxidants on human
health, agricultural crops, forestry, materials and visibility; February-March; Goteborg, Sweden.
Goteborg, Sweden: Swedish Environmental Research Institute; pp. 92-104; report no. IVL-EM
1570.
Ashmore, M. R.; Bell, J. N. B. (1991) The role of ozone in global change. Ann. Bot. 67: 39-48.
Ashmore, M. R.; Bell, J. N. B. (1994) Clearing the air—how filtration experiments have demonstrated the hidden
effects of air pollution on vegetation. In: Kuttler, W.; Jochimsen, M., eds. Immissionsokologische
Forschung im Wandel der Zeit Festschrift fur Robert Guderian. Westarp Wissenschaften,
Uhlichstrasse; pp. 53-60.
Ashmore, M. R.; Onal, M. (1984) Modification by sulphur dioxide of the responses of Hordeum vulgare to
ozone. Environ. Pollut. Ser. A 36: 31-43.
Ashmore, M. R.; Bell, J. N. B.; Mimmack, A. (1988) Crop growth along a gradient of ambient air pollution.
Environ. Pollut. 53: 99-121.
Atkinson, C. J.; Wookey, P. A.; Mansfield, T. A. (1991) Atmospheric pollution and the sensitivity of stomata on
barley leaves to abscisic acid and carbon dioxide. New Phytol. 117: 535-541.
5-287
-------
Avissar, R.; Avissar, P.; Mahrer, Y.; Bravdo, B. A. (1985) A model to simulate response of plant stomata to
environmental conditions. Agric. For. Meteorol. 34: 21-29.
Aycock, M. K., Jr. (1972) Combining ability estimates for weather fleck in Nicotiana tabacum L. Crop Sci.
12: 2-674.
Baldocchi, D. D.; Hicks, B. B.; Camara, P. (1987) A canopy stomatal resistance model for gaseous deposition to
vegetated surfaces. Atmos. Environ. 21: 91-101.
Ball, J. T.; Woodrow, I. E.; Berry, J. A. (1987) A model predicting stomatal conductance and its contribution to
the control of photosynthesis under different environmental conditions. In: Biggins, J., ed. Progress
in photosynthesis research, v. IV: proceedings of the Vllth international congress on photosynthesis;
August 1986; Providence, RI. Dordrecht, The Netherlands: Martinus Nijhoff Publishers; pp.
221-224.
Barnes, J. D.; Brown, K. A. (1990) The influence of ozone and acid mist on the amount and wettability of the
surface waxes in Norway spruce [Picea abies (L.) Karst.]. New Phytol. 114: 531-535.
Barnes, J. D.; Davison, A. W. (1988) The influence of ozone on the winter hardiness of Norway spruce [Picea
abies (L.) Karst.]. New Phytol. 108: 159-166.
Barnes, J. D.; Pfirrmann, T. (1992) The influence of CO2 and O3, singly and in combination, on gas exchange,
growth and nutrient status of radish (Raphanus sativus L.). New Phytol. 121: 403-412.
Barnes, J. D.; Davison, A. W.; Booth, T. A. (1988a) Ozone accelerates structural degradation of epicuticular wax
on Norway spruce needles. New Phytol. 110: 309-318.
Barnes, J. D.; Reiling, K.; Davison, A. W.; Renner, C. J. (1988b) Interaction between ozone and winter stress.
Environ. Pollut. 53: 235-254.
Barnes, J. D.; Eamus, D.; Brown, K. A. (1990a) The influence of ozone, acid mist and soil nutrient status on
Norway spruce [Picea abies (L.) Karst.]: I. plant-water relations. New Phytol. 114: 713-720.
Barnes, J. D.; Eamus, D.; Brown, K. A. (1990b) The influence of ozone, acid mist and soil nutrient status on
Norway spruce [Picea abies (L.) Karst.]: II. photosynthesis, dark respiration and soluble
carbohydrates of trees during late autumn. New Phytol. 115: 149-156.
Barnes, J. D.; Velissariou, D.; Davison, A. W.; Holevas, C. D. (1990c) Comparative ozone sensitivity of old and
modern Greek cultivars of spring wheat. New Phytol. 116: 707-714.
Barrett, S. C. H.; Bush, E. J. (1991) Population processes in plants and the evolution of resistance to gaseous air
pollutants. In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg, M. T., eds. Ecological genetics and air
pollution. New York, NY: Springer-Verlag; pp. 137-165.
Barrett, L. B.; Waddell, T. E. (1973) Cost of air pollution damage: a status report. Research Triangle Park, NC:
U.S. Environmental Protection Agency, National Environmental Research Center; publication no.
AP-85. Available from: NTIS, Springfield, VA; PB-222040.
Bazzaz, F. A. (1990) The response of natural ecosystems to the rising global CO2 levels. Annu. Rev. Ecol. Syst.
21: 167-196.
Beadle, C. L.; Jarvis, P. G.; Talbot, H.; Neilson, R. E. (1985a) Stomatal conductance and photosynthesis in a
mature Scots pine forest. II. Dependence on environmental variables of single shoots. J. Appl. Ecol.
22: 573-586.
5-288
-------
Beadle, C. L.; Neilson, R. E.; Talbot, H.; Jarvis, P. G. (1985b) Stomatal conductance and photosynthesis in a
mature Scots pine forest. I. Diurnal, seasonal and spatial variation in shoots. J. Appl. Ecol.
22: 557-571.
Becker, K. H.; Brockmann, K. J.; Bechara, J. (1990) Production of hydrogen peroxide in forest air by reaction of
ozone with terpenes. Nature (London) 346: 256-258.
Bell, J. N. B.; Ashmore, M. R.; Wilson, G. B. (1991) Ecological genetics and chemical modifications of the
atmosphere. In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg, M. T., eds. Ecological genetics and air
pollution. New York, NY: Springer-Verlag; pp. 33-59.
Beloin, N. J. (1972) Fading of dyed fabrics by air pollution. Text. Chem. Color. 4: 77-82.
Beloin, N. J. (1973) Fading of dyed fabrics exposed to air pollutants. Text. Chem. Color. 5: 128-133.
Bender, J.; Weigel, H.-J.; Jager, H.-J. (1990) Regression analysis to describe yield and metabolic responses of
beans (Phaseolus vulgaris) to chronic ozone stress. Angew Bot. 64: 329-343.
Bender, J.; Weigel, H. J.; Jager, H. J. (1991) Response of nitrogen metabolism in beans (Phaseolus vulgaris L.)
after exposure to ozone and nitrogen dioxide, alone and in sequence. New Phytol. 119: 261-267.
Bennett, J. H. (1979) Foliar exchange of gases. In: Heck, W. W.; Krupa, S. V.; Linzon, S. N., eds. Methodology
for the assessment of air pollution effects on vegetation: a handbook from a specialty conference;
April 1978; Minneapolis, MN. Pittsburgh, PA: Air Pollution Control Association; pp. 10-1 - 10-29.
Bennett, J. P.; Runeckles, V. C. (1977) Effects of low levels of ozone on plant competition. J. Appl. Ecol.
14: 877-880.
Bennett, J. H.; Hill, A. C.; Gates, D. M. (1973) A model for gaseous pollutant sorption by leaves. J. Air Pollut.
Control Assoc. 23: 957-962.
Benoit, L. F.; Skelly, J. M.; Moore, L. D.; Dochinger, L. S. (1982) Radial growth reductions of Pinus strobus L.
correlated with foliar ozone sensitivity as an indicator of ozone-induced losses in eastern forests.
Can. J. For. Res. 12: 673-678.
Benoit, L. F.; Skelly, J. M.; Moore, L. D.; Dochinger, L. S. (1983) The influence of ozone on Pinus strobus L.
pollen germination. Can. J. For. Res. 13: 184-187.
Berrang, P.; Karnosky, D. F.; Bennett, J. P. (1989) Natural selection for ozone tolerance mPopulus tremuloides'.
field verification. Can. J. For. Res. 19: 519-522.
Berrang, P.; Karnosky, D. F.; Mickler, R. A.; Bennett, J. P. (1986) Natural selection for ozone tolerance in
Populus tremuloides. Can. J. For. Res. 16: 1214-1216.
Berrang, P.; Karnosky, D. F.; Bennett, J. P. (1991) Natural selection for ozone tolerance mPopulus tremuloides:
an evaluation of nationwide trends. Can. J. For. Res. 21: 1091-1097.
Berry, C. R. (1961) White pine emergence tipburn, a physiogenic disturbance. Asheville, NC: U.S. Department
of Agriculture-Forest Service, Southeastern Forest Experiment Station; station paper no. 130.
Berry, C. R. (1964) Differences in concentrations of surface oxidant between valley and mountaintop conditions
in the southern Appalachians. J. Air Pollut. Control Assoc. 14: 238-239.
5-289
-------
Berry, C. R.; Hepting, G. H. (1964) Injury to eastern white pine by unidentified atmospheric constituents. For.
Sci. 10: 2-13.
Berry, C. R.; Ripperton, L. A. (1963) Ozone, a possible cause of white pine emergence tipburn. Phytopathology
53: 552-557.
Beyers, J. L.; Riechers, G. H.; Temple, P. J. (1992) Effects of long-term ozone exposure and drought on the
photosynthetic capacity of ponderosa pine (Pinus ponderosa Laws.). New Phytol. 122: 81-90.
Billen, N.; Schatzle, H.; Seufert, G.; Arndt, U. (1990) Performance of some growth variables. Environ. Pollut.
68: 419-434.
Billings, W. D. (1978) Plants and the ecosystem. 3rd ed. Belmont, CA: Wadsworth Publishing Company, Inc.;
pp. 1-62, 83-108.
Bingham, G. E.; Coyne, P. I. (1977) A portable, temperature-controlled, steady-state porometer for field
measurements of transpiration and photosynthesis. Photosynthetica 11: 148-160.
Bisessar, S. (1982) Effect of ozone, antioxidant protection, and early blight on potato in the field. J. Am. Soc.
Hortic. Sci. 107: 597-599.
Bisessar, S.; Palmer, K. T. (1984) Ozone, antioxidant spray and Meloidogyne hapla effects on tobacco. Atmos.
Environ. 18: 1025-1027.
Bisessar, S.; Temple, P. J. (1977) Reduced ozone injury on virus-infected tobacco in the field. Plant Dis. Rep.
61: 961-963.
Blank, L. W.; Payer, H. D.; Pfirrmann, T.; Gnatz, G.; Kloos, M; Runkel, K.-H.; Schmolke, W.; Strube, D.;
Rehfuess, K. E. (1990a) Effects of ozone, acid mist and soil characteristics on clonal Norway
spruce (Picea abies (L.) Karst.) - an introduction to the joint 14 month tree exposure experiment in
closed chambers. Environ. Pollut. 64: 189-207.
Blank, L. W.; Payer, H. D.; Pfirrmann, T.; Rehfuess, K. E. (1990b) Effects of ozone, acid mist and soil
characteristics on clonal Norway spruce (Picea abies (L.) Karst.) - overall results and conclusions of
the the joint 14 month tree exposure experiment in closed chambers. Environ. Pollut. 64: 385-395.
Blaschke, H.; Weiss, M. (1990) Impact of ozone, acid mist and soil characteristics on growth and development
of fine roots and ectomycorrhiza of young clonal Norway spruce. Environ. Pollut. 64: 255-263.
Blum, U.; Tingey, D. T. (1977) A study of the potential ways in which ozone could reduce root growth and
nodulation of soybean. Atmos. Environ. 11: 737-739.
Blum, U.; Heagle, A. S.; Burns, J. C.; Linthurst, R. A. (1983) The effects of ozone on fescue-clover forage:
regrowth, yield and quality. Environ. Exp. Bot. 23: 121-132.
Blumthaler, M.; Ambach, W. (1990) Indication of increasing solar ultraviolet-B radiation flux in alpine regions.
Science (Washington, DC) 248: 206-208.
Bogaty, H.; Campbell, K. S.; Appel, W. D. (1952) The oxidation of cellulose by ozone in small concentrations.
Text. Res. J. 22: 81-83.
Bohm, M. (1992) Air quality and deposition. In: Olson, R. K.; Binkley, D.; Bohm, M., eds. The response of
western forests to air pollution. New York, NY: Springer-Verlag; pp. 63-152. (Ecological studies:
analysis and synthesis: v. 97).
5-290
-------
Bohm, M; McCune, B.; Vandetta, T. (1995) Ozone regimes in or near forests of the western United States:
I. regional patterns. J. Air Waste Manage. Assoc. 45: 235-246.
Bolsinger, M.; Lier, M. E.; Lansky, D. M.; Hughes, P. R. (1991) Influence of ozone air pollution on
plant-herbivore interactions. Part I: Biochemical changes in ornamental milkweed (Asclepias
curassavica L.; Asclepiadaceae) induced by ozone. Environ. Pollut. 72: 69-83.
Bolsinger, M.; Lier, M. E.; Hughes, P. R. (1992) Influence of ozone air pollution on plant-herbivore interactions.
Part 2: effects of ozone on feeding preference, growth and consumption rates of monarch butterflies
(Danaus plexippus). Environ. Pollut. 77: 31-37.
Bormann, F. H. (1985) Air pollution and forests: an ecosystem perspective. BioScience 35: 434-441.
Bors, W.; Langebartels, C.; Michel, C.; Sandermann, H., Jr. (1989) Polyamines as radical scavengers and
protectants against ozone damage. Phytochemistry 28: 1589-1595.
Botkin, D. B.; Smith, W. H.; Carlson, R. W. (1971) Ozone suppression of white pine net photosynthesis. J. Air
Pollut. Control Assoc. 21: 778-780.
Botkin, D. B.; Smith, W. H.; Carlson, R. W.; Smith, T. L. (1972) Effects of ozone on white pine saplings:
variation in inhibition and recovery of net photosynthesis. Environ. Pollut. 3: 273-289.
Boutton, T. W.; Flagler, R. B. (1990) Growth and water-use efficiency of shortleaf pine as affected by ozone and
acid rain. Presented at: 83rd annual meeting of the Air and Waste Management Association; June;
Pittsburgh, PA. Pittsburgh, PA: Air and Waste Management Association; paper no. 90-187.7.
Braden, J. B.; Kolstad, C. D., eds. (1991) Measuring the demand for environmental quality. Amsterdam, The
Netherlands: North-Holland. (Tinbergen, J.; Jorgenson, D. W.; Waelbroeck, J., eds. Contributions to
economic analysis: no. 198).
Bradley, C. E.; Haagen-Smit, A. J. (1951) The application of rubber in the quantitative determination of ozone.
Rubber Chem. Technol. 24: 750-755.
Bradshaw, A. D.; McNeilly, T. (1991) Evolution in relation to environmental stress. In: Taylor, G. E., Jr.;
Pitelka, L. F.; Clegg, M. T., eds. Ecological genetics and air pollution. New York, NY:
Springer-Verlag; pp. 11-31.
Braun, S.; Fltickiger, W. (1989) Effect of ambient ozone and acid mist on aphid development. Environ. Pollut.
56: 177-187.
Brennan, E.; Leone, L; Greenhalgh, B.; Smith, G. (1987) Chlorophyll content of soybean foliage in relation to
seed yield and ambient ozone pollution. JAPCA 37: 1429-1433.
Brennan, E. G.; Clarke, B. B.; Greenhalgh-Weidmar, B.; Smith, G. (1990) An assessment of the impact of
ambient ozone on field-grown crops in New Jersey using the EDU method: part 2—soybean
(Glycine max (L.) Merr). Environ. Pollut. 66: 361-373.
Brewer, P. F.; Heagle, A. S. (1983) Interactions between Glomus geosporum and exposure of soybeans to ozone
or simulated acid rain in the field. Phytopathology 73: 1035-1040.
Brewer, R. F.; Guillemet, F. B.; Creveling, R. K. (1961) Influence of N-P-K fertilization on incidence and
severity of oxidant injury to mangels and spinach. Soil Sci. 92: 298-301.
5-291
-------
Brown, K. A.; Roberts, T. M. (1988) Effects of ozone on foliar leaching in Norway spruce (Picea abies L.
Karst): confounding factors due to NOX production during ozone generation. Environ. Pollut.
55: 55-73.
Brown, K. A.; Roberts, T. M.; Blank, L. W. (1987) Interaction between ozone and cold sensitivity in Norway
spruce: a factor contributing to the forest decline in central Europe? New Phytol. 105: 149-155.
Brown, V. C.; McNeill, S.; Ashmore, M. R. (1992) The effects of ozone fumigation on the performance of the
black bean aphid, Aphis fabae Scop., feeding on broad beans, Viciafaba L. Agric. Ecosyst.
Environ. 38: 71-78.
Briihl, C.; Crutzen, P. J. (1989) On the disproportionate role of tropospheric ozone as a filter against solar UV-B
radiation. Geophys. Res. Lett. 16: 703-706.
Bruhn, J. N. (1980) Effects of oxidant air pollution on ponderosa and Jeffrey pine foliage decomposition
[Ph.D. dissertation]. Berkeley, CA: University of California. Available from: University Microfilms,
Ann Arbor, MI; publication no. 82-00036.
Busing, R. T.; Clebsch, E. E. C.; Eagar, C. C.; Pauley, E. F. (1988) Two decades of change in a Great Smokey
Mountains spruce-fir forest. Bull. Torrey Bot. Club 115: 25-31.
Byres, D. P.; Dean, T. J.; Johnson, J. D. (1992a) Long-term effects of ozone and simulated acid rain on the
foliage dynamics of slash pine (Pinus elliottii var elliottii Engelm.). New Phytol. 120: 61-67.
Byres, D. P.; Johnson, J. D.; Dean, T. J. (1992b) Seasonal response of slash pine (Pinus elliottii var. elliottii
Engelm.) photosynthesis to long-term exposure to ozone and acidic precipitation. New Phytol.
122: 91-96.
Bytnerowicz, A.; Miller, P. R.; Olszyk, D. M.; Dawson, P. J.; Fox, C. A. (1987a) Gaseous and paniculate air
pollution in the San Gabriel Mountains of southern California. Atmos. Environ. 21: 1805-1814.
Bytnerowicz, A.; Miller, P. R.; Olszyk, D. M. (1987b) Dry deposition of nitrate, ammonium and sulfate to a
Ceanothus crassifolius canopy and surrogate surfaces. Atmos. Environ. 21: 1749-1757.
Bytnerowicz, A.; Olszyk, D. M.; Fox, C. A.; Dawson, P. J.; Kats, G.; Morrison, C. L.; Wolf, J. (1988)
Responses of desert annual plants to ozone and water stress in an in situ experiment. JAPCA
38: 1145-1151.
Bytnerowicz, A.; Poth, M.; Takemoto, B. K. (1990) Effects of photochemical smog and mineral nutrition on
ponderosa pine seedlings. Environ. Pollut. 67: 233-248.
Callaway, J. M.; Darwin, R. F.; Neese, R. J. (1985) Economic valuation of acidic deposition: preliminary results
from the 1985 NAPAP assessment. Richland, WA: U.S. Environmental Protection Agency, National
Acid Precipitation Assessment Program.
Cameron, J. W. (1975) Inheritance in sweet corn for resistance to acute ozone injury. J. Am. Soc. Horde. Sci.
100: 577-579.
Campbell, G. G.; Schurr, G. G.; Slawikowski, D. E.; Spence, J. W. (1974) Assessing air pollution damage to
coatings. J. Paint Technol. 46: 59-71.
Cape, J. N.; Unsworth, M. H. (1988) Deposition, uptake and residence of pollutants. In: Schulte-Hostede, S.;
Darrall, N. M.; Blank, L. W.; Wellburn, A. R., eds. Air pollution and plant metabolism. London,
United Kingdom: Elsevier Applied Science; pp. 1-18.
5-292
-------
Carson, R. T. (1991) Constructed markets. In: Braden, J. B.; Kolstad, C. D., eds. Measuring the demand for
environmental quality. Amsterdam, The Netherlands: North-Holland; pp. 121-162. (Tinbergen, J.;
Jorgenson, D. W.; Waelbroeck, J., eds. Contributions to economic analysis: no. 198).
Carter, G. A.; Mitchell, R. J.; Chappelka, A. H.; Brewer, C. H. (1992) Response of leaf spectral reflectance in
loblolly pine to increased atmospheric ozone and precipitation acidity. J. Exp. Bot. 43: 577-584.
Cass, G. R.; Nazaroff, W. W.; Tiller, C.; Whitmore, P. M. (1991) Protection of works of art from damage due to
atmospheric ozone. Atmos. Environ. Part A 25: 441-451.
Cathey, H. M.; Heggestad, H. E. (1972) Reduction of ozone damage to Petunia hybrida Vilm. by use of growth
regulating chemicals and tolerant cultivars. J. Am. Soc. Hortic. Sci. 97: 695-700.
Cathey, H. M.; Heggestad, H. E. (1982) Ozone sensitivity of woody plants: modification by ethylenediurea.
J. Am. Soc. Hortic. Sci. 107: 1042-1045.
Chameides, W. L. (1989) The chemistry of ozone deposition to plant leaves: role of ascorbic acid. Environ. Sci.
Technol. 23: 595-600.
Chapin, F. S., Ill; Bloom, A. J.; Field, C. B.; Waring, R. H. (1987) Plant responses to multiple environmental
factors. BioScience 37: 49-57.
Chappelka, A. H., Ill; Chevone, B. L; Burk, T. E. (1985) Growth response of yellow-poplar (Liriodendron
tulipifera L.) seedlings to ozone, sulfur dioxide, and simulated acidic precipitation, alone and in
combination. Environ. Exp. Bot. 25: 233-244.
Chappelka, A. H.; Chevone, B. L; Burk, T. E. (1988a) Growth response of green and white ash seedlings to
ozone, sulfur dioxide, and simulated acid rain. For. Sci. 34: 1016-1029.
Chappelka, A. H.; Chevone, B. L; Seiler, J. R. (1988b) Growth and physiological responses of yellow-poplar
seedlings exposed to ozone and simulated acidic rain. Environ. Pollut. 49: 1-18.
Chappelka, A. H.; Kraemer, M. E.; Mebrahtu, T.; Rangappa, M.; Benepal, P. S. (1988c) Effects of ozone on
soybean resistance to the Mexican bean beetle (Epilachna varivestis Mulsant). Environ. Exp. Bot.
28: 53-60.
Chappelka, A. H.; Kush, J. S.; Meldahl, R. S.; Lockaby, B. G. (1990) An ozone-low temperature interaction in
loblolly pine (Pinus taeda L.). New Phytol. 114: 721-726.
Chappelka, A. H.; Hildebrand, E.; Skelly, J. M.; Mangis, D.; Renfro, J. R. (1992) Effects of ambient ozone
concentrations on mature eastern hardwood trees growing in Great Smoky Mountains National Park
and Shenandoah National Park. Presented at: 85th annual meeting of the Air and Waste
Management Association; June; Kansas City, MO. Pittsburgh, PA: Air and Waste Management
Association; paper no. 92-150.04.
Chevrier, N.; Sarhan, F.; Chung, Y. S. (1988) Oxidative damages and repair in Euglena gracilis exposed to
ozone. I. SH groups and lipids. Plant Cell Physiol. 29: 321-327.
Chevrier, N.; Chung, Y. S.; Sarhan, F. (1990) Oxidative damages and repair in Euglena gracilis exposed to
ozone: II. membrane permeability and uptake of metabolites. Plant Cell Physiol. 31: 987-992.
Clarke, B. B.; Greenhalgh-Weidman, B.; Brennan, E. G. (1990) An assessment of the impact of ambient ozone
on field-grown crops in New Jersey using the EDU method: part 1—white potato (Solanum
tuberosum). Environ. Pollut. 66: 351-360.
5-293
-------
Cobb, F. W., Jr.; Stark, R. W. (1970) Decline and mortality of smog-injured ponderosa pine. J. For. 68: 147-149.
Coleman, J. S.; Jones, C. G. (1988) Plant stress and insect performance: cottonwood, ozone and a leaf beetle.
Oecologia 76: 57-61.
Coleman, J. S.; Jones, C. G.; Smith, W. H. (1987) The effect of ozone on cottonwood - leaf rust interactions:
independence of abiotic stress, genotype, and leaf ontogeny. Can. J. Bot. 65: 949-953.
Coleman, J. S.; Jones, C. G.; Smith, W. H. (1988) Interactions between an acute ozone dose, eastern cottonwood,
and Marssonina leaf spot: implications for pathogen community dynamics. Can. J. Bot. 66:
863-868.
Collatz, G. J.; Ball, J. T.; Grivet, C.; Berry, J. A. (1991) Physiological and environmental regulation of stomatal
conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer.
Agric. For. Meteorol. 54: 107-136.
Cook, L. M.; Wood, R. J. (1976) Genetic effects of pollutants; environmental review: 5. Biologist 23: 129-139.
Cooley, D. R.; Manning, W. J. (1987) The impact of ozone on assimilate partitioning in plants: a review.
Environ. Pollut. 47: 95-113.
Cooley, D. R.; Manning, W. J. (1988) Ozone effects on growth and assimilate partitioning in alfalfa, Medicago
sativa L. Environ. Pollut. 49: 19-36.
Costonis, A. C.; Sinclair, W. A. (1972) Susceptibility of healthy and ozone-injured needles of Pinus strobus to
invasion by Lophodermium pinastri and Aureobasidium pullulans. Eur. J. For. Pathol. 2: 65-73.
Cowling, D. W.; Koziol, M. J. (1982) Mineral nutrition and plant response to air pollutants. In: Unsworth,
M. H.; Ormrod, D. P., eds. Effects of gaseous air pollution in agriculture and horticulture. London,
United Kingdom: Butterworth Scientific; pp. 349-375.
Crabtree, J.; Malm, F. S. (1956) Deterioration of rubber from use and with age. In: McPherson, A. T.; Klemin,
A., eds. Engineering uses of rubber. New York, NY: Reinhold Publishing Corp.; pp. 140-170.
Cregg, B. M.; Halpin, J. E.; Dougherty, P. M.; Teskey, R. O. (1989) Comparative physiology and morphology of
seedling and mature forest trees. In: Noble, R. D.; Martin, J. L.; Jensen, K. F., eds. Air pollution
effects on vegetation including forest ecosystems: proceedings of the second US-USSR symposium;
September 1988; Corvallis, OR; Raleigh, NC; Gatlinburg, TN. Broomall, PA: U.S. Department of
Agriculture, Forest Service, Northeastern Forest Experiment Station; pp. 111-118.
Crocker, T. D. (1980) [Statement before the Select Committee on Small Business and the Committee on
Environment and Public Works, U.S. Senate.] In: Economic impact of acid rain: hearings before the
Select Committee on Small Business and the Committee on Environment and Public Works, U.S.
Senate, Ninety-sixth Congress, September 23, 1980. Washington, DC: Government Printing Office.
Crocker, T. D. (1985) On the value of the condition of a forest stock. Land Econ. 61: 244-254.
Crocker, T. D.; Forster, B. A. (1985) Some economic implications of the alternative biological and chemical
explanations of the impacts of acid deposition on forest ecosystems. Presented at: International
symposium on acidic deposition; Muskoka, Canada.
Cure, W. W.; Sanders, J. S.; Heagle, A. S. (1986) Crop yield response predicted with different characterizations
of the same ozone treatments. J. Environ. Qual. 15: 251-254.
5-294
-------
Dahlsten, D. L.; Rowney, D. L. (1980) Influence of air pollution on population dynamics of forest insects and on
tree mortality. In: Miller, P. R., ed. Proceedings of the symposium on effects of air pollutants on
Mediterranean and temperate forest ecosystems; June; Riverside, CA. Berkeley, CA:
U.S. Department of Agriculture, Pacific Southwest Forest and Range Experiment Station;
pp. 125-130; Forest Service general technical report no. PSW-43. Available from: NTIS,
Springfield, VA; PB81-133720.
Daines, R. H.; Leone, I. A.; Brennan, E. (1960) Air pollution as it affects agriculture in New Jersey.
New Brunswick, NJ: New Jersey Agricultural Experiment Station, Rutgers; bulletin no. 794.
Damicone, J. P.; Manning, W. J.; Herbert, S. J.; Feder, W. A. (1987a) Growth and disease response of soybeans
from early maturity groups to ozone and Fusarium oxysporum. Environ. Pollut. 48: 117-130.
Damicone, J. P.; Manning, W. J.; Herbert, S. J.; Feder, W. A. (1987b) Foliar sensitivity of soybeans from early
maturity groups to ozone and inheritance of injury response. Plant Dis. 71: 332-336.
Dammgen, U.; Griinhage, L.; Ktisters, A.; Jager, H.-J. (1994) Response of a grassland ecosystem to air
pollutants:—II the chemical climate: fluxes of sedimenting airborne matter. Environ. Pollut.
85: 35-42.
Dann, M. S.; Pell, E. J. (1989) Decline of activity and quantity of ribulose bisphosphate carboxylase/oxygenase
and net photosynthesis in ozone-treated potato foliage. Plant Physiol. 91: 427-432.
Darley, E. F.; Kettner, K. A.; Stephens, E. R. (1963) Analysis of peroxyacyl nitrates by gas chromatography with
electron capture detection. Anal. Chem. 35: 589-591.
Darrall, N. M. (1989) The effect of air pollutants on physiological processes in plants. Plant Cell Environ.
12: 1-30.
Dassel, K. A.; Rawlings, J. O. (1988) Experimental design strategy for the Weibull dose response model.
Environ. Pollut. 53: 333-349.
Davidson, A. (1993) Update of ozone trends in California's South Coast Air Basin. Air Waste 43: 226-227.
Davidson, S. R.; Ashmore, M. R.; Garretty, C. (1992) Effects of ozone and water deficit on the growth and
physiology of Fagus sylvatica. For. Ecol. Manage. 51: 187-193.
Davies, K. M. (1979) Influence of environmental factors on interply adhesion. In: Proceedings of the
international rubber conference; pp. 80-89.
Davies, W. J.; Zhang, J. (1991) Root signals and the regulation of growth and development of plants in drying
soil. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 55-76.
Davies, W. J.; Mansfield, T. A.; Wellburn, A. R. (1980) A role for abscisic acid in drought endurance and
drought avoidance. In: Skoog, F., ed. Plant growth substances 1979: proceedings of the 10th
international conference on plant growth substances; July 1979; Madison, WI. New York, NY:
Springer-Verlag; pp. 242-253.
Davis, D. D.; Skelly, J. M. (1992a) Growth response of four species of eastern hardwood tree seedlings exposed
to ozone, acidic precipitation, and sulfur dioxide. J. Air Waste Manage. Assoc. 42: 309-311.
Davis, D. D.; Skelly, J. M. (1992b) Foliar sensitivity of eight eastern hardwood tree species to ozone. Water Air
Soil Pollut. 62: 269-277.
5-295
-------
Davison, A. W.; Barnes, J. D.; Renner, C. J. (1988) Interactions between air pollutants and cold stress.
In: Schulte-Hostede, S.; Darrall, N. M; Blank, L. W.; Wellburn, A. R., eds. Air pollution and plant
metabolism. London, United Kingdom: Elsevier Applied Science; pp. 307-328.
Dean, T. J.; Johnson, J. D. (1992) Growth response of young slash pine trees to simulated acid rain and ozone
stress. Can. J. For. Res. 22: 839-848.
DeHayes, D. H.; Thornton, F. C.; Waite, C. E.; Ingle, M. A. (1991) Ambient cloud deposition reduces cold
tolerance of red spruce seedlings. Can. J. For. Res. 21: 1292-1295.
De Santis, F.; Di Palo, V.; Allegrini, I. (1992) Determination of some atmospheric pollutants inside a museum:
relationship with the concentration outside. Sci. Total Environ. 127: 211-223.
De Temmerman, L.; Vandermeiren, K.; Guns, M. (1992) Effects of air filtration on spring wheat grown in
open-top field chambers at a rural site. I. Effect on growth, yield and dry matter partitioning.
Environ. Pollut. 77: 1-5.
Deveau, J. L.; Ormrod, D. P.; Allen, O. B.; Beckerson, D. W. (1987) Growth and foliar injury responses of
maize, soybean and tomato seedlings exposed to mixtures of ozone and sulphur dioxide. Agric.
Ecosyst. Environ. 19: 223-240.
De Vos, N. E.; Hill, R. R., Jr.; Pell, E. J.; Cole, R. H. (1982) Quantitative inheritance of ozone resistance in
potato. Crop Sci. 22: 992-995.
Diaz, H. F.; Bradley, R. S.; Eischeid, J. K. (1989) Precipitation fluctuations over global land areas since the late
1800's. J. Geophys. Res. [Atmos.] 94: 1195-1210.
Dickson, R. E.; Isebrands, J. G. (1991) Leaves as regulators of stress response. In: Mooney, H. A.; Winner, W.
E.; Pell, E. J., eds. Response of plants to multiple stresses. San Diego, CA: Academic Press, Inc.;
pp. 3-34.
Dimauro, P. J.; Paris, H. L.; Path, M. A. (1979) Wax protection. Rubber Chem. Technol. 52: 973-984.
Dobson, M. C.; Taylor, G.; Freer-Smith, P. H. (1990) The control of ozone uptake by Picea abies (L.) Karst. and
P. sitchensis (Bong.) Carr. during drought and interacting effects on shoot water relations. New
Phytol. 116: 465-474.
Dohmen, G. P. (1987) Secondary effects of air pollution: ozone decreases brown rust disease potential in wheat.
Environ. Pollut. 43: 189-194.
Dohmen, G. P. (1988) Indirect effects of air pollutants: changes in plant/parasite interactions. Environ. Pollut. 53:
197-207.
Dohmen, G. P.; Koppers, A.; Langebartels, C. (1990) Biochemical response of Norway spruce (Picea abies (L.)
Karst.) towards 14-month exposure to ozone and acid mist: effects of amino acid, glutathione and
polyamine liters. Environ. Pollut. 64: 375-383.
Dorset, B. C. M. (1972) Pollution and fading fabrics. Text. Manuf. 99: 27-29.
Dowding, P. (1988) Air pollutant effects on plant pathogens. In: Schulte-Hostede, S.; Darrall, N. M.; Blank, L.
W.; Wellburn, A. R., eds. Air pollution and plant metabolism. London, United Kingdom: Elsevier
Applied Scientific; pp. 329-355.
5-296
-------
Dragoescu, N.; Hill, R. R., Jr.; Pell, E. J. (1987) An autotetraploid model for genetic analysis of ozone tolerance
in potato, Solarium tuberosum L. Genome 29: 85-90.
Druzik, J. R.; Adams, M. S.; Tiller, C.; Cass, G. R. (1990) The measurement and model predictions of indoor
ozone concentrations in museums. Atmos. Environ. Part A 24: 1813-1823.
Duchelle, S. F.; Skelly, J. M. (1981) Response of common milkweed to oxidant air pollution in the Shenandoah
National Park in Virginia. Plant Dis. 65: 661-663.
Duchelle, S. F.; Skelly, J. M.; Chevone, B. I. (1982) Oxidant effects on forest tree seedling growth in the
Appalachian mountains. Water Air Soil Pollut. 18: 363-373.
Duchelle, S. F.; Skelly, J. M.; Sharick, T. L.; Chevone, B. L; Yang, Y.-S.; Nellessen, J. E. (1983) Effects of
ozone on the productivity of natural vegetation in a high meadow of the Shenandoah National Park
of Virginia. J. Environ. Manage. 17: 299-308.
Dueck, Th. A.; Dil, E. W.; Pasman, F. J. M. (1987) Adaptation of grasses in the Netherlands to air pollution.
New Phytol. 108: 167-174.
Dugger, W. M., Jr.; Taylor, O. C.; Cardiff, E.; Thompson, C. R. (1962) Relationship between carbohydrate
content and susceptibility of pinto bean plants to ozone damage. Proc. Am. Soc. Hortic. Sci.
81: 304-315.
Dunn, D. B. (1959) Some effects of air pollution on Lupinus in the Los Angeles area. Ecology 40: 621-625.
Dunning, J. A.; Heck, W. W.; Tingey, D. T. (1974) Foliar sensitivity of pinto bean and soybean to ozone as
affected by temperature, potassium nutrition and ozone dose. Water Air Soil Pollut. 3: 305-313.
Duriscoe, D. M.; Stolte, K. W. (1989) Photochemical oxidant injury to ponderosa pine (Pinus ponderosa Laws.)
and Jeffrey pine (Pinus jeffreyi Grev. and Barf.) in the national parks of the Sierra Nevada of
California. In: Olson, R. K.; Lefohn, A. S., eds. Effects of air pollution on western forests
[an A&WMA symposium; June; Anaheim, CA]. Pittsburgh, PA: Air and Waste Management
Asssociation; pp. 261-278. (APCA transactions series: no. 16).
Eagar, C.; Adams, M. B., eds. (1992) Ecology and decline of red spruce in the eastern United States. New York,
NY: Springer-Verlag. (Ecological studies: v. 96).
Eamus, D.; Murray, M. (1991) Photosynthetic and stomatal conductance responses of Norway spruce and beech
to ozone, acid mist and frost - a conceptual model. Environ. Pollut. 72: 23-44.
Eason, G.; Reinert, R. A. (1991) Responses of closely related Bush Blue Lake snap bean cultivars to increasing
concentrations of ozone. J. Am. Soc. Hortic. Sci. 116: 520-524.
Ebel, B.; Rosenkrantz, J.; Schiffgens, A.; Ltitz, C. (1990) Cytological observations on spruce needles after
prolonged treatment with ozone and acid mist. Environ. Pollut. 64: 323-335.
Edinger, J. G.; McCutchan, M. H.; Miller, P. R.; Ryan, B. C.; Schroeder, M. J.; Behar, J. V (1972) Penetration
and duration of oxidant air pollution in the South Coast Air Basin of California. J. Air Pollut.
Control Assoc. 22: 882-886.
Edwards, N. T. (1991) Root and soil respiration responses to ozone in Pinus taeda L. seedlings. New Phytol.
118: 315-321.
5-297
-------
Edwards, G. S.; Kelly, J. M. (1992) Ectomycorrhizal colonization of loblolly pine seedlings during three growing
seasons in response to ozone, acidic precipitation, and soil Mg status. Environ. Pollut. 76: 71-77.
Edwards, D. C.; Storey, E. B. (1959) A quantitative ozone test for small specimens. Chem. Can. 11: 34-38.
Edwards, G. S.; Pier, P. A.; Kelly, J. M. (1990a) Influence of ozone and soil magnesium status on the cold
hardiness of loblolly pine (Pinus taeda L.) seedlings. New Phytol. 115: 157-164.
Edwards, N. T.; Taylor, G. E., Jr.; Adams, M. B.; Simmons, G. L.; Kelly, J. M. (1990b) Ozone, acidic rain and
soil magnesium effects on growth and foliar pigments of Pinus taeda L. Tree Physiol. 6: 95-104.
Edwards, G. S.; Edwards, N. T.; Kelly, J. M.; Mays, P. A. (1991) Ozone, acidic precipitation, and soil Mg
effects on growth and nutrition of loblolly pine seedlings. Environ. Exp. Bot. 31: 67-78.
Edwards, N. T.; Edwards, G. L.; Kelly, J. M.; Taylor, G. E., Jr. (1992a) Three-year growth responses of Pinus
taeda L. to simulated rain chemistry, soil magnesium status, and ozone. Water Air Soil Pollut. 63:
105-118.
Edwards, G. S.; Friend, A. L.; O'Neill, E. G.; Tomlinson, P. T. (1992b) Seasonal patterns of biomass
accumulation and carbon allocation in Pinus taeda seedlings exposed to ozone, acidic precipitation,
and reduced soil Mg. Can. J. For. Res. 22: 640-646.
Edwards, G. S.; Kelly, J. M.; Mays, P. A. (1992c) Ozone, acidic precipitation and soil Mg impacts on soil and
loblolly pine seedling nutrient status after three growing seasons. Water Air Soil Pollut.
63: 281-294.
Edwards, G. S.; Sherman, R. E.; Kelly, J. M. (1995) Red spruce and loblolly pine nutritional responses to acidic
precipitation and ozone. Environ. Pollut. 89: 9-15.
Ehleringer, J. R. (1991) Estimating costs of air pollution resistance. In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg,
M. T., eds. Ecological genetics and air pollution. New York, NY: Springer-Verlag; pp. 203-207.
Eissenstat, D. M.; Syvertsen, J. P.; Dean, T. J.; Yelenosky, G.; Johnson, J. D. (1991a) Sensitivity of frost
resistance and growth in citrus and avocado to chronic ozone exposure. New Phytol. 118: 139-146.
Eissenstat, D. M.; Syvertsen, J. P.; Dean, T. J.; Johnson, J. D.; Yelenosky, G. (1991b) Interaction of simulated
acid rain with ozone on freeze resistance, growth, and mineral nutrition in citrus and avocado. J.
Am. Soc. Hortic. Sci. 116: 838-845.
Elkiey, T.; Ormrod, D. P. (1979a) Leaf diffusion resistance responses of three petunia cultivars to ozone and/or
sulfur dioxide. J. Air Pollut. Control Assoc. 29: 622-625.
Elkiey, T.; Ormrod, D. P. (1979b) Petunia cultivar sensitivity to ozone and sulphur dioxide. Sci. Hortic.
(Amsterdam) 11: 269-280.
Elkiey, T.; Ormrod, D. P.; Pelletier, R. L. (1979) Stomatal and leaf surface features as related to the ozone
sensitivity of petunia cultivars. J. Am. Soc. Hortic. Sci. 104: 510-514.
Elliott, C. L.; Eberhardt, J. C.; Brennan, E. G. (1987) The effect of ambient ozone pollution and acidic rain on
the growth and chlorophyll content of green and white ash. Environ. Pollut. 44: 61-70.
Enders, G.; Dlugi, R.; Steinbrecher, R.; Clement, B.; Daiber, R.; Eijk, J. V.; Gab, S.; Haziza, M.; Helas, G.;
Herrmann, U.; Kessel, M.; Kesselmeier, J.; Kotzias, D.; Kourtidis, K.; Kurth, H.-H.; McMillen, R.
T.; Roider, G.; Schurmann, W.; Teichmann, U.; Torres, L. (1992) Biosphere/atmosphere
5-298
-------
interactions: integrated research in a European coniferous forest ecosystem. Atmos. Environ. Part A
26: 171-189.
Endress, A. G.; Post, S. L. (1985) Altered feeding preference of Mexican bean beetle Epilachna varivestis for
ozonated soybean foliage. Environ. Pollut. Ser. A 39: 9-16.
Engle, R. L.; Gabelman, W. H. (1966) Inheritance and mechanism for resistance to ozone damage in onion,
Allium cepa L. Proc. Am. Soc. Hortic. Sci. 89: 423-430.
Ennis, C. A.; Lazrus, A. L.; Kok, G. L.; Zimmerman, P. R.; Monson, R. K. (1990) A branch chamber system
and techniques for simultaneous pollutant exposure experiments and gaseous flux determinations.
Tellus Ser. B 42: 170-182.
Ensing, I; Hofstra, G.; Adomait, E. J. (1986) The use of cultivar yield data to estimate losses due to ozone in
peanut. Can. J. Plant Sci. 66: 511-520.
Enyedi, A. J.; Eckardt, N. A.; Pell, E. J. (1992) Activity of ribulose biphosphate carboxylase/oxygenase from
potato cultivars with differential response to ozone stress. New Phytol. 122: 493-500.
Ernst, W. H. O.; Tonneijck, A. E. C.; Pasman, F. J. M. (1985) Ecotypic response of Silene cucubalus to air
pollutants (SO2, O3). J. Plant Physiol. 118: 439-450.
Evans, P. A.; Ashmore, M. R. (1992) The effects of ambient air on a semi-natural grassland community. Agric.
Ecosyst. Environ. 38: 91-97.
Eversman, S.; Sigal, L. L. (1987) Effects of SO2, O3, and SO2 and O3 in combination on photosynthesis and
ultrastructure of two lichen species. Can. J. Bot. 65: 1806-1818.
Fankhauser, R. K. (1976) Ozone levels in the vicinity of 33 cities. J. Air Pollut. Control Assoc. 26: Ill-Ill.
Farquhar, G. D.; Ehleringer, J. R.; Hubick, K. T. (1989) Carbon isotope discrimination and photosynthesis. Annu.
Rev. Plant Physiol. Plant Mol. Biol. 40: 503-537.
Feder, W. A. (1968) Reduction in tobacco pollen germination and tube elongation, induced by low levels of
ozone. Science (Washington, DC) 160: 1122.
Feder, W. A. (1970) Plant response to chronic exposure of low levels of oxidant type air pollution. Environ.
Pollut. 1: 73-79.
Feder, W. A. (1986) Using pollen to predict species response to ozone stress. Phytopathology 76: 1097.
Feder, W. A.; Shrier, R. (1990) Combination of U.V.-B. and ozone reduces pollen tube growth more than either
stress alone. Environ. Exp. Bot. 30: 451-454.
Feder, W. A.; Sullivan, F. (1969) Differential susceptibility of pollen grains to ozone injury. Phytopathology 59:
399.
Federal Register. (1993) Natural resource damage assessments under the Oil Pollution Act of 1990. F. R.
(January 15) 58: 4601-4614.
Fenn, M. (1991) Increased site fertility and litter decomposition rate in high-pollution sites in the San Bernardino
Mountains. For. Sci. 37: 1163-1181.
5-299
-------
Perm, M. E.; Bytnerowicz, A. (1993) Dry deposition of nitrogen and sulfur to ponderosa and Jeffrey pine in the
San Bernardino National Forest in southern California. Environ. Pollut. 81: 277-285.
Fenn, M. E.; Dunn, P. H. (1989) Litter decomposition across an air-pollution gradient in the San Bernardino
Mountains. Soil Sci. Soc. Am. J. 53: 1560-1567.
Fincher, J. (1992) Comparison of structural changes in red spruce (Picea mbens Sarg.) during cold hardening in
mature trees and in seedlings used in pollutant exposure studies. For. Ecol. Manage. 51: 105-113.
Fincher, J.; Gumming, J. R.; Alscher, R. G.; Rubin, G.; Weinstein, L. (1989) Long-term ozone exposure affects
winter hardiness of red spruce (Picea rubens Sarg.) seedlings. New Phytol. 113: 85-96.
Fisher, H. L. (1957) Antioxidation and antiozonation. In: Chemistry of natural and synthetic rubbers. New York,
NY: Reinhold Publishing Corporation; pp. 49-55.
Flagler, R. B.; Younger, V. B. (1982) Ozone and sulfur dioxide effects on three tall fescue cultivars. J. Environ.
Qual. 11: 413-416.
Flagler, R. B.; Patterson, R. P.; Heagle, A. S.; Heck, W. W. (1987) Crop physiology & metabolism: ozone and
soil moisture deficit effects on nitrogen metabolism of soybean. Crop Sci. 27: 1177-1184.
Fletcher, R. A.; Hofstra, G. (1985) Triadimefon a plant multi-protectant. Plant Cell Physiol. 26: 775-780.
Floyd, R. A.; West, M. S.; Hogsett, W. E.; Tingey, D. T. (1989) Increased 8-hydroxyguanine content of
chloroplast DNA from ozone-treated plants. Plant Physiol. 91: 644-647.
Fluckiger, W.; Braun, S.; Bolsinger, M. (1988) Air pollution: effect on hostplant-insect relationships.
In: Schulte-Hostede, S.; Darrall, N. M.; Blank, L. W.; Wellburn, A. R., eds. Air pollution and plant
metabolism. London, United Kingdom: Elsevier Applied Science; pp. 366-380.
Fowler, D.; Cape, J. N. (1982) Air pollutants in agriculture and horticulture. In: Unsworth, M. H.; Ormrod, D.
P., eds. Effects of gaseous air pollution in agriculture and horticulture. London, United Kingdom:
Butterworth Scientific; pp. 3-26.
Fox, D. G.; Bartuska, A. M.; Byrne, J. G.; Cowling, E.; Fisher, R.; Likens, G. E.; Lindberg, S. E.; Linthurst, R.
A.; Messer, J.; Nichols, D. S. (1989) A screening procedure to evaluate air pollution effects on
Class I wilderness areas. Ft. Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky
Mountain Forest and Range Experiment Station; general technical report RM-168. Available from:
NTIS, Springfield, VA; PB89-162150.
Foy, G. (1990) Economic sustainability and the preservation of environmental assets. Environ. Manage.
14: 771-778.
Fravel, D. R.; Benson, D. M.; Reinert, R. A. (1984) Response of shore juniper to ozone alone and in mixture
with sulfur dioxide and nitrogen dioxide. Hortscience 19: 694-695.
Fredericksen, T. S.; Joyce, B. J.; Skelly, J. M.; Steiner, K. C.; Kolb, T. E.; Kouterick, K. B.; Savage, J. E.;
Snyder, K. R. (1994) Physiology, morphology, and ozone uptake of leaves of black cherry
seedlings, saplings, and canopy trees. Environ. Pollut.: in press.
Freeman, A. M., III. (1979) The benefits of air and water pollution control: a review and synthesis of recent
estimates. Washington, DC: Council on Environmental Quality. Available from: NTIS, Springfield,
VA; PB80-178759.
5-300
-------
Freer-Smith, P. H.; Dobson, M. C. (1989) Ozone flux to Picea sitchensis (Bong) Carr and Picea abies (L) Karst
during short episodes and the effects of these on transpiration and photosynthesis. Environ. Pollut.
59: 161-176.
Freer-Smith, P. H.; Taylor, G. (1992) Comparative evaluation of the effects of gaseous pollutants, acidic
deposition and mineral deficiencies on gas exchange of trees. Agric. Ecosyst. Environ. 42: 321-332.
Friend, A. D. (1991) Use of a model of photosynthesis and leaf microenvironment to predict optimal stomatal
conductance and leaf nitrogen partitioning. Plant Cell Environ. 14: 895-905.
Friend, A. L.; Tomlinson, P. T. (1992) Mild ozone exposure alters 14C dynamics in foliage of Pinus taeda L.
TreePhysiol. 11: 215-227.
Friend, A. L.; Tomlinson, P. T.; Dickson, R. E.; O'Neill, E. G.; Edwards, N. T.; Taylor, G. E., Jr. (1992)
Biochemical composition of loblolly pine reflects pollutant exposure. Tree Physiol. 11: 35-47.
Fuentes, J. D.; Gillespie, T. J. (1992) A gas exchange system to study the effects of leaf surface wetness on the
deposition of ozone. Atmos. Environ. Part A 26: 1165-1173.
Fuentes, J. D.; Gillespie, T. J.; den Hartog, G.; Neumann, H. H. (1992) Ozone deposition onto a deciduous forest
during dry and wet conditions. Agric. For. Meteorol. 62: 1-18.
Fuhrer, J.; Egger, A.; Lehnherr, B.; Grandjean, A.; Tschannen, W. (1989) Effects of ozone on the yield of spring
wheat (Triticum aestivum L., cv. Albis) grown in open-top field chambers. Environ. Pollut. 60:
273-289.
Fuhrer, G.; Dunkl, M.; Knoppick, D.; Selinger, H.; Blank, L. W.; Payer, H. D.; Lange, O. L. (1990) Effects of
low-level long-term ozone fumigation and acid mist on photosynthesis and stomata of clonal
Norway spruce (Picea abies (L.) Karst.). Environ. Pollut. 64: 279-293.
Fuhrer, J.; Grimm, A. G.; Tschannen, W.; Shariat-Madari, H. (1992) The response of spring wheat (Triticum
aestivum L.) to ozone at higher elevations: II. changes in yield, yield components and grain quality
in response to ozone flux. New Phytol. 121: 211-219.
Gab, S.; Hellpointner, E.; Turner, W. V.; Korte, F. (1985) Hydroxymethyl hydroperoxide and bis(hydroxymethyl)
peroxide from gas-phase ozonolysis of naturally occuring alkenes. Nature (London) 316: 535-536.
Ganslandt, E.; Svensson, S. (1980) Stress relaxation tests for determination of ozone attack on rubber. Polym.
Test. 1: 81-89.
Garcia, P.; Dixon, B.; Mjelde, J.; Adams, R. (1986) Measuring the benefits of environmental change using a
duality approach: the case of ozone and Illinois cash grain farms. J. Environ. Econ. Manage.
13: 69-80.
Garner, J. H. B. (1991) Ozone exposure and nitrogen loading in the forests of eastern North America.
In: Berglund, R. L.; Lawson, D. R.; McKee, D. J., eds. Tropospheric ozone and the environment:
papers from an international conference; March 1990; Los Angeles, CA. Pittsburgh, PA: Air &
Waste Management Association; pp. 289-310. (A&WMA transactions series no. TR-19).
Garner, J. H. B. (1994) Nitrogen oxides, plant metabolism, and forest ecosystem response. In: Alscher, R. G.;
Wellburn, A. R., eds. Plant responses to the gaseous environment: molecular, metabolic and
physiological aspects, [3rd international symposium on air pollutants and plant metabolism];
June 1992; Blacksburg, VA. London, United Kingdom: Chapman & Hall; pp. 301-314.
5-301
-------
Garner, J. H. B.; Pagano, T.; Cowling, E. B. (1989) An evaluation of the role of ozone, acid deposition, and
other airborne pollutants in the forests of eastern North America. Asheville, NC: U.S. Department
of Agriculture, Forest Service, Southeastern Forest Experiment Station; general technical
report SE-59.
Gillespie, C. T.; Winner, W. E. (1989) Development of lines of radish differing in resistance to O3 and SO2. New
Phytol. 112: 353-361.
Goldstein, R.; Person, S. (1994) Response of plants to interacting stresses (ROPIS): program rationale, design,
and implications. J. Environ. Qual. 23: 407-411.
Goodyear, S. N.; Ormrod, D. P. (1988) Tomato response to concurrent and sequential NO2 and O3 exposures.
Environ. Pollut. 51: 315-326.
Gorissen, A.; van Veen, J. A. (1988) Temporary disturbance of translocation of assimilates in Douglas firs
caused by low levels of ozone and sulfur dioxide. Plant Physiol. 88: 559-563.
Gorissen, A.; Schelling, G. C.; van Veen, J. A. (1991a) Concentration-dependent effects of ozone on
translocation of assimilates in Douglas fir. J. Environ. Qual. 20: 169-173.
Gorissen, A.; Joosten, N. N.; Jansen, A. E. (1991b) Effects of ozone and ammonium sulphate on carbon
partitioning to mycorrhizal roots of juvenile Douglas fir. New Phytol. 119: 243-250.
Graham, S.; Ormrod, D. P. (1989) Sorption of ozone by 'New Yorker' tomato leaves. Environ. Pollut.
58: 213-220.
Grandjean, A.; Fuhrer, J. (1989) Growth and leaf senescence in spring wheat (Triticum aestivum) grown at
different ozone concentrations in open-top field chambers. Physiol. Plant. 77: 389-394.
Grandjean Grimm, A.; Fuhrer, J. (1992a) The response of spring wheat (Triticum aestivum L.) to ozone at higher
elevations: I. measurement of ozone and carbon dioxide fluxes in open-top field chambers. New
Phytol. 121: 201-210.
Grandjean Grimm, A.; Fuhrer, J. (1992b) The response of spring wheat (Triticum aestivum L.) to ozone at higher
elevations. III. Responses of leaf and canopy gas exchange, and chlorophyll fluorescence to ozone
flux. New Phytol. 122: 321-328.
Greenhut, G. K. (1983) Resistance of a pine forest to ozone uptake. Boundary Layer Meteorol. 27: 387-391.
Gregorius, H.-R. (1989) The importance of genetic multiplicity for tolerance of atmospheric pollution. In: Scholz,
F.; Gregorius, H.-R.; Rudin, D., eds. Genetic effects of air pollutants in forest tree populations:
proceedings of the joint meeting of the IUFRO working parties; August 1987; Grosshansdorf, West
Germany. Berlin, Germany: Springer-Verlag; pp. 163-172.
Greitner, C. S.; Winner, W. E. (1988) Increases in 813C values of radish and soybean plants caused by ozone.
New Phytol. 108: 489-494.
Greitner, C. S.; Winner, W. E. (1989) Effects of O3 on alder photosynthesis and symbiosis with Frankia.
New Phytol. Ill: 647-656.
Grime, J. P. (1979) Plant strategies and vegetation processes. Chichester, United Kingdom: John Wiley & Sons.
Grosjean, D.; Parmar, S. (1991) Removal of air pollutant mixtures from museum display cases. Stud. Conserv.
36: 129-141.
5-302
-------
Grosjean, D.; Whitmore, P. M.; De Moor, C. P.; Cass, G. R.; Drazik, J. R. (1987) Fading of alizarin and related
artists' pigments by atmospheric ozone: reaction products and mechanisms. Environ. Sci. Technol.
21: 635-643.
Grosjean, D.; Whitmore, P. M.; Cass, G. R.; Drazik, J. R. (1988a) Ozone fading of natural organic colorants:
mechanisms and products of the reaction of ozone with indigos. Environ. Sci. Technol. 22: 292-298.
Grosjean, D.; Whitmore, P. M.; De Moor, C. P.; Cass, G. R.; Drazik, J. R. (1988b) Ozone fading of organic
colorants: products and mechanism of the reaction of ozone with curcumin. Environ. Sci. Technol.
22: 1357-1361.
Grosjean, D.; Whitmore, P. M.; Cass, G. R.; Drazik, J. R. (1989) Ozone fading of triphenylmethane colorants:
reaction products and mechanisms. Environ. Sci. Technol. 23: 1164-1167.
Grosjean, D.; Grosjean, E.; Williams, E. L., II. (1993) Fading of artists' colorants by a mixture of photochemical
oxidants. Atmos. Environ. Part A 27: 765-772.
Gross, L. J.; Kirschbaum, M. U. F.; Pearcy, R. W. (1991) A dynamic model of photosynthesis in varying light
taking account of stomatal conductance, C3-cycle intermediates, photorespiration and Rubisco
activation. Plant Cell Environ. 14: 881-893.
Gralke, N. E.; Miller, P. R.; Wilborn, R. D.; Hahn, S. (1989) Photosynthetic response of giant sequoia seedlings
and rooted branchlets of mature foliage to ozone fumigation. In: Olson, R. K.; Lefohn, A. S., eds.
Effects of air pollution on western forests [an A&WMA symposium; June; Anaheim, CA].
Pittsburgh, PA: Air and Waste Management Association; pp. 429-441 (APCA transactions series:
no. 16).
Granhage, L.; Jager, H.-J. (1994a) Atmospheric ozone exposure-potential for vegetation: how suitable are critical
levels? In: Fuhrer, J.; Achermann, B., eds. Critical levels for ozone: a UN-ECE workshop report;
November 1993; Bern, Switzerland. Liebefeld-Bern, Switzerland: Federal Research Station for
Agricultural Chemistry and Environmental Hygiene; pp. 222-230.
Granhage, L.; Jager, H.-J. (1994b) Influence of the atmospheric conductivity on the ozone exposure of plants
under ambient conditions: considerations for establishing ozone standards to protect vegetation.
Environ. Pollut. 85: 125-129.
Granhage, L.; Dammgen, U.; Haenel, H.-D.; Jager, H.-J.; Holl, A.; Schmitt, J.; Hanewald, K. (1993a) A new
potential air-quality criterion derived from vertical flux densities of ozone and from plant response.
Angew. Bot. 67: 9-13.
Granhage, L.; Dammgen, U.; Hertstein, U.; Jager, H.-J. (1993b) Response of grassland ecosystem to air
pollutants: I—experimental concept and site of the Braunschweig grassland investigation program.
Environ. Pollut. 81: 163-171.
Granhage, L.; Dammgen, U.; Haenel, H.-D.; Jager, H.-J. (1994) Response of a grassland ecosystem to air
pollutants: III—the chemical climate: vertical flux densities of gaseous species in the atmosphere
near the ground. Environ. Pollut. 85: 43-49.
Guderian, R. (1977) Discussion of the suitability of plant responses as a basis for air pollution control measures.
In: Air pollution: phytotoxicity of acidic gases and its significance in air pollution control.
Berlin, Federal Republic of Germany: Springer Verlag; pp. 75-97. (Billings, W. D.; Golley, F.;
Lange, O. L.; Olson, J. S., eds. Ecological studies: analysis and synthesis, v. 22).
5-303
-------
Guderian, R., ed. (1985) Air pollution by photochemical oxidants: formation, transport, control, and effects on
plants. New York, NY: Springer-Verlag. (Billings, W. D.; Golley, F.; Lange, O. L.; Olson, J. S.;
Remmert, H., eds. Ecological studies: analysis and synthesis: v. 52).
Guderian, R.; Tingey, D. T.; Rabe, R. (1985) Effects of photochemical oxidants on plants. In: Guderian, R., ed.
Air pollution by photochemical oxidants: formation, transport, control, and effects on plants. Berlin,
Federal Republic of Germany: Springer-Verlag; pp. 127-333. (Billings, W. D.; Golley, F.; Lange, O.
L.; Olson, J. S.; Remmert, H., eds. Ecological studies: analysis and synthesis, v. 52).
Gumpertz, M. L.; Pantula, S. G. (1992) Nonlinear regression with variance components. JASA J. Am. Stat.
Assoc. 87: 201-209.
Gumpertz, M. L.; Rawlings, J. O. (1991) Nonlinear regression for split plot experiments. In: Proceedings of the
1990 Kansas State University conference on applied statistics and agricultural experimental stations.
Manhattan, KS; pp. 156-168.
Gumpertz, M. L.; Rawlings, J. O. (1992) Nonlinear regression with variance components: modeling effects of
ozone on crop yield. Crop Sci. 32: 219-224.
Gupta, A. S.; Alscher, R. G.; McCune, D. (1991) Response of photosynthesis and cellular antioxidants to ozone
mPopulus leaves. Plant Physiol. 96: 650-655.
Hacskaylo, E. (1973) The Torrey symposium on current aspects of fungal development: IV. dependence of
mycorrhizal fungi on hosts. Bull. Torrey Bot. Club 100: 217-223.
Hain, F. P. (1987) Interactions of insects, trees and air pollutants. Tree Physiol. 3: 93-102.
Hain, F. P.; Arthur, F. H. (1985) The role of atmospheric deposition in the latitudinal variation of Fraser fir
mortality caused by the balsam woolly adelgid, Adelges piceae (Ratz.) (Hemipt, Adelgidae):
a hypothesis. Z. Angew. Entomol. 99: 145-152.
Hale-Marie, B.; Dutton, R. G.; Allen, O. B.; Ormrod, D. P.; Goodyear, S. N.; Pyear, L. G. (1991) Design and
verification of a programmable gas dispensing system for exposing plants to dynamic concentrations
of air pollutants. J. Air Waste Manage. Assoc. 41: 460-463.
Hampp, R.; Einig, W.; Egger, B. (1990) Energy and redox status, and carbon allocation in one- to three-year-old
spruce needles. Environ. Pollut. 68: 305-318.
Hanson, G. P.; Addis, D. H. (1975) The stigma: not a selection site for ozone tolerance in Petunia hybrida.
Genetics 80: S40.
Hanson, P. J.; McLaughlin, S. B.; Edwards, N. T. (1988) Net CO2 exchange of Pinus taeda shoots exposed to
variable ozone levels and rain chemistries in field and laboratory settings. Physiol. Plant.
74: 635-642.
Harkov, R.; Brennan, E. (1980) The influence of soil fertility and water stress on the ozone response of hybrid
poplar trees. Phytopathology 70: 991-994.
Harley, J. L.; Smith, S. E. (1983) Mycorrhizal symbiosis. New York, NY: Academic Press.
Hausladen, A.; Madamanchi, N. R.; Fellows, S.; Alscher, R. G.; Amundson, R. G. (1990) Seasonal changes in
antioxidants in red spruce as affected by ozone. New Phytol. 115: 447-458.
5-304
-------
Hayes, E. M; Skelly, J. M. (1977) Transport of ozone from the northeast U.S. into Virginia and its effect on
eastern white pines. Plant Dis. Rep. 61: 778-782.
Haylock, J. C.; Rush, J. L. (1976) Studies on the ozone fading of anthraquinone dyes on nylon fibers. Text. Res.
J. 46: 1-8.
Haylock, J. C.; Rush, J. L. (1978) Studies on the ozone fading of anthraquinone dyes on nylon fibers. Part II:
In-service performance. Text. Res. J. 48: 143-149.
Haynes, R. W.; Adams, D. M. (1992) Assessing economic impacts of air pollution damage to U.S. forests. In: de
Steiguer, J. E., ed. The economic impact of air pollution on timber markets: studies from North
America and Europe. Asheville, NC: U.S. Department of Agriculture, Southeastern Forest
Experiment Station; general technical report no. SE-75.
Haynie, F. H.; Spence, J. W. (1984) Air pollution damage to exterior household paints. J. Air Pollut.
Control Assoc. 34: 941-944.
Haynie, F. H.; Spence, J. W.; Upham, J. B. (1976) Effects of gaseous pollutants on materials - a chamber study.
Research Triangle Park, NC: U.S. Environmental Protection Agency, Environmental Sciences
Research Laboratory; EPA report no. EPA-600/3-76/015. Available from: NTIS, Springfield, VA;
PB-251580.
Heagle, A. S. (1970) Effect of low-level ozone fumigations on crown rust of oats. Phytopathology 60: 252-254.
Heagle, A. S. (1975) Response of three obligate parasites to ozone. Environ. Pollut. 9: 91-95.
Heagle, A. S. (1977) Effect of ozone on parasitism of corn by Helminthosporium maydis. Phytopathology
67: 616-618.
Heagle, A. S. (1979) Effects of growth media, fertiliser rate and hour and season of exposure on sensitivity of
four soybean cultivars to ozone. Environ. Pollut. 18: 313-322.
Heagle, A. S. (1989) Ozone and crop yield. Annu. Rev. Phytopathol. 27: 397-423.
Heagle, A. S.; Heck, W. W. (1974) Predisposition of tobacco to oxidant air pollution injury by previous exposure
to oxidants. Environ. Pollut. 7: 247-252.
Heagle, A. S.; Key, L. W. (1973a) Effect of ozone on the wheat stem rust fungus. Phytopathology 63: 397-400.
Heagle, A. S.; Key, L. W. (1973b) Effect of Puccinia graminis f. sp. tritici on ozone injury in wheat.
Phytopathology 63: 609-613.
Heagle, A. S.; Letchworth, M. B. (1982) Relationships among injury, growth, and yield responses of soybean
cultivars exposed to ozone at different light intensities. J. Environ. Qual. 11: 690-694.
Heagle, A. S.; Strickland, A. (1972) Reaction of Erysiphe graminis f. sp. hordei to low levels of ozone.
Phytopathology 62: 1144-1148.
Heagle, A. S.; Body, D. E.; Neely, G. E. (1974) Injury and yield responses of soybean to chronic doses of ozone
and sulfur dioxide in the field. Phytopathology 64: 132-136.
Heagle, A. S.; Philbeck, R. B.; Letchworth, M. B. (1979a) Injury and yield responses of spinach cultivars to
chronic doses of ozone in open-top field chambers. J. Environ. Qual. 8: 368-373.
5-305
-------
Heagle, A. S.; Spencer, S.; Letchworth, M. B. (1979b) Yield response of winter wheat to chronic doses of ozone.
Can. J. Bot. 57: 1999-2005.
Heagle, A. S.; Philbeck, R. B.; Rogers, H. H.; Letchworth, M. B. (1979c) Dispensing and monitoring ozone in
open-top field chambers for plant-effects studies. Phytopathology 69: 15-20.
Heagle, A. S.; Letchworth, M. B.; Mitchell, C. A. (1983a) Effects of growth medium and fertilizer rate on the
yield response of soybeans exposed to chronic doses of ozone. Phytopathology 73: 134-139.
Heagle, A. S.; Heck, W. W.; Rawlings, J. O.; Philbeck, R. B. (1983b) Effects of chronic doses of ozone and
sulfur dioxide on injury and yield of soybeans in open-top field chambers. Crop Sci. 23: 1184-1191.
Heagle, A. S.; Heck, W. W.; Lesser, V. M.; Rawlings, J. O.; Mowry, F. L. (1986a) Injury and yield response of
cotton to chronic doses of ozone and sulfur dioxide. J. Environ. Qual. 15: 375-382.
Heagle, A. S.; Lesser, V. M.; Rawlings, J. O.; Heck, W. W.; Philbeck, R. B. (1986b) Response of soybeans to
chronic doses of ozone applied as constant or proportional additions to ambient air. Phytopathology
76: 51-56.
Heagle, A. S.; Flagler, R. B.; Patterson, R. P.; Lesser, V. M.; Shafer, S. R.; Heck, W. W. (1987a) Injury and
yield response of soybean to chronic doses of ozone and soil moisture deficit. Crop Sci.
27: 1016-1024.
Heagle, A. S.; Heck, W. W.; Lesser, V. M.; Rawlings, J. O. (1987b) Effects of daily ozone exposure duration
and concentration fluctuation on yield of tobacco. Phytopathology 77: 856-862.
Heagle, A. S.; Kress, L. W.; Temple, P. J.; Kohut, R. J.; Miller, J. E.; Heggestad, H. E. (1988a) Factors
influencing ozone dose-yield response relationships in open-top field chamber studies. In: Heck, W.
W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from air pollutants: proceedings of
an international conference; October, 1987; Raleigh, NC. New York, NY: Elsevier Applied Science;
pp. 141-179.
Heagle, A. S.; Miller, J. E.; Heck, W. W.; Patterson, R. P. (1988b) Injury and yield response of cotton to chronic
doses of ozone and soil moisture deficit. J. Environ. Qual. 17: 627-635.
Heagle, A. S.; Philbeck, R. B.; Ferrell, R. E.; Heck, W. W. (1989a) Design and performance of a large, field
exposure chamber to measure effects of air quality on plants. J. Environ. Qual. 18: 361-368.
Heagle, A. S.; Rebbeck, J.; Shafer, S. R.; Blum, U.; Heck, W. W. (1989b) Effects of long-term ozone exposure
and soil moisture deficit on growth of a ladino clover-tall fescue pasture. Phytopathology 79:
128-136.
Heagle, A. S.; McLaughlin, M. R.; Miller, J. E.; Joyner, R. L.; Spruill, S. E. (1991a) Adaptation of a white
clover population to ozone stress. New Phytol. 119: 61-68.
Heagle, A. S.; Miller, J. E.; Rawlings, J. O.; Vozzo, S. F. (1991b) Effect of growth stage on soybean response to
chronic ozone exposure. J. Environ. Qual. 20: 562-570.
Heagle, A. S.; McLaughlin, M. R.; Miller, J. E.; Joyner, R. L. (1992) Response of two white clover clones to
peanut stunt virus and ozone. Phytopathology 82: 254-258.
Heagle, A. S.; Miller, J. E.; Sherrill. D. E.; Rawlings, J. O. (1993) Effects of ozone and carbon dioxide mixtures
on two clones of white clover. New Phytol. 123: 751-762.
5-306
-------
Heagle, A. S.; Miller, J. E.; Sherrill, D. E. (1994) A white clover system to estimate effects of tropospheric
ozone on plants. J. Environ. Qual. 23: 613-621.
Heath, R. L. (1988) Biochemical mechanisms of pollutant stress. In: Heck, W. W.; Taylor, O. C.; Tingey, D. T.,
eds. Assessment of crop loss from air pollutants: proceedings of an international conference;
October, 1987; Raleigh, NC. London, United Kingdom: Elsevier Applied Science; pp. 259-286.
Heck, W. W.; Dunning, J. A. (1967) The effects of ozone on tobacco and pinto bean as conditioned by several
ecological factors. J. Air Pollut. Control Assoc. 17: 112-114.
Heck, W. W.; Heagle, A. S. (1970) Measurement of photochemical air pollution with a sensitive monitoring
plant. J. Air Pollut. Control Assoc. 20: 97-99.
Heck, W. W.; Tingey, D. T. (1971) Ozone. Time-concentration model to predict acute foliar injury. In: Englund,
H. M.; Beery, W. T., eds. Proceedings of the second international clean air congress; December
1970; Washington, DC. New York, NY: Academic Press; pp. 249-255.
Heck, W. W.; Dunning, J. A,; Hindawi, I. J. (1965) Interactions of environmental factors on the sensitivity of
plants to air pollution. J. Air Pollut. Control Assoc. 15: 511-515.
Heck, W. W.; Dunning, J. A.; Hindawi, I. J. (1966) Ozone: nonlinear relation of dose and injury in plants.
Science (Washington, DC) 151: 577-578.
Heck, W. W.; Fox, F. L.; Brandt, C. S.; Dunning, J. A. (1969) Tobacco, a sensitive monitor for photochemical
air pollution. Cincinnati, OH: U.S. Department of Health, Education, and Welfare, National Air
Pollution Control Administration; publication no. AP-55. Available from: NTIS, Springfield, VA;
PB-190257.
Heck, W. W.; Larsen, R. L; Heagle, A. S. (1980) Measuring the acute dose-response of plants to ozone.
In: Teng, P. S.; Krupa, S. V., eds. Crop loss assessment: proceedings of E. C. Stakman
commemorative symposium. St. Paul, MN: University of Minnesota, Agricultural Experiment
Station; pp. 32-49; miscellaneous publication no. 7.
Heck, W. W.; Taylor, O. C.; Adams, R.; Bingham, G.; Miller, J.; Preston, E.; Weinstein, L. (1982) Assessment
of crop loss from ozone. J. Air Pollut. Control Assoc. 32: 353-361.
Heck, W. W.; Adams, R. M.; Cure, W. W.; Heagle, A. S.; Heggestad, H. E.; Kohut, R. J.; Kress, L. W.;
Rawlings, J. O.; Taylor, O. C. (1983) A reassessment of crop loss from ozone. Environ. Sci.
Technol. 17: 573A-581A.
Heck, W. W.; Cure, W. W.; Rawlings, J. O.; Zaragoza, L. J.; Heagle, A. S.; Heggestad, H. E.; Kohut, R. J.;
Kress, L. W.; Temple, P. J. (1984) Assessing impacts of ozone on agricultural crops: II. crop yield
functions and alternative exposure statistics. J. Air Pollut. Control Assoc. 34: 810-817.
Heck, W. W.; Dunning, J. A.; Reinert, R. A.; Prior, S. A.; Rangappa, M.; Benepal, P. S. (1988) Differential
responses of four bean cultivars to chronic doses of ozone. J. Am. Soc. Hortic. Sci. 113: 46-51.
Heck, W. W.; Heagle, A. S.; Miller, J. E.; Rawlings, J. O. (1991) A national program (NCLAN) to assess the
impact of ozone on agricultural resources. In: Berglund, R. L.; Lawson, D. R.; McKee, D. J., eds.
Tropospheric ozone and the environment: papers from an international conference; March 1990; Los
Angeles, CA. Pittsburgh, PA: Air & Waste Management Association; pp. 225-254. (A&WMA
transactions series no. TR-19).
5-307
-------
Heck, W. W.; Heagle, J. E.; Miller, J. E. (1994) Factors affecting plant response to ozone: an overview.
In: Kuttler, W.; Jochimsen, M, eds. Immissionsokologische Forschung im Wandel der Zeit
Festschrift fur Robert Guderian. Westarp Wissenschaften, Uhlichstrasse; pp. 113-130.
Heggestad, H. E. (1988) Reduction in soybean seed yields by ozone air pollution? JAPCA 38: 1040-1041.
Heggestad, H. E.; Bennett, J. H. (1981) Photochemical oxidants potentiate yield losses in snap beans attributable
to sulfur dioxide. Science (Washington, DC) 213: 1008-1010.
Heggestad, H. E.; Lesser, V. M. (1990) Effects of ozone, sulfur dioxide, soil water deficit, and cultivar on yields
of soybean. J. Environ. Qual. 19: 488-495.
Heggestad, H. E.; Menser, H. A. (1962) Leaf spot-sensitive tobacco strain Bel W-3, a biological indicator of the
air pollutant ozone. Phytopathology 52: 735.
Heggestad, H. E.; Middleton, J. T. (1959) Ozone in high concentrations as cause of tobacco leaf injury. Science
(Washington, DC) 129: 208-210.
Heggestad, H. E.; Gish, T. J.; Lee, E. H.; Bennett, J. H.; Douglass, L. W. (1985) Interaction of soil moisture
stress and ambient ozone on growth and yields of soybeans. Phytopathology 75: 472-477.
Heggestad, H. E.; Anderson, E. L.; Gish, T. J.; Lee, E. H. (1988) Effects of ozone and soil water deficit on roots
and shoots of field-grown soybeans. Environ. Pollut. 50: 259-278.
Held, A. A.; Mooney, H. A.; Gorham, J. N. (1991) Acclimation to ozone stress in radish: leaf demography and
photosynthesis. New Phytol. 118: 417-423.
Hershaft, A.; Freeman, A. M., Ill; Crocker, T. D.; Stevens, J. B. (1978) Critical review of estimating benefits of
air and water pollution control. Washington, DC: U.S. Environmental Protection Agency, Office of
Research and Development; EPA report no. EPA-600/5-78-014. Available from: NTIS, Springfield,
VA; PB-285555.
Hewitt, C. N.; Kok, G. L.; Fall, R. (1990) Hydroperoxides in plants exposed to ozone mediate air pollution
damage to alkene emitters. Nature (London) 344: 56-58.
Hibben, C. R.; Taylor, M. P. (1975) Ozone and sulphur dioxide effects on the lilac powdery mildew fungus.
Environ. Pollut. 9: 107-114.
Hicks, B. B.; Baldocchi, D. D.; Meyers, T. P.; Hosker, R. P., Jr.; Matt, D. R. (1987) A preliminary multiple
resistance routine for deriving dry deposition velocities from measured quantities. Water Air Soil
Pollut. 36: 311-330.
Higgs, E. S. (1987) Changing value perspectives in natural resource allocation: from market to ecosystem. Trans.
Am. Fish. Soc. 116: 525-531.
Hiltbrunner, E.; Fluckiger, W. (1992) Altered feeding preference of beech weevil Rhynchaenus fagi L. for beech
foliage under ambient air pollution. Environ. Pollut. 75: 333-336.
Hinckley, T.; Ford, D.; Segura, G.; Sprugel, D. (1992) Key processes from tree to stand level. In: Wall, G., ed.
Implications of climate change for Pacific Northwest forest management. Waterloo, ON, Canada:
University of Waterloo, Department of Geography; pp. 33-43. (Department of Geography
publication series: occasional paper no. 15).
5-308
-------
Ho, I.; Trappe, J. M. (1984) Effects of ozone exposure on mycorrhiza formation and growth of Festuca
arundinacea. Environ. Exp. Bot. 24: 71-74.
Hofmann, C. M.; Miller, R. L. (1969) Resistance of passenger tires to atmospheric exposure. J. Mater. 4: 31-43.
Hofstra, G.; Beckerson, D. W. (1981) Foliar responses of five plant species to ozone and a sulphur dioxide/ozone
mixture after a sulphur dioxide pre-exposure. Atmos. Environ. 15: 383-389.
Hofstra, G.; Tonneijck, A. E. G.; Allen, O. B. (1985) Cumulative effects of low levels of SO2 on O3 sensitivity
in bean and cucumber. Atmos. Environ. 19: 195-198.
Hogsett, W. E.; Plocher, M.; Wildman, V.; Tingey, D. T.; Bennett, J. P. (1985a) Growth response of two
varieties of slash pine seedlings to chronic ozone exposures. Can. J. Bot. 63: 2369-2376.
Hogsett, W. E.; Tingey, D. T.; Holman, S. R. (1985b) A programmable exposure control system for
determination of the effects of pollutant exposure regimes on plant growth. Atmos. Environ.
19: 1135-1145.
Hogsett, W. E.; Olszyk, D.; Ormrod, D. P.; Taylor, G. E., Jr.; Tingey, D. T. (1987a) Air pollution exposure
systems and experimental protocols: volume 1: a review and evaluation of performance.
Corvallis, OR: U.S. Environmental Protection Agency, Environmental Research Laboratory;
EPA report no. EPA/600/3-87/037a. Available from: NTIS, Springfield, VA; PB88-181680.
Hogsett, W. E.; Olszyk, D.; Ormrod, D. P.; Taylor, G. E., Jr.; Tingey, D. T. (1987b) Air pollution exposure
systems and experimental protocols: volume 2: description of facilities. Corvallis, OR:
U.S. Environmental Protection Agency, Environmental Research Laboratory; EPA report no.
EPA/600/3-87/037b. Available from: NTIS, Springfield, VA; PB88-181698.
Hogsett, W. E.; Tingey, D. T.; Lee, E. H. (1988) Ozone exposure indices: concepts for development and
evaluation of their use. In: Heck, W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss
from air pollutants: proceedings of an international conference; October 1987; Raleigh, NC. New
York, NY: Elsevier Applied Science; pp. 107-138.
Hogsett, W. E.; Tingey, D. T.; Hendricks, C.; Rossi, D. (1989) Sensitivity of western conifers to SO2 and
seasonal interaction of acid fog and ozone. In: Olson, R. K.; Lefohn, A. S., eds. Effects of air
pollution on western forests [an A&WMA symposium; June; Anaheim, CA]. Pittsburgh, PA: Air
Pollution Control Association; pp. 469-491 (APCA transactions series: no. 16).
Hogsett, W. E.; Herstrom, A. A.; Laurence, J. A.; Lee, E. H.; Weber, J. E.; Tingey, D. T. (1995) Risk
characterization of tropospheric ozone to forests. In: Lee, S. D.; Schneider, T., eds. Comparative
risk analysis and priority setting for air pollution issues: proceedings of the 4th U.S.-Dutch
international symposium; June 1993; Keystone, CO. Pittsburgh, PA: Air & Waste Management
Association; pp. 119-145. (AWMA publication no. VTP-43).
Holley, J. D.; Hofstra, G.; Hall, R. (1985) Effect of reducing oxidant injury and early blight on fresh weight and
tuber density of potato. Phytopathology 75: 529-532.
Horton, S. J.; Reinert, R. A.; Heck, W. W. (1990) Effects of ozone on three open-pollinated families of Pinus
taeda L. grown in two substrates. Environ. Pollut. 65: 279-292.
Hosker, R. P., Jr.; Lindberg, S. E. (1982) Review: atmospheric deposition and plant assimilation of gases and
particles. Atmos. Environ. 16: 889-910.
5-309
-------
Houpis, J. L. I; Costella, M. P.; Cowles, S. (1991) A branch exposure chamber for fumigating ponderosa pine to
atmospheric pollution. J. Environ. Qual. 20: 467-474.
Houston, D. B. (1974) Response of selected Pinus strobus L. clones to fumigations with sulfur dioxide and
ozone. Can. J. For. Res. 4: 65-68.
Houston, D. B.; Dochinger, L. S. (1977) Effects of ambient air pollution on cone, seed, and pollen characteristics
in eastern white and red pines. Environ. Pollut. 12: 1-5.
Howell, R. K.; Graham, J. H. (1977) Interaction of ozone and bacterial leafspot of alfalfa. Plant Dis. Rep.
61: 565-567.
Huang, T. R.; Aycock, M. K., Jr.; Mulchi, C. L. (1975) Heterosis and combining ability estimates for air
pollution damage, primarily ozone, in Maryland tobacco. Crop Sci. 15: 785-789.
Huevel, H. M.; Huisman, R.; Schmidt, H. M. (1978) Ozone fading of disperse blue 3 on nylon 6 fibers.
The influence of physical fiber properties. Text. Res. J. 48: 376-384.
Hughes, P. R. (1988) Insect populations on host plants subjected to air pollution. In: Heinrichs, E. A., ed. Plant
stress-insect interactions. New York, NY: John Wiley & Sons, Inc.; pp. 249-319. (Metcalf, R. L.;
Stumm, W., eds. Environmental science and technology series).
Ingham, R. E.; Trofymow, J. A.; Ingham, E. R.; Coleman, D. C. (1985) Interactions of bacteria, fungi, and their
nematode grazers: effects on nutrient cycling and plant growth. Ecol. Monogr. 55: 119-140.
Irving, P. M.; Kress, L. W.; Prepejchal, W.; Smith, H. J. (1988) Studies on the interaction of ozone with drought
stress or with sulfur dioxide on soybeans and corn. Argonne, IL: U.S. Environmental Protection
Agency, Argonne National Laboratory; technical report no. ANL-88-31.
Jacobson, J. S. (1977) The effects of photochemical oxidants on vegetation. In: Ozon und Begleitsubstanzen im
photochemischen Smog: das Kolloquium [Ozone and related substances in photochemical smog: the
colloquium]; September 1976; Dtisseldorf, Federal Republic of Germany. Dtisseldorf,
Federal Republic of Germany: VDI-Verlag GmbH; pp. 163-173. (VDI-Berichte nr. 270).
James, R. L.; Cobb, F. W., Jr.; Miller, P. R.; Parmeter, J. R., Jr. (1980a) Effects of oxidant air pollution on
susceptibility of pine roots to Fames annosus. Phytopathology 70: 560-563.
James, R. L.; Cobb, F. W., Jr.; Wilcox, W. W.; Rowney, D. L. (1980b) Effects of photochemical oxidant injury
of ponderosa and Jeffrey pines on susceptibility of sapwood and freshly cut stumps to Fames
annosus. Phytopathology 70: 704-708.
Jeffords, M. R.; Endress, A. G. (1984) Possible role of ozone in tree defoliation by the gypsy moth (Lepidoptera:
Lymantriidae). Environ. Entomol. 13: 1249-1252.
Jensen, K. F. (1981) Ozone fumigation decreased the root carbohydrate content and dry weight of green ash
seedlings. Environ. Pollut. Ser. A 26: 147-152.
Jensen, K. F.; Dochinger, L. S. (1989) Response of eastern hardwood species to ozone, sulfur dioxide and acid
precipitation. JAPCA 39: 852-855.
Jensen, K. F.; Patton, R. L. (1990) Response of yellow-poplar (Liriodendron tulipifera L.) seedlings to simulated
acid rain and ozone -1. Growth modifications. Environ. Exp. Bot. 30: 59-66.
5-310
-------
Jensen, K. F.; Roberts, B. R. (1986) Changes in yellow poplar stomatal resistance with SO2 and O3 fumigation.
Environ. Pollut. Ser. A 41: 235-245.
Johnsen, I.; Mortensen, L.; Moseholm, L.; Ro-Poulsen, H. (1988) Ozone sensitivity of open-top chamber grown
cultivars of spring wheat and spring rape. In: Mathy, P., ed. Air pollution and ecosystems:
proceedings of an international symposium; May 1987; Grenoble, France. Boston, MA: D. Reidel
Publishing Company; pp. 637-640.
Johnson, A. H.; Siccama, T. G. (1983) Acid deposition and forest decline. Environ. Sci. Technol.
17: 294A-305A.
Johnson, D. W.; Taylor, G. E. (1989) Role of air pollution in forest decline in eastern North America. Water Air
Soil Pollut. 48: 21-43.
Johnson, A. H.; Friedland, A. J.; Siccama, T. C. (1984) Recent changes in the growth of forest trees in the
northeastern United States. In: Davis, D. D.; Millen, A. A.; Dochinger, L., eds. Air pollution and
the productivity of the forest: proceedings of the symposium; October 1983; Washington, DC.
Arlington, VA: Izaak Walton League of America; pp. 121-142.
Johnson, I. R.; Melkonian, J. J.; Thornley, J. H. M.; Riha, S. J. (1991) A model of water flow through plants
incorporating shoot/root message control of stomatal conductance. Plant Cell Environ. 14: 531-544.
Johnson, A. H.; McLaughlin, S. B.; Adams, M. B.; Cook, E. R.; DeHayes, D. H.; Eagar, C.; Fernandez, I. J.;
Johnson, D. W.; Kohut, R. J.; Mohnen, V. A.; Nicholas, N. S.; Peart, D. R.; Schier, G. A.; White,
P. S. (1992) Synthesis and conclusions from epidemiological and mechanistic studies of red spruce
decline. In: Eagar, C.; Adams, M. B., eds. Ecology and decline of red spruce in the eastern United
States. New York, NY: Springer-Verlag; pp. 385-411. (Ecological studies: v. 96).
Johnston, J. W., Jr.; Heagle, A. S. (1982) Response of chronically ozonated soybean plants to an acute ozone
exposure. Phytopathology 72: 387-389.
Johnston, J. W., Jr.; Shriner, D. S. (1986) Yield response of Davis soybeans to simulated acid rain and gaseous
pollutants in the field. New Phytol. 103: 695-707.
Johnston, W. J.; Haaland, R. L.; Dickens, R. (1983) Inheritance of ozone resistance in tall fescue. Crop Sci. 23:
235-236.
Jones, P. D. (1989) Global temperature variations since 1861: the influence of the southern oscillation and a look
at recent trends. In: Crutzen, J. C.; Gerard, P. J.; Zander, R., eds. Proceedings of the 28th
international astrophysical colloqium. Universite de Liege; pp. 287-302.
Jones, H. G. (1992) Plant and microclimate: a quantitative approach to environmental plant physiology. 2nd ed.
Cambridge, United Kingdom: Cambridge University Press; pp. 32-41.
Jones, C. G.; Coleman, J. S. (1988) Plant stress and insect behavior: cottonwood, ozone and the feeding and
oviposition preference of a beetle. Oecologia 76: 51-56.
Jones, H. C.; Noggle, J. C.; McDuffie, C., Jr. (1988) Effects of chronic exposure to simulated power plant
emissions and ozone on soybean production. J. Environ. Qual. 17: 701-707.
Kamath, Y. K.; Ruetsch, S. B.; Weigmann, H.-D. (1983) Microspectrophotometric study of ozone fading of
disperse dyes in nylon. Text. Res. J. 53: 391-402.
5-311
-------
Kargiolaki, H.; Osborne, D. J.; Thompson, F. B. (1991) Leaf abscission and stem lesions (intumescences) on
poplar clones after SO2 and O3 fumigation: a link with ethylene release? J. Exp. Bot.
42: 1189-1198.
Karnosky, D. F. (1977) Evidence for genetic control of response to sulfur dioxide and ozone in Populus
tremuloides. Can. J. For. Res. 7: 437-440.
Karnosky, D. F. (1981a) Chamber and field evaluations of air pollution tolerances of urban trees. J. Arboric.
7: 99-105.
Karnosky, D. F. (1981b) Changes in eastern white pine stands related to air pollution stress. Mitt. Forstl.
Bundesversuchsanst. Wien 137: 41-45.
Karnosky, D. F. (1989a) Mechanisms of genetic control of air pollution tolerance in forest trees. In: Noble,
R. D.; Martin, J. L.; Jensen, K. F., eds. Air pollution effects on vegetation including forest
ecosystems: proceedings of the second US-USSR symposium;September 1988; Corvallis, OR.
Broomall, PA: Northeastern Forest Experiment Station; pp. 127-134.
Karnosky, D. F. (1989b) Air pollution induced population changes in North American forests. In: Bucher, J. B.;
Bucher-Wallin, L, eds. Air pollution and forest decline, v. I: proceedings of the 14th international
meeting for specialists in air pollution effects on forest ecosystems; October 1988; Interlaken,
Switzerland. Birmensdorf; pp. 315-317.
Karnosky, D. F. (1991) Ecological genetics and changes in atmospheric chemistry: the application of knowledge.
In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg, M. T., eds. Ecological genetics and air pollution [papers
from a symposium; April 1989; Phoenix, AZ]. New York, NY: Springer-Verlag; pp. 321-336.
Karnosky, D. F.; Steiner, K. C. (1981) Provenance and family variation in response of Fraxinus americana and
F. pennsylvanica to ozone and sulfur dioxide. Phytopathology 71: 804-807.
Karnosky, D. F.; Scholz, F.; Geburek, T.; Rudin, D. (1989) Implications of genetic effects of air pollution on
forest ecosystems - knowledge gaps. In: Scholz, F.; Gregorius, H.-R.; Rudin, D., eds. Genetic
effects of air pollutants in forest tree populations: proceedings of the joint meeting of the IUFRO
working parties; August 1987; Grosshansdorf, West Germany. Berlin, Germany: Springer-Verlag;
pp. 199-201.
Karnosky, D. F.; Gagnon, Z. E.; Reed, D. D.; Witter, J. A. (1992a) Effects of genotype on the response of
Populus tremuloides Michx. to ozone and nitrogen deposition. Water Air Soil Pollut. 62: 189-199.
Karnosky, D. F.; Gagnon, Z. E.; Reed, D. D.; Witter, J. A. (1992b) Growth and biomass allocation of
symptomatic and asymptomatic Populus tremuloides clones in response to seasonal ozone
exposures. Can. J. For. Res. 22: 1785-1788.
Kasana, M. S. (1991) Sensitivity of three leguminous crops to O3 as influenced by different stages of growth and
development. Environ. Pollut. 69: 131-149.
Kasana, M. S. (1992) Effects of ozone fumigation on a tropical fibre plant, kenaf (Hibiscus cannabinus L.).
Agric. Ecosyst. Environ. 38: 61-70.
Kats, G.; Dawson, P. J.; Bytnerowicz, A.; Wolf, J. W.; Thompson, C. R.; Olszyk, D. M. (1985) Effects of ozone
or sulfur dioxide on growth and yield of rice. Agric. Ecosyst. Environ. 14: 103-117.
5-312
-------
Keane, K. D.; Manning, W. J. (1988) Effects of ozone and simulated acid rain on birch seedling growth and
formation of ectomycorrhizae. Environ. Pollut. 52: 55-65.
Kearns, E. V.; Assmann, S. M. (1993) The guard cell-environment connection. Plant Physiol. 102: 711-715.
Keeling, C. D.; Bacastow, R. B.; Carter, A. F.; Piper, S. C.; Whorf, T. P.; Hermann, M.; Mook, W. G.;
Roeloffzen, H. (1989) A three-dimensional model of atmospheric CO2 transport based on observed
winds: 1. analysis of observational data. In: Peterson, D. H., ed. Aspects of climate variability in the
Pacific and the western Americas. Washington, DC: American Geophysical Union; pp. 165-236.
(Geophysical monograph: no. 55).
Kelleher, T. J.; Feder, W. A. (1978) Phytotoxic concentrations of ozone on Nantucket Island: long range
transport from the middle Atlantic states over the open ocean confirmed by bioassay with
ozone-sensitive tobacco plants. Environ. Pollut. 17: 187-194.
Keller, T. (1988) Growth and premature leaf fall in American aspen as bioindications for ozone. Environ. Pollut.
52: 183-192.
Keller, T.; Matyssek, R. (1990) Limited compensation of ozone stress by potassium in Norway spruce. Environ.
Pollut. 67: 1-14.
Kendrick, J. B., Jr.; Middleton, J. T.; Darley, E. F. (1954) Chemical protection of plants from ozonated olefin
(smog) injury. Phytopathology 44: 494-495.
Kerfourn, C.; Garrec, J. P. (1992) Modifications in the alkane composition of cuticular waxes from spruce
needles (Picea abies) and ivy leaves (Hedera helix) exposed to ozone fumigation and acid fog:
comparison with needles from declining spruce trees. Can. J. Bot. 70: 861-869.
Kerr, N.; Morris, M. A.; Zeronian, S. H. (1969) The effect of ozone and laundering on a vat-dyed cotton fabric.
Am. Dyest. Rep. 58: 34-36.
Kerstiens, G.; Lendzian, K. J. (1989) Interaction between ozone and plant cuticles: I. ozone deposition and
permeability. New Phytol. 112: 13-19.
Kickert, R. N.; Krupa, S. V. (1991) Modeling plant response to tropospheric ozone: a critical review.
Environ. Pollut. 70: 271-383.
Knudson Butler, L.; Tibbitts, T. W. (1979) Variation in ozone sensitivity and symptom expression among
cultivars of Phaseolus vulgaris L. J. Am. Soc. Hortic. Sci. 104: 208-210.
Kobriger, J. M.; Tibbitts, T. W.; Brenner, M. L. (1984) Injury, stomatal conductance, and abscisic acid levels of
pea plants following ozone plus sulfur dioxide exposures at different times of the day.
Plant Physiol. 76: 823-826.
Kohut, R.; Laurence, J. A. (1983) Yield response of red kidney bean Phaseolus vulgaris to incremental ozone
concentrations in the field. Environ. Pollut. Ser. A 32: 233-240.
Kohut, R. J.; Amundson, R. G.; Laurence, J. A. (1986) Evaluation of growth and yield of soybean exposed to
ozone in the field. Environ. Pollut. Ser. A 41: 219-234.
Kohut, R. J.; Amundson, R. G.; Laurence, J. A.; Colavito, L.; Van Leuken, P.; King, P. (1987) Effects of ozone
and sulfur dioxide on yield of winter wheat. Phytopathology 77: 71-74.
5-313
-------
Kohut, R. I; Laurence, J. A.; Amundson, R. G. (1988a) Effects of ozone and sulfur dioxide on yield of red
clover and timothy. J. Environ. Qual. 17: 580-585.
Kohut, R. J.; Laurence, J. A.; Colavito, L. J. (1988b) The influence of ozone exposure dynamics on the growth
and yield of kidney bean. Environ. Pollut. 53: 79-88.
Kohut, R. J.; Laurence, J. A.; Amundson, R. G.; Raba, R. M; Melkonian, J. J. (1990) Effects of ozone and
acidic precipitation on the growth and photosynthesis of red spruce after two years of exposure.
Water Air Soil Pollut. 51: 277-286.
Kopp, R. J.; Krupnick, A. J. (1987) Agricultural policy and the benefits of ozone control. Am. J. Agric. Econ.
69: 956-962.
Kopp, R. J.; Vaughn, W. J.; Hazilla, M.; Carson, R. (1985) Implications of environmental policy for
U.S. agriculture: the case of ambient ozone standards. J. Environ. Manage. 20: 321-331.
Kostka-Rick, R.; Manning, W. J. (1992a) Partitioning of biomass and carbohydrates in field-grown radish under
ambient concentrations of ozone, and treated with the anti-ozonant ethylene-diurea (EDU).
New Phytol. 121: 187-200.
Kostka-Rick, R.; Manning, W. J. (1992b) Effects and interactions of ozone and the anti-ozonant EDU at different
stages of radish (Raphanus sativus L.) development. J. Exp. Bot. 43: 1621-1631.
Kostka-Rick, R.; Manning, W. J. (1993) Dose-response studies with ethylenediurea (EDU) and radish.
Environ. Pollut. 79: 249-260.
Kotzias, D.; Fytainos, K.; Giess, F. (1990) Reaction of monoterpenes with ozone, sulphur dioxide and nitrogen
dioxide—gas-phase oxidation of SO2 and formation of sulphuric acid. Atmos. Environ. Part A
24: 2127-2132.
Kozlowski, T. T. (1980) Impacts of air pollution on forest ecosystems. Bioscience 30: 88-93.
Kozlowski, T. T. (1985) SO2 effects on plant community structure. In: Winner, W. E.; Mooney, H. A.;
Goldstein, R. A., eds. Sulfur dioxide and vegetation: physiology, ecology, and policy issues.
Stanford, CA: Stanford University Press; pp. 431-453.
Kozlowski, T. T.; Kramer, P. J.; Pallardy, S. G. (1991) The physiological ecology of woody plants. San Diego,
CA: Academic Press, Inc.; pp. 338-375. (Mooney, H. A., ed. Physiological ecology: a series of
monographs, texts, and treatises).
Kramer, G. F.; Lee, E. H.; Rowland, R. A.; Mulchi, C. L. (1991) Effects of elevated CO2 concentration on the
polyamine levels of field-grown soybean at three O3 regimes. Environ. Pollut. 73: 137-152.
Krause, C. R.; Weidensaul, T. C. (1978) Effects of ozone on the sporulation, germination, and pathogenicity of
Botrytis cinerea. Phytopathology 68: 195-198.
Krause, G. H. M.; Riley, W. D.; Feder, W. A. (1975) Effects of ozone on petunia and tomato pollen tube
elongation in vivo. Proc. Am. Phytopathol. Soc. 2: 100.
Kress, L. W.; Skelly, J. M. (1982) Response of several eastern forest tree species to chronic doses of ozone and
nitrogen dioxide. Plant Dis. 66: 1149-1152.
Kress, L. W.; Skelly, J. M.; Hinkelmann, K. H. (1982a) Relative sensitivity of 18 full-sib families of Pinus taeda
to O3. Can. J. For. Res. 12: 203-209.
5-314
-------
Kress, L. W.; Skelly, J. M; Hinkelmann, K. H. (1982b) Growth impact of O3, NO2 and/or SO2 on Pinus taeda.
Environ. Monit. Assess. 1: 229-239.
Kress, L. W.; Miller, J. E.; Smith, H. J. (1985) Impact of ozone on winter wheat yield. Environ. Exp. Bot. 25:
211-228.
Kress, L. W.; Miller, J. E.; Smith, H. J.; Rawlings, J. O. (1986) Impact of ozone and sulphur dioxide on soybean
yield. Environ. Pollut. Ser. A 41: 105-123.
Kress, L. W.; Allen, H. L.; Mudano, J. E.; Heck, W. W. (1988) Response of loblolly pine to acidic precipitation
and ozone. Presented at: 81st annual meeting of the Air Pollution Control Association; June; Dallas,
TX. Pittsburgh, PA: Air Pollution Control Association; paper no. 88-70.5.
Kress, L. W.; Allen, H. L.; Mudano, J. E.; Stow, T. K. (1992) Impact of ozone on loblolly pine seedling foliage
production and retention. Environ. Toxicol. Chem. 11: 1115-1128.
Krupa, S.; Fries, N. (1971) Studies on ectomycorrhizae of pine. I. Production of volatile organic compounds.
Can. J. Bot. 49: 1425-1431.
Krupa, S. V.; Kickert, R. N. (1989) The greenhouse effect: impacts of ultraviolet-B (UV-B) radiation, carbon
dioxide (CO2), and ozone (O3) on vegetation. Environ. Pollut. 61: 263-393.
Krupa, S. V.; Manning, W. J.; Nosal, M. (1993) Use of tobacco cultivars as biological indicators of ambient
ozone pollution: an analysis of exposure-response relationships. Environ. Pollut. 81: 137-146.
Krupa, S. V.; Nosal, M.; Legge, A. H. (1994) Ambient ozone and crop loss: establishing a cause-effect
relationship. Environ. Pollut. 83: 269-276.
Krupa, S. V.; Griinhage, L.; Jager, H.-J.; Nosal, M.; Manning, W. J.; Legge, A. H.; Hanewald, K. (1995)
Ambient ozone (O3) and adverse crop response: a unified view of cause and effect. Environ. Pollut.
87: 119-126.
Kuikman, P. J.; Van Elsas, J. D.; Jansen, A. G.; Burgers, S. L. G. E.; van Veen, J. A. (1990) Population
dynamics and activity of bacteria and protozoa in relation to their spatial distribution in soil.
Soil Biol. Biochem. 22: 1063-1073.
Ktippers, M.; Schulze, E.-D. (1985) An empirical model of net photosynthesis and leaf conductance for the
simulation of diurnal courses of CO2 and H2O exchange. Aust. J. Plant Physiol. 12: 513-526.
Lackey, R. T. (1994) Ecological risk assessment. Fisheries 19(9): 14-17.
Laisk, A.; Kull, O.; Moldau, H. (1989) Ozone concentration in leaf intercellular air spaces is close to zero. Plant
Physiol. 90: 1163-1167.
Lake, G. J.; Mente, P. G. (1992) Ozone cracking and protection of elastomers at high and low temperatures.
J. Nat. Rubber Res. 7: 1-13.
Landry, L. G.; Pell, E. J. (1993) Modification of Rubisco and altered proteolytic activity in Distressed hybrid
poplar (Populus maximowizii x trichocarpa). Plant Physiol. 101: 1355-1362.
Lange, O. L.; Heber, U.; Schulze, E.-D.; Ziegler, H. (1989) 3-D atmospheric pollutants and plant metabolism. In:
Schulze, E.-D.; Lange, O. L.; Oren, R., eds. Forest decline and air pollution: a study of spruce
(Picea abies) on acid soils.Berlin, Germany: Springer-Verlag; pp. 238-273. (Ecological studies: v.
77).
5-315
-------
Langebartels, C.; Kerner, K.; Leonard!, S.; Schraudner, M.; Trost, M.; Heller, W.; Sandermann, H., Jr. (1991)
Biochemical plant responses to ozone: I. differential induction of polyamine and ethylene
biosynthesis in tobacco. Plant Physiol. 95: 882-889.
Larsen, R. I.; Heck, W. W. (1984) An air quality data analysis system for interrelating effects, standards, and
needed source reductions: part 8. an effective mean O3 crop reduction mathematical model. J. Air
Pollut. Control Assoc. 34: 1023-1034.
Larsen, R. I.; Heagle, A. S.; Heck, W. W. (1983) An air quality data analysis system for interrelating effects,
standards, and needed source reductions: part 7. an O3-SO2 leaf injury mathematical model. J. Air
Pollut. Control Assoc. 33: 198-207.
Larsen, J. B.; Yang, W.; Tiedemann, A. V. (1990) Effects of ozone on gas exchange, frost resistance, flushing
and growth of different provenances of European silver fir (Abies alba Mill.). Eur. J. For. Pathol.
20: 211-218.
Lattimer, R. P.; Layer, R. W.; Rhee, C. K. (1984) Mechanisms of antiozonant protection: antiozonant-rubber
reactions during ozone exposure. In: 32nd annual conference on mass spectrometry and allied
topics. Bethesda, MD: American Society for Mass Spectrometry; pp. 357-358.
Laurence, J. A.; Wood, F. A. (1978a) Effects of ozone on infection of soybean by Pseudomonas glycinea.
Phytopathology 68: 441-445.
Laurence, J. A.; Wood, F. A. (1978b) Effect of ozone on infection of wild strawberry by Xanthomonas fragariae.
Phytopathology 68: 689-692.
Laurence, J. A.; Kohut, R. J.; Amundson, R. G. (1989) Response of red spruce seedlings exposed to ozone and
simulated acidic precipitation in the field. Arch. Environ. Contam. Toxicol. 18: 285-290.
Laurence, J. A.; Kohut, R. J.; Amundson, R. G. (1993) Use of TREGRO to simulate the effects of ozone on the
growth of red spruce seedlings. For. Sci. 39: 453-464.
Le Sueur-Brymer, N. M.; Ormrod, D. P. (1984) Carbon dioxide exchange rates of fruiting soybean plants
exposed to ozone and sulphur dioxide singly or in combination. Can. J. Plant Sci. 64: 69-75.
Lechowicz, M. J. (1987) Resource allocation by plants under air pollution stress: implications for
plant-pest-pathogen interactions. Bot. Rev. 53: 281-300.
Lee, E. H.; Bennett, J. H. (1982) Superoxide dismutase: a possible protective enzyme against ozone injury in
snap beans (Phaseolus vulgaris L.). Plant Physiol. 69: 1444-1449.
Lee, J. J.; Preston, E. M.; Lewis, R. A. (1978) A system for the experimental evaluation of the ecological effects
of sulfur dioxide. In: Proceedings of the 4th joint conference on sensing of environmental
pollutants; November 1977; New Orleans, LA. Washington, DC: American Chemical Society;
pp. 49-53.
Lee, E. H.; Tingey, D. T.; Hogsett, W. E. (1987) Selection of the best exposure-response model using various
7-hour ozone exposure statistics. Research Triangle Park, NC: U.S. Environmental Protection
Agency, Office of Air Quality Planning and Standards.
Lee, E. H.; Tingey, D. T.; Hogsett, W. E. (1988) Evaluation of ozone exposure indices in exposure-response
modeling. Environ. Pollut. 53: 43-62.
5-316
-------
Lee, E. H.; Tingey, D. T.; Hogsett, W. E. (1989) Interrelation of experimental exposure and ambient air quality
data for comparison of ozone exposure indices and estimating agricultural losses. Corvallis, OR:
U.S. Environmental Protection Agency, Environmental Research Laboratory; EPA report no.
EPA-600/3-89-047. Available from: NTIS, Springfield, VA; PB89-195036.
Lee, W. S.; Chevone, B. I.; Seiler, J. R. (1990a) Growth and gas exchange of loblolly pine seedlings as
influenced by drought and air pollutants. Water Air Soil Pollut. 51: 105-116.
Lee, W. S.; Chevone, B. I.; Seiler, J. R. (1990b) Growth response and drought susceptibility of red spruce
seedlings exposed to simulated acidic rain and ozone. For. Sci. 36: 265-275.
Lee, E. H.; Hogsett, W. E.; Tingey, D. T. (1991) Efficacy of ozone exposure indices in the standard setting
process. In: Berglund, R. L.; Lawson, D. R.; McKee, D. J., eds. Tropospheric ozone and the
environment: papers from an international conference; March 1990; Los Angeles, CA.
Pittsburgh, PA: Air & Waste Management Association; pp. 255-271. (A&WMA transactions
series no. TR-19).
Lee, E. H.; Hogsett, W. E.; Tingey, D. T. (1994a) Alternative attainment criteria for a secondary federal standard
for ozone. In: Nriagu, J. O.; Simmons, M. S., eds. Environmental oxidants. New York, NY: John
Wiley & Sons; pp. 549-584. (Nriagu, J. O., ed. Advances in environmental sciences and technology
series: v. 28).
Lee, E. H.; Hogsett, W. E.; Tingey, D. T. (1994b) Attainment and effects issues regarding alternative secondary
ozone air quality standards. J. Environ. Qual. 23: 1129-1140.
Lefohn, A. S. (1984) A comparison of ambient ozone exposures for selected nonurban sites. Presented at:
77th annual meeting of the Air Pollution Control Association; June; San Francisco, CA. Pittsburgh,
PA: Air Pollution Control Association; paper no. 84-104.1.
Lefohn, A. S. (1988) Author's reply [a response to comments by Parry and Day, 1988]. Atmos. Environ.
22: 2058-2060.
Lefohn, A. S.; Benedict, H. M. (1982) Development of a mathematical index that describes ozone concentration,
frequency and duration. Atmos. Environ. 16: 2529-2532.
Lefohn, A. S.; Foley, J. K. (1992) NCLAN results and their application to the standard-setting process:
protecting vegetation from surface ozone exposures. J. Air Waste Manage. Assoc. 42: 1046-1052.
Lefohn, A. S.; Irving, P. M. (1988) Characterizing ambient ozone exposure regimes in agricultural areas.
Presented at: 81st annual meeting of the Air Pollution Control Association; June; Dallas, TX.
Pittsburgh, PA: Air Pollution Control Association; 88-69.1.
Lefohn, A. S.; Jones, C. K. (1986) The characterization of ozone and sulfur dioxide air quality data for assessing
possible vegetation effects. J. Air Pollut. Control Assoc. 36: 1123-1129.
Lefohn, A. S.; Manning, W. J. (1995) Ozone exposures near Class I Wilderness arears in New Hampshire and
Vermont. Atmos. Environ. 29: 601-606.
Lefohn, A. S.; Ormrod, D. P. (1984) A review and assessment of the effects of pollutant mixtures on vegetation
—research recommendations: proceedings of the vegetation effects workshop; April 1983; Raleigh,
NC. Corvallis, OR: U.S. Environmental Protection Agency, Corvallis Environmental Research
Laboratory; EPA report no. EPA-600/3-84-037. Available from: NTIS, Springfield, VA;
PB84-177732.
5-317
-------
Lefohn, A. S.; Pinkerton, J. E. (1988) High resolution characterization of ozone data for sites located in forested
areas of the United States. JAPCA 38: 1504-1511.
Lefohn, A. S.; Runeckles, V. C. (1987) Establishing standards to protect vegetation - ozone exposure/dose
considerations. Atmos. Environ. 21: 561-568.
Lefohn, A. S.; Tingey, D. T. (1984) The co-occurrence of potentially phytotoxic concentrations of various
gaseous air pollutants. Atmos. Environ. 18: 2521-2526.
Lefohn, A. S.; Tingey, D. T. (1985) Comments on "Injury response of Phaseolus vulgaris to ozone flux density."
Atmos. Environ. 19: 206-207.
Lefohn, A. S.; Knudsen, H. P.; Logan, J. A.; Simpson, J.; Bhumralkar, C. (1987a) An evaluation of the kriging
method to predict 7-h seasonal mean ozone concentrations for estimating crop losses. JAPCA 37:
595-602.
Lefohn, A. S.; Davis, C. E.; Jones, C. K.; Tingey, D. T.; Hogsett, W. E. (1987b) Co-occurrence patterns of
gaseous air pollutant pairs at different minimum concentrations in the United States.
Atmos. Environ. 21: 2435-2444.
Lefohn, A. S.; Laurence, J. A.; Kohut, R. J. (1988a) A comparison of indices that describe the relationship
between exposure to ozone and reduction in the yield of agricultural crops. Atmos. Environ.
22: 1229-1240.
Lefohn, A. S.; Laurence, J. A.; Kohut, R. J. (1988b) A comparison of indices that describe the relationship
between exposure to ozone and reduction in the yield of agricultural crops [response to comments
by V. C. Runeckles]. Atmos. Environ. 22: 1242-1243.
Lefohn, A. S.; Runeckles, V. C.; Krupa, S. V.; Shadwick, D. S. (1989) Important considerations for establishing
a secondary ozone standard to protect vegetation. JAPCA 39: 1039-1045.
Lefohn, A. S.; Shadwick, D. S.; Somerville, M. C.; Chappelka, A. H.; Lockaby, B. G.; Meldahl, R. S. (1992a)
The characterization and comparision of ozone exposure indices used in assessing the response of
loblolly pine to ozone. Atmos. Environ. Part A 26: 287-298.
Lefohn, A. S.; Foley, J. K.; Spence, J.; Shadwick, D. S. (1992b) Linking surface-level ozone exposures in the
United States with potential vegetation effects. In: Berglund, R. L., ed. Tropospheric ozone and the
environment II: effects, modeling and control [papers from an international specialty conference];
November; Atlanta, GA. Pittsburgh, PA: Air & Waste Management Association; pp. 473-488.
(A&WMA transactions series no. 20).
Lefohn, A. S.; McEvoy, L. R., Jr.; Tingey, D. T.; Sebaugh, J. L.; Hogsett, W. E. (1993) Potential bias from
non-continuous monitoring of ambient ozone concentrations for characterizing hourly and daily
7- and 12-hour average concentrations. Atmos Environ. Part A 27: 145-152.
Lefohn, A. S.; Edwards, P. J.; Adams, M. B. (1994) The characterization of ozone exposures in rural
West Virginia and Virginia. J. Air Waste Manage. Assoc. 44: 1276-1283.
Legge, A. H.; Savage, D. J.; Walker, R. B. (1978) Special techniques: B. a portable gas-exchange leaf chamber.
In: Heck, W. W.; Krupa, S. V.; Linzon, S. N., eds. Methodology for the assessment of air pollution
effects on vegetation: a handbook from a specialty conference; April; Minneapolis, MN. Pittsburgh,
PA: Air Pollution Control Association; pp. 16-12 - 16-24.
5-318
-------
Lenschow, D. H.; Pearson, R., Jr.; Stankov, B. B. (1982) Measurements of ozone vertical flux to ocean and
forest. J. Geophys. Res. C: Oceans Atmos. 87: 8833-8837.
Leonard!, S.; Langebartels, C. (1990) Fall exposure of beech saplings (Fagus sylvatica L.) to ozone and
simulated acid mist: effects on gas exchange and teachability. Water Air Soil Pollut. 54: 143-153.
Leone, I. A.; Brennan, E. (1970) Ozone toxicity in tomato as modified by phosphorus nutrition. Phytopathology
60: 1521-1524.
Leone, I. A.; Brennan, E.; Daines, R. H. (1966) Effect of nitrogen nutrition on the response of tobacco to ozone
in the atmosphere. J. Air Pollut. Control Assoc. 16: 191-196.
Lesser, V. M; Rawlings, J. O.; Spruill, S. E.; Somerville, M. C. (1990) Ozone effects on agricultural crops:
statistical methodologies and estimated dose-response relationships. Crop Sci. 30: 148-155.
Letham, D. S.; Palni, L. M. S. (1983) The biosynthesis and metabolism of cytokinins. Annu. Rev. Plant Physiol.
34: 163-197.
Leuning, R.; Neumann, H. H.; Thurtell, G. W. (1979a) Ozone uptake by corn (Zea mays L.): a general approach.
Agric. Meteorol. 20: 115-135.
Leuning, R.; Unsworth, M. H.; Neumann, H. N.; King, K. M. (1979b) Ozone fluxes to tobacco and soil under
field conditions. Atmos. Environ. 13: 1155-1163.
Lewis, E.; Brennan, E. (1977) A disparity in the ozone response of bean plants grown in a greenhouse, growth
chamber or open-top chamber. J. Air Pollut. Control Assoc. 27: 889-891.
Logan, J. A. (1989) Ozone in rural areas of the United States. J. Geophys. Res. [Atmos.] 94: 8511-8532.
Long, R. P.; Davis, D. D. (1991) Black cherry growth response to ambient ozone and EDU. Environ. Pollut. 70:
241-254.
Losch, R.; Tenhunen, J. D. (1981) Stomatal responses to humidity—phenomenon and mechanism. In: Jarvis,
P. G.; Mansfield, T. A., eds. Stomatal physiology. Cambridge, United Kingdom: Cambridge
University Press; pp. 137-161. (Society for Experimental Biology seminar series: no. 8).
Lucas, P. W.; Cottam, D. A.; Sheppard, L. J.; Francis, B. J. (1988) Growth responses and delayed winter
hardening in Sitka spruce following summer exposure to ozone. New Phytol. 108: 495-504.
Luck, R. F. (1980) Impact of oxidant air pollution on ponderosa and Jeffrey pine cone production. In: Miller, P.
R., ed. Proceedings of symposium on effects of air pollutants on Mediterranean and temperate forest
ecosystems; June; Riverside, CA. Berkeley, CA: U.S. Department of Agriculture, Pacific Southwest
Forest and Range Experiment Station; p. 240; Forest Service general technical report no. PSW-43.
Available from: NTIS, Springfield, VA; PB81-133720.
Ludwig, F. L.; Shelar, E., Jr. (1980) Empirical relationships between observed ozone concentrations and
geographical areas with concentrations likely to be above 120 ppb. J. Air Pollut. Control Assoc. 30:
894-897.
Luethy-Krause, B.; Landolt, W. (1990) Effects of ozone on starch accumulation in Norway spruce (Picea abies).
Trees 4: 107-110.
Ltitz, C.; Heinzmann, U.; Gtilz, P. G. (1990) Surface structures and epicuticular wax composition of spruce
needles after long-term treatment with ozone and acid mist. Environ. Pollut. 64: 313-322.
5-319
-------
Luxmoore, R. J. (1988) Assessing the mechanisms of crop loss from air pollutants with process models.
In: Heck, W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from air pollutants:
proceedings of an international conference; October 1987; Raleigh, NC. Essex, United Kingdom:
Elsevier Science Publishers, Ltd.; pp. 417-444.
MacDowall, F. D. H. (1965) Predisposition of tobacco to ozone damage. Can. J. Plant Sci. 45: 1-12.
Macdowall, F. D. H.; Cole, A. F. W. (1971) Threshold and synergistic damage to tobacco by ozone and sulfur
dioxide. Atmos. Environ. 5: 553-559.
Mackay, C. E.; Senaratna, T.; McKersie, B. D.; Fletcher, R. A. (1987) Ozone induced injury to cellular
membranes in Triticum aestivum L. and protection by the triazole S-3307. Plant Cell Physiol.
28: 1271-1278.
MacLean, D. C. (1990) Joint action of ozone and hydrogen fluoride on foliar senescence in maize.
Environ. Pollut. 63: 283-292.
Madamanchi, N. R.; Hausladen, A.; Alscher, R. G.; Amundson, R. G.; Fellows, S. (1991) Seasonal changes in
antioxidants in red spruce (Picea rubens Sarg.) from three field sites in the northeastern
United States. New Phytol. 118: 331-338.
Madamanchi, N. R.; Anderson, J. V.; Alscher, R. G.; Cramer, C. L.; Hess, J. L. (1992) Purification of multiple
forms of glutathione reductase from pea (Pisum sativum L.) seedlings and enzyme levels in
ozone-fumigated pea leaves. Plant Physiol. 100: 138-145.
Magel, E.; Holl, W.; Ziegler, H. (1990) Alteration of physiological parameters in needles of cloned spruce trees
(Picea abies (L.) Karst.) by ozone and acid mist. Environ. Pollut. 64: 337-345.
Mahoney, M. J.; Chevone, B. L; Skelly, J. M; Moore, L. D. (1985) Influence of mycorrhizae on the growth of
loblolly pine seedlings exposed to ozone and sulfur dioxide. Phytopathology 75: 679-682.
Maier-Maercker, U.; Koch, W. (1991a) Experiments on the control capacity of stomata of Picea abies (L.) Karst.
after fumigation with ozone and in environmentally damaged material. Plant Cell Environ. 14:
175-184.
Maier-Maercker, U.; Koch, W. (1991b) Experiments on the water budget of densely and sparsely needled spruces
[Picea abies (L.) Karst.] in a declining stand. Trees (Berlin) 5: 164-170.
Maier-Maercker, U.; Koch, W. (1992a) The effect of air pollution on the mechanism of stomatal control.
Trees (Berlin) 7: 12-25.
Maier-Maercker, U.; Koch, W. (1992b) Histological examination of spruce needles from a long-term gas
exchange experiment in pure and polluted air in the field. Trees (Berlin) 6: 186-194.
Makansi, M. (1986) Effect of ageing on dyeability of nylon yarns. Text. Chem. Color. 18(1): 27-35.
Mandl, R. H.; Weinstein, L. H.; McCune, D. C.; Keveny, M. (1973) A cylindrical, open-top chamber for the
exposure of plants to air pollutants in the field. J. Environ. Qual. 2: 371-376.
Mandl, R. H.; Laurence, J. A.; Kohut, R. J. (1989) Development and testing of open-top chambers for exposing
large, perennial plants to air pollutants. J. Environ. Qual. 18: 534-540.
Manion, P. D.; Lachance, D. (1992) Foreword. In: Manion, P. D.; Lachance, D., eds. Forest decline concepts. St.
Paul, MN: APS Press; pp. 1-2.
5-320
-------
Mann, L. K.; McLaughlin, S. B.; Shriner, D. S. (1980) Seasonal physiological responses of white pine under
chronic air pollution stress. Environ. Exp. Bot. 20: 99-105.
Manning, W. I; Keane, K. D. (1988) Effects of air pollutants on interactions between plants, insects,
and pathogens. In: Heck, W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from
air pollutants: proceedings of an international conference; October 1987; Raleigh, NC.
Essex, United Kingdom: Elsevier Science Publishers, Ltd.; pp. 365-386.
Manning, W. I; Krupa, S. V. (1992) Experimental methodology for studying the effects of ozone on crops and
trees. In: Lefohn, A. S., ed. Surface level ozone exposures and their effects on vegetation. Chelsea,
MI: Lewis Publishers, Inc.; pp. 93-156.
Manning, W. I; Feder, W. A.; Perkins, I.; Glickman, M. (1969) Ozone injury and infection of potato leaves by
Botrytis cinerea. Plant Dis. Rep. 53: 691-693.
Manning, W. I; Feder, W. A.; Papia, P. M.; Perkins, I. (197la) Effect of low levels of ozone on growth and
susceptibility of cabbage plants to Fusarium oxysporum F. sp. conglutinans. Plant Dis. Rep.
55: 47-49.
Manning, W. I; Feder, W. A.; Papia, P. M.; Perkins, I. (1971b) Influence of foliar ozone injury on root
development and root surface fungi of pinto bean plants. Environ. Pollut. 1: 305-312.
Manning, W. I; Bergman, J. R.; O'Brien, J. T. (1991) Ozone injury on native vegetation in Class I wilderness
areas in New Hampshire and Vermont. Presented at: 84th annual meeting & exhibition of the Air &
Waste Management Association; June; Vancouver, BC, Canada. Pittsburgh, PA: Air & Waste
Management Association; paper no. 91-144.5.
5-321
-------
Mansfeld, F. (1980) Regional air pollution study: effects of airborne sulfur pollutants on materials.
Research Triangle Park, NC: U.S. Environmental Protection Agency, Environmental Sciences
Research Laboratory; EPA report no. EPA-600/4-80-007. Available from: NTIS, Springfield, VA;
PB81-126351.
Mansfield, T. A.; McCune, D. C. (1988) Problems of crop loss assessment when there is exposure to two or
more gaseous pollutants. In: Heck, W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop
loss from air pollutants. London, United Kingdom: Elsevier Applied Science; pp. 317-344.
Martin, B.; Bytnerowicz, A.; Thorstenson, Y. R. (1988) Effects of air pollutants on the composition of stable
carbon isotopes, 813C, of leaves and wood, and on leaf injury. Plant Physiol. 88: 218-223.
Matsui, M.; Koike, T.; Shibata, K. (1988) Ozone fading of phenolphthalein and aurin. J. Soc. Dyers Colour 104:
482-486.
Matsushima, J.; Yonemori, K.; Iwao, K. (1985) Sensitivity of satsuma mandarin to ozone as related to stomatal
function indicated by transpiration rate, change of stem diameter, and leaf temperature. J. Am. Soc.
Hortic. Sci. 110: 106-108.
Matyssek, R.; Gtinthardt-Goerg, M. S.; Saurer, M.; Keller, T. (1992) Seasonal growth, 813C in leaves and stem,
and phloem structure of birch (Betula pendula) under low ozone concentrations. Trees 6: 69-76.
Matyssek, R.; Gtinthardt-Goerg, M. S.; Landolt, W.; Keller, T. (1993a) Whole-plant growth and leaf formation in
ozonated hybrid poplar (Populus x euramericana). Environ. Pollut. 81: 207-212.
Matyssek, R.; Keller, T.; Koike, T. (1993b) Branch growth and leaf gas exchange of Populus tremula exposed to
low ozone concentrations throughout two growing seasons. Environ. Pollut. 79: 1-7.
McBride, J. R.; Semion, V. P.; Miller, P. R. (1975) Impact of air pollution on the growth of Ponderosa pine.
Calif. Agric. 29: 8-9.
McCool, P. M. (1988) Effect of air pollutants on mycorrhizae. In: Schulte-Hostede, S; Darrall, N. M.; Blank, L.
W.; Wellburn, A. R., eds. Air pollution and plant metabolism. London, United Kingdom: Elsevier
Applied Science; pp. 356-365.
McCool, P. M.; Menge, J. A. (1984) Interaction of ozone and mycorrhizal fungi on tomato as influenced by
fungal species and host variety. Soil Biol. Biochem. 16: 425-427.
McCool, P. M.; Musselman, R. C. (1990) Impact of ozone on growth of peach, apricot, and almond. Hortscience
25: 1384-1385.
McCool, P. M.; Menge, J. A.; Taylor, O. C. (1982) Effect of ozone injury and light stress on response of tomato
to infection by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatus. J. Am. Soc.
Hortic. Sci. 107: 839-842.
McCool, P. M.; Musselman, R. C.; Teso, R. R.; Oshima, R. J. (1986) Determining crop yield losses from air
pollutants. Calif. Agric. 40(July-August): 9-10.
McCool, P. M.; Musselman, R. C.; Teso, R. R. (1987) Air pollutant yield-loss assessment for four vegetable
crops. Agric. Ecosyst. Environ. 20: 11-21.
McCool, P. M.; Musselman, R. C.; Younglove, T.; Teso, R. R. (1988) Response of kidney bean to sequential
ozone exposures. Environ. Exp. Bot. 28: 307-313.
5-322
-------
McFadden, D. (1994) Contingent valuation and social choice. Am. J. Agric. Econ. 76: 689-708.
McGartland, A. M. (1987) The implications of ambient ozone standards for U.S. agriculture: a comment and
some further evidence. J. Environ. Manage. 24: 139-146.
Mcllveen, W. D.; Sports, R. A.; Davis, D. D. (1975) The influence of soil zinc on nodulation, mycorrhizae, and
ozone-sensitivity of pinto bean. Phytopathology 65: 645-647.
McLaughlin, S. B. (1994) Forest declines: some perspectives on linking processes and patterns. In: Alscher,
R. G.; Wellburn, A. R., eds. Plant responses to the gaseous environment: molecular, metabolic and
physiological aspects. London, United Kingdom: Chapman & Hall; pp. 315-338.
McLaughlin, S. B.; Downing, D. J. (1995) Interactive effects of ambient ozone and climate measured on growth
of mature forest trees. Nature (London) 374: 252-254.
McLaughlin, S. B.; Kohut, R. J. (1992) The effects of atmospheric deposition and ozone on carbon allocation
and associated physiological processes in red spruce. In: Eager, C.; Adams, M. B., eds. Ecology and
decline of red spruce in the eastern United States. New York, NY: Springer-Verlag; pp. 338-382.
(Ecological studies: v. 96).
McLaughlin, S. B.; Taylor, G. E. (1981) Relative humidity: important modifier of pollutant uptake by plants.
Science (Washington, DC) 211: 167-169.
McLaughlin, S. B.; McConathy, R. K.; Duvick, D.; Mann, L. K. (1982) Effects of chronic air pollution stress on
photosynthesis, carbon allocation, and growth of white pine trees. For. Sci. 28: 60-70.
McLeod, A. R.; Baker, C. K. (1988) The use of open field systems to assess yield response to gaseous
pollutants. In: Heck, W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from air
pollutants. London: Elsevier Applied Science; pp. 181-210.
McLeod, A. R.; Fackrell, J. E.; Alexander, K. (1985) Open-air fumigation of field crops: criteria and design for a
new experimental system. Atmos. Environ. 19: 1639-1649.
McLeod, A. R.; Shaw, P. J. A.; Holland, M. R. (1992) The Liphook Forest Fumigation Project: studies of
sulphur dioxide and ozone effects on coniferous trees. For. Ecol. Manage. 51: 121-127'.
McQuattie, C. J.; Schier, G. A. (1992) Effect of ozone and aluminum on pitch pine (Pinus rigida) seedlings:
anatomy of mycorrhizae. Can. J. For. Res. 22: 1901-1916.
Mebrahtu, T.; Mersie, W.; Rangappa, M. (1990a) Generation mean analysis of inheritance of insensitivity to
ozone injury in two crosses of beans (Phaseolus vulgaris L.). J. Hort. Sci. 65: 19-24.
Mebrahtu, T.; Mersie, W.; Rangappa, M. (1990b) Inheritance of ambient ozone insensitivity in common bean
(Phaseolus vulgaris L.). Environ. Pollut. 67: 79-89.
Mebrahtu, T.; Mersie, W.; Rangappa, M. (1990c) A seven-parental diallel analysis of ozone insensitivity in
common beans. J. Genet. Breed. 44: 69-74.
Mehlhorn, H.; Wellburn, A. R. (1987) Stress ethylene formation determines plant sensitivity to ozone. Nature
(London) 327: 417-418.
Mehlhorn, H.; Seufert, G.; Schmidt, A.; Kunert, K. J. (1986) Effect of SO2 and O3 on production of antioxidants
in conifers. Plant Physiol. 82: 336-338.
5-323
-------
Mehlhorn, H.; O'Shea, J. M.; Wellburn, A. R. (1991) Atmospheric ozone interacts with stress ethylene formation
by plants to cause visible plant injury. J. Exp. Bot. 42: 17-24.
Meier, S.; Grand, L. F.; Schoeneberger, M. M.; Reinert, R. A.; Brack, R. I. (1990) Growth, ectomycorrhizae and
nonstractural carbohydrates of loblolly pine seedlings exposed to ozone and soil water deficit.
Environ. Pollut. 64: 11-27.
Mendelsohn, R.; Markstrom, D. (1988) The use of travel cost and hedonic methods in assessing environmental
benefits. In: Peterson, G. L.; Driver, B. L.; Gregory, R., eds. Amenity resource valuation:
integrating economics with other disciplines. State College, PA: Venture Publishing, Inc.;
pp. 160-166.
Menser, H. A.; Heggestad, H. E. (1966) Ozone and sulfur dioxide synergism: injury to tobacco plants. Science
(Washington, DC) 153: 424-425.
Menser, H. A.; Hodges, G. H. (1967) Nitrogen nutrition and susceptibility of tobacco leaves to ozone. Tobacco
Sci. 11: 151-154.
Menser, H. A.; Street, O. E. (1962) Effects of air pollution, nitrogen levels, supplemental irrigation, and plant
spacing on weather fleck and leaf losses of Maryland tobacco. Tobacco 155: 192-196.
Menser, H. A.; Heggestad, H. E.; Street, O. E. (1963) Response of plants to air pollutants. II. Effects of ozone
concentration and leaf maturity on injury to Nicotiana tabacum. Phytopathology 53: 1304-1308.
Mersie, W.; Mebrahtu, T.; Rangappa, M. (1989) Ozone-metolachlor interactions on corn (Lea mays), bean
(Phaseolus vulgaris), and soybean (Glycine max). Weed Technol. 3: 650-653.
Mersie, W.; Mebrahtu, T.; Rangappa, M. (1990) Response of corn to combinations of atrazine, propyl gallate and
ozone. Environ. Exp. Bot. 30: 443-449.
Meyer, D. A.; Sommer, J. G. (1957) The development of weather and aging resistant pneumatic tires and
mechanical rubber goods: final technical report. Dayton, OH: The Dayton Rubber Company;
ordinance project no.TTI-718. Available from: NTIS, Springfield, VA; AD-142212.
Middleton, J. T.; Kendrick, J. B., Jr.; Schwalm, H. W. (1950) Injury to herbaceous plants by smog or air
pollution. Plant Dis. Rep. 34: 245-252.
Miller, P. L. (1973) Oxidant-induced community change in a mixed conifer forest. In: Naegele, J. A., ed. Air
pollution damage to vegetation. Washington, DC: American Chemical Society; pp. 101-117.
(Advances in chemistry series: v. 122).
Miller, P. R. (1984) Ozone effects in the San Bernardino National Forest. In: Davis, D. D.; Millen, A. A.;
Dochinger, L., eds. Air pollution and the productivity of the forest: proceedings of the symposium;
October 1983; Washington, DC. Arlington, VA: Izaak Walton League of America; pp. 161-197.
Miller, P. R.; Elderman, M. J. (1977) Photochemical oxidant air pollutant effects on a mixed conifer forest
ecosystem: a progress report, 1976. Corvallis, OR: U.S. Environmental Protection Agency, Corvallis
Environmental Research Laboratory; EPA report no. EPA-600/3-77-104. Available from: NTIS,
Springfield, VA; PB-274531.
Miller, P. R.; Millecan, A. A. (1971) Extent of oxidant air pollution damage to some pines and other conifers in
California. Plant Dis. Rep. 55: 555-559.
5-324
-------
Miller, J. E.; Pursley, W. A. (1990) Effects of ozone and UV-B radiation on growth, UV-B absorbing pigments,
and antioxidants in soybean. Plant Physiol. 93(suppl. 1): 101.
Miller, P. R.; Parmeter, J. R., Jr.; Flick, B. H.; Martinez, C. W. (1969) Ozone dosage response of ponderosa pine
seedlings. J. Air Pollut. Control Assoc. 19: 435-438.
Miller, P. R.; McCutchan, M. H.; Ryan, B. C. (1972) Influence of climate and topography on oxidant air
pollution concentrations that damage conifer forests in southern California. Mitt. Forstl.
Bundesversuchsanst. Wien (97): 585-607.
Miller, P. M.; Tomlinson, H.; Taylor, G. S. (1976) Reducing severity of ozone damage to tobacco and beans by
combining benomyl or carboxin with contact nematicides. Plant Dis. Rep. 60: 433-436.
Miller, P. R.; Taylor, O. C.; Wilhour, R. G. (1982) Oxidant air pollution effects on a western coniferous forest
ecosystem. Corvallis, OR: U.S. Environmental Protection Agency, Environmental Research
Laboratory; EPA report no. EPA-600/D-82-276. Available from: NTIS, Springfield, VA;
PB83-189308.
Miller, P. R.; Taylor, O. C.; Poe, M. P. (1986) Spatial variation of summer ozone concentrations in the
San Bernardino mountains. Presented at: 79th annual meeting of the Air Pollution Control
Association; June; Minneapolis, MN. Pittsburgh, PA: Air Pollution Control Association;
paper no. 86-39.2.
Miller, P. R.; McBride, J. R.; Schilling, S. L.; Gomez, A. P. (1989a) Trend of ozone damage to conifer forests
between 1974 and 1988 in the San Bernardino Mountains of southern California. In: Olson, R. K.;
Lefohn, A. S., eds. Effects of air pollution on western forests [an A&WMA symposium; June;
Anaheim, CA]. Pittsburgh, PA: Air and Waste Management Association; pp. 309-323. (APCA
transactions series: no. 16).
Miller, J. E.; Heagle, A. S.; Vozzo, S. F.; Philbeck, R. B.; Heck, W. W. (1989b) Effects of ozone and water
stress, separately and in combination, on soybean yield. J. Environ. Qual. 18: 330-336.
Miller, J. E.; Patterson, R. P.; Pursley, W. A.; Heagle, A. S.; Heck, W. W. (1989c) Response of soluble sugars
and starch in field-grown cotton to ozone, water stress, and their combination. Environ. Exp. Bot.
29: 477-486.
Miller, P. R.; McBride, J. R.; Schilling, S. L. (1991) Chronic ozone injury and associated stresses affect relative
competitive capacity of species comprising the California mixed conifer forest type. In: Memorias
del primer simposial nacional; Agricultura sostenible: Una opcion para desarollo sin deterioro
ambiental. Montecillo, Edo. Mexico, Mexico: Comision de Estudios Ambientales, Colegio de
Postgraduados; pp. 161-172.
Miller, P. R.; Grulke, N. E.; Stolte, K. W. (1994) Effects of air pollution on giant sequoia ecosystems In: Aune,
P. S., technical coordinator. Proceedings of the symposium on giant sequoias: their place in the
ecosystem and society; June 1992; Visalia, CA. Albany, CA: U.S. Department of Agriculture,
Forest Service, Pacific Southwest Research Station; pp. 90-98; report no. PSW-GTR-151.
Millers, L; Shriner, D. S.; Rizzo, D. (1989) History of hardwood decline in the eastern United States. Broomall,
PA: U.S. Department of Agriculture, Northeastern Forest Experiment Station; general technical
report NE-126.
Mitchell, R. C.; Carson, R. T. (1989) Using surveys to value public goods: the contingent valuation method.
Washington, DC: Resources for the Future.
5-325
-------
Moldau, H.; Sober, I; Sober, A. (1990) Differential sensitivity of stomata and mesophyll to sudden exposure of
bean shoots to ozone. Photosynthetica 24: 446-458.
Moldau, H.; Kull, O.; Sober, J.; Norby, R. J. (199la) Differential response of CO2 uptake parameters of soil- and
sand-grown Phaseolus vulgaris (L.) plants to absorbed ozone flux. Environ. Pollut. 74: 251-262.
Moldau, H.; Sober, J.; Karolin, A.; Kallis, A. (1991b) CO2 uptake and respiration losses in vegetative bean plants
due to ozone absorption. Photosynthetica 25: 341-349.
Monteith, J. L.; Unsworth, M. H. (1990) Principles of environmental physics. 2nd ed. London, United Kingdom:
Edward Arnold.
Monies, R. A.; Blum, U.; Heagle, A. S. (1982) The effects of ozone and nitrogen fertilizer on tall fescue, ladino
clover, and a fescue-clover mixture. I. Growth, regrowth, and forage production. Can. J. Bot. 60:
2745-2752.
Moore, R. A. F.; Ruetsch, S. B.; Weigmann, H.-D. (1984) The role of dye diffusion in the ozone fading of acid
and disperse dyes in polyamides. Text. Chem. Color. 16(12): 23-29.
Morris, M. A. (1966) Effect of weathering on cotton fabrics. Davis, CA: Western Regional Research Cooperative
Project; California Agricultural Experiment Station bulletin no. 823.
Mortensen, L. M. (1990a) Effects of ozone on growth and dry matter partitioning in different provenances of
Norway spruce (Picea abies (L.) Karst). Norw. J. Agric. Sci. 4: 61-66.
Mortensen, L. M. (1990b) The effects of low O3 concentrations on growth of Triticum aestivum L. at different
light and air humidity levels. Norw. J. Agric. Sci. 4: 337-342.
Mortensen, L. M. (1990c) Effects of ozone on growth of Triticum aestivum L. at different light, air humidity,
and CO2 levels. Norw. J. Agric. Sci. 4: 343-348.
Mortensen, L. M. (1992a) Effects of ozone on growth of seven grass and one clover species. Acta Agric. Scand.
Sect. B Soil Plant Sci. 42: 235-239.
Mortensen, L. M. (1992b) Effects of ozone concentration on growth of tomato at various light, air humidity and
carbon dioxide levels. Sci. Hortic. (Amsterdam) 49: 17-24.
Mortensen, L. M.; Nilsen, J. (1992) Effects of ozone and temperature on growth of several wild plant species.
Norw. J. Agric. Sci. 6: 195-204.
Mortensen, L. M.; Skre, O. (1990) Effects of low ozone concentrations on growth of Betula pubescens Ehrh.,
Betula verrucosa Ehrh. wAAlnus incana (L.) Moench. New Phytol. 115: 165-170.
Mudano, J. E.; Allen, H. L.; Kress, L. W. (1992) Stem and foliage elongation of young loblolly pine as affected
by ozone. For. Sci. 38: 324-335.
Mueller, W. J.; Stickney, P. B. (1970) A survey and economic assessment of the effects of air pollution on
elastomers: final report. Columbus, OH: Battelle Memorial Institute, Columbus Laboratories;
National Air Pollution Control Administration contract no. CPA-22-69-146.
Mukammal, E. I. (1965) Ozone as a cause of tobacco injury. Agric. Meteorol. 2: 145-165.
Mulcahy, D. L. (1979) The rise of the angiosperms: a genecological factor. Science (Washington, DC)
206: 20-23.
5-326
-------
Mulcahy, D. L.; Mulcahy, G. B. (1983) Pollen selection: an overview. In: Mulcahy, D. L.; Ottaviano, E., eds.
Pollen: biology and implications for plant breeding. New York, NY: Elsevier Science Publishers;
pp. xv-xvii.
Mulchi, C. L.; Sammons, D. J.; Baenziger, P. S. (1986) Yield and grain quality responses of soft red winter
wheat exposed to ozone during anthesis. Agron. J. 78: 593-600.
Mulchi, C. L.; Lee, E.; Tuthill, K.; Olinick, E. V. (1988) Influence of ozone stress on growth processes, yields
and grain quality characteristics among soybean cultivars. Environ. Pollut. 53: 151-169.
Mulchi, C. L.; Slaughter, L.; Saleem, M.; Lee, E. H.; Pausch, R.; Rowland, R. (1992) Growth and physiological
characteristics of soybean in open-top chambers in response to ozone and increased atmospheric
CO2. Agric. Ecosyst. Environ. 38: 107-118.
Mumford, R. A.; Lipke, H.; Laufer, D. A.; Feder, W. A. (1972) Ozone-induced changes in corn pollen. Environ.
Sci. Technol. 6: 427-430.
Murray, J. J.; Howell, R. K.; Wilton, A. C. (1975) Differential response of seventeen Poa pratensis cultivars to
ozone and sulfur dioxide. Plant Dis. Rep. 59: 852-854.
Murray, D. R.; Atwater, M. A.; Yocom, J. E. (1986) Assessment of the costs of materials damage from air
pollution in Los Angeles, California. Presented at: 79th annual meeting of the Air Pollution Control
Association; June; Minneapolis, MN. Pittsburgh, PA: Air Pollution Control Association; paper no.
86-85.9.
Musselman, R. C.; Taschenberg, E. F. (1985) Usefulness of vineyard fungicides as antioxidants for grapevines.
Plant Dis. 69: 406-408.
Musselman, R. C.; Oshima, R. J.; Gallavan, R. E. (1983) Significance of pollutant concentration distribution in
the response of 'red kidney' beans to ozone. J. Am. Soc. Hortic. Sci. 108: 347-351.
Musselman, R. C.; Forsline, P. L.; Kender, W. J. (1985) Effects of sulfur dioxide and ambient ozone on Concord
grapevine growth and productivity. J. Am. Soc. Hortic. Sci. 110: 882-888.
Musselman, R. C.; McCool, P. M.; Oshima, R. J.; Teso, R. R. (1986a) Field chambers for assessing crop loss
from air pollutants. J. Environ. Qual. 15: 152-157.
Musselman, R. C.; Huerta, A. J.; McCool, P. M.; Oshima, R. J. (1986b) Response of beans to simulated ambient
and uniform ozone distributions with equal peak concentration. J. Am. Soc. Hortic. Sci. Ill:
470-473.
Musselman, R. C.; McCool, P. M.; Younglove, T. (1988) Selecting ozone exposure statistics for determining
crop yield loss from air pollutants. Environ. Pollut. 53: 63-78.
Musselman, R. C.; Younglove, T.; McCool, P. M. (1994) Response of Phaseolus vulgaris L. to differing ozone
regimes having indentical total exposure. Atmos. Environ. 28: 2727-2731.
Nast, W.; Mortensen, L.; Fischer, K.; Fitting, I. (1993) Effects of air pollutants on the growth and antioxidative
system of Norway spruce exposed in open-top chambers. Environ. Pollut. 80: 85-90.
National Air Pollution Control Administration. (1968) Air quality data from the national air surveillance
networks and contributing state and local networks: 1966 edition. Durham, NC: U.S. Department of
Health, Education, and Welfare; publication no. APTD 68-9. Available from: NTIS, Springfield,
VA; PB-195155.
5-327
-------
Neighbour, E. A.; Pearson, M; Mehlhorn, H. (1990) Purafil-filtration prevents the development of ozone-induced
frost injury: a potential role for nitric oxide. Atmos. Environ. Part A 24: 711-715.
Neufeld, H. S.; Renfro, J. R.; Hacker, W. D.; Silsbee, D. (1992) Ozone in Great Smoky Mountains National
Park: dynamics and effects on plants. In: Berglund, R. L., ed. Tropospheric ozone and the
environment II: effects, modeling and control [papers from an international specialty conference];
November; Atlanta, GA. Pittsburgh, PA: Air & Waste Management Association; pp. 594-617.
(A&WMA transactions series no. 20).
Nipe, M. R. (1981) Atmospheric contaminant fading. Text. Chem. Color. 13: 136-146.
Norby, R. J.; Richter, D. D.; Luxmoore, R. J. (1985) Physiological processes in soybean inhibited by gaseous
pollutants but not by acid rain. New Phytol. 100: 79-85.
Norby, R. J.; Takemoto, B. K.; Johnston, J. W.; Shriner, D. S. (1986) Acetylene reduction rate as a physiological
indicator of the response of field-grown soybeans to simulated acid rain and ambient gaseous
pollutants. Environ. Exp. Bot. 26: 285-290.
Nouchi, L; Aoki, K. (1979) Morning glory as a photochemical oxidant indicator. Environ. Pollut. 18: 289-303.
Nouchi, L; Mayumi, H.; Yamazoe, F. (1984) Foliar injury response of petunia and kidney bean to simultaneous
and alternate exposures to ozone and PAN. Atmos. Environ. 18: 453-460.
Nouchi, L; Ito, O.; Harazono, Y.; Kobayashi, K. (1991) Effects of chronic ozone exposure on growth, root
respiration and nutrient uptake of rice plants. Environ. Pollut. 74: 149-164.
Odum, E. P. (1971) Fundamentals of ecology. 3rd ed. Philadelphia, PA: W. B. Saunders Company;
pp. 1-38, 106-136.
Odum, E. P. (1985) Trends expected in stressed ecosystems. BioScience 35: 419-422.
Odum, E. P. (1989) Ecology and our endangered life-support systems. Sunderland, MA: Sinauer Associates, Inc.;
pp. 58-66, 108-118.
Odum, E. P. (1993) Ecology and our endangered life-support systems. Sunderland, MA: Sinauer Associates, Inc.;
pp. 7-108.
Okano, K.; Ito, O.; Takeba, G.; Shimizu, A.; Totsuka, T. (1985) Effects of O3 and NO2 alone or in combination
on the distribution of 13C-assimilate in kidney bean plants. Jpn. J. Crop Sci. 54: 152-159.
Olszyk, D. M.; Tibbitts, T. W. (1981) Stomatal response and leaf injury of Pi sum sativum L. with SO2 and
O3 exposures: I. influence of pollutant level and leaf maturity. Plant Physiol. 67: 539-544.
Olszyk, D. M.; Tibbitts, T. W.; Hertzberg, W. M. (1980) Environment in open-top field chambers utilized for air
pollution studies. J. Environ. Qual. 9: 610-615.
Olszyk, D. M.; Bytnerowicz, A.; Kats, G.; Dawson, P. J.; Wolf, J.; Thompson, C. R. (1986a) Crop effects from
air pollutants in air exclusion systems vs. field chambers. J. Environ. Qual. 15: 417-422.
Olszyk, D. M.; Bytnerowicz, A.; Kats, G.; Dawson, P. J.; Wolf, J.; Thompson, C. R. (1986b) Effects of sulfur
dioxide and ambient ozone on winter wheat and lettuce. J. Environ. Qual. 15: 363-369.
Olszyk, D. M.; Maas, E. V.; Kats, G.; Francois, L. E. (1988) Soil salinity and ambient ozone: lack of stress
interaction for field-grown alfalfa. J. Environ. Qual. 17: 299-304.
5-328
-------
Olszyk, D. M; Dawson, P. I; Morrison, C. L.; Takemoto, B. K. (1990a) Plant response to nonfiltered air
vs. added ozone generated from dry air or oxygen. J. Air Waste Manage. Assoc. 40: 77-81.
Olszyk, D. M.; Kats, G.; Morrison, C. L.; Dawson, P. J.; Gocka, L; Wolf, J.; Thompson, C. R. (1990b)
'Valencia' orange fruit yield with ambient oxidant or sulfur dioxide exposures. J. Am. Soc. Hortic.
Sci. 115: 878-883.
Olszyk, D. M.; Takemoto, B. K.; Kats, G.; Dawson, P. J.; Morrison, C. L.; Preston, J. W.; Thompson, C. R.
(1992) Effects of open-top chambers on 'Valencia' orange trees. J. Environ. Qual. 21: 128-134.
Olszyk, D.; Bytnerowicz, A.; Kats, G.; Reagan, C.; Hake, S.; Kerby, T.; Millhouse, D.; Roberts, B.; Anderson,
C.; Lee, H. (1993) Cotton yield losses and ambient ozone concentrations in California's San Joaquin
Valley. J. Environ. Qual. 22: 602-611.
Ormrod, D. P.; Kemp, W. G. (1979) Ozone response of tomato plants infected with cucumber mosaic virus
and/or tobacco mosaic virus. Can. J. Plant Sci. 59: 1077-1083.
Ormrod, D. P.; Adedipe, N. O.; Hofstra, G. (1971) Responses of cucumber, onion and potato cultivars to ozone.
Can. J. Plant Sci. 51: 283-288.
Ormrod, D. P.; Adedipe, N. O.; Hofstra, G. (1973) Ozone effects on growth of radish plants as influenced by
nitrogen and phosphorus nutrition and by temperature. Plant Soil 39: 437-439.
Ormrod, D. P.; Marie, B. A.; Allen, O. B. (1988) Research approaches to pollutant crop loss functions. In: Heck,
W. W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from air pollutants: proceedings
of an international conference; October 1987; Raleigh, NC. Essex, United Kingdom: Elsevier
Science Publishers, Ltd.; pp. 27-44.
Oshima, R. J. (1975) Development of a system for evaluating and reporting economic crop losses caused by air
pollution in California. III. Ozone dosage-crop loss conversion function—alfalfa, sweet corn.
IIIA. Procedures for production, ozone effects on alfalfa and sweet corn, and evaluation of these
systems. Sacramento, CA: California Air Resources Board; report no. ARB-R-3-690-75-35.
Available from: NTIS, Springfield, VA; PB-272994.
Oshima, R. J. (1978) The impact of sulfur dioxide on vegetation: a sulfur dioxide-ozone response model:
final report. Riverside, CA: University of California, Statewide Air Pollution Research Center; ARE
agreement no. A6-162-30. Available from: NTIS, Springfield, VA; PB-283604.
Oshima, R. J.; Poe, M. P.; Braegelmann, P. K.; Baldwin, D. W.; Van Way, V (1976) Ozone dosage-crop loss
function for alfalfa: a standardized method for assessing crop losses from air pollutants. J. Air
Pollut. Control Assoc. 26: 861-865.
Oshima, R. J.; Braegelmann, P. K.; Baldwin, D. W.; Van Way, V.; Taylor, O. C. (1977a) Reduction of tomato
fruit size and yield by ozone. J. Am. Soc. Hortic. Sci. 102: 289-293.
Oshima, R. J.; Braegelmann, P. K.; Baldwin, D. W.; Van Way, V; Taylor, O. C. (1977b) Responses of five
cultivars of fresh market tomato to ozone: a contrast of cultivar screening with foliar injury and
yield. J. Am. Soc. Hortic. Sci. 102: 286-289.
Otto, H. W.; Daines, R. H. (1969) Plant injury by air pollutants: influence of humidity on stomatal apertures and
plant response to ozone. Science (Washington, DC) 163: 1209-1210.
Parmeter, J. R., Jr.; Bega, R. V.; Neff, T. (1962) A chlorotic decline of ponderosa pine in southern California.
Plant Dis. Rep. 46: 269-273.
5-329
-------
Parsons, D. I; Pitelka, L. F. (1991) Plant ecological genetics and air pollution stress: a commentary on
implications for natural populations. In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg, M. T., eds.
Ecological genetics and air pollution. New York, NY: Springer-Verlag; pp. 337-343.
Pathak, S. N.; Love, D. V.; Roy, D. N. (1986) Determination of a chemical basis of air-pollution stress in wood
of mature white pine trees in the susceptive forest ecosystems. Water Air Soil Pollut. 31: 385-392.
Patton, R. L.; Jensen, K. F.; Schier, G. A. (1991) Responses of red spruce seedlings to ozone and acid
deposition. Can. J. For. Res. 21: 1354-1359.
Pearcy, R. W.; Bjorkman, O.; Caldwell, M. M.; Keeley, J. E.; Monson, R. K.; Strain, B. R. (1987) Carbon gain
by plants in natural environments. BioScience 37: 21-29.
Pedersen, B. S. (1989) Ozone injury to Jeffrey and ponderosa pines surrounding Lake Tahoe, California and
Nevada. In: Olson, R. K.; Lefohn, A. S., eds. Effects of air pollution on western forests
[an A&WMA symposium; June; Anaheim, CA]. Pittsburgh, PA: Air and Waste Management
Association; pp. 279-292. (APCA transactions series: no. 16).
Pell, E. J. (1976) Influence of benomyl soil treatment on pinto bean plants exposed to peroxyacetyl nitrate and
ozone. Phytopathology 66: 731-733.
Pell, E. J. (1988) Secondary metabolism and air pollutants. In: Gaseous air pollution and plant metabolism:
proceedings of the 2nd international symposium; pp. 222-237.
Pell, E. J.; Gardner, W. (1979) Enhancement of peroxyacetyl nitrate injury to petunia foliage by benomyl.
HortScience 14: 61-62.
Pell, E. J.; Pearson, N. S. (1984) Ozone-induced reduction in quantity and quality of two potato cultivars.
Environ. Pollut. Ser. A 35: 345-352.
Pell, E. J.; Puente, M. (1986) Emission of ethylene by oat plants treated with ozone and simulated acid rain.
New Phytol. 103: 709-715.
Pell, E. J.; Lukezic, F. L.; Levine, R. G.; Weissberger, W. C. (1977) Response of soybean foliage to reciprocal
challenges by ozone and a hypersensitive-response-inducing pseudomonad. Phytopathology 67:
1342-1345.
Pell, E. J.; Pearson, N. S.; Vinten-Johansen, C. (1988) Qualitative and quantitative effects of ozone and/or sulfur
dioxide on field-grown potato plants. Environ. Pollut. 53: 171-186.
Pell, E. J.; Winner, W. E.; Vinten-Johansen, C.; Mooney, H. A. (1990) Response of radish to multiple stresses. I.
Physiological and growth responses to changes in ozone and nitrogen. New Phytol. 115: 439-446.
Pell, E. J.; Eckardt, N.; Enyedi, A. J. (1992) Timing of ozone stress and resulting status of ribulose bisphosphate
carboxylase/oxygenase and associated net photosynthesis. New Phytol. 120: 397-405.
Pell, E. J.; Temple, P. J.; Friend, A. L.; Mooney, H. A.; Winner, W. E. (1994) Compensation as a plant response
to ozone and associated stresses: an analysis of ROPIS experiments. J. Environ. Qual. 23: 429-436.
Pellissier, M.; Lacasse, N. L.; Cole, H., Jr. (1972) Effectiveness of benzimidazole, benomyl, and thiabendazole in
reducing ozone injury to pinto beans. Phytopathology 62: 580-582.
5-330
-------
Percy, K. E.; Jensen, K. F.; McQuattie, C. J. (1992) Effects of ozone and acidic fog on red spruce needle
epicuticular wax production, chemical composition, cuticular membrane ultrastructure and needle
wettability. New Phytol. 122: 71-80.
Peterson, D. L.; Arbaugh, M. J. (1988) An evaluation of the effects of ozone injury on radial growth of
ponderosa pine (Pinus ponderosa) in the southern Sierra Nevada. JAPCA 38: 921-927.
Peterson, D. L.; Arbaugh, M. J. (1992) Mixed conifer forests of the Sierra Nevada. In: Olson, R. K.; Binkley, D.;
Bohm, M., eds. The response of western forests to air pollution. New York, NY: Springer-Verlag;
pp. 433-459. (Billings, W. D.; Golley, F.; Lange, O. L.; Olson, J. S.; Remmert, H., eds. Ecological
studies: analysis and synthesis: v. 97).
Peterson, D. L.; Arbaugh, M. J.; Wakefield, V. A.; Miller, P. R. (1987) Evidence of growth reduction in
ozone-injured Jeffrey pine (Pinus jeffreyi Grev. and Barf.) in Sequoia and Kings Canyon National
Parks. JAPCA 37: 906-912.
Peterson, D. L.; Arbaugh, M. J.; Robinson, L. J. (1989) Ozone injury and growth trends of ponderosa pine in the
Sierra Nevada. In: Olson, R. K.; Lefohn, A. S., eds. Effects of air pollution on western forests [an
A&WMA symposium; June; Anaheim, CA]. Pittsburgh, PA: Air and Waste Management
Association; pp. 293-307. (APCA transactions series: no. 16).
Peterson, D. L.; Arbaugh, M. J.; Robinson, L. J. (1991) Regional growth changes in ozone-stressed ponderosa
pine (Pinus ponderosa) in the Sierra Nevada, California, USA. Holocene 1: 50-61.
Peterson, G. L.; Swanson, C. S.; McCollum, D. W.; Thomas, M. H., eds. (1992) Valuing wildlife resources in
Alaska. Boulder, CO: Westview Press. (Field, D. R., ed. Social behavior and natural
resources series).
Peterson, D. L.; Silsbee, D. G.; Poth, M.; Arbaugh, M. J.; Biles, F. E. (1995) Growth response of bigcone
Douglas fir (Pseudotsuga macrocarpa) to long-term ozone exposure in southern California. J. Air
Waste Manage. Assoc. 45: 36-45.
Phipps, R. L.; Whiton, J. C. (1988) Decline in long-term growth trends of white oak. Can. J. For. Res. 18: 24-32.
Pier, P. A.; Thornton, F. C.; McDuffie, C., Jr.; Hanson, P. J. (1992) CO2 exchange rates of red spruce during the
second season of exposure to ozone and acidic cloud deposition. Environ. Exp. Bot. 32: 115-124.
Pitcher, L. H.; Brennan, E.; Hurley, A.; Dunsmuir, P.; Tepperman, J. M.; Zilinskas, B. A. (1991) Overproduction
of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in
transgenic tobacco. Plant Physiol. 97: 452-455.
Pitelka, L. F. (1988) Evolutionary responses of plants to anthropogenic pollutants. Trends in Ecology and
Evolutions: 233-236.
Pleijel, H.; Skarby, L.; Wallin, G.; Sellden, G. (1991) Yield and grain quality of spring wheat (Triticum aestivum
L., cv. Drabant) exposed to different concentrations of ozone in open-top chambers. Environ. Pollut.
69: 151-168.
Pleijel, H.; Skarby, L.; Ojanpera, K.; Sellden, G. (1992) Yield and quality of spring barley, Hordeum vulgare L.,
exposed to different concentrations of ozone in open-top chambers. Agric. Ecosyst. Environ. 38:
21-29.
Pleijel, H.; Wallin, G.; Karlsson, P. E.; Skarby, L.; Sellden, G. (1994) Ozone deposition to an oat crop (Avena
sativa L.) grown in open-top chambers and in the ambient air, Atmos. Environ. 28: 1971-1979.
5-331
-------
Posthumus, A. C. (1984) Monitoring levels and effects of air pollutants. In: Treshow, M, ed. Air pollution and
plant life. New York, NY: John Wiley & Sons; pp. 73-95. (Polunin, N., ed. Environment
monographs and symposia).
Povilaitis, B. (1967) Gene effects for tolerance to weather fleck in tobacco. Can. J. Genet. Cytol. 9: 327-334.
Powles, S. B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol.
35: 15-44.
Price, H.; Treshow, M. (1972) Effects of ozone on the growth and reproduction of grasses. In: Proceedings of
the international air pollution conference; May; Melbourne, Australia. Melbourne, Australia:
Clean Air Society of Australia and New Zealand; pp. 275-280.
Price, A.; Lucas, P. W.; Lea, P. J. (1990) Age dependent damage and glutathione metabolism in ozone fumigated
barley: a leaf section approach. J. Exp. Bot. 41: 1309-1317.
Prokipcak, B.; Ormrod, D. P. (1986) Visible injury and growth responses of tomato and soybean to combinations
of nickel, copper and ozone. Water Air Soil Pollut. 27: 329-340.
Pye, J. M. (1988) Impact of ozone on the growth and yield of trees: a review. J. Environ. Qual. 17: 347-360.
Qiu, Z.; Chappelka, A. H.; Somers, G. L.; Lockaby, B. G.; Meldahl, R. S. (1992) Effects of ozone and simulated
acidic precipitation on above- and below-ground growth of loblolly pine (Pinus taedd). Can. J. For.
Res. 22: 582-587.
Queiroz, O. (1988) Air pollution, gene expression and post-translational enzyme modifications.
In: Schulte-Hostede, S.; Darrall, N. M.; Blank, L. W.; Wellburn, A. R., eds. Air pollution and plant
metabolism. London, United Kingdom: Elsevier Applied Science; pp. 238-254.
Rafarel, C. R.; Ashenden, T. W. (1991) A facility for the large-scale exposure of plants to gaseous atmospheric
pollutants. New Phytol. 117: 345-349.
Randall, A. (1991) The value of biodiversity. Ambio 20: 64-68.
Rawlings, J. O.; Cure, W. W. (1985) The Weibull function as a dose-response model to describe ozone effects
on crop yields. Crop Sci. 25: 807-814.
5-332
-------
Rawlings, J. O.; Lesser, V. M; Dassel, K. A. (1988a) Statistical approaches to assessing crop loss. In: Heck, W.
W.; Taylor, O. C.; Tingey, D. T., eds. Assessment of crop loss from atmospheric pollutants:
proceedings of an international conference; October, 1987; Raleigh, NC. New York, NY: Elsevier
Science; pp. 389-416.
Rawlings, J. O.; Lesser, V. M.; Heagle, A. S.; Heck, W. W. (1988b) Alternative ozone dose metrics to
characterize ozone impact on crop yield loss. J. Environ. Qual. 17: 285-291.
Razumovskii, S. D.; Batashova, L. S. (1970) Mechanism of protection against ozone by
N-phenyl-N'-isopropyl-p-phenylenediamine. Rubber Chem. Technol. 43: 1340-1348.
Razumovskii, S. D.; Podmasteriev, V. V.; Zaikov, G. E. (1988) Kinetics and mechanism of stress relaxation of
polyisoprene vulcanizates under ozone ageing. Polym. Degrad. Stab. 20: 37-47.
Rebbeck, J.; Brennan, E. (1984) The effect of simulated acid rain and ozone on the yield and quality of
glasshouse-grown alfalfa. Environ. Pollut. Ser. A 36: 7-16.
Rebbeck, J.; Blum, U.; Heagle, A. S. (1988) Effects of ozone on the regrowth and energy reserves of a ladino
clover-tall fescue pasture. J. Appl. Ecol. 25: 659-681.
Rebbeck, J.; Jensen, K. F.; Greenwood, M. S. (1992) Ozone effects on the growth of grafted mature and juvenile
red spruce. Can. J. For. Res. 22: 756-760.
Reddy, G. B.; Reinert, R. A.; Eason, G. (1991a) Effect of acid rain and ozone on soil and secondary needle
nutrients of loblolly pine. In: Wright, R. J.; Baligar, V. C.; Murrmann, R. P., eds. Plant-soil
interactions at low pH: proceedings of the second international symposium; June 1990;
Beckley, WV. Dordrecht, The Netherlands: Kluwer Academic Publishers; pp. 139-145.
Reddy, G. B.; Reinert, R. A.; Eason, G. (1991b) Enzymatic changes in the rhizosphere of loblolly pine exposed
to ozone and acid rain. Soil Biol. Biochem. 23: 1115-1119.
Reddy, G. N.; Arteca, R. N.; Dai, Y.-R.; Flores, H. E.; Negm, F. B.; Pell, E. J. (1993) Changes in ethylene and
polyamines in relation to mRNA levels of the large and small subunits of ribulose bisphosphate
carboxylase/oxygenase in ozone-stressed potato foliage. Plant Cell Environ. 16: 819-826.
Reich, P. B. (1987) Quantifying plant response to ozone: a unifying theory. Tree Physiol. 3: 63-91.
Reich, P. B.; Amundson, R. G. (1985) Ambient levels of ozone reduce net photosynthesis in tree and crop
species. Science (Washington, DC) 230: 566-570.
Reich, P. B.; Schoettle, A. W.; Stroo, H. F.; Troiano, J.; Amundson, R. G. (1985) Effects of O3, SO2, and acidic
rain on mycorrhizal infection in northern red oak seedlings. Can. J. Bot. 63: 2049-2055.
Reich, P. B.; Schoettle, A. W.; Stroo, H. F.; Amundson, R. G. (1986a) Acid rain and ozone influence
mycorrhizal infection in tree seedlings. J. Air Pollut. Control Assoc. 36: 724-726.
Reich, P. B.; Schoettle, A. W.; Amundson, R. G. (1986b) Effects of O3 and acidic rain on photosynthesis and
growth in sugar maple and northern red oak seedlings. Environ. Pollut. Ser. A 40: 1-15.
Reich, P. B.; Schoettle, A. W.; Stroo, H. F.; Troiano, J.; Amundson, R. G. (1987) Effects of ozone and acid rain
on white pine (Pinus strobus) seedlings grown in five soils. I. Net photosynthesis and growth. Can.
J. Bot. 65: 977-987.
5-333
-------
Reich, P. B.; Shoettle, A. W.; Stroo, H. F.; Amundson, R. G. (1988) Effects of ozone and acid rain on white
pine (Pinus strobus) seedlings grown in five soils. III. Nutrient relations. Can. J. Bot.
66: 1517-1531.
Reich, P. B.; Ellsworth, D. S.; Kloeppel, B. D.; Fownes, J. H.; Gower, S. T. (1990) Vertical variation in canopy
structure and CO2 exchange of oak-maple forests: influence of ozone, nitrogen, and other factors on
simulated canopy carbon gain. Tree Physiol. 7: 329-345.
Reiling, K.; Davison, A. W. (1992a) Spatial variation in ozone resistance of British populations of Plantago
major L. New Phytol. 122: 699-708.
Reiling, K.; Davison, A. W. (1992b) The response of native, herbaceous species to ozone: growth and
fluorescence screening. New Phytol. 120: 29-37.
Reiling, K.; Davison, A. W. (1992c) Effects of a short ozone exposure given at different stages in the
development of Plantago major L. New Phytol. 121: 643-647.
Reinert, R. A. (1984) Plant response to air pollutant mixtures. Ann. Rev. Phytopathol. 22: 421-442.
Reinert, R. A.; Gooding, G. V., Jr. (1978) Effect of ozone and tobacco streak virus alone and in combination on
Nicotiana tabacum. Phytopathology 68: 15-17.
Reinert, R. A.; Gray, T. N. (1981) The response of radish to nitrogen dioxide, sulfur dioxide, and ozone, alone
and in combination. J. Environ. Qual. 10: 240-243.
Reinert, R. A.; Henderson, W. R. (1980) Foliar injury and growth of tomato cultivars as influenced by ozone
dose and plant age. J. Am. Soc. Hortic. Sci. 105: 322-324.
Reinert, R. A.; Nelson, P. V. (1979) Sensitivity and growth of twelve Elatior begonia cultivars to ozone.
HortScience 14: 747-748.
Reinert, R. A.; Nelson, P. V. (1980) Sensitivity and growth of five Elatior begonia cultivars to SO2 and O3, alone
and in combination. J. Am. Soc. Hortic. Sci. 105: 721-723.
Reinert, R. A.; Heggestad, H. E.; Heck, W. W. (1982) Response and genetic modification of plants for tolerance
to air pollutants. In: Christiansen, M. N.; Lewis, C. F., eds. Breeding plants for less favorable
environments. New York, NY: John Wiley & Sons; pp. 259-292.
Reinert, R. A.; Rufty, R. C.; Eason, G. (1988) Interaction of tobacco etch or tobacco vein mottling virus and
ozone onbiomass changes inburley tobacco. Environ. Pollut. 53: 209-218.
Resh, H. M.; Runeckles, V. C. (1973) Effects of ozone on bean rust Uromyces phaseoli. Can. J. Bot.
51: 725-727.
Retzlaff, W. A.; Williams, L. E.; DeJong, T. M. (1991) The effect of different atmospheric ozone partial
pressures on photosynthesis and growth of nine fruit and nut tree species. Tree Physiol. 8: 93-105.
Retzlaff, W. A.; DeJong, T. M.; Williams, L. E. (1992a) Photosynthesis and growth response of almond to
increased atmospheric ozone partial pressures. J. Environ. Qual. 21: 208-216.
Retzlaff, W. A.; Williams, L. E.; DeJong, T. M. (1992b) Photosynthesis, growth, and yield response of
'Casselman' plum to various ozone partial pressures during orchard establishment. J. Am. Soc.
Hortic. Sci. 117: 703-710.
5-334
-------
Rich, S.; Turner, N. C. (1972) Importance of moisture on stomatal behavior of plants subjected to ozone. J. Air
Pollut. Control Assoc. 22: 718-721.
Rich, S.; Waggoner, P. E.; Tomlinson, H. (1970) Ozone uptake by bean leaves. Science (Washington, DC) 169:
79-80.
Richards, B. N. (1987) The microbiology of terrestrial ecosystems. Essex, United Kingdom: Longman Scientific
and Technical.
Richards, B. L.; Middleton, J. T.; Hewitt, W. B. (1958) Air pollution with relation to agronomic crops:
V. oxidant stipple of grape. Agron. J. 50: 559-561.
Roberts, B. R. (1990) Physiological response of yellow-poplar seedlings to simulated acid rain, ozone fumigation
and drought. For. Ecol. Manage. 31: 215-224.
Roberts, B. R.; Cannon, W. N., Jr. (1992) Growth and water relationships of red spruce seedlings exposed to
atmospheric deposition and drought. Can. J. For. Res. 22: 193-197.
Rodecap, K. D.; Tingey, D. T. (1986) Ozone-induced ethylene release from leaf surfaces. Plant Sci. 44: 73-76.
Rogers, H. H.; Bingham, G. E.; Cure, J. D.; Smith, J. M; Surano, K. A. (1983) Responses of selected plant
species to elevated carbon dioxide in the field. J. Environ. Qual. 12: 569-574.
Roose, M. L. (1991) Genetics of response to atmospheric pollutants. In: Taylor, G. E., Jr.; Pitelka, L. F.; Clegg,
M. T., eds. Ecological genetics and air pollution. New York, NY: Springer-Verlag; pp. 111-126.
Roose, M. L.; Bradshaw, A. D.; Roberts, T. M. (1982) Evolution of resistance to gaseous air pollutants.
In: Unsworth, M. H.; Ormrod, D. P., eds. Effects of gaseous air pollution in agriculture and
horticulture. London, United Kingdom: Butterworth Scientific; pp. 379-409.
Rosen, P. M.; Runeckles, V. C. (1976) Interaction of ozone and greenhouse whitefly in plant injury.
Environ. Conserv. 3: 70-71.
Runeckles, V. C. (1984) Impact of air pollutant combinations on plants. In: Treshow, M., ed. Air pollution and
plant life. New York, NY: John Wiley & Sons; pp. 239-258. (Polunin, N., ed. Environmental
monographs and symposia).
Runeckles, V. C.; Chevone, B. I. (1992) Crop responses to ozone. In: Lefohn, A. S., ed. Surface level ozone
exposures and their effects on vegetation. Chelsea, MI: Lewis Publishers; pp. 189-270.
Runeckles, V. C.; Krupa, S. V. (1994) The impact of UV-B radiation and ozone on terrestrial vegetation.
Environ. Pollut. 83: 191-213.
Runeckles, V. C.; Palmer, K. (1987) Pretreatment with nitrogen dioxide modifies plant response to ozone.
Atmos. Environ. 21: 717-719.
Runeckles, V. C.; Rosen, P. M. (1977) Effects of ambient ozone pretreatment on transpiration and susceptibility
to ozone injury. Can. J. Bot. 55: 193-197.
5-335
-------
Runeckles, V. C.; Wright, E. F.; White, D. (1990) A chamberless field exposure system for determining the
effects of gaseous air pollutants on crop growth and yield. Environ. Pollut. 63: 61-77.
Russell, C. S. (1993) Old lessons and new contexts in economic-ecological modeling. In: Milon, J. W.; Shogren,
I; Young, M, eds. Integrating economic and ecological indicators: proceedings of the symposium
of the Resource Policy Consortium; May; Washington, DC.
Salmon, R. L. (1970) Systems analysis of the effects of air pollution on materials. Raleigh, NC: National Air
Pollution Control Administration, Economic Effects Research Division; report no. APTD-0943.
Available from: NTIS, Springfield, VA; PB-209192.
Salvin, V. S. (1969) Ozone fading of dyes. Text. Chem. Color. 1: 245-251.
Salvin, V. S. (1970) Survey and economic assessment of the effects of air pollution on textile fibers and dyes.
Raleigh, NC: U.S. Department of Health, Education, and Welfare, National Air Pollution Control
Administration; contract no. PH-22-68-2.
Salvin, V. S.; Walker, R. A. (1955) Service fading of disperse dyestuffs by chemical agents other than the oxides
of nitrogen. Text. Res. J. 25: 571-585.
Samuelson, L. J.; Edwards, G. S. (1993) A comparison of sensitivity to ozone in seedlings and trees of Quercus
rubra L. New Phytol. 125: 373-379.
Sanders, J. S.; Reinert, R. A. (1982) Screening azalea cultivars for sensitivity to nitrogen dioxide, sulfur dioxide,
and ozone alone and in mixtures. J. Am. Soc. Hortic. Sci. 107: 87-90.
Sanders, G. E.; Turnbull, N. D.; Clark, A. G.; Colls, J. J. (1990) The growth and development of Viciafaba L.
in filtered and unfiltered open-top chambers. New Phytol. 116: 67-78.
Sanders, G. E.; Robinson, A. D.; Geissler, P. A.; Colls, J. J. (1992) Yield stimulation of a commonly grown
cultivar of Phaseolus vulgahs L. at near-ambient ozone concentrations. New Phytol. 122: 63-70.
Sasek, T. W.; Richardson, C. J.; Fendick, E. A.; Bevington, S. R.; Kress, L. W. (1991) Carryover effects of acid
rain and ozone on the physiology of multiple flushes of loblolly pine seedlings. For. Sci.
37: 1078-1098.
Saurer, M.; Fuhrer, J.; Siegenthaler, U. (1991) Influence of ozone on the stable carbon isotope composition, 813C,
of leaves and grain of spring wheat (Triticum aestivum L.). Plant Physiol. 97: 313-316.
Schenone, G.; Botteschi, G.; Fumagalli, L; Montinaro, F. (1992) Effects of ambient air pollution in open-top
chambers on bean (Phaseolus vulgaris L.): I. effects on growth and yield. New Phytol.
122: 689-697.
Schier, G. A.; McQuattie, C. J.; Jensen, K. F. (1990) Effect of ozone and aluminum on pitch pine (Pinus rigida)
seedlings: growth and nutrient relations. Can. J. For. Res. 20: 1714-1719.
Scholz, F.; Gergorius, H.-R.; Rudin, D., eds. (1989) Genetic effects of air pollutants in forest tree populations:
proceedings of the joint meeting of the IUFRO working parties. Berlin, Federal Republic of
Germany: Springer-Verlag.
5-336
-------
Schulze, E.-D.; Hall, A. E. (1982) Stomatal responses, water loss and CO2 (carbon dioxide) assimilation rates of
plants in contrasting environments (leaf conductance, dry, low and variable irradiance, and cold
environments). In: Lange, O. L.; Nobel, P. S.; Osmond, C. B.; Ziegler, H., eds. Physiological plant
ecology II: water relations and carbon assimilation. Berlin, Germany: Springer; pp. 181-230.
(Encyclopedia of plant physiology new series: 12B).
Schulze, E.-D.; Cermak, I; Matyssek, R.; Penka, M; Zimmermann, R.; Vasicek, F.; Gries, W.; Kucera, J. (1985)
Canopy transpiration and water fluxes in the xylem of the trunk of Larix and Picea trees -
a comparison of xylem flow, porometer and cuvette measurements. Oecologia 66: 475-483.
Scotto, J.; Cotton, G.; Urbach, F.; Berger, D.; Fears, T. (1988) Biologically effective ultraviolet radiation: surface
measurements in the United States, 1974 to 1985. Science (Washington, DC) 239: 762-764.
Searcy, K. B.; Mulcahy, D. L. (1985) The parallel expression of metal tolerance in pollen and sporophytes of
Silene dioica (L.) Clairv., S. alba (Mill.) Krause and Mimulus guttatus DC. Theor. Appl. Genet. 69:
597-602.
Segerson, K. (1991) Air pollution and agriculture: a review and evaluation of policy interactions. In: Just, R. E.;
Bockstael, N., eds. Commodity and resource policies in agricultural systems. Berlin, Germany:
Springer-Verlag; pp. 349-367.
Seiler, J. R.; Cazell, B. H. (1990) Influence of water stress on the physiology and growth of red spruce
seedlings. Tree Physiol. 6: 69-11.
Senser, M. (1990) Influence of soil substrate and ozone plus acid mist on the frost resistance of young Norway
spruce. Environ. Pollut. 64: 265-278.
Shafer, S. R. (1988) Influence of ozone and simulated acidic rain on microorganisms in the rhizosphere of
sorghum. Environ. Pollut. 51: 131-152.
Shafer, S. R.; Heagle, A. S. (1989) Growth responses of field-grown loblolly pine to chronic doses of ozone
during multiple growing seasons. Can. J. For. Res. 19: 821-831.
Shafer, S. R.; Schoeneberger, M. M. (1991) Ozone-induced alteration of biomass allocation and nitrogen derived
from air in the leguminous plant-Rhizobium-VAM system. In: Keister, D. L.; Cregan, P. B., eds.
The rhizosphere and plant growth: papers presented at a symposium; May 1989; Beltsville, MD.
Dordrecht, The Netherlands: Kluwer Academic Publishers; paper no. 377. (Beltsville symposia in
agricultural research: no. 14).
Shafer, S. R.; Heagle, A. S.; Camberato, D. M. (1987) Effects of chronic doses of ozone on field-grown loblolly
pine: seedling responses in the first year. JAPCA 37: 1179-1184.
Shafer, S. R.; Reinert, R. A.; Eason, G.; Spruill, S. E. (1993) Analysis of ozone concentration - biomass response
relationships among open-pollinated families of loblolly pine. Can. J. For. Res. 23: 706-715.
Sharpe, P. J. H.; Spence, R. D.; Rykiel, E. J., Jr. (1989) Diagnosis of sequential ozone effects on carbon
assimilation, translocation and allocation in cottonwood and loblolly pine. New York, NY: National
Council of the Paper Industry for Air and Steam Improvement, Inc.; technical bulletin no. 565.
Shaver, C. L.; Cass, G. R.; Druzik, J. R. (1983) Ozone and the deterioration of works of art. Environ. Sci.
Technol. 17: 748-752.
5-337
-------
Shaw, P. J. A.; Dighton, I; Poskitt, I; McLeod, A. R. (1992) The effects of sulphur dioxide and ozone on the
mycorrhizas of Scots pine and Norway spruce in a field fumigation system. Mycol. Res.
96: 785-791.
Sheffield, R. M; Cost, N. D.; Bechtold, W. A.; McClure, J. P. (1985) Pine growth reductions in the southeast.
Asheville, NC: U.S. Department of Agriculture, Forest Service, Southeastern Forest Experiment
Station; resource bulletin SE-83.
Shelburne, V. B.; Reardon, J. C.; Paynter, V. A. (1993) The effects of acid rain and ozone on biomass and leaf
area parameters of shortleaf pine (Pinus echinata Mill.). Tree Physiol. 12: 163-172.
Shimizu, H.; Oikawa, T.; Totsuka, T. (1984) Effects of low concentrations of NO2 and O3 alone and in mixture
on the growth of sunflower plants. Kenkuritsu Kogai Kenkyusho Kenkyu Hokoku 65: 121-136.
Shortle, J. S.; Phillips, M.; Dunn, J. W. (1988) Economic assessment of crop damages due to air pollution: the
role of quality effects. Environ. Pollut. 53: 377-385.
Showman, R. E. (1991) A comparison of ozone injury to vegetation during moist and drought years. J. Air
Waste Manage. Assoc. 41: 63-64.
Shriner, D. S.; Johnson, J. W., Jr. (1987) The effects of acid rain, alone and in combination with gaseous
pollutants, on growth and yield of crop plants. In: Hutchinson, T. C.; Meema, K. M., eds. Effects of
atmospheric pollutants on forests, wetlands and agricultural ecosystems: proceedings of the NATO
advanced research workshop; May 1985; Toronto, Canada. Berlin, Germany: Springer-Verlag; pp.
481-491. (NATO ASI series G: Ecological sciences, v. 16).
Shriner, D. S.; Heck, W. W.; McLaughlin, S. B.; Johnson, D. W.; Irving, P. M.; Joslin, J. D.; Peterson, C. E.
(1991) Response of vegetation to atmospheric deposition and air pollution. In: Irving, P. M., ed.
Acidic deposition: state of science and technology, volume III, terrestrial, materials, health and
visibility effects. Washington, DC: The U.S. National Acid Precipitation Assessment Program.
(State of science and technology report no. 18).
Sigal, L. L.; Johnston, J. W., Jr. (1986) Effects of acidic rain and ozone and nitrogen fixation and photosynthesis
in the lichen Lobaria pulmonaria (L.) Hoffrn. Environ. Exp. Bot. 26: 59-64.
Sigal, L. L.; Nash, T. H., III. (1983) Lichen communities on conifers in southern California mountains:
an ecological survey relative to oxidant air pollution. Ecology 64: 1343-1354.
Sigal, L. L.; Suter, G. W., II. (1987) Evaluation of methods for determining adverse impacts of air pollution on
terrestrial ecosystems. Environ. Manage. 11: 675-694.
Simini, M.; Skelly, J. M.; Davis, D. D.; Savage, J. E.; Comrie, A. C. (1992) Sensitivity of four hardwood species
to ambient ozone in north central Pennsylvania. Can. J. For. Res. 22: 1789-1799.
Simmons, G. L.; Kelly, J. M. (1989) Influence of O3, rainfall acidity, and soil Mg status on growth and
ectomycorrhizal colonization of loblolly pine roots. Water Air Soil Pollut. 44: 159-171.
Skarby, L.; Troeng, E.; Bostrom, C.-A. (1987) Ozone uptake and effects on transpiration, net photosynthesis, and
dark respiration in Scots pine. For. Sci. 33: 801-808.
5-338
-------
Skelly, J. M. (1980) Photochemical oxidant impact on Mediterranean and temperate forest ecosystems: real and
potential effects. In: Miller, P. R., ed. Proceedings of symposium on effects of air pollutants on
Mediterranean and temperate forest ecosystems; June; Riverside, CA. Berkeley, CA:
U.S. Department of Agriculture, Forest Service; pp. 38-50; report no. PSW-43. Available from:
NTIS, Springfield, VA; PB81-133720.
Skelly, J. M. (1989) Forest decline versus tree decline - the pathological considerations. Environ. Monit. Assess.
12: 23-27.
Skelly, J. M.; Croghan, C. F.; Hayes, E. M. (1977) Oxidant levels in remote mountainous areas of southwestern
Virginia and their effects on native white pine (Pinus strobus L.). In: Dimitriades, B., ed.
International conference on photochemical oxidant pollution and its control - proceedings: v. II;
September 1976; Raleigh, NC. Research Triangle Park, NC: U.S. Environmental Protection Agency,
Environmental Sciences Research Laboratory; pp. 611-620; EPA report no. EPA-600/3-77-001b.
Available from: NTIS, Springfield, VA; PB-264233.
Skelly, J. M.; Yang, Y.-S.; Chevone, B. L; Long, S. J.; Nellessen, J. E.; Winner, W. E. (1984) Ozone
concentrations and their influence on forest species in the Blue Ridge Mountains of Virginia.
In: Davis, D. D.; Millen, A. A.; Dochinger, L., eds. Air pollution and the productivity of the forest:
proceedings of the symposium; October 1983; Washington, DC. Arlington, VA: Izaak Walton
League of America Endowment; pp. 143-159.
Slaughter, L. H.; Mulchi, C. L.; Lee, E. H.; Tuthill, K. (1989) Chronic ozone stress effects on yield and grain
quality of soft red winter wheat. Crop Sci. 29: 1251-1255.
Smith, W. H. (1974) Air pollution - effects on the structure and function of the temperate forest ecosystem.
Environ. Pollut. 6: 111-129.
Smith, V. K. (1989) Taking stock in progress with travel cost recreation demand methods: theory and
implementation. Mar. Resour. Econ. 6: 279-310.
Smith, W. H. (1990) Air pollution and forests: interactions between air contaminants and forest ecosystems.
2nd ed. New York, NY: Springer-Verlag; pp. 1-7.
Smith, W. H. (1992) Air pollution effects on ecosystem processes. In: Barker, J. R.; Tingey, D. T., eds.
Air pollution effects on biodiversity. New York, NY: Van Nostrand Reinhold; pp. 234-260.
Smith, V. K. (1993) Nonmarket valuation of environmental resources: an interpretive appraisal. Land Econ.
69: 1-26.
Smith, G.; Greenhalgh, B.; Brennan, E.; Justin, J. (1987) Soybean yield in New Jersey relative to ozone pollution
and antioxidant application. Plant Dis. 71: 121-125.
Smith, G.; Neyra, C.; Brennan, E. (1990) The relationship between foliar injury, nitrogen metabolism, and
growth parameters in ozonated soybeans. Environ. Pollut. 63: 79-93.
Snyder, R. G.; Simon, J. E.; Reinert, R. A.; Simini, M.; Wilcox, G. E. (1991) Effects of air quality on growth,
yield, and quality of watermelon. HortScience 26: 1045-1047.
Solomon, P. A.; Salmon, L. G.; Fall, T.; Cass, G. R. (1992) Spatial and temporal distribution of atmospheric
nitric acid and paniculate nitrate concentrations in the Los Angeles area. Environ. Sci. Technol. 26:
1596-1601.
5-339
-------
Somerville, M. C.; Shadwick, D. S.; Meldahl, R. S.; Chappelka, A. H.; Lockaby, B. G. (1992) Use of a
non-linear model in examining growth responses of loblolly pine to ozone and acid precipitation.
Atmos. Environ. Part A 26: 279-286.
Spence, J. W.; Haynie, F. H. (1972) Paint technology and air pollution: a survey and economic assessment.
Research Triangle Park, NC: U.S. Environmental Protection Agency, Office of Air Programs;
publication no. AP-103. Available from: NTIS, Springfield, VA; PB-210736.
Spence, R. D.; Rykiel, E. J., Jr.; Sharpe, P. J. H. (1990) Ozone alters carbon allocation in loblolly pine:
assessment with carbon-11 labeling. Environ. Pollut. 64: 93-106.
Stan, H.-J.; Schicker, S. (1982) Effect of repetitive ozone treatment on bean plants - stress ethylene production
and leaf necrosis. Atmos. Environ. 16: 2267-2270.
Stark, R. W.; Cobb, F. W., Jr. (1969) Smog injury, root diseases and bark beetle damage in ponderosa pine.
Calif. Agric. 23(9): 13-15.
Steiner, K. C.; Davis, D. D. (1979) Variation among Fraxinus families in foliar response to ozone. Can. J. For.
Res. 9: 106-109.
Stolte, K. W.; Duriscoe, D. M.; Cook, E. R.; Cline, S. P. (1992) Methods of assessing responses of trees, stands
and ecosystems to air pollution. In: Olson, R. K.; Binkley, D.; Bohm, M., eds. The response of
western forests to air pollution. New York, NY: Springer-Verlag; pp. 259-330. (Billings, W. D.;
Golley, F.; Lange, O. L.; Olson, J. S.; Remmert, H., eds. Ecological studies: analysis and synthesis:
v. 97).
Stow, T. K.; Allen, H. L.; Kress, L. W. (1992) Ozone impacts on seasonal foliage dynamics of young loblolly
pine. For. Sci. 38: 102-119.
Stroo, H. F.; Reich, P. B.; Schoettle, A. W.; Amundson, R. G. (1988) Effects of ozone and acid rain on white
pine (Pinus strobus) seedlings grown in five soils. II. Mycorrhizal infection. Can. J. Bot.
66: 1510-1516.
Sumizono, T.; Inoue, T. (1986) Responses of foliar gas exchanges of poplar clones in relation to resistance to
ozone. Bull. For. For. Prod. Res. Inst. (Jpn) 33: 35-44.
Sutton, R.; Ting, I. P. (1977) Evidence for the repair of ozone-induced membrane injury. Am. J. Bot.
64: 404-411.
Takemoto, B. K.; Shriner, D. S.; Johnston, J. W., Jr. (1987) Physiological responses of soybean (Glycine max L.
Merr) to simulated acid rain and ambient ozone in the field. Water Air Soil Pollut. 33: 373-384.
Takemoto, B. K.; Bytnerowicz, A.; Olszyk, D. M. (1988a) Depression of photosynthesis, growth, and yield in
field-grown green pepper (Capsicum annuum L.) exposed to acidic fog and ambient ozone.
Plant Physiol. 88: 477-482.
Takemoto, B. K.; Hutton, W. J.; Olszyk, D. M. (1988b) Responses of field-grown Medicago sativa L. to acidic
fog and ambient ozone. Environ. Pollut. 54: 97-107.
Takemoto, B. K.; Olszyk, D. M.; Johnson, A. G.; Parada, C. R. (1988c) Yield responses of field-gown crops to
acidic fog and ambient ozone. J. Environ. Qual. 17: 192-197.
5-340
-------
Takemoto, B. K.; Bytnerowicz, A.; Olszyk, D. M. (1989) Physiological responses of field-grown strawberry
(Fragaria x ananassa Duch.) exposed to acidic fog and ambient ozone. Environ. Exp. Bot.
29: 379-386.
Taylor, G. E., Jr. (1994) Role of genotype in the response of loblolly pine to tropospheric ozone: effects at the
whole-tree, stand, and regional level. J. Environ. Qual. 23: 63-82.
Taylor, G.; Davies, W. J. (1990) Root growth of Fagus sylvatica: impact of air quality and drought at a site in
southern Britain. New Phytol. 116: 457-464.
Taylor, G. E., Jr.; Hanson, P. J. (1992) Forest trees and tropospheric ozone: role of canopy deposition and leaf
uptake in developing exposure-response relationships. Agric. Ecosyst. Environ. 42: 255-273.
Taylor, O. C.; MacLean, D. C. (1970) Nitrogen oxides and the peroxyacyl nitrates. In: Jacobson, J. S.; Hill, A.
C., eds. Recognition of air pollution injury to vegetation: a pictorial atlas. Pittsburgh, PA: Air
Pollution Control Association; pp. E1-E14.
Taylor, G. E., Jr.; Norby, R. J. (1985) The significance of elevated levels of ozone on natural ecosystems of
North America. In: Lee, S. D., ed. Evaluation of the scientific basis for ozone/oxidants standards:
proceedings of an APCA international specialty conference; November 1984; Houston, TX.
Pittsburgh, PA: Air Pollution Control Association; pp. 152-175. (APCA transactions: TR-4).
Taylor, G. E., Jr.; Pitelka, L. F. (1992) Genetic diversity of plant populations and the role of air pollution.
In: Barker, J. R.; Tingey, D. T., eds. Air pollution effects on biodiversity. New York, NY: Van
Nostrand Reinhold; pp. 111-130.
Taylor, O. C.; Stephens, E. R.; Darley, E. F.; Cardiff, E. A. (1960) Effect of air-borne oxidants on leaves of
pinto bean and petunia. J. Am. Soc. Hortic. Sci. 75: 435-444.
Taylor, G. E., Jr.; McLaughlin, S. B.; Shriner, D. S. (1982) Effective pollutant dose. In: Unsworth, M. H.;
Ormrod, D. P., eds. Effects of gaseous air pollution in agriculture and horticulture. London, United
Kingdom: Butterworth Scientific; pp. 458-460.
Taylor, G. E., Jr.; Norby, R. J.; McLauglin, S. B.; Johnson, A. H.; Turner, R. S. (1986) Carbon dioxide
assimilation and growth of red spruce (Picea rubens Sarg.) seedlings in response to ozone,
precipitation chemistry, and soil type. Oecologia 70: 163-171.
Taylor, G. E., Jr.; Hanson, P. J.; Baldocchi, D. D. (1988a) Pollutant deposition to individual leaves and plant
canopies: sites of regulation and relationship to injury. In: Heck, W. W.; Taylor, O. C.; Tingey, D.
T., eds. Assessment of crop loss from air pollutants. New York, NY: Elsevier Applied Science; pp.
227-257.
Taylor, G. E., Jr.; Ross-Todd, B. M.; Gunderson, C. A. (1988b) Action of ozone on foliar gas exchange in
Glycine max L. Merr: a potential role for endogenous stress ethylene. New Phytol. 110: 301-307.
Telewski, F. W. (1992) Ethylene production by different age class ponderosa and Jeffery pine needles as related
to ozone exposure and visible injury. Trees 6: 195-198.
Temple, P. J. (1988) Injury and growth of Jeffrey pine and giant sequoia in response to ozone and acidic mist.
Environ. Exp. Bot. 28: 323-333.
Temple, P. J. (1989) Oxidant air pollution effects on plants of Joshua Tree National Monument. Environ. Pollut.
57: 35-47.
5-341
-------
Temple, P. J. (1990a) Growth and yield responses of processing tomato (Lycopersicon esculentum Mill.) cultivars
to ozone. Environ. Exp. Bot. 30: 283-291.
Temple, P. J. (1990b) Growth form and yield responses of four cotton cultivars to ozone. Agron. J.
82: 1045-1050.
Temple, P. J. (1991) Variations in responses of dry bean (Phaseolus vulgaris) cultivars to ozone. Agric. Ecosyst.
Environ. 36: 1-11.
Temple, P. J.; Benoit, L. F. (1988) Effects of ozone and water stress on canopy temperature, water use, and
water use efficiency of alfalfa. Agron. J. 80: 439-447.
Temple, P. J.; Bisessar, S. (1979) Response of white bean to bacterial blight, ozone, and antioxidant protection in
the field. Phytopathology 69: 101-103.
Temple, P. J.; Taylor, O. C.; Benoit, L. F. (1985) Cotton yield responses to ozone as mediated by soil moisture
and evapotranspiration. J. Environ. Qual. 14: 55-60.
Temple, P. J.; Taylor, O. C.; Benoit, L. F. (1986) Yield response of head lettuce (Lactuca sativa L.) to ozone.
Environ. Exp. Bot. 26: 53-58.
Temple, P. J.; Lennox, R. W.; Bytnerowicz, A.; Taylor, O. C. (1987) Interactive effects of simulated acidic fog
and ozone on field-grown alfalfa. Environ. Exp. Bot. 27: 409-417.
Temple, P. J.; Benoit, L. F.; Lennox, R. W.; Reagan, C. A.; Taylor, O. C. (1988a) Combined effects of ozone
and water stress on alfalfa growth and yield. J. Environ. Qual. 17: 108-113.
Temple, P. J.; Kupper, R. S.; Lennox, R. W.; Rohr, K. (1988b) Injury and yield responses of differentially
irrigated cotton to ozone. Agron. J. 80: 751-755.
Temple, P. J.; Kupper, R. S.; Lennox, R. L.; Rohr, K. (1988c) Physiological and growth responses of
differentially irrigated cotton to ozone. Environ. Pollut. 53: 255-263.
Temple, P. J.; Riechers, G. H.; Miller, P. R. (1992) Foliar injury responses of ponderosa pine seedlings to ozone,
wet and dry acidic deposition, and drought. Environ. Exp. Bot. 32: 101-113.
Temple, P. J.; Riechers, G. H.; Miller, P. R.; Lennox, R. W. (1993) Growth responses of ponderosa pine to
long-term exposure to ozone, wet and dry acidic deposition, and drought. Can. J. For. Res.
23: 59-66.
Tenhunen, J. D.; Meyer, A.; Lange, O. L.; Gates, D. M. (1980) Development of a photosynthesis model with an
emphasis on ecological applications. V. Test of the applicability of a steady-state model to
description of net photosynthesis of Primus armeniaca under field conditions. Oecologia
45: 147-155.
Tepperman, J. M.; Dunsmuir, P. (1990) Transformed plants with elevated levels of chloroplastic SOD are not
more resistant to superoxide toxicity. Plant Mol. Biol. 14: 501-511.
Teskey, R. O.; Dougherty, P. M.; Wiselogel, A. E. (1991) Design and performance of branch chambers suitable
for long-term ozone fumigation of foliage in large trees. J. Environ. Qual. 20: 591-595.
Teso, R. R.; Oshima, R. J.; Carmean, M. I. (1979) Ozone-pesticide interactions. Calif. Agric. 33: 13-15.
Tevini, M.; Teramura, A. H. (1989) UV-B effects on terrestrial plants. Photochem. Photobiol. 50: 479-487.
5-342
-------
Thorne, L.; Hanson, G. P. (1976) Relationship between genetically controlled ozone sensitivity and gas exchange
rate in Petunia hybrida Vilm. J. Am. Soc. Hortic. Sci. 101: 60-63.
Thornton, F. C.; Pier, P. A.; McDuffie, C., Jr. (1992) Plant and environment interactions: red spruce response to
ozone and cloudwater after three years exposure. J. Environ. Qual. 21: 196-202.
Tiedemann, A. V.; Ostlander, P.; Firsching, K. H.; Fehrmann, H. (1990) Ozone episodes in southern Lower
Saxony (FRG) and their impact on the susceptibility of cereals to fungal pathogens. Environ. Pollut.
67: 43-59.
Tiedemann, A. V.; Weigel, H.-J.; Jager, H.-J. (1991) Effects of open-top chamber fumigations with ozone on
three fungal leaf diseases of wheat and the mycoflora of the phyllosphere. Environ. Pollut.
72: 205-224.
Tingey, D. T. (1977) Ozone induced alterations in plant growth and metabolism. In: Dimitriades, B., ed.
International conference on photochemical oxidant pollution and its control - proceedings: v. II;
September 1976; Raleigh, NC. Research Triangle Park, NC: U.S. Environmental Protection Agency,
Environmental Sciences Research Laboratory; pp. 601-609; EPA report no. EPA-600/3-77-001b.
Available from: NTIS, Springfield, VA; PB-264233.
Tingey, D. T. (1984) The effects of ozone on plants in the United States. In: Grennfelt, P., ed. Proceedings of
the international workshop on the evaluation of the effects of photochemical oxidants on human
health, agricultural crops, forestry, materials and visibility; February-March; Goteborg, Sweden.
Goteborg, Sweden: Swedish Environmental Research Institute; pp. 60-75; report no. IVL-EM 1570.
Tingey, D. T.; Blum, U. (1973) Effects of ozone on soybean nodules. J. Environ. Qual. 2: 341-342.
Tingey, D. T.; Hogsett, W. E. (1985) Water stress reduces ozone injury via a stomatal mechanism. Plant Physiol.
77: 944-947.
Tingey, D. T.; Taylor, G. E., Jr. (1982) Variation in plant response to ozone: a conceptual model of
physiological events. In: Unsworth, M. H.; Ormrod, D. P., eds. Effects of gaseous air pollution in
agriculture and horticulture. London, United Kingdom: Butterworth Scientific; pp. 113-138.
Tingey, D. T.; Fites, R. C.; Wickliff, C. (1976a) Differential foliar sensitivity of soybean cultivars to ozone
associated with differential enzyme activities. Physiol. Plant. 37: 69-72.
Tingey, D. T.; Wilhour, R. G.; Standley, C. (1976b) The effect of chronic ozone exposures on the metabolite
content of ponderosa pine seedlings. For. Sci. 22: 234-241.
Tingey, D. T.; Hogsett, W. E.; Lee, E. H. (1989) Analysis of crop loss for alternative ozone exposure indices. In:
Schneider, T.; Lee, S. D.; Wolters, G. J. R.; Grant, L. D., eds. Atmospheric ozone research and its
policy implications: proceedings of the 3rd US-Dutch international symposium; May 1988;
Nijmegen, The Netherlands. Amsterdam, The Netherlands: Elsevier Science Publishers; pp. 219-227.
(Studies in environmental science 35).
Tingey, D. T.; Hodsett, W. E.; Henderson, S. (1990) Definition of adverse effects for the purpose of establishing
secondary national ambient air quality standards. J. Environ. Qual. 19: 635-639.
5-343
-------
Tingey, D. T.; Hogsett, W. E.; Lee, E. H.; Herstrom, A. A.; Azevedo, S. H. (1991) An evaluation of various
alternative ambient ozone standards based on crop yield loss data. In: Berglund, R. L.; Lawson, D.
R.; McKee, D. J., eds. Tropospheric ozone and the environment: papers from an international
conference; March 1990; Los Angeles, CA. Pittsburgh, PA: Air & Waste Management Association;
pp. 272-288. (A&WMA transactions series no. TR-19).
Tjoelker, M. G.; Luxmoore, R. J. (1991) Soil nitrogen and chronic ozone stress influence physiology, growth and
nutrient status of Pinus taeda L. and Liriodendron tulipifera L. seedlings. New Phytol. 119: 69-81.
Todd, A. G.; Ormrod, D. P.; Hale, B. A.; Goodyear, S. N. (1991) Temperature effects on tomato response to
ozone at constant vapor pressure deficit. Biotronics 20: 43-52.
Toivonen, P. M. A.; Hofstra, G.; Wukasch, R. T. (1982) Assessment of yield losses in white bean due to ozone
using the antioxidant EDU. Can. J. Plant Pathol. 4: 381-386.
Tonneijck, A. E. G. (1984) Effects of peroxyacetyl nitrate (PAN) and ozone on some plant species. In: Grennfelt,
P., ed. Proceedings of the international workshop on the evaluation of the effects of photochemical
oxidants on human health, agricultural crops, forestry, materials and visibility; February-March;
Goteborg, Sweden. Goteborg, Sweden: Swedish Environmnetal Research Institute; pp. 118-127;
report no. IVL-EM 1570.
Tonneijck, A. E. G. (1994) Use of several plant species as indicators of ambient ozone: exposure-response
relationships. In: Fuhrer, J.; Achermann, B., eds. Critical levels for ozone: a UN-ECE workshop
report; November 1993; Bern, Switzerland. Liebefeld-Bern, Switzerland: Swiss Federal Research
Station for Agricultural Chemistry and Environmental Hygiene; pp. 288-292. (Schriftenreihe der
FAC Liebefeld no. 16).
Tonneijck, A. E. G.; Bugter, R. J. F. (1991) Biological monitoring of ozone effects on indicator plants in the
Netherlands: initial research on exposure-response functions. VDI Ber. (901): 613-624.
Tonneijck, A. E. G.; van Dijk, C. J. (1994) Combined effects of ozone and ammonia on growth and yield of
bean (Phaseolus vulgaris L. cv. Pros). In: Fuhrer, J.; Achermann, B., eds. Critical levels for ozone:
a UN-ECE workshop report; November 1993; Bern, Switzerland. Liebefeld-Bern, Switzerland:
Swiss Federal Research Station for Agricultural Chemistry and Environmental Hygiene; pp.
282-286. (Schriftenreihe der FAC Liebefeld no. 16).
Torn, M. S.; Degrange, J. E.; Shinn, J. H. (1987) The effects of acidic deposition on Alberta agriculture:
a review (v. 8). Calgary, AB, Canada: Acid Deposition Research Program; report no.
ADRP-B-08/87.
Townsend, A. M.; Dochinger, L. S. (1974) Relationship of seed source and developmental stage to the ozone
tolerance of Acer rubrum seedlings. Atmos. Environ. 8: 957-964.
Treshow, M. (1980) Pollution effects on plant distribution. Environ. Conserv. 7: 279-286.
Troiano, J.; Colavito, L.; Heller, L.; McCune, D. C.; Jacobson, J. S. (1983) Effects of acidity of simulated rain
and its joint action with ambient ozone on measures of biomass and yield in soybean. Environ. Exp.
Bot. 23: 113-119.
Trumble, J. T.; Hare, J. D.; Musselman, R. C.; McCool, P. M. (1987) Ozone-induced changes in host-plant
suitability: interactions of Keiferia lycopersicella and Lycopersicon esculentum. J. Chem. Ecol.
13: 203-218.
5-344
-------
Tseng, E. C.; Seller, J. R.; Chevone, B. I. (1988) Effects of ozone and water stress on greenhouse-grown Fraser
fir seedling growth and physiology. Environ. Exp. Bot. 28: 37-41.
Turner, N. C.; Rich, S.; Tomlinson, H. (1972) Stomatal conductance, fleck injury, and growth of tobacco
cultivars varying in ozone tolerance. Phytopathology 62: 63-67.
Twardus, D.; Miller-Weeks, M; Gillespie, A. (1993) Forest health assessment for the northeastern area 1993.
Washington, DC: U.S. Department of Agriculture, Forest Service, Northeastern Area and
Northeastern Forest Experiment Station; report no. NA-TP-01-95.
U.S. Code. (1991) Clean Air Act as amended by the Air Quality Act of 1967, PL 90-148; Clean Air Act
Amendments of 1970, PL 91-604; Technical Amendments to the Clean Air Act, PL 92-157;
PL 93-15, April 9, 1973; PL 93-319, June 22, 1974; Clean Air Act Amendments of 1977,
PL 95-95, August 7, 1977; Health Services Research, Health Statistics, and Health Care Technology
Act of 1978, PL 95-623, November 9, 1978; PL 96-209, March 14, 1980; PL 96-300, July 2, 1980;
PL 97-23, July 17, 1981; PL 97-375, December 21, 1982; PL 98-45, U. S. C. 42: §7401-7626.
U.S. Environmental Protection Agency. (1978) Air quality criteria for ozone and other photochemical oxidants.
Research Triangle Park, NC: Office of Health and Environmental Assessment, Environmental
Criteria and Assessment Office; report no. EPA-600/8-78-004. Available from: NTIS,
Springfield, VA; PB80-124753.
U.S. Environmental Protection Agency. (1986) Air quality criteria for ozone and other photochemical oxidants.
Research Triangle Park, NC: Office of Health and Environmental Assessment, Environmental
Criteria and Assessment Office; report nos. EPA-600/8-84-020aF-eF. 5v. Available from: NTIS,
Springfield, VA; PB87-142949.
U.S. Environmental Protection Agency. (1992) Summary of selected new information on effects of ozone on
health and vegetation: supplement to 1986 air quality criteria for ozone and other photochemical
oxidants. Research Triangle Park, NC: Office of Health and Environmental Assessment,
Environmental Criteria and Assessment Office; report no. EPA/600/8-88/105F. Available from:
NTIS, Springfield, VA; PB92-235670.
U.S. Environmental Protection Agency. (1993) Air quality criteria for oxides of nitrogen. Research Triangle Park,
NC: Office of Health and Environmental Assessment, Environmental Criteria and Assessment
Office; report nos. EPA/600/8-9 !/049aF-cF. 3v. Available from: NTIS, Springfield, VA;
PB95-124533, PB95-124525, and PB95-124517.
Umbach, D. M.; Davis, D. D. (1984) Severity and frequency of SO2-induced leaf necrosis on seedlings of
57 tree species. For. Sci. 30: 587-596.
Unsworth, M. H.; Heagle, A. S.; Heck, W. W. (1984a) Gas exchange in open-top field chambers -
I. measurement and analysis of atmospheric resistances to gas exchange. Atmos. Environ.
18: 373-380.
Unsworth, M. H.; Heagle, A. S.; Heck, W. W. (1984b) Gas exchange in open-top field chambers - II. resistances
to ozone uptake by soybeans. Atmos. Environ. 18: 381-385.
Upham, J. B.; Haynie, F. H.; Spence, J. W. (1976) Fading of selected drapery fabrics by air pollutants. J. Air
Pollut. Control Assoc. 26: 790-792.
Velissariou, D.; Barnes, J. D.; Davison, A. W. (1992) Has inadvertent selection by plant breeders affected the O3
sensitivity of modern Greek cultivars of spring wheat? Agric. Ecosyst. Environ. 38: 79-89.
5-345
-------
Venne, H.; Scholz, F.; Vornweg (1989) Effects of air pollutants on reproductive processes of poplar (Populus
spp.) and Scots pine (Pinus sylvestris L.). In: Scholz, F.; Gregorius, H.-R.; Rudin, D., eds. Genetic
effects of air pollutants in forest tree populations: proceedings of the joint meeting of the IUFRO
working parties; August 1987; Grosshansdorf, Federal Republic of Germany. Berlin, Federal
Republic of Germany: Springer-Verlag; pp. 89-103.
Waddell, T. E. (1974) The economic damages of air pollution. Washington, DC: U.S. Environmental Protection
Agency, Washington Environmental Research Center; EPA report no. EPA-600/5-74-012. Available
from: NTIS, Springfield, VA; PB-235 701.
Wallin, G.; Skarby, L.; Sellden, G. (1990) Long-term exposure of Norway spruce, Picea abies (L.) Karst, to
ozone in open-top chambers: I. effects on the capacity of net photosynthesis, dark respiration and
leaf conductance of shoots of different ages. New Phytol. 115: 335-344.
Walmsley, L.; Ashmore, M. R.; Bell, J. N. B. (1980) Adaptation of radish Raphanus sativus L. in response to
continuous exposure to ozone. Environ. Pollut. Ser. A 23: 165-177.
Walsh, N. E.; Charlesworth, D. (1992) Evolutionary interpretations of differences in pollen tube growth rates. Q.
Rev. Biol. 67: 19-37.
Wang, D.; Bormann, F. H.; Karnosky, D. F. (1986a) Regional tree growth reductions due to ambient ozone:
evidence from field experiments. Environ. Sci. Technol. 20: 1122-1125.
Wang, D.; Karnosky, D. F.; Bormann, F. H. (1986b) Effects of ambient ozone on the productivity of Populus
tremuloides Michx. grown under field conditions. Can. J. For. Res. 16: 47-55.
Waring, R. H.; Schlesinger, W. H. (1985) Forest ecosystems: concepts and management. Orlando, FL: Academic
Press, Inc.; pp. 1-37, 211-238.
Weber, J. A.; Gates, D. M. (1990) Gas exchange in Quercus rubra (northern red oak) during a drought: analysis
of relations among photosynthesis, transpiration, and leaf conductance. Tree Physiol. 7: 215-225.
Weber, D. E.; Reinert, R. A.; Barker, K. R. (1979) Ozone and sulfur dioxide effects on reproduction and
host-parasite relationships of selected plant-parasitic nematodes. Phytopathology 69: 624-628.
Weber, J. A.; Clark, C. S.; Hogsett, W. E. (1993) Analysis of the relationships among O3 uptake, conductance,
and photosynthesis in needles of Pinus ponderosa. Tree Physiol. 13: 157-172.
Weidmann, P.; Einig, W.; Egger, B.; Hampp, R. (1990) Contents of ATP and ADP in needles of Norway spruce
in relation to their development, age, and to symptoms of forest decline. Trees 4: 68-74.
Weigel, H. J.; Adaros, G.; Jaeger, H.-J. (1987) An open-top chamber study with filtered and non-filtered air to
evaluate the effects of air pollutants on crops. Environ. Pollut. 47: 231-244.
Weinstein, D. A.; Beloin, R. M.; Yanai, R. D. (1991) Modeling changes in red spruce carbon balance and
allocation in response to interacting ozone and nutrient stresses. Tree Physiol. 9: 127-146.
Weinstock, L.; Kender, W. J.; Musselman, R. C. (1982) Microclimate within open-top air pollution chambers and
its relation to grapevine physiology. J. Am. Soc. Hortic. Sci. 107: 923-926.
Weir, R. J. (1977) Genetic variation in loblolly pine (Pinus taeda L.) tolerance to ozone [Ph.D. thesis]. Raleigh,
NC: North Carolina State University.
Wenghoefer, H. M. (1974) Environmental effects on RFL adhesion. Rubber Chem. Technol. 47: 1066-1073.
5-346
-------
Wesely, M. L.; Eastman, J. A.; Cook, D. R.; Hicks, B. B. (1978) Daytime variations of ozone eddy fluxes to
maize. Boundary Layer Meteorol. 15: 361-373.
Westman, W. E. (1977) How much are nature's services worth? Measuring the social benefits of ecosystem
functioning is both controversial and illuminating. Science (Washington, DC) 197: 960-964.
Whitmore, P. M.; Cass, G. R. (1988) The ozone fading of traditional Japanese colorants. Stud. Conserv.
33: 29-40.
Whitmore, P. M.; Cass, G. R.; Druzik, J. R. (1987) The ozone fading of traditional natural organic colorants on
paper. J. Am. Inst. Conserv. 26: 45-58.
Whittaker, J. B.; Kristiansen, L. W.; Mikkelsen, T. N.; Moore, R. (1989) Responses to ozone of insects feeding
on a crop and a weed species. Environ. Pollut. 62: 89-101.
Wieser, G.; Havranek, W. M. (1993) Ozone uptake in the sun and shade crown of spruce: quantifying the
physiological effects of ozone exposure. Trees 7: 227-232.
Wilton, A. C.; Murray, J. J.; Heggestad, H. E.; Juska, F. V. (1972) Tolerance and susceptibility of Kentucky
bluegrass (Poa pratensis L.) cultivars to air pollution: in the field and in an ozone chamber.
J. Environ. Qual. 1: 112-114.
Wiltshire, J. J. J.; Wright, C. J.; Unsworth, M. H. (1992) A new method for exposing mature trees to ozone
episodes. For. Ecol. Manage. 51: 115-120.
Wiltshire, J. J. J.; Wright, C. J.; Unsworth, M. H.; Craigon, J. (1993) The effects of ozone episodes on autumn
leaf fall in apple. New Phytol. 124: 433-437.
Winner, W. E.; Atkinson, C. J. (1986) Absorption of air pollution by plants, and consequences for growth.
Trends Ecol. Evol. 1: 15-18.
Winner, W. E.; Cotter, I. S.; Powers, H. R., Jr.; Skelly, J. M. (1987) Screening loblolly pine seedling responses
to SO2 and O3: analysis of families differing in resistance to fusiform rust disease. Environ. Pollut.
47: 205-220.
Winner, W. E.; Lefohn, A. S.; Cotter, I. S.; Greitner, C. S.; Nellessen, J.; McEvoy, L. R., Jr.; Olson, R. L.;
Atkinson, C. J.; Moore, L. D. (1989) Plant responses to elevational gradients of O3 exposures in
Virginia. Proc. Natl. Acad. Sci. U. S. A. 86: 8828-8832.
Wiselogel, A. E.; Bailey, J. K.; Newton, R. J.; Fong, F. (1991) Growth response of loblolly pine (Pinus taeda L.)
seedlings to ozone fumigation. Environ. Pollut. 71: 43-56.
Wolfenden, J.; Wellburn, A. R. (1991) Effects of summer ozone on membrane lipid composition during
subsequent frost hardening in Norway spruce [Picea abies (L.) Karst]. New Phytol. 118: 323-329.
Wolfenden, J.; Wookey, P. A.; Lucas, P. W.; Mansfield, T. A. (1992) Action of pollutants individually and in
combination. In: Barker, J. R.; Tingey, D. T., eds. Air pollution effects on biodiversity. New York,
NY: Van Nostrand Reinhold; pp. 72-92.
Wolff, G. T.; Lioy, P. J. (1980) Development of an ozone river associated with synoptic scale episodes in the
eastern United States. Environ. Sci. Technol. 14: 1257-1260.
Wolff, G. T.; Lioy, P. J.; Wight, G. D. (1980) Transport of ozone associated with an air mass. J. Environ. Sci.
Health Part A 15: 183-199.
5-347
-------
Wolff, G. T.; Lioy, P. I; Taylor, R. S. (1987) The diurnal variations of ozone at different altitudes on a rural
mountain in the eastern United States. JAPCA 37: 45-48.
Wolff, G. T.; Lioy, P. I; Wight, G. D.; Pasceri, R. E. (1977a) Aerial investigation of the ozone plume
phenomenon. J. Air Pollut. Control Assoc. 27: 460-463.
Wolff, G. T.; Lioy, P. J.; Wight, G. D.; Meyers, R. E.; Cederwall, R. T. (1977b) An investigation of long-range
transport of ozone across the midwestern and eastern United States. In: Dimitriades, B., ed.
International conference on photochemical oxidant pollution and its control - proceedings: volume I;
September 1976; Raleigh, NC. Research Triangle Park, NC: U.S. Environmental Protection Agency,
Environmental Sciences Research Laboratory; pp. 307-317; report no. EPA-600/3-77-001a.
Available from: NTIS, Springfield, VA; PB-264232.
Wolff, G. T.; Lioy, P. J.; Wight, G. D.; Meyers, R. E.; Cederwall, R. T. (1977c) An investigation of long-range
transport of ozone across the midwestern and eastern United States. Atmos. Environ. 11: 797-802.
Wolters, J. H. B.; Martens, M. J. M. (1987) Effects of air pollutants on pollen. Bot. Rev. 53: 372-414.
Woodbury, P. B.; Amundson, R. G.; Kohut, R. J.; Laurence, J. A. (1992) Stomatal conductance, whole-tree
water use, and foliar carbohydrate status of red spruce saplings exposed to ozone, acid precipitation,
and drought. In: Berglund, R. L., ed. Tropospheric ozone and the environment II: effects, modeling
and control [papers from an international specialty conference]; November; Atlanta, GA. Pittsburgh,
PA: Air & Waste Management Association; pp. 618-628. (A&WMA transactions series no. 20).
Woodman, J. N.; Cowling, E. B. (1987) Airborne chemicals and forest health. Environ. Sci. Technol.
21: 120-126.
Woodward, F. I. (1992) Tansley review no. 41: predicting plant responses to global environmental change. New
Phytol. 122: 239-251.
Woodwell, G. M. (1970) Effects of pollution on the structure and physiology of ecosystems: changes in natural
ecosystems caused by many different types of disturbances are similar and predictable.
Science (Washington, DC) 168: 429-433.
Wukasch, R. T.; Hofstra, G. (1977a) Ozone andBotrytis interactions in onion-leaf dieback: open-top chamber
studies. Phytopathology 67: 1080-1084.
Wukasch, R. T.; Hofstra, G. (1977b) Ozone and Botrytis spp. interaction in onion leaf dieback: field studies.
J. Am. Soc. Hortic. Sci. 102: 543-546.
Yang, Y.-S.; Skelly, J. M.; Chevone, B. I. (1982) Clonal response of eastern white pine to low doses of O3, SO2,
and NO2, singly and in combination. Can. J. For. Res. 12: 803-808.
Yarwood, C. E.; Middleton, J. T. (1954) Smog injury and rust infection. Plant Physiol. 29: 393-395.
Yocom, J. E.; Grappone, N. (1976) Effects of power plant emissions on materials. Palo Alto, CA: Electric Power
Research Institute; report no. EPRI/EC-139. Available from: NTIS, Springfield, VA; PB-257 539.
Yocom, J. E.; Kawecki, J. M.; Hoffnagle, G. F. (1985) Estimating materials damage from oxidant pollutants. In:
Proceedings of the APCA specialty conference: evaluation of the scientific basis for ozone/oxidants
standards; November 1984; Houston, TX. Pittsburgh, PA: Air Pollution Control Association.
Yocom, J. E.; Baer, N. S.; Robinson, E. (1986) Air pollution effects on physical and economic systems.
In: Stern, ed. Air pollution, v. VI. New York, NY: Academic Press; pp. 145-246.
5-348
-------
Yokouchi, Y.; Ambe, Y. (1985) Aerosols formed from the chemical reaction of monoterpenes and ozone. Atmos.
Environ. 19: 1271-1276.
Zeiger, E.; Farquhar, G. D.; Cowan, I. R. (1987) Stomatal physiology. Stanford, CA: Stanford University Press.
Zeronian, S. H.; Alger, K. W.; Omaye, S. T. (1971) Reaction of fabrics made from synthetic fibers to air
contaminated with nitrogen dioxide, ozone, or sulfur dioxide. In: Englund, H. M; Beery, W. T.,
eds. Proceedings of the second international clean air congress; December 1970; Washington, DC.
New York, NY: Academic Press; pp. 468-476.
5-349
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Appendix A
Abbreviations and Acronyms
ADOM
AGL
AIRS
AM
AQCD
AQCR
AUSPEX
C
C
CA
CAA
CAAA
CAL-RAMS
CAR
CASAC
CBM
CCM
CFC
CH3OH
CH4
CI
CIT
CL
CMB
CNG
CO
C02
CTWM
DIAL
Acid Deposition and Oxidant Model
Above ground level
Aerometric Information Retrieval System
Alveolar macrophage
Air Quality Criteria Document
Air Quality Control Region
Atmospheric Utility Signatures, Predictions, and Experiments
Carbon
Concentration
Chromotropic acid
Clean Air Act
Clean Air Act Amendments of 1990
Coast and Lake Regional Atmospheric Modeling System
Centriacinar region
Clean Air Scientific Advisory Committee
Carbon-bond mechanism
Community Climate Model
Chlorofluorocarbon
Methanol
Methane
Chemical ionization
California Institute of Technology
Chemiluminescence
Chemical mass balance
Compressed natural gas
Carbon monoxide
Carbon dioxide
Complex Terrain Wind Model
Differential absorption lidar
A-1
-------
DNPH
DOAS
DWM
BCD
EKMA
EMS
EPA
EPEM
EPRI
EPS
ERAQS
ETBE
EtOH
FDDA
FeSO4
FEV,
FVC
FID
FTIR
GC
GMEP
GPT
H+
HC
HCFC
HCHO
HNO2
HNO3
HO2
H202
HPLC
H2S04
1C
ID
I/O
2,4-Dinitrophenylhydrazine
Differential optical absorption spectrometry
Diagnostic Wind Model
Electron capture detection
Empirical Kinetic Modeling Approach
Emissions Modeling System
U.S. Environmental Protection Agency
Event Probability Exposure Model
Electric Power Research Institute
Emissions Preprocessor System
Eastern Regional Air Quality Study
Ethyl-tertiary-butyl ether
Ethanol
Four-dimensional data assimilation
Ferrous sulfate
Forced expiratory volume in 1 s
Forced vital capacity
Flame ionization detection
Fourier transform infrared absorption spectroscopy
Gas chromatography
Geocoded Model of Emissions and Projections
Gas-phase titration
Hydrogen ion
Hydrocarbon
Hydrochlorofluorocarbon
Formaldehyde
Nitrous acid
Nitric acid
Hydroperoxyl
Hydrogen peroxide
High-performance liquid chromatography
Sulfuric acid
Ion chromatography
Identification (number)
Indoor/outdoor
A-2
-------
IR
Infrared radiation
IR
LMOS
LPG
MBTH
MCCP
MM4/MM5
MOBILE
MODELS 3
MPAN
MSA
MSCET
MTBE
NA
NAAQS
NADP
NAMS
NAPAP
NAPBN
NAS
NBKI
NBS
NCAR
NCLAN
NDDN
NEM
NF
NH3
NH4HSO4
NH4OH
(NH4)2S04
Incremental reactivity
Lake Michigan Oxidant Study
Liquified petroleum gas
3 -Methyl-2-benzothiazolone hydr azone
Mountain Cloud Chemistry Program
Mesoscale Model, versions 4 and 5
U.S. Environmental Protection Agency emissions model for mobile
sources
Modeling framework that consolidates all of the U.S. Environmental
Protection Agency's three-dimensional photochemical air
quality models
Peroxymethacryloyl nitrate
Metropolitan Statistical Area
Month and state current emissions trends
Methyl-tertiary-butyl ether
Not available
National Ambient Air Quality Standards
National Atmospheric Deposition Program
National Air Monitoring Station
National Acid Precipitation Assessment Program
Western National Air Pollution Background Network
National Academy of Sciences
Neutral buffered potassium iodide
National Bureau of Standards; now National Institute of
Standards and Technology
National Center for Atmospheric Research
National Crop Loss Assessment Network
National Dry Deposition Network
National Air Quality Standards Exposure Model
National forest
Ammonia
Ammonium bisulfate
Ammonium hydroxide
Ammonium sulfate
A-3
-------
NIST
NM
NMHC
NMOC
NO
NO2
N2O
NO3
NOX
NP
NPN
NTP
03
OAQPS
Obs.
OH
OHBA
PAMS
PAN
PANs
PAR
PEL
PBzN
PDFID
PF/TPLIF
pH
PL
PLANR
PMN
ppmC
PPN
PSD
PVOC
QE
QH
r
National Institute of Standards and Technology
National monument
Nonmethane hydrocarbon
Nonmethane organic compound
Nitric oxide
Nitrogen dioxide
Nitrous oxide
Nitrate
Nitrogen oxides
National park
n-propyl nitrate
National Toxicology Program
Ozone
Office of Air Quality Planning and Standards
Observations
Hydroxyl
Hydroxybenzoic acid
Photochemical Aerometric Monitoring System
Peroxyacetyl nitrate
Peroxyacyl nitrates
Proximal alveolar region
Planetary boundary layer
Peroxybenzoyl nitrate
Cryogenic preconcentration-direct flame ionization detection
Photofragmentation two-photon laser-induced fluorescence
Hydrogen ion concentration
Liquid-phase vapor pressure
Practice for Low-cost Application in Nonattainment Regions
Polymorphonuclear leukocyte (also called neutrophil)
Parts per million carbon
Peroxypropionyl nitrate
Passive sampling device
Polar volatile organic compound
Latent heat flux
Heat flux
Linear regression correlation coefficient
A-4
-------
R2
RADM
RAPS
REHEX
RMSD
ROG
ROM
ROMNET
RT
SAB
SAI
SAPRC
SARMAP
SAROAD
SCAQS
SIP
SLAMS
SJVAQS
SO2
S042
SOS
SRM
SRP
STEM-II
SUM06
SUM07
SUM08
SURE
T
TAMS
TDLAS
Multiple correlation coefficient
Regional Acid Deposition Model
Regional Air Pollution Study
Regional Human Exposure Model
Root-mean-square difference
Reactive organic gas
Regional Oxidant Model
Regional Ozone Modeling for Northeast Transport program
Respiratory tract
Science Advisory Board
Systems Applications International
Statewide Air Pollution Research Center, University
of California, Riverside
San Joaquin Valley Air Quality Study (SJVAQS)/Atmospheric Utility
Signatures, Predictions, and Experiments (AUSPEX) Regional
Model Adaptation Project
Storage and Retrieval of Aerometric Data (U.S. Environmental
Protection Agency centralized database; superseded by
Aerometric Information Retrieval System [AIRS])
South Coast Air Quality Study (California)
State Implementation Plan
State and Local Air Monitoring Station
San Joaquin Valley Air Quality Study
Sulfur dioxide
Sulfate
Southern Oxidant Study
Standard reference material
Standard reference photometer
Sulfur Transport Eulerian Model (version II)
Seasonal sum of all hourly average concentrations DO.06 ppm
Seasonal sum of all hourly average concentrations DO.07 ppm
Seasonal sum of all hourly average concentrations DO.08 ppm
Sulfate Regional Experiment Program
Temperature
Toxic Air Monitoring Study (U.S. Environmental Protection Agency)
Tunable-diode laser absorption spectroscopy
A-5
-------
TEA
Tg
TGTP
TNMHC
TPLIF
TTFMS
UAM
UV
UV-B
VMT
VOC
VE
WFM
WMO/UNEP
W126
Triethanolamine
Teragram
The Global Thinking Project
Total nonmethane hydrocarbons
Two-photon laser-induced fluorescence
Two-tone frequency-modulated spectroscopy
Urban Airshed Model
Ultraviolet
Ultraviolet radiation of wavelengths 280 to 320 nm
Vehicle miles traveled
Volatile organic compound
Minute ventilation; expired volume per minute
White Face Mountain
World Meteorological Organization/United Nations Environment
Program
Cumulative integrated exposure index with a sigmoidal weighting
function
A-6
-------
Appendix B
Colloquial and Latin Names
Alder
Alder, red
Alder, speckled
Alfalfa
Almond
Apple
Apricot
Ash, green
Ash, white
Aspen, trembling
Avocado
Azalea
Barley, spring
Basswood (linden)
Bean, broad
Bean, bush
Bean, kidney, pinto, snap, white
Beech, European
Beet, sugar
Begonia
Begonia, bedding
Bentgrass
Birch, European white
Birch, downy
Birch, paper
Blackberry, common
Black-gram
Bluegrass, Kentucky
Alnus serrulata (Alton) Willdenow
Alnus rubra Bong.
Alnus incana (L.) Moench.
Medicago sativa L.
Prunus amygdalus Batsch cv. Nonpariel
Mains spp.
Prunus armeniaca L.
Fraxinus pennsylvanica Marsh.
Fraxinus americana L.
Populus tremuloides L.
Per sea americana Mill.
Rhododendron spp.
Hordeum vulgare L.
Tilia americana L.
Viciafaba L.
Phaseolus vulgaris L. var. humulis Alef.
Phaseolus vulgaris L.
Fagus sylvatica L.
Beta vulgaris L.
Begonia sp.
Begonia semperflorens Link & Otto
Agrostis capillaris L.
Betula pendula Roth.
Betula pubescens Ehrb.
Betula papyri/era Marsh.
Rubus allegheniensis Porter
Vigna mungo L.
B-l
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Buckhorn
Cabbage
Campion, bladder
Campion, moss
Carnation
Cedar, incense
Cedar, western red
Celery
Chestnut, American
Cherry, black
Chickpea
Clover, ladino, white
Clover, red
Corn
Cotton
Cottonwood (poplar)
Cress, garden
Cucumber
Dock
Fenugreek
Fescue, tall
Fir, balsam
Fir, Douglas
Fir, Douglas, big-cone
Fir, Fraser
Fir, silver
Fir, white
Geranium
Golden-rain
Poa praetensis L.
Plantago lanceolata L.
Brassica oleracea capitata L.
Silene cucabalus Wibel.
Silene acaulis L.
Dianthus caryophyllus L.
Libocedrus decurrens Torr. =
Calocedrus decurrens [Torr.] Florin.
Thuja plicata Donn ex D. Don
Apium graveolens L. var. dulce Pers.
Castenea dentata (Marsh.) Borkh.
Prunus serotina Ehrh.
Cicer arietinum L.
Trifolium rep ens L.
Trifolium pratense L.
Zea mays L.
Gossypium hirsutum L.
Populus deltoides Marsh
Lepidium sativum L.
Cucumis sativus L.
Rumex obtusifolius L.
Trigonella foenum-graecum L.
Festuca elatior L. = Festuca praetensis Huds.
Abies balsamea (L.) Mill.
Pseudotsuga menziesii (Mirb.) Franco.
Pseudotsuga macrocarpa (Vasey) Mayr
Abies balsamea (L.)fraseri (Pursh) Poir.
Abies alba Mill.
Abies concolor Lindl.
Pelargonium x hortorum Bailey
Koelreuteria paniculata Laxm.
Grape
Grape, wild
Vitis labruscana Bailey
Vitis spp.
B-2
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Grapefruit, Ruby Red
Grass, colonial bent
Grass, orchard
Grass, red
Grass, rye
Gum, sweet
Hemlock, eastern
Citrus parodist L.
Agrostis tennis Sibthorp.
Dactylis glomerata L.
Festuca rubra Gaud.
Lolium perenne L.
Liquidambar styraciflua L.
Hemlock, western
Ivy
Kenaf
Juniper, shore
Lemon, Volkamer
Lettuce
Lichen
Lichen, parmelia
Lichen, umbilical
Lilac
Locust, black
Locust, honey
Lupine
Mangel
Maple, red
Maple, sugar
Milkweed
Milkweed
Mint
Oak, California black
Oak, Canyon live
Oak, red
Oak, white
Oats
Tsuga canadensis (L.) Carr.
Tsuga heterophylla (Raf.) Sarg.
Hedera helix L.
Hibiscus cannabinus L.
Juniperus conferta Parl.
Citrus volkameriana Ten. & Pasq
Lactuca sativa L.
Lobaria spp.
Flavoparmelia caperata
Umbilicaria mammulata
Syringa vulgaris L.
Robinia pseudoacacia L.
Gleditsia triacanthos L.
Lupinus bicolor Lindl.
Beta vulgaris L.
Acer rubrum L.
Acer saccharum Marsh
Asclepias syriaca L.
Asclepias sp.
Mentha piperita L.
Quercus kelloggii Newb.
Quercus chrysolepis Liebm.
Quercus rubra L.
Quercus alba L.
Avena sativa L.
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Onion
Orange
Pea
Peach
Pepper
Pear
Petunia
Pine, eastern white
Pine, Coulter
Pine, Jeffrey
Pine, loblolly
Pine, pitch
Pine, ponderosa
Pine, Scots
Pine, shortleaf
Pine, Sierra lodgepole
Pine, slash
Pine, sugar
Pine, Table Mountain
Pine, Virginia
Plane, London
Plantain, (plantago) common
Plum
Poinsettia
Poplar, hybrid
Poplar, yellow or tulip
Potato
Radish
Radish
Rape, spring
Rhododendron, azalea
Rice, domestic
Sassafras
Sequoia, giant
Allium cepa L.
Citrus sinensis (L.) Osbeck
Pisum sativum L.
Prunus persica (L.) Batsch cv. Halford
Capsicum annuum L.
Pyrus pyrifolia Rhd. cv. 20th Century
Petunia hybrida Vilm.
Pinus strobus L.
Pinus coulteri D. Don
Pinus jeffreyi Grev. & Balf.
Pinus taeda L.
Pinus rigida Mill.
Pinus ponderosa Laws.
Pinus sylvestris L.
Pinus echinata Mill.
Pinus contorta var. murrayana (Grev. & Balf.)
Engelm.
Pinus elliotti Englem. ex Vasey
Pinus lambertiana Dougl.
Pinus pungens Lamb.
Pinus virginiana Mill.
Platanus x acerifolia (Ait.) Willd.
Plantago major L.
Prunus domestica L.
Euphorbia pulcherrima Willd.
Populus maximowiczii x P. trichocarpa
Liriodendron tulipifera L.
Solanum tuberosum L.
Raphanus sativus L.
Raphanus sativus L. cv. Cherry Bell
Brassica napus L. var. napus
Rhododendron obtusum (Lindl.) Planch.
Oryza sativa L.
Sassafras albidum [Nutt.] Nees
Sequoiadendron giganteum Buchholz
B-4
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Sorghum, hybrid
Sorghum bicolor (L.) Moench x Sorghum x
Soybean
Spinach
Spruce, Norway
Spruce, red
Spruce, sitka
Strawberry, cultivated
Strawberry, wild
Sunflower
Skunk bush
Sycamore
Timothy
Tobacco
Tomato
Virgin's Bower
Watermelon
Wheat
drummondii (Steudel) Millsp. & Chase
Glycine max (L.) Merr.
Spinacea oleracea L.
Picea abies (L.) Karst.
Picea rubens Sarg.
Picea sitchensis (Bong.) Carr.
Fragaria x ananassa Duch.
Fragaria virginiana Duch.
Helianthus annuus L.
Rhus trilobata Nutt.
Platanus occidentalis L.
Phleum prat ens e L.
Nicotiana tabacum L.
Lycopericon esculentum Mill.
Clematis virginiana L.
Citrullus lanatus (Thunb.) Mastsum & Nakai
Triticum aestivum L.
B-5
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