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.

II-ii
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.

II-iii

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-1

Volume II

5. Environmental Effects of Ozone and Related Photochemical

Oxidants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-1

Appendix A: Abbreviations and Acronyms . . . . . . . . . . . . . . . . . . . . . . . . A-1

Appendix B: Colloquial and Latin Names . . . . . . . . . . . . . . . . . . . . . . . . . B-1

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-1

II-v

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

II-vii
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

II-viii
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

II-ix
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

II-x
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-1

APPENDIX 5B: COLLOQUIAL AND LATIN NAMES . . . . . . . . . . . . . . . B-1

II-xi
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

II-xii
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

II-xiii
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

Since U.S. Environmental Protection Agency (1986) .......... 5-174

5-31 Effects of Ethylene Diurea on Ozone Responses ............. 5-181

5-32 San Bernardino Forest—Status 1972 ...................... 5-189

5-33 Ecosystem Response to Pollutant Stress ................... 5-192

5-34 Growing Season Summary Statistics for Ozone Monitoring Sites

in or Near Forests for the Period 1980 through 1988 .......... 5-197

5-35 Interactions of Ozone and Forest Tree Ectomycorrhizae ........ 5-213

5-36 Interaction of Air Pollution and Temperate Forest Ecosystems

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

II-xiv
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

II-xv
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 proportionaladdition 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

II-xvi
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

II-xvii
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 μg/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

II-xviii
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

II-xix
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

II-xx
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, N1G 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

II-xxi
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

II-xxii
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

II-xxiii

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

II-xxv
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 11th 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

II-xxvi
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 (MD52), 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

II-xxvii
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

II-xxviii
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

II-xxix
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
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
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
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 (Pinus 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
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 wellcharacterized 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; Grünhage and Jäger, 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

O3.

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
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).

5-6
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 sativa) 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.

5-7
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

5-8
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 (Grünhage et al., 1994; Dämmgen 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 wellcharacterized 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

5-9
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

5-10
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

5-11
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

5-12
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 exposureresponse 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

5-13
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

5-14
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

5-15
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

5-16
Table 5-1. Comparison of Fumigation Systems for Ozone Exposure-Plant Respons

Fumigation System

Simulation of

Field Losses

Replication of

Experimental Unit

Range of

Treatment Levels

Like

Factor

Controlled-environment chambers Low Low High Greenhouse chambers Low Medium High Closed-top field chambers Medium High High Open-top field chambers Medium to high High High Mechanical field exclusion High Low to medium Low Open-field fumigation High Low Low 

Natural gradients High Low Low 

5-17
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
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;

Gäb 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; Gäb 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
Figure 5-2. Uptake of ozone (O3) 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 O3. 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
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
O3 uptake (and response) varies with time and exposure, data for validating the models are

still needed.

Grünhage and Jäger (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; Küppers 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
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 (CO2), 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
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 ponderosa). 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, Lütz 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
Figure 5-4. Simulation of the effects of diurnal variation in stomatal aperture and in

ozone (O3) concentration on O3 uptake: (A) diurnal O3 concentrations,

(B) simulated conductance, and (C) O3 uptake.

5-25
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
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
Figure 5-5. Effects of ozone (O3) 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
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 (Betula pendula) 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.

Figure 5-6. Effect of ozone (O3) 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
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 taeda). 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 (Malus

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).

5-30
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;

5-31
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 Ferson, 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.

5-32
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 rubra) 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

5-33
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

5-34
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

5-35
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 americana) and green ash (F. pennsylvanica) could

5-36
Table 5-2. Examples of Intraspecific Variation of Foliar Symptoms

in Ozone Response

Species

Genetic

Unita

Ozone

Concentration Duration

Range of

Responseb Reference

Ornamental,

Non-woody

Plants

Petunia sp.

(Petunia)

Cultivars 400 ppb

4 h/day

4 days 20 to 60% (3) Elkiey and Ormrod

(1979a,b),

Elkiey et al. (1979)

Poa pratensis L.

(Kentucky bluegrass)

Cultivars 400 ppb

300 ppb

2 h

4 h

0 to 90% (3)

30 to 60% (3)

Murray et al. (1975),

Wilton et al. (1972)

Trees

Acer rubrum L.

(Red maple)

Populations 750 ppb

7 h/day

3 days 19 to 34% (2) Townsend and

Dochinger (1974)

Fraxinus americana L.

(White ash)

Half-sib

families

500 ppb

250 ppb

7.5 h

6 h

0 to 50% (3)

2 to 33% (2)

Karnosky and Steiner

(1981),

Steiner and Davis

(1979)

Fraxinus pennsylvanica

Marsh. (Green ash)

Half-sib

families

500 ppb

250 ppb

7.5 h

6 h

0 to 40% (3)

2 to 39% (2)

Karnosky and Steiner

(1981),

Steiner and Davis

(1979)

Gleditsia triacanthos L.

(Honeylocust)

Cultivars Ambient 1 growing

season

0 to 34% (3) Karnosky (1981a)

Pinus ponderosa

Dougl. ex P.

Laws and C. Laws

(Ponderosa pine)

Half-sib

families

1.5 × ambient 3 growing

seasons

0 to 28% (2) Temple et al. (1992)

Pinus strobus L.

(Eastern white pine)

Clones 300 ppb 6 h 0 to 60% (3) Houston (1974)

Pinus taeda L.

(Loblolly pine)

Half-sib

families

250 ppb

ambient +

60 ppb

8 h

1 growing

season

3 to 29% (2)

1 to 42% (1)

Kress et al. (1982a),

Adams et al. (1988)

Populus tremuloides

Michx. (Trembling

aspen)

Clones 200 ppb

150 ppb

3 h

6 h

7 to 56% (1)

10 to 91% (1)

Karnosky (1977),

Berrang et al. (1991)

a

Cultivars = 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.

b

Range 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.

5-37
Table 5-3. Examples of Intraspecific Variation in Growth Responses

Following Ozone Exposures

Species

Genetic

Unita

Ozone

Concentration Duration

Range of

Responseb Reference

Crops and

Non-woody

Plants

Agrostis capillaris L.

(Bentgrass)

Populations 60 ppb 4 weeks −45 to +20% (2) Dueck et al.

(1987)

Begonia semperflorens

Hort. (Bedding

begonia)

Cultivars 500 ppb

4 h/day

250 ppb

4 h/day

2 days

4 days

−59 to 0% (2)

−16 to +10% (2)

Reinert and Nelson

(1979),

Reinert and Nelson

(1980)

Festuca arundinacea

Schreb. (Fescue)

Cultivars 400 ppb

6 h/day

7 days −53 to −35% (2) Flagler and

Younger (1982)

Lycopersicon

esculentum L.

(Tomato)

Cultivars 400 ppb

1.5 × ambient

2 h

1 growing

season

−50 to −4% (2)

−54 to −17% (3)

Reinert and

Henderson (1980),

Temple (1990a)

Phaseolus vulgaris L.

(Snapbean)

Cultivars 60 ppb

7 h

72 ppb

7 h

80 ppb

7 h/day

mean -

44 days

mean -

54 days

42 days

−26 to −2% (3)

−73 to −44% (3)

−68 to −50% (3)

Heck et al. (1988),

Temple (1991),

Eason and Reinert

(1991)

Plantago major L.

(Common plantago)

Populations 70 nL/

1-7 h/day

2 weeks −24 to 0% (1) Reiling and

Davison (1992a)

Raphanns sativus L.

(Radish)

Within

cultivar

0.1 μL/

1-4 h/day

3 days/week

3 weeks −40 to −5% (2) Gillespie and

Winner (1989)

Silene cucabalus

(Bladder campion)

Populations 35 ppb

12 h/day

4 weeks −75 to −48% (2) Ernst et al. (1985)

Solanum tuberosum L.

(Potato)

Cultivars 150 ppb

6 h/day

8 days −10 to 0% (2)

−40 to 0% (2)

Pell and Pearson

(1984),

Ormrod et al.

(1971)

Spinacia oleracea L.

(Spinach)

Cultivars 130 ppb

7 h/day

38 days −56 to −28% (2) Heagle et al.

(1979a)

Trees and Other

Woody Plants

Acer rubrum L.

(Red maple)

Populations 750 ppb

7 h/day

3 days −36 to −17% (1) Townsend and

Dochinger (1974)

Abies alba Mill.

(Silver fir)

Populations 250 ppb

7 h/day

10 days −18 to +3% (1) Larsen et al.

(1990)

Pinus elliottii

Engelm. (Slash pine)

Half-sib

families

3 × ambient 3 growing

seasons

−20 to 0% (1) Dean and Johnson

(1992)

5-38
Table 5-3 (cont’d). Examples of Intraspecific Variation in Growth Responses

Following Ozone Exposures

Species

Genetic

Unita

Ozone

Concentration Duration

Range of

Responseb Reference

Pinus taeda L.

(Loblolly pine)

Full-sib

families

50 ppb

6 h/day

1.9 × ambient

28 days

2 growing

seasons

−18 to 0% (1)

−19 to 0% (2)

Kress et al.

(1982b),

Shafer and

Heagle (1989)

Pinus taeda L.

(Loblolly pine)

Half-sib

families

Ambient +

60 ppb

2.5 × ambient

250 ppb

1 growing

season

1 growing

season

8 h

−27.5 to +3% (2)

−19 to −2% (2)

−22 to +30% (2)

Adams et al.

(1988),

Qiu et al. (1992),

Winner et al.

(1987)

Populus tremuloides

Michx. (Trembling

aspen)

Clones 26.4 ppm-h

ambient

92 days

3 growing

seasons

−74 to −5% (2)

−24 to −12% (2)

Karnosky et al.

(1992a),

Wang et al.

(1986a,b)

Rhododendron

obtusum

(Lindl) Planch.

(Azalea)

Cultivars 250 ppb -

3 h/day

6 days −43% to 0% (2) Sanders and

Reinert (1982)

a

Cultivars = 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.

b

Range 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
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
Figure 5-8.

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 cepa) (Engle and Gabelman, 1966), some bean (Phaseolus vulgaris) cultivars

5-41
(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 arundinacea) (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
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
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 1,386 34 2.4%

Intermediate 98 3 3.1%

Sensitive 57 14 24.6%

a

Resistant = 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
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 hybrida) 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
Table 5-5. Examples of Ozone Effects on Pollen Germination

and Tube Elongation

Species

Pollen

Germination

Pollen Tube

Elongation Reference

Nicotiana tobacum L.

(Tobacco)

Decrease Decrease Feder (1968)

Feder and Shrier (1990)

Petunia hybrida

(Petunia)

Not tested Decrease Feder and Shrier (1990)

Pinus strobus L.

(Eastern white pine)

No effect Decrease Benoit et al. (1983)

Zea mays L.

(Corn)

Decrease Not tested 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.

5-46
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-Insect 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
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 (Vicia faba)

(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, Lymantria 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 syriaca) (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

5-48
Table 5-6. Ozone Effects on Insect Pests

Host Plant/Insect Exposurea Experimental Conditionsb Effect of Ozone on Insect CROP SPECIESBroad bean/aphid 3 day, 0.085 ppm

<24 h, 0.1 ppm>24 h, 0.1 ppm 8 h/day,episodic

Chamber, whole plantChamber, whole plantChamber, whole plantChamber, whole plant

3-13% decreased growth rate17% increased growth rate12% decreased growth rate15% increased growth rate

Dohmen Brown 

Pea/aphid 4-8 day, var. Chamber, whole plant Variable effects on growth WhittakKidney bean/aphid 14 day, var. OTC 15-50% reduction in growth of

insect

Braun a

Soybean/beetle

(cv. Corsoy)(cvs. Essex, Forrest)

16 day, var.21 day, 7 h/day, var.

ChamberOTC

Variable feeding preference0.11>0.0>0.05>0.03 ppm;feeding preference increased andgreater larval growth

Endress Chappe

Tomato/pinworm 2-4 day, 3 h/day

0.28 ppm

Chamber, detached leafChamber, whole plant

80% increase in larvaldevelopment; no effect onfecundity

Trumbl

NATURALVEGETATIONMilkweed/monarch

butterfly

17-19 day, 7 h/day0.150-0.178 ppm

Chamber, whole plant No feeding preference but greater

larval growth rate

Bolsing

Dock/aphid 15 day, var. Chamber, whole plant 10% increased growth rate WhittakDock/beetle 15 day, var. Chamber, whole plant 10% larger egg batches; fourfold

greater larval survival

Whittak

TREES SPECIESEuropean beech/aphid 2 mo, var. OTC 75% increase in number Braun aEuropean beech/weevil 72 h, var. OTC Twofold increase in feeding

preference

Hiltbrun

5-49
Table 5-6 (cont’d). Ozone Effects on Insect Pests

Host Plant/Insect Exposurea Experimental Conditionsb Effect of Ozone on Insect TREE SPECIES(cont’d)Cottonwood/beetle 5 h, 0.2 ppm OTC 22-60% greater consumption of

foliage but decreased fecundity

Jones aColema

Ponderosa pine/bark

beetle

Natural None, field Increased infestation but

decreased survival

Hain (1

White oak/gypsy moth 11 day, 7 h/day, var. Chamber, leaf disks Variable feeding preference

0.15 > 0.03 > 0.09 ppm

Jeffords 

avar. indicates a range of exposures.bChamber indicates closed chamber; OTC indicates open-top field chamber.

5-50
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

vaporariorum, 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 insectsystems 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

5-51
Table 5-7. Ozone-Plant-Pathogen Interactionsa

Host Plant Pathogen Effect of O3 on Disease Effect of Disease on O3 Response OBLIGATE FUNGIKidney bean Uromyces phaseoli Increased number of

smaller pustules

Reduced injury on severelydiseased leaves

Resh an

Barley Erysiphe graminis Reduced infection but

greater spore production

Not reported Heagle 

Cottonwood Melampsora medusae Reduced infection and

development

Not reported Colema

Lilac Microsphaera alni No effect Not reported Hibben 

Oats Puccinia coronata Reduced infection and

development

No effect Heagle 

Wheat Erysiphe graminis Increased infection and

development

Not reported Tiedem

Puccinia graminis Reduced infection and

development

Reduced leaf injury Heagle 

Puccinia graminis Reduced development Not reported Heagle 

Puccinia recondita Reduced infection and

development

Not reported Dohmen 

FACULTATIVE FUNGIBarley Drechslera teres Increased infection Not reported Tiedem

Gerlachia nivalis Increased infection Not reported TiedemHelminthosporiumsativum

No effect Not reported Tiedem

Cabbage Fusarium oxysporum Decreased development Not reported Mannin

Corn Helminthosporium

maydis

Increased development Not reported Heagle 

5-52
Table 5-7 (cont’d). Ozone-Plant-Pathogen Interactionsa

Host Plant Pathogen Effect of O3 on Disease Effect of Disease on O3 Response FACULTATIVE FUNGI (cont’d)Cottonwood Marssonina brunnea Increased infection Not reported Colem

Geranium Botrytis cinerea Decreased infection Not reported Kraus

Onion Botrytis (3 spp.) Increased infection and

development

Not reported Wuka

Potato Botrytis cinerea Increased infection and

development

Not reported Manni

Alternaria solani Increased infection Not reported Holley 

Alternaria solani Increased infection Not reported Bisess

Soybean Fusarium oxysporum Increased infection Increased leaf injury Damic

Wheat Gerlachia nivalis Increased infection Not reported Tiedem

Helminthosporiumsativum

No effect Not reported Tiedem

Helminthosporiumsativum

Increased infection Not reported Tiedem

Septoria (2 spp.) Increased infection Not reported TiedemSeptoria (2 spp.) Increased infection Not reported Tiedem

Jeffrey pine Heterobasidium annosum Increased development Not reported James 

Ponderosa pine Heterobasidium annosum Increased development Not reported James 

White pine Vertcicladiella procera Slightly increased incidence Not reported Coston

Lophodermium pinastre Slightly increased incidence Not reported Coston

5-53
Table 5-7 (cont’d). Ozone-Plant-Pathogen Interactionsa

Host Plant Pathogen Effect of O3 on Disease Effect of Disease on O3 Response BACTERIAAlfalfa Xanthomonas alfalfae Reduced development Reduced leaf injury Howell 

Soybean Pseudomonas glycinea Reduced incidence No effect Laurenc

Pseudomonas spp. Reduced infection Reduced leaf injury Pell et 

White bean Xanthomonas phaseoli No effect Reduced leaf injury Temple 

Wild strawberry Xanthomonas fragariae Reduced incidence No effect Laurenc

NEMATODES

Begonia Aphelenchoides

fragariae

Reduced nematodereproduction

Reduced leaf injury Weber 

Soybean Belonolaimus

longicaudatus

Stimulation or no effect Not reported Weber 

Heterodera glycines Reduced nematode

reproduction

Not reported Weber 

Paratrichodorus minor Reduced nematode

reproduction

Reduced leaf injury Weber 

Pratylenchus penetrans No effect Not reported Weber 

Tobacco Meloidogyne hapla Possible stimulationb Increased leaf injury Bisessa

aSee Appendix A for abbreviations and acronyms.bBased on studies using the protectant EDU (see Section 5.2.1.2).

5-54
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. (1991a,

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.

5-55
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

5-56
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

5-57
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 leaf’s 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

5-58
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 sitchensis) (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

5-59
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

5-60
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

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Table 5-8. Field Studies of Ozone-Drought Stress Interactions in Crop Speci

(Adapted in part from Heagle et al., 1988a)

Estimated Yield Loss (%) per Seasonal Mean

O3 Concentration (ppm)b

Crop/Cultivar Year Response

Significant

Interactionc 0.04 0.05 0.06 0.07 0.08 

Soybean

Williams 1982 Yield No 7 13 19 24 30 Hegg

Hegg

Williams andCorsoy 79

1983 Yield

Yield

WWDS

76

1311

1815

2419

3023 Hegg

Williams Root length

Root length

WWDS

No significant O3 effect

[33 36 52]d

Hegg

Forrest 1982 Yield

Yield

WWDS

3

13

9

21

2128

3935

6041

HeggHegg

Davis 1983 Yield

DS

WW 4 7 12 16 21 Heag

YieldDS

No significant O3 effect

Davis 1984 Yield No 4 7 12 18 24 HeagCorsoy 79 1986 Yield

Yield

WWDS

20

40

80

13

0

21

1

Irving 

Young 1986 Yield No 6 11 17 25 34 Mille

Cotton

Acala SJ-2 1981 Yield

Yield

WWDS

31

72

13

3

21

7

3012

Temp

Acala SJ-2 1982 Yield No 6 15 26 40 55 TempMcNair 235 1985 Yield No 7 13 21 30 40 HeagAcala SJ-2 1986 Shoot dry mass WWe [22 26 42]f Temp

Shoot dry mass DSe [20 37 44]fShoot dry mass DS (severe)e [+14 +22 27]f

5-62
Table 5-8 (cont’d). Field Studies of Ozone-Drought Stress Interactions in Crop S

(Adapted in part from Heagle et al., 1988a)

Estimated Yield Loss (%) per Seasonal Mean

O3 Concentration (ppm)b

Crop/Cultivar Year Response

Significant

Interactionc 0.04 0.05 0.06 0.07 0.08 

Alfalfa

WL-514WL-514

19841985

YieldYield

NoNog

64

97

1310

1714

2018

Temp

Tall Fescue-Ladino Clover

Kentucky 31

and Regal

19841984

YieldYield

NoNo

56

8

11

1217

1724

2232

Heag

aSee Appendix A for abbreviations and acronyms.bWhere a significant interaction was observed, separate responses are listed for well-watered (WW) and drought-stressed (DS) plant

response is listed.

cBased 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 relat

root lengths in DS treatments ranged from 136 to 11% with increasing O3 exposure. eInteraction 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, an0.015 ppm.

gPolynomial regression analysis showed slightly greater response in WW than DS plots.

5-63
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 wellwatered 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
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
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 Decreased reduction of growth due

to O3

Tjoelker and Luxmoore (1991)

Ponderosa pine No injury or growth interactions Bytnerowicz et al. (1990)

Poplar Maximum injury in mid-range but

no growth interaction

Harkov and Brennan (1980)

Yellow poplar No growth interaction Tjoelker and Luxmoore (1991)

Ladino clover/tall fescue No growth interaction Montes et al. (1982)

Mangel Increased injury Brewer et al. (1961)

Radish Increased reduction of growth

due to O3

Ormrod et al. (1973)

Increased reduction of growth

due to O3

Pell et al. (1990)

Spinach Increased injury Brewer et al. (1961)

Tobacco Decreased injury Menser and Street (1962)

Minimum injury in mid-range MacDowall (1965)

Maximum injury in mid-range Leone et al. (1966)

Maximum injury in mid-range Menser and Hodges (1967)

Phosphorus

Radish No growth interaction Ormrod et al. (1973)

Tomato Increased injury Leone and Brennan (1970)

Potassium

Norway spruce Decreased reduction of CO2

assimilation due to O3

Keller and Matyssek (1990)

Pinto bean Decreased injury Dunning et al. (1974)

Soybean Decreased injury 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 Decreased injury Heck et al. (1965)

Soybean Maximum injury and growth

reduction in mid-range

Heagle (1979)

a

See Appendix A for abbreviations and acronyms.

5-66
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
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., 1991a) 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
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
Table 5-10. Some Statistical Models of Combined Ozone and Sulfur Dioxide Resp

Species

Type of

Interaction Model 

CornGolden Jubilee Synergistic Injury = −11.39 + 5.471ln(IHT) − 9.59[O3] + 11.81[SO2] − 86.63[SO2]

2 +

428.95[O3][SO2] (IHT = initial plant height, used as a covariate; [O3] and [SO2], ppm)

CucumberNational Pickling Synergistic Injury = 2.70 + 1.95 n; at [SO2] = 0.10 ppm

Injury = 2.40 + 0.21 n; at [SO2] = 0.05 ppmInjury = 2.39 + 0.39 n; at [SO2] = 0.03 ppmInjury = 1.86 + 0.166 n; at [SO2] = 0.02 ppm(n = number of daily 8-h SO2 exposures; O3 exposure, 0.15 ppm, 6 h)

Snap Bean

Maple Arrow Additive; no

interaction

Injury = 4.44 + 34.19[O3] + 19.98[SO2]([O3] and [SO2], ppm) 

White BeanSeafarer Antagonistic Injury = 6.31 − 0.90 n; at [SO2] = 0.10 ppm

Injury = 5.95 − 0.45 n; at [SO2] = 0.05 ppm(n = number of daily 8-h SO2 exposures; O3 exposure: 0.15 ppm, 6 h)

Potato

Norchip Additive; no

interaction

Yield = 1.27 − 0.0037[O3] + 0.00092[SO2]

(Yield = number of Grade No. 1 tubers per plant; [O3]: ppm, 10 h/day seasonal mean;[SO2], ppm, 3 h/day)

Soybean

Davis Antagonistic Polynomial model:

Yield = 534.5 − 3988.6[O3] − 479.7[SO2] + 2661.0[O3][SO2] + 1,0960[O3]

2

Weibull model:Yield = 531 × exp[−([O3]/0.133)] × exp[−([SO2]/0.892)](Yield = g/m of row; [O3]: ppm, seasonal 7 h/day mean; [SO2]: ppm, seasonal 4 h/day m

Amsoy-71 andCorsoy-79 (pooled)

Nointeraction

Yield = 1934.4*exp[−([O3]/0.124)2.666]* exp[−([SO2]/1.511)1.044](Yield = kg/ha; [O3]: ppm, seasonal 7 h/day mean; [SO2]: ppm, seasonal 4 h/day mean)

5-70
Table 5-10 (cont’d). Some Statistical Models of Combined Ozone and Sulfur Dioxide 

Species

Type of

Interaction Model 

TomatoNew Yorker Injury = −75.78 + 20.48ln[PI] − 29.16[O3] + 1,016[O3]

2 + 9.02[SO2] − 17.29[SO2]

2 + 258.

[O3][SO2] (PI = plastochron index, used as a covariate; [O3] and [SO2]: ppm)

aSee Appendix A for abbreviations and acronyms.

bReport includes models for other growth variables.

5-71
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 annuus)

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

5-72
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 1μg/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 echinata) 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 No.

Interaction

References No.

No Interaction

References

Tree Species

CONIFERS

Jeffrey pine 0 — 1 62

Loblolly pine 1 41 13 1, 10, 16-21, 26, 32, 43, 47, 49, 55

Ponderosa pine 0 — 2 65, 66

Shortleaf pine 1 52 1 8

Slash pine 2 9, 13 0 —

White pine 1 47 3 44, 46, 56

Douglas fir 0 — 1 25

Norway spruce 1 3, 4 9 2, 5-7, 15, 24, 30, 36, 50

Red spruce 2 31, 39 5 33, 34, 38, 40, 62

Sequoia 1 63 0 —

Totals 9 35

HARDWOODS

Green ash 0 — 1 23

White ash 0 — 1 23

European beech 1 14 1 35

Paper birch 1 29 0 —

Sugar maple 0 — 2 44, 45

Red oak 0 2 44, 45

Yellow poplar 3 11, 12, 27 1 48

Totals 5 8

Crop Species

FORAGES AND FIELD CROPS

Alfalfa 1 59 4 42, 53, 59, 64

Sorghum 1 51 0 —

Soybean 1 67 4 28, 37, 53, 57

Wheat 0 — 1 53

Totals 2 5

HORTICULTURAL CROPS

Snap bean 0 — 1 53

Celery 0 — 1 60

Corn 0 — 1 60

Pepper 0 — 2 58, 60

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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

Species No.

Interaction

References No.

No Interaction

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 0 — 1 30

Lichen (Lobaria) 0 — 1 54

Totals 0 2

TOTALS 19 63

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. Führer 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 × 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 × 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 papyrifera) were reversed by increased acidity of SAR (Keane and Manning,

1988). Similarly, in both avocado and lemon (Citrus volkameriana) 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 (McIlveen 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 (Juniperus

conferta) (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-1-[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

(1-[(2,4-dichlorophenyl)-4-ethyl-1,3-dioxolan-2-yl]methyl-1H-1,2,4-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]-1-[4-chlorophenoxy]-3,3-dimethyl-2-[1,2,4-triazol-1-yl]- 1-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-dichlorobenzyltributyl phosphonium chloride) and SADH (Alar®; succinic acid, 2,2-dimethylhydrazide) 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-N-[2-ethyl-6-methlphenyl]-N-[2-methoxy-1-methylethyl] acetamide)

(Mersie et al., 1989) and atrazine (2-chloro-4-ethylamino-6-isopropylamino-s-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, n-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

(Brühl 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 × 10-5[CO2] + 3.40 × 10-8[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 × ambient. No significant O3/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 temperaturedependent 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 (Lösch 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, Grünhage and Jäger (1994a,b) and Grünhage 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 (Grünhage 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

(5-1) Index n

i 1

wi × f(Ci),

where Ci is the hourly mean concentration, f(Ci) is some function of Ci, and wi 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 wi. Based on the weighting function, the exposure indices can be

arranged into the categories described below (description from Lee et al., 1989).

· One Event: wi = 0 for all Ci, except for the few concentrations where wi = 1.

Examples of such indices are the second highest daily maximum 1-h

concentration (2HDM), the maximum of 7-h (P7) and 1-h (P1) maximum daily

averages, and the 90th or higher percentiles of hourly distribution.

· Mean: wi = 0 for all Ci outside the period of interest (P) and wi = vi/Σi=1

n vi

for all Ci inside the period P, where vi is a function of Ci or some

environmental variable. Examples are the seasonal mean of 7-h daily means

(M7) (Heagle et al., 1979b); the effective mean (me), where me

v is the index in

Equation 5-1 with f(Ci

)=Ci

-1/v and wi = 1 for some parameter v (Larsen and

Heck, 1984); the solar-weighted mean where vi is the hourly solar radiation

value (Rawlings et al., 1988b).

· Cumulative: wi = 1 for all Ci. An example is the seasonal sum of all hourly

concentrations (i.e., total exposure, denoted as SUM00).

· Concentration Weighting: wi = g(Ci

) 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 wi = Ci

(-1-1/v) for some v (Larsen et al.,

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1983); the index with the allometric function, g(Ci

)=Ci

a

, a > 0; the index with

sigmoidal weighting function, g(Ci) = 1/[1 + M × exp(−AxCi)], 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(Ci) =

0 for Ci < 0.08 ppm and wi = 1/Ci for Ci ≥ 0.08 ppm.

· Multicomponent: wi = g(Ci, 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(Ci)=Ci − 0.10 and wi = 0 for Ci < 0.10 ppm and wi = 1

for Ci ≥ 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(Ci

)=Ci and wi = 0 for Ci < 0.10 ppm and

wi = 1 for Ci ≥ 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 shortlived 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 proportionaladdition 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 SUM00 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 × 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 (SUM00) 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 identifing 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

SUM00 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

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Figure 5-9. Distribution pattern showing the number of ozone concentrations

within specified ranges for the 1983 winter wheat proportionaladdition experiment for the (A) 1.4 × ambient air and (B) 1.8 ×

ambient air treatments and for (C) San Bernardino, CA, in 1987.

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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., SUM00),

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 midto 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 M

Exposure Patterns on the Growth, Productivity, or Yield of Plantsa

Species Facilityb

Total Number

of Chambers Exposure Patternsc

Exposure

Duration

Concentration (ppm)/Exposured

(ppm-h) Variable Effecte 

Glycine max L.Merrill cv. Davis,Forrest, Bragg,and Ransom

OTC inpots

24 16 combinations of CF

or NF + over 4 quarters(31-days/quarter)

124 days M7 (ppm): CF range from 0.016 to

0.038 over the 4 quarters, NF+rangefrom 0.096 to 0.098 over the4 quarters

Totalseedweight

Forrest: greater effect in Q3 quarters. Davis: no consistsignificant but similar effectQ4. Ransom: no significan

or Q2, and equal responses Bragg: no significant O3 effe

significant decreases in Q3 a

Medicago sativa L. OTC in

pots

8 E, DP 133 days Equal SUM07 (ppm-h): DPH=113,

DPL=63, EH=117, EL=72Equal SUM00 (ppm-h): DPH=183,DPL=140, EH=193, EL=145M7 (ppm): DPH=0.099, DPL=0.074,EH=0.084, EL=0.064

Shootdryweight

91 and 67% reductions for ESignificant difference betweDP regimes. Treatment meaCF<DPL<EL<DPH<EH.

Phaseolus vulgarisL.cv. Calif. DarkRed Kidney Bean

GC inpots

8 U, V 3 weeks

(1 day/

week)

Equal SUM00 (ppm-h/day):UL=VL=0.69; UH=VH=0.92Equal Max concentration (ppm):UL=VL=0.30, UH=VH=0.40

Pod andseed dryweights

6% less yield when exposed Response to O3 same in repr

vegetative growth stages.

Phaseolus vulgarisL.cv. Calif. DarkRed Kidney Bean

GC inpots

8 U, V 3 weeks

(1 day/

week)

Equal SUM00 (ppm-h/day):UL=VL=1.20; UH=VH=1.68Max concentration. (ppm): UL=0.20,VL=0.50,UH=0.28, VH=0.715

Pod andseed dryweights

38% less yield when exposeNo significant difference behigh. Beans in reproductive when exposed.

Phaseolus vulgarisL.cv. Calif. Dark RedKidney Bean

GC inpots

8 Square wave (SW),

Triangular (T),Flattened triangular (FT),Rhomboid (R)

7 weeks

(3 days/

week)

Equal SUM00 (ppm-h/day):SW=T=FT=R=0.60. Max concentration(ppm): SW=0.12, T=0.36,FT=R=0.24.

Top dryweight

SW had significantly higher three patterns. Treatment mR=T<FT<SW

Phaseolus vulgarisL.cv. Calif. DarkRed Kidney Bean

GC inpots

10 Initial exposure of 0.3 ppm

for 3-h and second exposureof 0.3 ppm at 2-6 (or 1-5)days after initial exposure

2-6 days

in 1984

and

1-5 days

in 1985

Equal maximum concentration of0.30 ppm.

Total dryweight

Reductions due to the seconsignificant when exposures wapart in 1984 and 5 days ap

aSee Appendix A for abbreviations and acronyms.bGC = Controlled environmental growth chamber, or CSTR; OTC = Open-top chamber.cCA = Constant addition, PA = Proportional addition, CF = Charcoal-filtered, NF = Nonfiltered, NF+ = Nonfiltered plus ozone, E = Episodic, DP = Daily peak, U = 

HE = High elevation.

dH = High, L = low. eSignificant at the 0.05 level, NS = not significant.

5-94
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 SUM00 index weights all concentrations equally, the SUM00 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. (1991a) 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, Pr

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

Species Facilityb

Total No.

of Plots

Duration

[dates and (days)] Concentration (ppm)/ Exposure (ppm-h)c Variable Effec

PART ABrassicanapus L.var. Napuscv. Callypso

OTCin pots

1987: 181988: 241989: 16

1987: 05-13 to 08-10 (89)1988: 05-02 to 08-24 (113)1989: 05-08 to 08-01 (84)

1987: M24 (M8) in ppb range from 5 (9) to 16 (43).1988: M24 (M8) in ppb range from 3 (5) to 16 (48).1989: M24 (M8) in ppb range from 6 (5) to 22 (62).

Seeddryweight

1987: 27% reduction at 1988: 18% reduction at 1989: 11% reduction at 

Gossypiumhirsutum L.cv. Acala SJ2

OTC 1981: 12

1982: 12

1981: 07-06 to 09-15 (72)1982: 06-04 to 09-09 (98)

1981: M7 (SUM06) range from 18 ppb (0 ppm-h) to 138(68).1982: M7 (SUM06) range from 12 ppb (0 ppm-h) to 111(71).

Lintdryweight

45 and 66% reductions a57 and 60% reductions a68 ppm-h.

Hordeumvulgare L.cf. Arenaand Alexis

OTCin pots

1988: 241989: 16

1988: 04-29 to 08-15 (108)1989: 05-08 to 08-15 (99)

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).

Seeddryweight

Arena: 14% (*) and 6% M8 = 48 ppb.Alexis: No reductions at 

Phaseoulusvulgaris L.cv. Calif. DarkRed KidneyBean

OTC 1980: 20

1982: 20

1980: 08-20 to 09-10 (22)1982: 08-11 to 10-06 (57)

1980: M7 (SUM06) range from 24 ppb (0 ppm-h) to 139(19).1982: M7 (SUM06) range from 19 ppb (0 ppm-h) to 110(40).

Seeddryweight

13 and 59% reductions a28 and 8% reductions at 19 ppm-h.

Phaseolusvulgaris L.cf. Rintintin

OTCin pots

1988 I: 41988 II: 61989 III: 8

1988 I: 06-15 to 08-04 (51)1988 II: 07-24 to 08-29 (37)1989 III: 06-04 to 07-25 (52)

I. M8 (max) in ppb range from 3 (19) to 48 (70).II. M8 (max) in ppb range from 2 (19) to 50 (105).III. M8 (max) in ppb range from 6 (26) to 109 (159).

Poddryweight

I. 2% reduction at M8 = II. 0% reduction at M8 III. 0% (NS) and 47% (*M8 = 50 and 109 ppb.

Solanumtuberosum L.cv. Norchip

OTC 1985: 15

1986: 39

1985: 06-14 to 08-22 (70)1986: 06-20 to 08-20 (62)

1985: M7 (SUM06) range from 22 ppb (0 ppm-h) to85 (47).1986: M7 (SUM06) range from 24 ppb (0 ppm-h) to88 (38).

Tuberweight

42 and 25% reductions a32 and 27% reductions a38 ppm-h.

Triticumaestivum L.cv. Vona

OTC 1982: 20

1983: 12

1982: 05-18 to 07-17 (61)1983: 06-12 to 07-17 (36)

1982: M7 (SUM06) range from 21 ppb (0 ppm-h)to 95 (41).1983: M7 (SUM06) range from 26 ppb (0 ppm-h)to 96 (22).

Seeddryweight

74 and 49% reductions a49 and 62% reductions a21 ppm-h.55 and 60% reductions a22 ppm-h.

5-97
Table 5-13 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the Growth

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

Species Facilityb

Total No.

of Plots

Duration

[dates and (days)] Concentration (ppm)/ Exposure (ppm-h)c Variable Effectd 

PART A (cont’d)Triticumaestivum L.cv. Starand Turbo

OTCin pots

1988: 61989: 10

1988: 04-27 to 08-23 (118)1989: 05-09 to 08-15 (98)

1988: M8 (max,SUM06) in ppb range from4 (58,0) to 51 (106,8.2).1989: M8 (max,SUM06) in ppb range from10 (34,0) to 113 (162,87).

Seeddryweight

Star: 20% (*) and 9% (NS) reductM8 = 51 ppb.Turbo: 25% (*) and 31% (*) reducM8 = 51 ppb.

Triticumaestivum L.,cv. Starand Turbo

OTCin pots

1988: 241989: 16

1988: 04-29 to 08-15 (108)1989: 05-08 to 08-15 (99)

1988: M8 (max 8-h mean) in ppb range from5 (15) to 48 (89).1989: M8 (max 8-h mean) in ppb range from11 (27) to 62 (101).

Seeddryweight

Star: 26% (*) and 12% (*) reductippb.Turbo: 34% (*) and 17% (*) reducM8 = 48 ppb.

PART BGlycine max L.Merr. cv. Davis

OTCin pots

1977: 81978: 8

1977: 06-17 to 10-10 (116)1978: 06-28 to 10-21 (116)

1977: M7 (max) in ppb range from 27 (78) to154 (277).1978: M7 (max) in ppb range from 28 (84) to131 (241).

Seeddryweight

47 and 37% reductions at M7 = 1

Glycine max L.Merr.cv. Williams

OTC 1981: 31

1982: 311983: 31

1981: 07-20 to 09-22 (65)1982: 07-14 to 09-22 (71)1983: 07-23 to 09-23 (63)

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.

Beandryweight

28, 20, and 32% reductions at M7 43 and 41% reductions at M7 = 91982 and 1983

Medicagosativa L.cv. WL-514

OTC 1984: 30

1985: 30

1984: 03-16 to 10-10 (209)1985: 03-23 to 10-09 (201)

1984: M12 in ppb range from 16 to 109.1985: M12 in ppb range from 10 to 94.

Top dryweight

29% (*) and 25% (*) reductions aM12 = 94 ppb.

Pinus rigidaMill.

OTCin pots

Exp. 1: 4Exp. 2: 4

Exp. 1: 13 weeksExp. 2: 13 weeks

1: M8 in ppb range from 0 to 200 (U).2: M8 in ppb range from 0 to 200 (U).

Totaldryweight

49 and 46% reductions at M8 = 2

Pinus taeda L. GC

in pots

1986: 151987: 15

1986: 09-15 to 12-04 (81)1987: 07-27 to 10-15 (81)

1986: SUM00 in ppm-h range from 0 to 99 (U).1987: SUM00 in ppm-h range from 0 to 99 (U).

Totaldryweight

43 and 28% reductions at SUM00 averaged across all families.Individual families show similarreductions (e.g., 35 and 33% reducSUM00 = 99 ppm-h for family 5.5reductions at SUM00 = 99 ppm-h 1.68).

5-98
Table 5-13 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the Growth

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

Species Facilityb

Total No.

of Plots

Duration

[dates and days] Concentration (ppm)/ Exposure (ppm-h)c Variable Effectd 

PART B (cont’d)Picea rubensSarg.

OTCin pots

1987: 121988: 12

1987: 05-30 to 12-15 (199)1988: 06-01 to 12-01 (184)

1987: SUM00 in ppm-h are 32, 61, 91, and 119.1987: SUM00 in ppm-h are 36, 70, 101, and 135.

Totaldryweight

0% (NS) reduction in biomass 8% (*) reduction at SUM00 = after second year of exposure.

Pisum sativum L.cv. Puget

ZAPS 1986: 14

1987: 14

1986: last 58 days1986: last 52 days

M12 and D25 (numbers of days with 1-hconcentrations >25 ppb) used in simple linearregression.

Peafreshweight

0% reductions at M12 = 100 pbased on linear regression mo

PopulustremuloidesMichx clones

OTCin pots

1988: 181989: 18

1988: 07-19 to 09-27 (71)1989: 07-20 to 09-20 (64)

1988: SUM00 in ppm-h are 5.0, 10.0, and19.4 (U).1989: SUM00 in ppm-h are 7.7, 15.4, and26.4 (U).

Stemand leafdryweights

36% (*) and 40% (*) reductioSUM00 = 19.4 ppm-h.

Triticumaestivum L.cv. Albis

OTC 1986: 12

1987: 161988: 16

1986: 05-06 to 07-31 (86)1987: 04-27 to 08-10 (92)1988: 05-04 to 08-01 (89)

1986: M24 (max) in ppb range from 12 (61) to47 (181).1987: M24 (max) in ppb range from 12 (54) to45 (175).1988: M24 (max) in ppb range from 17 (65) to45 (148).

Seeddry weight

1986: 61% reduction at M24 = 1987: 27% reduction at M24 = 1988: 65% reduction at M24 = 

Triticumaestivum L.cv. Albis

OTC 1989: 24

1990: 24

1989: 05-16 to 08-14 (91)1990: 05-14 to 08-09 (88)

1989: M7 (SUM06) range from 18 ppb (0 ppm-h)to 62 (3.8).1990: M7 (SUM06) range from 17 ppb (0 ppm-h)to 71 (5.6).

Seed dryweight

29 and 22% reduction at M7 = 29 and 17% reduction at SUM3.8 ppm-h.

Triticumaestivum L.cv. Severn,Potomac, Oasis,MD5518308

OTC 1984: 20

1985: 20

1984: 05-14 to 06-22 (40)1985: 05-06 to 06-15 (41)

1984: M4 (AOT03) in ppb (ppb-h) range from32 (0) to 93 (10).1985: M4 (AOT03) in ppb (ppb-h) range from30 (0) to 86 (9).

Seed dryweight

31% (*) and 9% (NS) reductioM4 = 86 ppb.

aSee Appendix A for abbreviations and acronyms.bGC = Controlled environmental growth chamber, or CSTR; OTC = open-top chamber; ZAPS = zonal air pollution system.cU = Uniform.d* = Significant at the 0.05 level; NS = not significant.

5-99
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
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
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., 1991a).

(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
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
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

SUM00 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 (Seiler 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 SingleYear, 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 exposuredynamic 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., SUM00), 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, SUM00 alone was an

inadequate descriptor of exposure for predicting response. However, for assessing the effects of long-term, low

concentrations typical of ambient condition, SUM00 may be adequate, because the response of field-grown plants to

SUM00 was roughly linear. SUM00 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 Predicte

20% Yield Reduction per SUM06 Exposure Response Models Used by

Lee et al. (1991) in Selected National Crop Loss Assessment Network Experim

(Concentrations are in parts per million.)

Experimentb

Percentiles

70 90

Number

of Obs.

Number of Occurrences

≥0.06 ≥0.08 ≥0.10

Chamber Min. 10 30 50 95 99 Max 

SOYBEANA80S0 - Corsoy NF+0.03-1 0.000 0.000 0.011 0.026 0.045 0.077 0.090 0.111 0.123 1,344 263 113 35 A83SO - Amsoy NF+0.03-1 0.000 0.001 0.014 0.028 0.049 0.083 0.098 0.123 0.168 1,992 467 223 90 A83SO - Corsoy NF+0.03-1 0.000 0.001 0.014 0.028 0.049 0.083 0.098 0.123 0.168 1,992 467 223 90 A85SO - Corsoy-79 D NF×2.00-1D 0.000 0.000 0.008 0.023 0.051 0.110 0.129 0.160 0.194 2,352 657 495 319 A85SO - Corsoy-79 W NF×2.00-1W 0.000 0.000 0.011 0.026 0.063 0.114 0.134 0.162 0.199 2,352 729 547 358 A86SO - Corsoy-79 D NF×2.5-1D 0.000 0.002 0.016 0.035 0.085 0.137 0.161 0.207 0.279 2,040 784 654 515 A86SO - Corsoy-79 W NF×2.0-1W 0.000 0.002 0.015 0.033 0.065 0.105 0.124 0.161 0.242 2,040 719 510 271 B83SO - Corsoy-79 D NF-1D 0.000 0.002 0.006 0.018 0.037 0.063 0.074 0.087 0.111 1,512 184 51 5 B83SO - Corsoy-79 W NF+0.03-1W 0.000 0.002 0.006 0.019 0.049 0.084 0.097 0.118 0.135 1,512 359 198 70 B83SO - Williams D NF+0.03-1D 0.000 0.002 0.006 0.019 0.049 0.084 0.098 0.118 0.137 1,512 364 204 66 B83SO - Williams W NF+0.03-1W 0.000 0.002 0.006 0.019 0.049 0.084 0.097 0.118 0.135 1,512 359 198 70 I81SO - Hodgson NF+0.06-1 0.000 0.004 0.007 0.015 0.031 0.083 0.090 0.105 0.132 1,680 323 191 29 R81SO - Davis NF-1 0.000 0.003 0.015 0.026 0.043 0.066 0.075 0.088 0.145 2,664 421 79 6 R82SO - Davis NF+0.02-1 0.000 0.001 0.013 0.026 0.047 0.080 0.091 0.123 0.203 2,160 471 218 56 R83SO - Davis Dry NF+0.02-1D 0.000 0.002 0.015 0.030 0.055 0.089 0.104 0.126 0.155 2,640 721 378 163 R83SO - Davis Wet NF+0.02-1W 0.000 0.002 0.015 0.030 0.054 0.087 0.101 0.119 0.138 2,640 698 359 140 R84SO - Davis Dry NF+0.015-1D 0.000 0.006 0.018 0.030 0.047 0.077 0.089 0.113 0.140 2,496 512 208 59 R84SO - Davis Wet NF+0.015-1W 0.000 0.006 0.018 0.029 0.046 0.075 0.089 0.110 0.159 2,496 486 193 62 R86SO - Young Dry NF×1.3-1D 0.000 0.003 0.013 0.024 0.047 0.089 0.107 0.137 0.206 2,568 597 345 175 R86SO - Young Wet NF×1.3-1W 0.000 0.003 0.013 0.023 0.046 0.087 0.101 0.129 0.198 2,568 573 323 136 SORGHUMA82SG - Dekalb NF+0.10-1 0.000 0.001 0.010 0.023 0.055 0.145 0.160 0.185 0.223 2,040 599 557 516 WHEATA82WH - Abe NF+0.03-1 0.000 0.002 0.015 0.027 0.047 0.079 0.094 0.113 0.149 1,344 300 130 43 A82WH - Arthur-71 NF+0.06-1 0.000 0.002 0.015 0.027 0.053 0.109 0.121 0.144 0.170 1,344 373 293 186 A83WH - Abe NF+0.06-1 0.000 0.004 0.019 0.032 0.054 0.108 0.123 0.159 0.186 1,296 365 295 186 A83WH - Arthur-71 NF+0.06-1 0.000 0.004 0.019 0.032 0.054 0.108 0.123 0.159 0.186 1,296 365 295 186 BTI82WH - VONA NF-1 0.000 0.011 0.025 0.034 0.042 0.057 0.064 0.072 0.098 1,464 114 2 0 BTI83WH - VONA NF-1 0.000 0.006 0.021 0.036 0.049 0.071 0.083 0.097 0.116 864 165 51 4 

5-108
Table 5-14 (cont’d). Summary of Ozone Exposures That Are Closest to Those Pred

20% Yield Reduction per SUM06 Exposure Response Models Used by

Lee et al. (1991) in Selected National Crop Loss Assessment Network Experim

(Concentrations are in parts per million.)

Experimentb

Percentiles

70 90

Number

of Obs.

Number of Occurrences

≥0.06 ≥0.08 ≥0.10

Chamber Min. 10 30 50 95 99 Max 

CORNA81MA - PAG 397 NF+0.06-2 0.000 0.000 0.008 0.020 0.052 0.111 0.126 0.150 0.187 1,968 552 461 306 A81MA - Pioneer NF+0.06-2 0.000 0.000 0.008 0.020 0.052 0.111 0.126 0.150 0.187 1,968 552 461 306 COTTONR82CO - Stoneville NF-1 0.000 0.003 0.018 0.029 0.044 0.065 0.074 0.087 0.152 2,856 390 64 7 R85CO - McNair Dry NF×1.99-1D 0.000 0.003 0.012 0.024 0.052 0.117 0.154 0.221 0.291 3,000 810 609 407 R85CO - McNair Wet NF×1.33-1W 0.000 0.003 0.012 0.024 0.041 0.073 0.091 0.129 0.166 3,000 487 226 118 PEANUTR80PN - NC-6 NF+0.015-1 0.000 0.004 0.017 0.029 0.043 0.066 0.076 0.091 0.112 2,688 369 101 5 TOBACCOR83TO - McNair 944 NF+0.020-1 0.000 0.003 0.018 0.037 0.061 0.089 0.104 0.121 0.155 1,968 611 288 117 

aSee Appendix A for abbreviations and acronyms.bSeparate analyses were performed for each water stress level, dry (D) and well-watered (W).

5-109
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

but with a Second Hourly Maximum Concentration

≥0.125 ppm

AIRS Site

Percentiles

70 90

Name Min. 10 30 50 95 99 Max 

060010003 Livermore, CA 0.000 0.000 0.010 0.030 0.040 0.050 0.060 0.090 0.140 

060371301 Lynwood, CA 0.000 0.000 0.010 0.020 0.030 0.050 0.070 0.100 0.140 060374002 Long Beach, CA 0.000 0.010 0.020 0.020 0.030 0.050 0.060 0.080 0.160 060375001 Hawthorne, CA 0.000 0.000 0.020 0.030 0.040 0.060 0.060 0.080 0.190 060830008 Santa Barbara, CA 0.000 0.010 0.020 0.030 0.040 0.050 0.060 0.080 0.190 060830010 Santa Barbara, CA 0.000 0.010 0.020 0.030 0.040 0.050 0.060 0.080 0.220 060833001 Santa Barbara County, CA 0.000 0.010 0.020 0.030 0.040 0.050 0.060 0.080 0.140 090010113 Bridgeport, CT 0.000 0.002 0.011 0.022 0.033 0.048 0.059 0.091 0.156 090091123 New Haven, CT 0.000 0.003 0.010 0.019 0.029 0.045 0.056 0.091 0.156 220191003 Westlake, LA 0.000 0.003 0.013 0.022 0.033 0.052 0.061 0.082 0.137 220330003 Baton Rouge, LA 0.000 0.001 0.009 0.021 0.034 0.059 0.069 0.094 0.168 220330004 Baton Rouge, LA 0.000 0.002 0.008 0.016 0.028 0.047 0.057 0.078 0.138 220331001 East Baton Rouge, LA 0.000 0.003 0.012 0.022 0.034 0.056 0.066 0.092 0.171 220470002 Iberville Parish, LA 0.000 0.005 0.014 0.023 0.034 0.057 0.068 0.093 0.149 220770001 New Roads, LA 0.000 0.001 0.011 0.021 0.033 0.052 0.062 0.083 0.141 230052003 Cape Elizabeth, ME 0.001 0.017 0.027 0.034 0.042 0.055 0.064 0.093 0.146 471630009 Kingsport, TN 0.001 0.001 0.005 0.017 0.032 0.054 0.062 0.078 0.125 481410027 El Paso, TX 0.000 0.010 0.020 0.030 0.040 0.050 0.060 0.080 0.260 481990002 Kountze, TX 0.000 0.000 0.010 0.020 0.030 0.050 0.060 0.080 0.130 482010024 Harris County, TX 0.000 0.000 0.010 0.020 0.030 0.060 0.070 0.110 0.230 482010062 Houston, TX 0.000 0.000 0.010 0.020 0.030 0.050 0.070 0.110 0.170 482011034 Houston, TX 0.000 0.000 0.010 0.010 0.030 0.050 0.060 0.100 0.220 482011037 Houston, TX 0.000 0.000 0.010 0.010 0.030 0.050 0.060 0.110 0.250 490350003 Salt Lake County, UT 0.000 0.001 0.008 0.029 0.042 0.056 0.062 0.083 0.125 

490353001 Salt Lake City, UT 0.000 0.002 0.014 0.029 0.041 0.053 0.061 0.079 0.140 

5-110
Table 5-16. Summary of Percentiles for Ozone Monitoring Sites in 1989

(April Through October) with a Maximum Three-Month SUM06 Value

≥ 24.4 pp

but with a Second Hourly Maximum Concentration <0.125 ppm

AIRS Site

Percentiles

70 90

Maxim

Uncorr

SUM06 (

Name Min. 10 30 50 95 99 Max 

040132004 Scottsdale, AZ 0.000 0.006 0.018 0.031 0.045 0.062 0.071 0.084 0.107 3

060070002 Chico, CA 0.000 0.010 0.020 0.030 0.040 0.060 0.070 0.080 0.100 3060170009 South Lake Tahoe, CA 0.000 0.020 0.030 0.040 0.050 0.060 0.070 0.080 0.100 4060430004 Yosemite National Park, CA 0.000 0.008 0.022 0.035 0.049 0.065 0.072 0.083 0.111 3060710006 San Bernardino County, CA 0.000 0.020 0.040 0.050 0.060 0.070 0.080 0.090 0.100 7061011002 Yuba City, CA 0.000 0.000 0.020 0.030 0.040 0.060 0.070 0.080 0.100 2120094001 Cocoa Beach, FL 0.002 0.017 0.024 0.032 0.042 0.059 0.068 0.077 0.094 2170190004 Champaign, IL 0.000 0.008 0.020 0.029 0.039 0.065 0.072 0.078 0.088 3170491001 Effingham County, IL 0.000 0.009 0.023 0.036 0.046 0.063 0.070 0.081 0.104 2180970042 Indianapolis, IN 0.001 0.006 0.021 0.034 0.046 0.063 0.072 0.085 0.103 2240030014 Anne Arundel, MD 0.000 0.006 0.021 0.032 0.045 0.064 0.073 0.090 0.120 2240053001 Essex, MD 0.000 0.002 0.010 0.024 0.038 0.059 0.069 0.089 0.121 2310550032 Omaha, NE 0.002 0.021 0.030 0.037 0.047 0.062 0.067 0.075 0.098 2350431001 Sandoval County, NM 0.000 0.010 0.020 0.030 0.040 0.060 0.060 0.070 0.090 2360310002 Essex County, NY 0.016 0.033 0.042 0.050 0.056 0.067 0.073 0.086 0.106 4370270003 Lenoir, NC 0.000 0.007 0.019 0.032 0.045 0.062 0.067 0.078 0.092 2370810011 Guilford County, NC 0.004 0.010 0.023 0.034 0.046 0.063 0.070 0.083 0.113 2371470099 Farmville, NC 0.000 0.010 0.023 0.034 0.044 0.062 0.070 0.083 0.100 2390030002 Allen County, OH 0.000 0.007 0.022 0.032 0.043 0.060 0.068 0.086 0.107 2391510016 Canton, OH 0.000 0.008 0.019 0.030 0.042 0.060 0.070 0.088 0.110 2420070003 New Brighton, PA 0.000 0.008 0.021 0.032 0.043 0.062 0.070 0.087 0.102 2420770004 Allentown, PA 0.000 0.003 0.016 0.028 0.039 0.060 0.070 0.087 0.102 2470090101 Smoky Mountain National Park,

TN

0.000 0.025 0.036 0.044 0.053 0.065 0.070 0.081 0.098 3

510130020 Arlington County, VA 0.000 0.001 0.010 0.023 0.037 0.059 0.071 0.088 0.116 2510610002 Fauquier County, VA 0.000 0.009 0.021 0.033 0.045 0.061 0.069 0.084 0.122 2511870002 Shenandoah National Park

(Dickey Ridge), VA

0.004 0.027 0.037 0.045 0.054 0.065 0.071 0.082 0.100 5

550270001 Horicon, WI 0.002 0.019 0.029 0.037 0.047 0.062 0.070 0.088 0.111 2

551390007 Oshkosh, WI 0.002 0.016 0.028 0.038 0.048 0.063 0.070 0.084 0.121 2

5-111
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 (SUM00), for several ranges of peak concentrations (Reich, 1987).

5-112
Figure 5-16. Percent reduction in net photosynthesis (Pn) and biomass growth of

coniferous species in relation to (A) total exposure (SUM00) and

(B) estimated total ozone uptake (Reich, 1987).

in O3 uptake. Imputed O3 uptake calculated as the product of SUM00 and mean diffusive

conductance (ks) for each species better correlated with Pn and growth than did SUM00.

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 SUM00 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 SUM00 (Figure 5-19). Seasonal sum of hourly

5-113
Figure 5-17.

Percent reduction in net photosynthesis (Pn) and biomass growth

of hardwood species in relation to (A) total exposure (SUM00) 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

saccharum) 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 SUM00, 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 SUM00

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
Figure 5-18. Percent reduction in net photosynthesis (Pn) and biomass growth of

agricultural crops in relation to (A) total exposure (SUM00) 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 SUM00, 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 SUM00 index did not appear to perform adequately. Using air quality

data, Lefohn et al. (1989) showed that the magnitude of the SUM00 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 SUM00

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 SUM00 values in the CF chamber, although

5-116
Figure 5-19.

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 SUM00 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 SUM00 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 SUM00 index was unable to capture the occurrence of the higher hourly

average concentrations in the ambient treatments. The authors indicated that the SUM00

index was inadequate because of the observed inconsistencies of the SUM00 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 SUM00 index does not describe properly the occurrence of the

higher hourly average concentrations.

5-117
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
Figure 5-21. A comparison between the resulting cumulative frequencies for the exposure

parameters, sum of all hourly average concentrations (SUM00) and the

sigmoidally weighted integrated exposure index, W126. The ozone data were

collected in 1981 at a site located in the Mark Twain National Forest, MO,

EPA AIRS site number 291230001 (Lefohn et al., 1989).

another. This statement does not provide any insight concerning whether the magnitude of a

SUM06 or a W126 value, calculated using monitoring data collected at a specific site over a

specified time interval (i.e., months and hours of the day), is associated more with mid-level

than high hourly average concentrations. The contribution of each range of hourly average

concentrations to the magnitude of the cumulative index value is related to the distribution of

the hourly average concentrations measured at the site.

5.5.2.5 Comparison of Effects on Vegetation of Cumulative "Peak" Versus "MidLevel" Ozone Exposures

Not all studies dealing with the response of crop plants to O3 exposures agree with

the conclusions emphasized in the foregoing pages of this section that "higher" hourly

concentrations should be given greater weight than "lower" concentrations. Based on their

studies, Tonneijck (1994), Krupa et al., (1993, 1994, 1995), Grünhage et al. (1993b), and

5-117
Grünhage and Jäger (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; Grünhage et al., 1993b; Grünhage and Jäger,

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 "midrange", 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 Conditionsa

Ozone Concentrations That May Produce 5% (20%) Injury (ppm):

Exposure time (h) Sensitive Plantsb Intermediate Plantsc Less Sensitive Plantsd

0.5 0.35 - 0.50

(0.45 - 0.60)

0.55 - 0.70

(0.65 - 0.85)

≥0.70 (0.85)

1.0 0.15 - 0.25

(0.20 - 0.35)

0.25 - 0.40

(0.35 - 0.55)

≥0.40 (0.55)

2.0 0.09 - 0.15

(0.13 - 0.25)

0.15 - 0.25

(0.25 - 0.35)

≥0.30 (0.40)

4.0 0.04 - 0.09

(0.10 - 0.15)

0.10 - 0.15

(0.15 - 0.30)

≥0.25 (0.35)

8.0 0.02 - 0.04

0.06 - 0.12

0.07 - 0.12

0.13 - 0.25

≥0.20 (0.30)

a

The concentrations in parenthesis are for the 20% injury level.

b

Examples of sensitive plants: oat, bean, and tobacco.

c

Examples of intermediate plants: legumes, clover, and wheat.

d

Examples 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 × duration [C × 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
Table 5-18. A Summary of Studies Reporting Effects of Peaks or Mid-Range Conce

Species Concentration (ppm) Exposure Pattern Exposure Duration Methodology Resp

Kidney Bean cv.California DarkRed Phaseolusvulgaris L.

0.280.20.1-0.50.14-0.7

UHbULcSimulated ambient:diurnal, variablediurnal, variable

One 6-h (0915-1515 h)exposure/week1/3 plants: at 6 weeks;1/3 plants: at 6 and 7 weeks;1/3 at 6, 7, and 8 weeks plantsharvested at end of exposure period

8 CSTR, inpots in soil

Greatesat 6 and7 weeksenesce8 week

Kidney Bean cv.California DarkRedPhaseolusvulgaris L.

0.30.40.06-0.30.08-0.4

UL "square wave"UH "square wave"Ambient, variableAmbient, variable

One 2-h (1051-1309 h)exposure/week for 6, 7, or 8 weeksOne 6-h (900-1500) exposure/week1/3 plants: at 6 weeks;1/3 plants: at 6 and 7 weeks;1/3 at 6, 7, and 8 weeks plantsharvested at end of exposure period

8 negativepressurechambers, inpots in soil

Square vs. ambdifferenresponsdose eq

Kidney Bean cv.California DarkRed Phaseolusvulgaris L.

1. 0.122. 0.36 peak, max

1-h avg = 0.28

3. 0.244. 0.24 1-h peak

UniformNarrow-based triangleBroad based pyramidTrapezoid

7 weeks3 days/week5 h daily

CSTR,15 plantsper chamber

Least inprofiles Greates3 > 1 bthan 2 

Alfalfa, Medicagosativa L.

Daily 7-h mean:0.063, 0.064,0.083, 0.084,peaks

≈ 0.2

7-h mean0.074,0.094, 0.099,peaks

≈ 0.10-0.15

Daily for 30 days:low episodic,high episodic,peaks at 1400-1500 h30 days:low daily peak,high daily peak,peaks at 1400 h

0900-1600 h;30 days × 5

8 OTC, inpots;alfalfa cut3× duringexposureperiod

Growth more founder eexposurGrowth less thaepisodicexposur

5-120
Table 5-18 (cont’d). A Summary of Studies Reporting Effects of Peaks or

Mid-Range Concentrationsa

Species Concentration (ppm) Exposure Pattern Exposure Duration Methodology Response 

Tobacco cv. Bel W3Nicotiana tobacum L.

Yearly mean range1979-88: 0.025-0045Weekly mean range1988: 0.01-0.055

Ambient, daily notgivenAmbient, daily notgiven

1 week1 week

4 pots in soil infield: 17 locations4 pots in soil infield: 17 locations

Foliar injuryFoliar injury

Tobacco cv. Bel W3,Nicotiana tobacum L.Bean, Phaseolusvulgaris L. cv.Stratego cv. Groffy

Years, 1979-19830.005-0.15, combinedin classes of 10 μg/m3

Years 1982-19830.015-0.075, combinedin classes of μg/m3

Ambient, daily notgivenAmbient, daily notgiven

1 week1 week

4 pots in soil infield: 40 locations4 pots in soil infield: 10 locations

Foliar injuryFoliar injury Stratego

Tobacco cv. Bel W3Bel B Nicotianatobacum L.

0.06-0.1000.06-0.103

Montague weeklymaxMt. Equinox weeklymax

1 week1 week

OTC (CF); OTC(NF); ambient6 plants in pots inpeat and Perlite6 plants in pots inpeat and Perlite

Foliar injury bottommostexpanded lea

aSee Appendix A for abbreviations and acronyms.bUH = Uniform high.cUL = Uniform low.

5-121
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
Figure 5-22. Fumigation schedule of uniform and simulated ambient ozone (O3)

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
Figure 5-23. Fumigation schedule of uniform and simulated ambient ozone (O3)

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
Figure 5-24. Experimental ozone exposure profiles.

Source: Musselman et al. (1994).

5-125
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
Figure 5-25. Ozone exposure profiles for the 1983 season.

Source: Hogsett et al. (1985b).

5-127
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 μg m3 (≈0.04 ppm), and cumulative dose of

hourly values >120 μg m3 (≈0.06 ppm). No peak concentrations were listed. The highest

effect intensity, a mean O3 concentration of 100 μg/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
Figure 5-26. (A) Mean foliar injury on tobacco Bel W3 and mean ozone (O3)

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 oxidantmonitoring 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
Figure 5-27. (A) Maximum foliar injury (percent of leaf area affected) on tobacco Bel W3

in relation to ozone (O3) concentrations expressed in classes of 10 μg/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
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 μg/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 μg/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 μg/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 fourleaf 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
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 overmature 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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Figure 5-28. (A) Summary hourly ambient ozone (O3) 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).

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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 μg 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 (Grünhage and Jäger, 1994b).

Under ambient conditions, however, exposure indices obtained from the chamber studies

frequently yield unsatisfactory results (Grünhage and Jäger, 1994a). Grünhage and Jäger

(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 (Grünhage 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.

Grünhage and Jäger (1994a,b) and Grünhage 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. Grünhage and Jäger (1994b) fit this

mathematical model to Bel W3 tobacco data to describe a dose-response relationship for leaf

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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. Grünhage

and Jäger (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., Lösch 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, Grünhage and Jäger (1994a,b) and Grünhage et al. (1993a)

proposed an ambient O3 exposure potential for characterizing O3 uptake and related it to the

DLA of Bel W3 tobacco. Grünhage and Jäger (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

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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 peakweighted, 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;

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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

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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 Concentrationsa,b

Parameters for Weibull Model

Concentration for

Predicted Yield

Losses of:

Crop α^ σ^ c

^ CFc 10%d 30%d

LEGUME CROPS

Soybean, Corsoy

Soybean, Davis (81)

Soybean, Davis (CA-82)e

Soybean, Davis (PA-82)e

Soybean, Essex (81)

Soybean, Forrest (82-I)

Soybean, Williams (81)

Soybean, Williams (82-I)

Soybean, Hodgson

Bean, Kidney (FP)f

Peanut, NC-6

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

0.133

0.128

0.12/

0.103

0.187

0.171

0.211

0.162

0.138

0.120

0.111

1.952

0.872

2.144

4.077

1.543

2.752

1.100

1.577

1.000

1.171

2.249

0.022

0.025

0.019

0.019

0.014

0.017

0.014

0.017

0.017

0.019

0.025

0.048

0.038

0.048

0.059

0.048

0.076

0.039

0.045

0.032

0.033

0.046

0.082

0.071

0.081

0.081

0.099

0.118

0.093

0.088

0.066

0.063

0.073

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

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

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

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

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

0.059

0.056

0.039

0.028

0.088

0.064

0.099

0.093

0.095

0.075

0.133

0.108

0.121

0.095

0.094

0.067

0.041

0.127

0.107

0.127

0.135

0.126

0.111

0.175

0.186

0.161

FIBER CROPS

Cotton, Acala SJ-2 (81-I)

Cotton, Acala SJ-2 (82-I)

Cotton, Stoneville

5,546.00

5,872.00

3,686.00

0.199

0.088

0.112

1.228

2.100

2.577

0.018

0.012

0.026

0.044

0.032

0.047

0.096

0.055

0.075

HORTICULTURAL

CROPS

Tomato, Murrieta (81)

Tomato, Murrieta (82)

Lettuce, Empire (T)

Spinach, America (T)

Spinach, Hybrid (T)

Spinach, Viroflay (T)

Spinach, Winter Bloom (T)

32.90

32.30

1,245.00

21.20

36.60

41.10

20.80

0.142

0.082

0.098

0.142

0.139

0.129

0.127

3.807

3.050

1.220

1.650

2.680

1.990

2.070

0.012

0.012

0.043

0.024

0.024

0.024

0.024

0.079

0.040

0.053

0.046

0.043

0.048

0.049

0.108

0.059

0.075

0.082

0.082

0.080

0.080

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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 Concentrationsa,b

Parameters for Weibull Model

Concentration for

Predicted Yield

Losses of:

Crop α^ σ^ c

^ CFc 10%d 30%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

a

Data 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.

b

All estimates of σ^ 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 estimated c 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.

c

The ozone (O3) concentration in the charcoal-filtered (CF) chambers expressed as a 7-h seasonal mean

concentration.

d

The 7-h seasonal mean O3 concentration (parts per million) that was predicted to cause a 10 or 30% yield loss

(compared to CF air).

e

CA and PA refer to constant and proportional O3 addition. f

Only 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
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 exposureresponse 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
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
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 exposureresponse 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 exposureresponse 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
Table 5-20. Summary of Ozone Exposure Indices Calculated for

3- or 5-Month Growing Seasons from 1982 to 1991a

3 mo (June-August)

No. of

HDM2c

ppm

M7

ppm

SUM00

ppm h

SUM06

ppm h

SIGMOID

ppm h

Year Sitesb Mean CVd Mean CV Mean CV Mean CV Mean CV

1982 99 0.114 23.7% 0.052 18.7% 82.9 19.1% 26.8 68.8% 26.3 56.7%

1983 102 0.125 24.9% 0.056 21.9% 86.1 22.1% 34.5 58.1% 33.0 52.3%

1984 104 0.117 24.6% 0.052 18.2% 84.1 19.9% 27.7 58.4% 27.4 47.9%

1985 117 0.117 24.6% 0.052 17.1% 84.6 18.0% 27.4 59.6% 27.4 47.6%

1986 123 0.115 21.8% 0.052 19.1% 85.3 18.0% 27.7 65.0% 27.7 51.8%

1987 121 0.119 22.9% 0.055 17.6% 86.9 17.3% 31.2 56.4% 30.4 46.8%

1988 139 0.129 21.3% 0.060 17.8% 97.6 19.6% 45.2 46.8% 42.9 42.4%

1989 171 0.105 23.1% 0.051 17.5% 86.4 19.9% 24.8 78.7% 25.8 59.4%

1990 188 0.105 21.6% 0.053 18.3% 85.7 21.0% 25.8 76.2% 26.6 59.2%

1991 199 0.106 22.0% 0.054 18.4% 87.7 21.3% 28.3 74.2% 28.9 59.5%

Among Years 0.113 11.1% 0.054 10.0% 87.0 9.9% 29.5 42.1% 29.4 31.0%

5 mo (May-September)

No. of

M7

ppm

SUM00

ppm h

SUM06

ppm h

SIGMOID

ppm h

Year Sites Mean CV Mean CV Mean CV Mean CV

1982 88 0.048 20.6% 122.9 22.3% 37.3 70.9% 37.1 57.8%

1983 87 0.051 22.1% 129.6 24.4% 44.4 61.9% 43.8 52.7%

1984 95 0.048 18.0% 126.2 19.1% 36.7 60.8% 37.6 46.9%

1985 114 0.048 18.4% 124.5 19.4% 36.2 63.8% 37.0 50.3%

1986 118 0.048 20.3% 123.3 21.4% 34.9 70.7% 35.6 55.7%

1987 116 0.050 20.3% 128.7 20.4% 42.2 62.0% 41.8 50.3%

1988 134 0.054 18.7% 141.7 22.0% 58.0 50.5% 55.6 45.0%

1989 158 0.047 18.6% 127.8 22.5% 32.7 87.8% 35.2 64.1%

1990 172 0.049 19.8% 129.4 22.7% 34.6 82.7% 37.0 62.1%

1991 190 0.050 19.8% 130.6 23.6% 36.8 80.7% 38.8 62.9%

Among Years 0.049 9.8% 129.0 9.9% 38.7 42.5% 39.6 29.8%

a

Updated 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. b

Indicates 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.

c

The 2HDM index is calculated for sites with at least 3 mo of available data. SUM00, 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.

d

CV = coefficient of variation.

Source: Tingey et al. (1991).

5-145
Table 5-21. Comparison of Exposure-Response Curves Calculated

Using the 3-Month, 24-Hour SUM06 Values for

54 National Crop Loss Assessment Network Casesa

Wiebull/Linwear Model

Parametersc

3 mo 24-h SUM06f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Barley (Linear) CM-72 Dry 7,741.1 −4.412 1,215 0.12 175.5 526.4

Barley (Linear) CM-72 Wet 8,776.6 15.485 1,175 NA 250.0 250.0

Corn (L) Pio 9,627.4 92.61 2.823 680 0.93 41.7 64.3

Corn (L) Pag 10,730.1 94.36 4.316 1,248 0.80 56.0 74.3

Cotton (L) Acala Dry 6,465.0 92.59 2.361 1,097 0.45 35.7 59.8

Cotton (L) Acala Wet 9,808.0 71.17 1.997 521 0.96 23.1 42.5

Cotton (L) Acala Dry 7,009.8 83.78 1.849 949 0.80 24.8 48.0

Cotton (L) Acala Wet 7,858.8 78.01 1.311 937 0.85 14.0 35.5

Cotton (L,

Linear)

Acala Dry 5.693 −0.0011 104 0.06 94.9 321.3

Cotton (L,

Linear)

Acala Wet 5.,883 −0.0017 90 0.20 60.3 204.0

Cotton Stoneville 3,576.1 94.6 2.012 226 0.91 30.9 56.7

Cotton McNair Dry 3,698.8 165.81 2.778 342 0.46 73.8 114.4

Cotton McNair Wet 4,811.0 117.02 1.534 366 0.89 27.0 59.7

Kidney Bean California

Light Red

2,488.2 27.41 3.885 333 0.72 15.4 21.0

Kidney Bean (L) California

Light Red

2,484.3 44.24 2.691 397 0.71 19.2 30.2

Lettuce (T) Empire 7,196.6 54.87 5.512 613 0.74 36.5 45.5

Peanut (L) NC-6 6,402.5 100.12 2.226 351 0.97 36.4 63.0

Potato Norchip 5,900.7 93.84 1.000 742 0.63 9.9 33.5

Potato Norchip 5,755.6 79.26 1.654 675 0.49 20.3 42.5

Sorghum Dekalb 8,046.2 178.05 2.338 441 0.48 68.0 114.6

Soybean Corsoy 2,652.6 57.1 1.726 166 0.91 15.5 31.4

Soybean Corsoy 1,891.7 65.21 5.160 282 0.63 42.2 53.4

Soybean Amsoy 1,907.2 75.91 2.739 390 0.41 33.4 52.1

Soybean Pella 2,619.9 174.13 1.000 311 0.51 18.3 62.1

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 Casesa

Wiebull/Linwear Model

Parametersc

3 mo 24-h SUM06f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Soybean Williams 2,368.4 146.37 1.000 527 0.27 15.4 52.2

Soybean Corsoy Dry 2,229.8 92.0 9.593 193 0.16 72.8 82.6

Soybean Corsoy Wet 2,913.8 311.04 1.527 330 0.38 71.3 158.4

Soybean Corsoy Dry 3,528.1 103.83 15.709 400 0.55 90.0 97.2

Soybean Corsoy Wet 4,905.0 117.98 3.590 401 0.80 63.0 88.5

Soybean Corsoy Dry 5,676.1 97.46 1.000 508 0.81 10.3 34.8

Soybean Corsoy Wet 5,873.9 65.73 1.319 512 0.89 11.9 30.1

Soybean Williams Dry 6,305.2 99.18 1.456 389 0.87 21.1 48.8

Soybean Williams Wet 7,338.4 78.71 1.344 377 0.94 14.8 36.5

Soybean Hodgson 2,052.4 79.97 1.000 361 0.78 8.4 28.5

Soybean Davis 3,929.7 131.57 1.000 524 0.64 13.9 46.9

Soybean Davis 4,815.5 85.71 1.734 346 0.87 23.4 47.3

Soybean Davis Dry 2,007.1 542.36 1.000 556 0.04 57.1 193.4

Soybean Davis Wet 4,568.0 158.57 1.539 495 0.61 36.8 81.2

Soybean Davis Dry 5,775.6 90.18 3.348 920 0.55 46.0 66.3

Soybean Davis Wet 8,082.7 113.89 1.442 927 0.71 23.9 55.7

Soybean Young Dry 5,978.8 183.63 1.448 244 0.93 38.8 90.1

Soybean Young Wet 7,045.0 145.63 1.277 424 0.93 25.0 65.0

Tobacco (L) McNair 5,177.4 172.55 1.186 306 0.81 25.9 72.3

Turnip (T) Just Right 12.7 25.68 1.806 0.810 0.96 7.4 14.5

Turnip (T) Purple Top 5.7 29.26 1.437 0.590 0.92 6.1 14.3

Turnip (T) Shogon 4.4 29.18 1.548 0.660 0.81 6.8 15.0

Turnip (T) Tokyo Cross 11.7 27.83 2.142 3.250 0.78 9.7 17.2

Wheat Abe 5,149.8 52.89 3.077 399 0.90 25.5 37.8

Wheat Arthur 4,455.8 60.87 2.176 264 0.92 21.6 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 Casesa

Wiebull/Linwear Model

Parametersc

3 mo 24-h SUM06f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Wheat Roland 5,028.9 52.32 1.173 405 0.91 7.7 21.7

Wheat Abe 6,043.1 47.39 7.711 226 0.74 35.4 41.5

Wheat Arthur 5,446.9 72.34 2.462 349 0.57 29.0 47.6

Wheat Vona 5,384.0 27.74 1.000 608 0.88 2.9 9.9

Wheat Vona 4,451.0 33.5 1.818 654 0.64 9.7 19.0

a

See Appendix A for abbreviations and acronyms.

b

Wet refers to experiments conducted under well-watered conditions, whereas dry refers to experiment

conducted under some controlled level of drought stress.

c

For 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.

d

The root mean square error, based on individual plot means.

e

Multiple correlation coefficient (R2) measures the proportion of total variation about the mean response

explained by the regression on individual plot means.

f

The 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 exposureresponse 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 Casesa

Weibullc

24-h W126f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Barley CM-72 Dry 8,133.2 1,109.6 1.000 1,214 0.13 116.9 395.8

Barley CM-72 Wet 8,927.2 57,439.6 1.000 1,175 NA 6,051.9 20,487.3

Corn (L) Pio 9,605.0 92.9 2.594 650 0.93 39.0 62.4

Corn (L) Pag 10,686.7 94.5 4.190 1,253 0.80 55.2 73.9

Cotton (L) Acala Dry 6,482.8 89.9 1.949 1,075 0.47 28.3 53.0

Cotton (L) Acala Wet 9,817.3 66.6 1.603 514 0.96 16.4 35.0

Cotton (L) Acala Dry 7,022.7 81.3 1.540 948 0.80 18.8 41.6

Cotton (L) Acala Wet 7,927.1 74.7 1.070 943 0.85 9.1 28.5

Cotton (L) Acala Dry 310.1 174.1 2.189 104 0.06 62.3 108.7

Cotton (L) Acala Wet 393.2 582.6 1.000 90 0.20 61.4 207.8

Cotton Stoneville 3,592.1 94.1 1.582 223 0.91 22.7 49.1

Cotton McNair Dry 3,700.9 174.1 2.430 344 0.45 68.9 113.9

Cotton McNair Wet 4,817.6 113.5 1.410 360 0.89 23.0 54.6

Kidney bean California

Light Red

2,484.7 28.0 3.706 332 0.72 15.3 21.2

Kidney bean (L) California

Light Red

2,475.2 44.2 2.353 401 0.70 17.0 28.5

Lettuce (T) Empire 7,197.4 54.6 4.921 614 0.74 34.6 44.3

Peanut (L) NC-6 6,386.0 97.4 1.905 370 0.96 29.9 56.7

Potato Norchip 5,867.2 96.3 1.000 754 0.62 10.1 34.3

Potato Norchip 5,777.9 113.9 1.299 675 0.48 20.1 51.5

Sorghum Dekalb 8,049.7 205.9 1.963 439 0.48 65.4 121.8

Soybean Corsoy 2,660.3 58.8 1.455 169 0.91 12.5 28.9

Soybean Corsoy 1,895.6 63.3 4.032 280 0.63 36.2 49.0

Soybean Amsoy 1,926.1 79.0 1.977 390 0.41 25.3 46.9

Soybean Pella 2,602.4 161.5 1.000 314 0.50 17.0 57.6

Soybean Williams 2,341.8 138.6 1.000 533 0.25 14.6 49.4

Soybean Corsoy Dry 2,229.3 88.2 8.632 192 0.16 67.9 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 Casesa

Weibullc

24-h W126f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Soybean Corsoy Wet 2,929.7 470.2 1.128 329 0.39 64.0 188.6

Soybean Corsoy Dry 3,533.5 113.2 11.095 403 0.54 92.4 103.1

Soybean Corsoy Wet 4,909.5 126.5 2.803 405 0.80 56.7 87.6

Soybean Corsoy Dry 5,597.1 95.7 1.000 526 0.80 10.1 34.1

Soybean Corsoy Wet 5,884.8 65.6 1.139 515 0.88 9.1 26.6

Soybean Williams Dry 6,314.1 106.3 1.243 391 0.87 17.4 46.4

Soybean Williams Wet 7,352.3 80.7 1.162 368 0.95 11.6 33.2

Soybean Hodgson 2,044.6 76.2 1.000 361 0.78 8.0 27.2

Soybean Davis 3,837.6 130.3 1.000 530 0.63 13.7 46.5

Soybean Davis 4,810.8 87.5 1.494 352 0.86 19.4 43.9

Soybean Davis Dry 1,992.3 537.6 1.000 558 0.03 56.6 191.7

Soybean Davis Wet 4,595.4 170.9 1.253 496 0.61 28.4 75.1

Soybean Davis Dry 5,770.1 90.6 2.796 928 0.54 40.5 62.7

Soybean Davis Wet 8,101.3 118.2 1.220 939 0.70 18.7 50.8

Soybean Young Dry 5,994.2 199.8 1.251 244 0.93 33.1 87.7

Soybean Young Wet 7,075.0 149.7 1.133 418 0.93 20.5 60.2

Tobacco (L) McNair 5,223.9 179.8 1.018 291 0.83 19.7 65.3

Turnip (T) Just Right 12.7 24.1 1.473 1.0 0.96 5.2 12.0

Turnip (T) Purple Top 5.8 28.2 1.155 1 0.92 4.0 11.6

Turnip (T) Shogon 4.4 28.2 1.174 1 0.82 4.1 11.7

Turnip (T) Tokyo Cross 11.7 26.8 1.710 3 0.78 7.2 14.7

Wheat Abe 5,138.1 53.3 2.602 407 0.89 22.4 35.8

Wheat Arthur 4,467.4 63.8 1.747 264 0.92 17.6 35.4

Wheat Rol 5,074.4 51.2 1.000 397 0.91 5.4 18.3

Wheat Abe 6,042.8 48.5 5.843 225 0.75 33.0 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 Casesa

Weibullc

24-h W126f

Values for Yield

Losses of

Species Cultivar Moistureb A B C RMSEd R2

e

10% 30%

Wheat Arthur 5,440.0 76.1 2.100 349 0.57 26.1 46.6

Wheat Vona 5,300.8 25.0 1.000 679 0.85 2.6 8.9

Wheat Vona 4,462.7 32.3 1.517 665 0.63 7.3 16.4

a

See Appendix A for abbreviations and acronyms.

b

Wet refers to experiments conducted under well-watered conditions, whereas dry refers to experiments

conducted under some controlled level of drought.

c

All 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.

d

The root mean square error, based on individual plot means.

e

Multiple correlation coefficient (R2) measures the proportion of total variation about the mean response

explained by the regression on individual plot means.

f

The 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 Casesa

50th PERCENTILEb SUM06 SEc SIGMOID SE M7 SE 2HDM SE

NCLAN Data (N = 49; wet and dry)d

NCLAN Data (N = 39; wet only)

24.4

22.3

3.4

1.0

21.5

19.4

2.0

2.3

0.049

0.046

0.003

0.003

0.094

0.090

0.006

0.010

NCLAN Data (N = 54; wet and dry)e

NCLAN Data (N = 42; wet only)e

26.4

23.4

3.2

3.1

23.5

22.9

2.4

4.7

NA

NA

NA

NA

0.099

0.089

0.011

0.008

NCLAN Data (N = 10; wet)

NCLAN Data (N = 10; dry)

25.9

45.7

4.5

23.3

23.4

40.6

3.2

0.1

0.041

0.059

0.001

0.014

0.110

0.119

0.042

0.017

Cotton Data (N = 5)

Soybean Data (N = 13)

Wheat Data (N = 6)

23.6

26.2

21.3

2.3

5.4

15.2

19.3

22.6

19.3

2.3

3.6

12.7

0.041

0.044

0.061

0.001

0.005

0.018

0.066

0.085

0.098

0.032

0.013

0.059

Cotton Data (N = 5)e

Soybean Data (N = 15)e

Wheat Data (N = 7)e

30.0

23.9

25.9

12.7

6.5

10.5

27.2

22.0

21.4

12.8

8.0

9.4

NA

NA

NA

NA

NA

NA

0.075

0.088

0.097

0.012

0.008

0.028

75th PERCENTILEb

NCLAN Data (N = 49; wet and dry)

NCLAN Data (N = 39; wet only)

14.2

14.3

4.2

2.7

11.9

12.6

5.6

2.3

0.040

0.039

0.007

0.005

0.051

0.056

0.010

0.006

NCLAN Data (N = 54; wet and dry)e

NCLAN Data (N = 42; wet only)e

16.5

17.2

4.3

3.0

14.5

14.7

3.2

2.4

NA

NA

NA

NA

0.073

0.070

0.006

0.006

NCLAN Data (N = 10; wet)

NCLAN Data (N = 10; dry)

16.4

24.0

3.7

0.8

13.7

22.3

3.2

0.1

0.040

0.053

0.001

0.022

0.080

0.093

0.032

0.003

Cotton Data (N = 5)

Soybean Data (N = 13)

Wheat Data (N = 6)

21.8

14.2

11.7

5.0

0.1

2.5

17.5

12.4

10.9

2.8

0.1

2.4

0.041

0.041

0.054

0.001

0.006

0.032

0.065

0.069

0.062

0.014

0.004

0.035

Cotton Data (N = 5)e

Soybean Data (N = 15)e

Wheat Data (N = 7)e

21.1

15.3

5.1

6.0

4.1

2.6

16.7

13.4

8.5

5.7

4.1

3.4

NA

NA

NA

NA

NA

NA

0.070

0.078

0.054

0.034

0.007

0.027

a

See Appendix A for abbreviations and acronyms.

b

The numbers in parentheses are the number of cases used in deriving the various exposure levels.

c

Standard error (SE).

d

NCLAN 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.

e

24-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 Studiesa

Weibull Equations (all 54 NCLAN studies):

50th Percentileb PRYL = 1 − exp(−[SUM06/89.497]**1.84461)

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]**1.36037)

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

Percent of Crops

50% 75%

Relative 10% 26.4 16.5

Yield Loss 20% 39.7 25.5

All 22 NCLAN Soybean Cases

Percent of Crops

50% 75%

Relative 10% 25.3 19.3

Yield Loss 20% 42.3 32.1

15 Well-Watered Soybean Cases

Percent of Crops

50% 75%

Relative 10% 24.2 15.2

Yield Loss 20% 40.4 26.4

All Seven NCLAN Wheat Cases

Percent of Crops

50% 75%

Relative 10% 25.9 5.2

Yield Loss 20% 32.0 9.3

a

See Appendix A for abbreviations and acronyms.

b

50th 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 Concentrationb Duration Facilityc Variabled Effecte R

Soybean 18 or 24 ppb vs. 59 or

72 ppb 9-h mean

13 weeks, twogrowing seasons

OTC Seed yield 12.5% reduction over filtered air

averaged over cultivars. Betweencultivar differences as great asozone effect.

M

Soybean 23, 40, and 66 ppb

7-h mean

84 days OTC Seed yield 15.8 and 29% reduction over

23 ppb.

M

Soybean 97 ppb vs. 38, 23, 16,

and 23 ppb 7-h mean

Four 31-dayperiods,one growingseason

OTC

in pots

Seed yield 30 to 56% reduction over control,

most loss in mid- to late-growthstage.

H

Soybean 17 to 122 ppb 7-h mean 69 days OTC Seed yield 8% at 35 ppb to 41% at 122 ppb. KSoybean 25 and 50 ppb 7-h mean About 90 days OTC Seed yield Predicted loss of 10%. HSoybean 20 and 50 ppb 12-h mean 107 days OTC Seed yield Predicted loss of 13%. MSoybean 25 and 55 ppb 7-h mean 64, 70, and

62 days,three growingseasons

OTC Seed yield Predicted loss of 15%. H

(

Soybean 27 and 54 ppb 7-h means About 109 and

103 days, twogrowing seasons

OTC Seed yield Predicted loss of 12 and 14%. H

Soybean Filtered and nonfiltered airconcentration not reported About 125 days, two growing

seasons

OTC Seed yield No difference. J

(

Soybean 10 to 130 ppb 8 weeks,

6.8 h/day

GC Biomass Predicted reduction of 16 or 33%

at 60 and 100 ppb vs. 25 ppb.

A

Soybean 200 ppb 12 h, up to

four times

GC Shoot and

root weight

No effect at maturity. S

5-154
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 Concentrationb Duration Facilityc Variabled Effecte 

Cotton 15 to 111 ppb 12-h mean 123 days OTC Leaf, stem,

and rootweight

Up to 42% reduction in leaand stem and 61% reductioroot weights.

Cotton 10 to 90 ppb 12-h mean 102 days OTC Lint weight 40 to 71% reduction at hig

concentration determinantcultivars more susceptible.

Cotton 25 to 74 ppb 12-h mean 123 days OTC Lint weight Predicted loss of 26.2% at

74 ppb.

Cotton 22 to 44 ppb 12-h mean 124 days OTC Lint weight Predicted loss of 19% at

44 ppb.

Cotton 26 to 104 ppb 7-h mean 119 days OTC Lint weight Predicted loss of 11% at

53 ppb.

Bean, fresh 35 to 132 ppb 7-h mean 42 days OTC in pots Green pod

weight

Significant yield reduction>10% in eight lines at 63 p7-h mean.

Bean, fresh 11 to 40 ppb 12-h mean,

7 to 42 ppm h

69 days OTC Pod weight 15.5% reduction at 45 ppb

(39 ppm h).

Bean, fresh 26 to 126 ppb 7-h mean 26 days and

44 days, earlyand late inseason

OTC in pots Pod weight 3.5 to 26% reduction in

resistant and sensitive cultiat 55 to 60 ppb.

Bean, fresh 24 to 109 ppb 8-h mean 43 days 34 days,

two growingseasons

OTC Pod weight 20% reduction at 80 ppb. 

Bean, dry 15 to 116 ppb 12-h mean,

339 ppb highest hour

54 days OTC Seed yield 55 to 75% reduction at 72 

12-h mean, 198 highest ho

5-155
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 Concentrationb Duration Facilityc Variabled Effecte 

Bean, dry 10 to 50 ppb 7-h mean 86 days OTC Seed weight 26 to 42% reduction 

38 to 50 ppb.

Bean, dry 300 ppb 3 h, two exposures GC Dry weight Growth response dete

if exposure separated 3 to 5 days.

Wheat, spring 14 to 46 ppb 24-h mean 79, 92, and 79 days

in three growingseasons

OTC Seed weight 13% reduction at 40 

Wheat, spring 21.6 to 80 and

24.6 to 93.5 ppm h

82 and 88 days intwo growing seasons

OTC Seed weight 48 to 54% reduction 

80 and 93.5 ppm h.

Wheat, spring 3 to 56 ppb 7-h mean 61 and 55 days in

two growing seasons

OTC Seed weight 7% reduction at 15 a

22 ppb.

Wheat, spring 8 to 101 and 20 to

221 ppb 8-h mean

118 and 98 days intwo growing seasons

OTC Seed weight 10% reduction at 17 

23 ppb.

Wheat, spring 0 to 38 ppb 8-h mean Entire growing

season

OTC Seed weight 5% reduction at 38 p

Wheat, spring 17 to 77 ppb 7-h mean 90 and 87 days in

two growing seasons

OTC Seed weight 9.5 to 11.6 reduction 

37 and 45 ppb.

Wheat, spring 25 to 75 ppb 8-h mean 40 days OTC Total weight Reductions at 75 ppbWheat, spring 6 to 10 ppb, 6 h/day 21 days GC Shoot dry

weight

Decreased 35 to 60% 101 ppb in low and hlight.

Wheat, spring 10 to 125 ppb,

6 h/day

21 and 17 days GC Top dry

weight

Reduced by up to 35

5-156
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 Concentrationb Duration Facilityc Variabled Effecte 

Wheat, winter 11 to 42 ppb

14-week mean

109 days OTC Seed weight No effect. 

Wheat, winter 30 to 93 ppb

4-h mean

39 and 40 days intwo growing seasons5 days/week 4 h/day

OTC Seed weight Exposures >60 ppb durin

anthesis reduce yield.

Wheat, winter 27 to 96 ppb

7-h mean

36 days OTC Seed weight/

head

50% reduction at 96 ppb. 

Wheat, winter 22 to 96 ppb

7-h mean

65 days and 36 daysin two growingseasons

OTC Seed weight 33 and 22% reductions at

42 and 54 ppb, respective

Wheat, winter 23 to 123 ppb

4 h/day

5 days at anthesis OTC Seed weight Up to 28% reduction. 

Barley, spring 6 to 45 ppb

7-h mean

96 days OTC Seed weight No effect. 

Barley, spring 0.6 to 27 ppb

monthly mean

Growing season OTC Seed weight No effect. 

Barley, spring 0.8 to 83 ppb

8-h mean

97, 108, and 98 daysin three growingseasons

OTC in pots Seed weight 0 to 13% reduction at

highest.

Rape, spring 25 to 75 ppb

8-h mean

31 days OTC Premature

senescence

Increased at 75 ppb. 

Rape, spring 0.8 to 83 ppb

8-h mean

89, 113, and 84 daysin three growingseasons

OTC in pots Seed weight 9.4 to 16% reduction at

30 or 51 ppb.

5-157
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 Concentrationb Duration Facilityc Variabled Effecte 

Rape, spring 43 to 60 ppb 8-h mean 89, 113, and

84 days inthree growingseasons

OTC in pots Seed weight 12 to 27% reduction. 

Tomato 13 to 0.109 ppm

12-h mean, 79.5 ppm-h

75 days OTC Fresh weight 17 to 54% reduction

at 0.109 ppm; noreduction at ambient.

Tomato 10 to 85 ppb, 6 h/day 12 to 21 days GC Shoot dry weight 35 to 62% reduction. Tomato 18 to 66 ppb 12-h mean 11 weeks OTC Fresh fruit

weight

No effect. 

Moss campion 5 to 80 ppb, 8 h/day Up to 90 days GC Dry weight 25% reduction at

80 ppb.

Buckhorn 5 to 80 ppb, 8 h/day Up to 90 days GC Dry weight 14% reduction at

50 ppb.

16 Other species 5 to 80 ppb, 8 h/day Up to 90 days GC Dry weight No effect. Radish 20 or 70 ppb 24-h mean 27 days GC Shoot and root

growth

36 and 45% reductionat 70 ppb.

Lettuce 21 to 128 ppb 7-h mean 52 days OTC Head weight Significant reduction

at 83 ppb, 35% at128 ppb.

Lettuce 10 to 34 ppb 7-week

mean

64 days OTC Fresh weight No effect. 

Faba bean 6 or 15 ppb 24-h mean 134 days OTC Seed weight No effect. 

Fenugreek 120 ppb, 7 h/day 4 weeks CC Dry weight No significant effect. 

5-158
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 Concentrationb Duration Facilityc Variabled Effecte 

Chickpea 120 ppb, 7 h/day 4 weeks CC Dry weight No significant effect. Gram, black 120 ppb, 7 h/day 4 weeks CC Dry weight No significant effect. Rice 0 to 200 ppb, 5 h/day 5 days/week

15 weeks

OTC Seed weight 12 to 21% reduction at

200 ppb.

Rice 50 ppb 24-h mean 8 weeks GC Dry weight No effect at 50 ppb. Watermelon 15 to 27 ppb 7-h mean 81 days OTC Fresh weight

and number(marketable)

20.8 and 21.5% reduction 27 ppb.

Pea 10 to 35 ppb 12-h mean 58 and 52 days in

two growingseasons

OF Fresh weight Linear decrease in yield w

increasing O3.

Green pepper 19 to 66 ppb 12-h mean 77 days OTC Fresh fruit

weight

12% reduction at 66 ppb. 

Green pepper 18 to 66 ppb 12-h mean 11 weeks OTC Fresh fruit

weight

13% reduction in fruit we66 ppb.

Celery 18 to 66 ppb 12-h mean 11 weeks OTC Shoot dy

weight

12% reduction at 66 ppb. 

aSee Appendix A for abbreviations and acronyms.bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposure

otherwise specified; accumulation based on 24 h/day unless otherwise noted.

cOTC = open-top chamber with plants in ground unless specified in pots; CC = closed chamber, outside; GC = controlled environm

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 base

in the experiment.

5-159
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
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 Concentrationb Duration Facilityc Variabled Effecte 

Strawberry 18 to 66 ppb 12-h mean 11 weeks OTC Fresh fruit

weight

20% increase in fruitweight at 66 ppb.

Timothy 10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

45% reduction at 55 p

Orchard grass 10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

28% reduction at 55 p

Kentucky bluegrass

10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

28% reduction at 55 p

Red grass 10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

23% reduction at 55 p

Tall fescue 10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

16% reduction at 55 p

Colonial bent grass 10 to 55 ppb 7-h mean 5 weeks GC Shoot dry

weight

No effect. 

Rye grass 62 ppb 7-h mean 5 weeks GC Shoot dry

weight

No effect. 

Red clover 6 to 59 ppb 7-h mean 5 weeks GC Shoot dry

weight

30% reduction at 59 p

Common plantain 70 ppb 7-h mean 8 weeks GC Total dry

weight

Reduced up to 36%depending on growthstage.

Red clover 19 to 62 ppb 12-h mean 83 and 91 days in

two growing seasons

OTC Dry weight 11% reduction at 62 p

Timothy 19 to 62 ppb 12-h mean 83 and 91 days in

two growing seasons

OTC Dry weight No effect. 

5-161
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 Concentrationb Duration Facilityc Variabled Effecte Ladino clovertall fescue pasture 22 to 114 ppb 12-h mean Five 3- to 4-week exposure periods.

Six 3- to 4-weekexposures in 2 years

OTC Shoot dry

weight,root dryweight

18 to 50% reduction in shoot dryweight (SDW) at 40 to 47 ppb cl25% reduction root dry weight at40 to 47 ppb. SDW increased by to 50% in fescue.

Ladino clover 28 to 46 ppb 12-h mean 180 and 191 days in

two growing seasons

OTC Dry weight Predicted yield of mix reduced 10

with 19% decrease in clover and19% increase in fescue at 46 ppb

Alfalfa 14 to 98 ppb 12-h mean 32 days OTC Dry weight 2.4% reduction at 40 ppb, 18.3%

reduction at 66 ppb.

Alfalfa 20 to 53 ppb 12-h mean 11 weeks OTC Dry weight 22% reduction at 53 ppb. Alfalfa 18 to 66 ppb 12-h mean 11 weeks OTC Shoot dry

weight

22% reduction at 36 ppb. 

Alfalfa 10 to 109 ppb 12-h mean 208 and 200 days in

two growing seasons

OTC Dry weight 0 to 25% reduction at levels of

38 ppb and above.

Alfalfa 60 to 80 ppb 6-h day 5 days/week for

8 weeks

GH Relative

growth rate

Reduced up to 40% in Saranac. 

Grape Not reported Two growing seasons OTC Yield No effects of ambient air vs. filtr

aSee Appendix A for abbreviations and acronyms.bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposure

otherwise specified; accumulation based on 24 h/day unless otherwise noted.

cOTC = open-top chamber with plants in ground unless specified in pots; GC = controlled environment growth chamber or CSTR; 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 base

in the experiment.

5-162
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 × 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 longlived 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 × 2.0), 1 week after the start of the regrowth period.

When exposures were at 0.081 and 0.066 ppm (NF × 1.7 and NF × 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

Species Concentrationb Duration Facilityc Variabled Effecte Almond 38 to 112 ppb 12-h mean 153 days OTC Total dry weight Linear reduction in

two cultivars, no effect three.

Almond 30 to 117 ppb 12-h mean 3.5 mo OTC Cross-sectional

area

6% reduction at 51 ppb. 

Almond 250 ppb, 4 h/week 16 weeks in each

of two growingseasons

CC Net growth 28 and 36% reduction in

years 1 and 2.

Plum 44 to 111 ppb 12-h mean 191 and 213 days OTC Number of fruit

per tree

29% fewer fruit at ambiand above.

Plum 30 to 117 ppb 12-h mean 3.5 mo OTC Cross-sectional

area

19% reduction at 51 ppb

Pear 30 to 117 ppb 12-h mean 3.5 mo OTC Cross-sectional

area

8% reduction at 51 ppb. 

Apricot 30 to 117 ppb 12-h mean 3.5 mo OTC Cross-sectional

area

53% reduction at 117 pp

Skunk bush 10 to 75 ppb 12-h mean 3 mo OTC in pots Growth Increase in leaf weight i

ambient air; no other eff

Black cherry 16 to 67 ppb 12-h mean Three growing

seasons

OTC Growth and leaf

dynamics

Leaf abscission increasewith increasing ozone.

Black cherry 40 or 80 ppb, 7 h/day,

5 days/week

8 or 12 weeks GC Growth Reduced leaf, stem, and

root dry weight, andheight at 80 ppb.

Red oak 18 to 87 ppm h

15 to 69 ppb 7-h mean

177 days OTC Tree canopy Reduced 41% at 82 ppm 

or 69 ppb 7-h mean.

Red oak 16 to 67 ppb 12-h mean Three growing

seasons

OTC Growth and leaf

dynamics

No effect. 

5-166
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 Concentrationb Duration Facilityc Variabled Effecte 

Red oak 40 or 80 ppb, 7 h/day,

5 days/week

8 or 12 weeks GC Growth Reduced root dry weight at 80 

Red maple 16 to 67 ppb 12-h mean Three growing

seasons

OTC Growth

and leafdynamics

No effect. 

Red maple 40 or 80 ppb, 7 h/day,

5 days/week

8 or 12 weeks GC Growth Reduced stem diameter and dry

weight at 80 ppb.

Tulip poplar 16 to 67 ppb 12-h mean Three growing

seasons

OTC Growth

and leafdynamics

Leaf abscission increased withincreasing ozone.

Yellow poplar 40 or 80 ppb, 7 h/day,

5 days/week

8 or 12 weeks GC Growth Reduced leaf dry weight and st

diameter at 80 ppb.

European beech 10 to 90 ppb weekly mean 5 years OTC Growth Reduced shoot growth and leaf

area.

Aspen 80 ppb, 6 h/day,

3 days/week

70 and 92 days intwo growing seasons

OTC Stem

weight

No effect on tolerant clones; 46reduction for sensitive clones in1 year 5% (tolerant), and 74%(sensitive) reductions in the secyear.

Aspen Filtered air or 80 ppb,

6 h/day, 3 days/week

93 days at two sitesin Michigan

OTC Growth 18 to 26% reduction in diamete

growth.

Aspen Ambient + 27, 51, or

102-ppb exposure periodmean

105 days CC Dry

weight

40% reduction; 44% reduction early growth the following year

5-167
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 Concentrationb Duration Facilityc Variabled Effecte 

Yellow poplar 0 to 200 ppb, 8 h/day,

3 days/week

4.5 mo GC Growth Up to a 24% reduction at

200 ppb but moderated bypH treatment.

Paper birch 60 to 80 ppb, 7 h/day,

5 days/week

12 weeks GH Dry weight Decreased shoot and root

weight and leaf area.

Downy birch 25 to 82 ppb, 7 h/day 50 days GC Dry weight Shoot and root dry weight

decreased linearly with ozo

Downy birch 25 to 82 ppb, 7 h/day 50 days GC Dry weight Shoot and root dry weight

decreased linearly with ozo

Red alder 25 to 82 ppb, 7 h/day 50 days GC Dry weight Shoot and root dry weight

decreased linearly with ozo

aSee Appendix A for abbreviations and acronyms.bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposure

otherwise specified, accumulation based on 24 h/day unless otherwise noted.

cOTC = open-top chamber with plants in ground unless specified in pots; CC = closed chamber, outside; GC = controlled environm

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 

developed in the experiment.

5-168
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 Habit Study Species

Location

(State)

Exposureb

Days Year Harvestsc

Weibull Parameters SUM06 for Loss of d

A B C 10% 30%

Fast D 1 Aspen, wild OR 84 1989 1 9.9 96.3 1.316 19.09 48.21

Fast D 1 Aspen, wild OR 84 1989 2 17.7 165.2 1.000 19.06 64.54

Fast D 2 Aspen, wild OR 118 1991 1 31.0 130.0 3.062 48.62 72.41

Fast D 2 Aspen, wild OR 118 1991 2 75.6 124.9 5.529 64.80 80.79

Fast D 3 Aspen, wild OR 112 1990 1 67.8 111.0 6.532 64.60 77.86

Fast D 3 Aspen, wild OR 112 1990 2 96.9 142.1 1.257 19.48 51.40

Fast D 4 Aspen 216 MI 82 1990 1 54.5 121.1 1.609 33.56 71.60

Fast D 4 Aspen 253 MI 82 1990 1 73.1 265.5 1.000 31.38 106.23

Fast D 4 Aspen 259 MI 82 1990 1 79.1 92.7 1.000 10.96 37.10

Fast D 4 Aspen 271 MI 82 1990 1 91.3 44.9 8.964 39.20 44.91

Fast D 5 Aspen 216 MI 98 1991 1 37.4 128.6 1.000 12.72 43.06

Fast D 5 Aspen 259 MI 98 1991 1 35.2 95.9 1.000 9.49 32.11

Fast D 5 Aspen 271 MI 98 1991 1 35.7 73.1 4.012 39.16 53.07

Fast D 6 Aspen, wild MI 98 1991 1 19.0 263.1 1.000 26.02 88.08

Slow E 7 Douglas fir OR 113 1989-90 1 16.8 462.7 1.844 111.17 215.37

Slow E 7 Douglas fir OR 113 1989-90 2 27.9 3.8E+17 1.000 250.00 250.00

Slow E 7 Douglas fir OR 234 1989-90 3 33.3 438.9 5.383 113.61 142.49

Slow E 7 Douglas fir OR 234 1989-90 4 83.5 2,887.0 1.000 119.61 404.91

Slow E 8 Douglas fir OR 118 1991-92 1 26.7 109.5 57.655 82.13 83.88

Slow E 8 Douglas fir OR 118 1991-92 2 85.9 -0.0058 (lin) 250.00 250.00

Slow E 8 Douglas fir OR 230 1991-92 3 119.1 218.7 12.254 72.80 80.42

Slow E 9 Ponderosa pine OR 111 1989 1 12.8 246.9 1.000 21.56 73.00

Slow E 9 Ponderosa pine OR 111 1989 2 25.8 365.2 1.000 31.89 107.95

Slow E 10 Ponderosa pine OR 113 1989-90 1 12.9 233.7 1.000 20.05 67.87

Slow E 10 Ponderosa pine OR 113 1989-90 2 25.7 358.8 1.000 30.77 104.18

Slow E 10 Ponderosa pine OR 234 1989-90 3 32.1 327.8 1.000 13.58 45.97

Slow E 10 Ponderosa pine OR 234 1989-90 4 90.1 634.3 1.000 26.27 88.94

Slow E 11 Ponderosa pine OR 118 1991-92 1 20.2 266.4 1.000 21.88 74.09

Slow E 11 Ponderosa pine OR 118 1991-92 2 47.1 206.5 1.000 16.96 57.42

Slow E 11 Ponderosa pine OR 230 1991-92 3 44.5 458.5 1.257 30.61 80.77

Slow E 12 Ponderosa pine OR 140 1992 1 134.6 235.8 2.570 64.56 103.76

Slow E 13 Ponderosa pine OR 84 1991 1 136.0 442.8 1.000 51.10 172.98

Fast D 14 Red alder OR 121 1990 1 42.4 217.0 1.427 34.08 80.10

Fast D 15 Red alder OR 113 1989 1 84.4 253.0 1.000 21.70 73.46

Fast D 15 Red alder OR 113 1989 2 206.8 179.9 5.294 95.76 120.57

Fast D 16 Red alder OR 118 1991 1 63.5 501.7 1.000 41.21 139.51

Fast D 16 Red alder OR 118 1991 2 248.8 2.0E+13 1.000 250.00 250.00

Fast D 17 Red alder OR 112 1992 1 54.1 274.4 1.107 29.50 88.79

Fast D 18 Black cherry TN 76 1989 1 53.7 79.1 1.123 12.91 38.23

Fast D 19 Black cherry TN 140 1992 1 37.1 176.6 1.168 16.90 48.00

Slow D 20 Red maple TN 55 1988 1 28.5 387.1 1.537 149.75 331.07

Fast D 21 Tulip poplar TN 75 1990-91 1 45.8 46.4 4.518 34.56 45.27

Fast D 21 Tulip poplar TN 184 1990-91 3 334.1 623.5 1.000 32.85 111.19

Fast D 22 Tulip poplar TN 81 1992 1 150.1 50.8 1.852 17.12 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 Habit Study Species

Location

(State)

Exposureb

Days Year Harvestsc

Weibull Parameters SUM06 for Loss of d

A B C 10% 30%

Fast E 23 Loblolly GAKR 15-91 AL 555 1988-89 3 22.7 4,402.5 1.000 76.89 260.30

Fast E 23 Loblolly GAKR 15-23 AL 555 1988-89 3 20.4 13,125.4 1.000 229.24 250.00

Slow D 24 Sugar maple MI 83 1990-91 1 4.12 100.0 40.069 104.79 108.03

Slow D 24 Sugar maple MI 180 1990-91 3 24.63 110.2 5.987 38.68 47.42

Slow E 25 Eastern white pine MI 83 1990-91 1 0.35 63.1 4.191 40.90 54.72

Slow E 25 Eastern white pine MI 180 1990-91 3 1.21 719.5 1.000 38.74 131.16

Slow E 26 Virginia pine MI 98 1992 1 78.3 3,045.1 1.000 250.00 250.00

a

See Appendix A for abbreviations and acronyms.

b

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.

c

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.

d

To 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.

e

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

tulipifera) 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 SUM00). 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 (Prunus 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

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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.)a

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]**1.14634)

Weibull Equations (28 deciduous seedling studies):

50th Percentile PRYL=1− exp(−[SUM06/142.709]**1.48845)

75th Percentile PRYL=1− exp(−[SUM06/87.724]**1.53324)

Weibull Equations (23 evergreen seedling studies):

50th Percentile PRYL=1− exp(−[SUM06/262.911]**1.23673)

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

50% 75%

Relative 10% 31.5 20.2

Biomass Loss 20% 52.1 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.)a

23 Evergreen Seedling Cases

Percent of Seedlings

50% 75%

Relative 10% 42.6 21.9

Biomass Loss 20% 78.2 45.9

a

See 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 SUM00 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 the Effects of Ozone on the Grow

Productivity of Evergreen Trees Published Since U.S. Environmental Protection Age

Species Concentrationb Duration Facilityc Variabled Effecte 

Avocado 0.010 to 0.108 ppm

12-h mean

4 and 8 mo intwo growing seasons

OTC in pots Leaf mass 20 and 61% reduction in leaf

mass at 86 and 108 ppb.

Orange 0.010 to 0.108 ppm

12-h mean

4 and 8 mo in twogrowing seasons

OTC in pots Leaf mass No effect. 

Orange 0.012 to 0.075 ppm

12-h mean

7 mo/season for5 years

OTC Fruit weight "On" production year: 11 and

31% reduction at 40 and 75 "off" year: no effect.

Ponderosa pine 0.036 to 0.051 ppm

24-h mean

June to August F Radial growth

rate

No change in growth rate onsymptomatic trees.

Ponderosa pine 0.013 to 0.095 ppm

12-h mean, 0.047 to0.0350 ppm h over3 years

Three growingseasons

OTC Growth 19.5% reduction at 95 ppb. 

Ponderosa pine 0.011 to 0.087 ppm

12-h mean

Three growingseasons

OTC Leaf weight 70 and 48% loss of 1- and

2-year-old needles at 87 ppb

Ponderosa pine 5, 122, or 169 ppm h 112 days OTC in pots Root growth 43% reduction in coarse and 

nongrowing roots; 50, 65, an62% reduction in coarse, fineand new growing roots,respectively.

Ponderosa pine 0.067 to 0.071 ppm

7-h mean

134 days OTC in pots Leaf, stem,

and root dryweight

20 to 33% reduction from filair at 67 ppb.

Lodgepole pine 0.067 to 0.071 ppm

7-h mean

134 days OTC in pots Leaf, stem,

and root dryweight

No effect. 

Jeffrey pine 0 to 0.0200 ppm, 4 h/day,

3 days/week

44 and 58 days intwo growing seasons

GC Root, stem,

and needlesdry weight

Reduced 10 to 20% ppb in1 year.

5-174
Table 5-30 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the G

Productivity of Evergreen Trees Published Since U.S. Environmental Protection Age

Species Concentrationb Duration Facilityc Variabled Effecte 

Jeffrey pine >0.10 ppm On 34 days of

1985

F Radial growth 11% reduction in symptomat

trees.

Western hemlock 0.067 to 0.071 ppm

7-h mean

134 days OTC in pots Leaf, stem, and

root dry weight

11 to 30% reduction at71 ppb.

Western red cedar 0.067 to 0.071 ppm

7-h mean

134 days OTC in pots Leaf, stem, and

root dry weight

No effect. 

Douglas fir 0.067 to 0.071 ppm

7-h mean

134 days OTC in pots Leaf, stem, and

root dry weight

No effect. 

Giant sequoia 0-0.0200 ppm, 4 h/day,

3 days/week

44 and 58 days intwo growingseasons

GC Root, stem,

and needlesdry weight

No effect. 

Red spruce 0.08 to 0.0166 ppm

8-h mean, 8 to

156 ppm h

135 days OTC Scion growth No effect on juvenile or

mature scion growth.

Red spruce 0.023 to 0.087 ppm

12-h mean

Two growingseasons

OTC in pots Dry weight No effect. 

Red spruce 0.120 ppm, 4 h/day,

twice per week

4 mo GC Growth No effect. 

Red spruce 0, 0.150 ppm, 6 h/day

or 150 ppb, 6 h, plus70 ppb 18 h/day

195 days GC Dry weight No effect. 

Red spruce 0.025 or 0.100 ppm,

4 h/day, 3 day/week

10 weeks GC Growth No effect. 

5-175
Table 5-30 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the G

Productivity of Evergreen Trees Published Since U.S. Environmental Protection Age

Species Concentrationb Duration Facilityc Variabled Effecte 

Red spruce 0.027 to 0.054 ppm

12-h mean

Three growingseasons

OTC in pots Dry weight, diameter,

and height

No effect. 

Norway spruce 0.080 to 0.100 ppm,

7 to 8 h/day

100 days GC Dry weight 0 to 14% reduction vs.

filtered air, fiveprovenances.

Norway spruce 0.014 to 0.070 ppm

8-h mean

5 to 6 mo in twogrowing seasons

OTC in pots Growth No effect. 

Norway spruce 0.010- to 0.090-ppm

weekly mean

5 years OTC Growth Reduced lateral shoot

growth in last year.

Sitka spruce 0.05 to 0.170 ppm,

7 h/day, 5 days/week

65 days GH Growth and winter

hardiness

No effect on growth,reduced winter hardiness.

Silver fir 0.010- to 0.090-ppm

weekly mean

5 years OTC Growth Increased dry matter

production.

Fraser fir 0.020 to 0.100 ppm,

4 h/day, 3/week

10 weeks GC Biomass No effect. 

White pine 0.020 to 0.140 ppm,

7 h/day, 3 day/week

3.5 mo GC Dry weight No effect. 

Loblolly pine 0.021 to 0.086 ppm

7-h mean

96 days OTC in pots Dry weight 18% reduction at 86 ppb;

20% reduction in foliageat 40 or 86 ppb.

Loblolly pine 0.021 to 0.117 ppm

7-h mean

Three growingseasons

OTC in pots Growth No effect on five familie

Loblolly pine 0.022 to 0.094 ppm

7-h mean

Three growingseasons

OTC in pots Dry weight 4% reduction at 30 to

38 ppm; 8% reduction at51 to 65 ppm.

Loblolly pine 0.032 to 0.108 ppm

7-h mean

18 weeks OTC in pots Dry weight 20% reduction in needles

at 108 ppm.

Loblolly pine 0.023 to 0.090 ppm

12-h mean, 46 to 0.209max 12-h

150 days OTC in pots Growth 10% reduction at 46 ppm

5-176
Table 5-30 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the G

Productivity of Evergreen Trees Published Since U.S. Environmental Protection Age

Species Concentrationb Duration Facilityc Variabled Effecte Loblolly pine 0.022 to 0.092 ppm

12-h mean, 37 to0.143 ppm 1-h max

Threegrowingseasons

OTC in pots Dry weight 0 to 13% reduction after 3 yea

about 45 to 50 ppm 12-h seasomean, depending on family.

Loblolly pine 0.007 to 0.166 ppm

12-h mean, 12-h max248 ppm

245 days OTC in pots Foliar weight 35% reduction at 166 ppm. 

Loblolly pine 0.007 to 0.132 ppm

12-h mean17 to 382 ppm h

Threegrowingseasons

OTC Foliage abscission Initiated above 130 to 220 ppm 

trees exposed to ambient or ab

Loblolly pine 0.021 to 0.137 ppm

12-h mean

60 to 397 ppm h

241 days OTC Shoot growth Shoot length reduced 30% at 1

Loblolly pine 0.020 to 0.137 ppm

12-h mean0.050 to 0.286 ppmmax 12-h mean

Twogrowingseasons

OTC Needle retention

and fascicle length

Needle retention decreased in ozone—fascicle length reduced ozone in early flushes, increaslater flushes.

Loblolly pine 0 to 0.150 ppm,

5 h/day, 5 days/week

6 to 12weeks

GC Dry weight 8% reduction at 150 ppm. 

Loblolly pine 0 to 0.320 ppm,

6 h/day, 4 days/week

8 weeks GC Height and

diameter growth

20% reduction in height growtreduction in diameter growth iopen-pollinated families.

Loblolly pine 0 to 0.120 ppm,

7 h/day, 5 days/week

12 weeks GC Dry weight Top dry weight increased up t

root dry weight reduced 6%.

Loblolly pine 0 to 0.320 ppm,

8 h/day, 4 days/week

9 weeks GC Relative growth

rate (RGR)

36% reduction in height RGR;10% reduction in diameter RG

5-177
Table 5-30 (cont’d). A Summary of Studies Reporting the Effects of Ozone on the G

Productivity of Evergreen Trees Published Since U.S. Environmental Protection Age

Species Concentrationb Duration Facilityc Variabled Effecte 

Loblolly pine 0.020 to 0.100 ppm, 4 h/day,

3 days/week

10 weeks GC Dry weight No effect. 

Slash pine 0.076 to 0.104 ppm 7-h mean

0.126 ppm 1-h max 122 and

155 ppm h

112 days GC Top and root

dry weight

18% reduction in top dry weightand 39% reduction in root dry weigh

at 122 ppm h.

Slash pine 200 to 1,000 ppm h 28 mo OTC Litterfall Twice as much litterfall at ozone

above 220 ppm h.

Slash pine 179 to 443 ppm h 24-h

SUM00 multiples of ambient

28 mo OTC Leaf area Reduced up to 33% by 443 ppm h. 

aSee Appendix A for abbreviations and acronyms.bMeans are seasonal means unless specified. Maximums are 1-h seasonal maxima unless otherwise specified. Cumulative exposures 

specified, accumulation based on 24 h/day unless otherwise noted.

cOTC = open-top chamber with plants in ground unless specified in pots; GC = controlled-environment growth chamber or CSTR; 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 base

in the experiment.

5-178
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 aboveand 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 (SUM00). 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; SUM00 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 SUM00 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 (N-[2-(2-oxo-1-imidagolidinyl)ethyl]-N ́-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
Table 5-31. Effects of Ethylene Diurea (EDU) on Ozone Responsesa

Crop/Species EDU Application

O3 Exposure Effects of EDU 

White bean Spray to runoff, 2,000 ppm Field; 34 h > 0.08 ppm Reduced O3 injury, 38%; delayed

defoliation; increased yield, 24%.

Spray to runoff, 2,000 ppm Field; hours > 0.08 ppm =

518 ppm h

Reduced O3 injury, 20 to 80%; inc

yield up to 35%.

Soil drench, 500 ppm,0.5 L/pot

Greenhouse (charcoal-filtered) No effect on growth. 

Soil drench, 500 ppm,4 L/6 m row

Field; 78 h > 0.12 ppm (0.2 ppmmax)

Reduced O3 injury up to 50%; reta

maturation.

Corn Spray to runoff, 500 ppm Field (no details) 19% yield reduction. Cotton Spray to runoff, 500 ppm Greenhouse (no details) Increased yield in nonfiltered air; 

yield in filtered air.

Potato Spray to runoff, 1.1 kg/ha,

five applications

Field; > 0.08 ppm on 18 days(0.138 ppm max)

Reduced O3 injury, 50%; increased 

weight, 35%.

Soil drench, 6.7 kg/ha,four applications

Field; 282 h > 0.08 ppm Reduced O3 injury; increased tube

20 to 30%.

Radish Soil drench, 100 mg/L,

2 L/m of row

Field; 0 h > 0.1 ppm, hours >

0.05 ppm = 0.76 ppm h

No response to O3. Reduced growlow O3 exposures.

Soil drench, up to 800 mg/L,100 mL/pot

Greenhouse, < 0.025 ppm Increased shoot growth at <300 m

reduced shoot growth at >300 mg/Reduced hypocotyl growth at all Elevels.

Soil drench, up to 400 mg/L,100 mL/pot

Greenhouse, 0.075 ppm/7 h, 6days/week, with one weekly peakto 0.14 ppm

Complete protection against O3 injat 100 mg/L.

5-181
Table 5-31 (cont’d). Effects of Ethylene Diurea (EDU) on Ozone Responses

Crop/Species EDU Application

O3 Exposure Effects of EDU 

Radish (cont’d) Soil drench, 150 mg/L,

60 mL/pot

Greenhouse, 0.07 ppm/7 h,5 days/week, with two weeklypeaks to 0.12 ppm

Reduced O3 injury, 90to 100%; less reductionin hypocotyl weight.

K(

Soybean Soil drench, 500 ppm,

0.5 L/pot

Greenhouse; 0.2 ppm,6 h/day, 2 days

Reduced O3 injury,

80 to 90%.

B

Soil drench, 500 ppm,4 L/6 m row

Field; 78 h > 0.12 ppm (0.2 ppmmax)

No effect on loss ofchlorophyll; no effecton seed weight.

SB

Tobacco Spray to runoff, 1 kg/ha,

seven applications

Field; > 0.08 ppm on 2 days Increased growth, 22%. B

(

Beech Stem injection 1 g/L;

0.25 mL

OTC; ambient and ambient+0.08 ppm, 8 h/day

No consistent effect. A

(

Black cherry Spray to runoff, 1,000 ppm,

seven applications per year

Field; 75 h > 0.08 ppm(over 4 years)

Twofold increase in growth. L

Other woody species:Red maple Spray to runoff, 500 ppm

or soil drench, 500 or2,000 ppm, 250 mL/pot

Up to 0.95 ppm, 3 h Reduced O3 injury. C

(

Paper birch Reduced O3 injury.

White ash Reduced O3 injury.Honey locust Reduced O3 injury.Golden-rain Reduced O3 injury.London plane Reduced O3 injury.Lilac Reduced O3 injury.

Basswood Reduced O3 injury.

aSee Appendix A for abbreviations and acronyms.

5-182
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 hotortorum], 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 ppm h, 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 ppm h 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 "selfmaintaining" 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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Figure 5-30. Effects of ozone (O3) 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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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

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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

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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 Anthropogenic pollutants insignificant. Unaffected; systems pristine.

I Pollutant concentrations low; no measurable

physiological response.

Ecosystem functions unaffected; pollutants

transferred from atmosphere to organic or

available nutrient compartments.

II 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.

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.

III 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.

(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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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, IC = 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).

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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 HNO3 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 μg/g) nitrogen

supply by 20%, but not those grown with a low (59 μg/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 (Böhm, 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

(Böhm, 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; Böhm, 1992; Böhm 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

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Table 5-34. Growing Season (May Through October) Summary Statistics for Ozone M

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 t

Elevation

(m)

Percent

Data

Capture

Percentiles (ppb) 

Siteb 5 10 25 50 Mean ± SDc 75 90 95Aptos, CA 78 100 0 10 10 20 25.1 ± 15 30 40 50 Ash Mountain, CA (AIRS) 526 50 20 30 50 60 64.1 ± 26 80 100 110 Ash Mountain, CA (NPS) 610 57 20 30 47 61 62.9 ± 24 80 93 100 Azusa, CA 185 93 0 0 0 20 43.3 ± 56 70 130 160 Banning, CA 722 98 10 10 20 40 49.6 ± 35 70 100 120 Bishop, CA 1,260 84 0 10 20 30 31.5 ± 16 40 50 60 Burbank, CA 170 95 0 0 0 20 36.3 ± 45 50 100 130 Camp Mather, CA 1,432 33 22 26 36 46 47.5 ± 16 59 70 76 Carmel Valley, CA 131 86 10 10 20 30 28.4 ± 14 40 50 50 Fresno County, CA 1,723 85 20 20 30 40 44.9 ± 17 60 70 80 Lake Gregory, CA 1,397 93 10 20 40 60 72.5 ± 49 100 140 170 Lassen NP, CA 1,788 36 17 21 28 36 37.8 ± 14 46 58 64 Kaweah, CA (AIRS) 1,901 35 10 20 40 60 59.7 ± 26 80 90 100 Kaweah, CA (NPS) 1,890 58 21 30 41 56 56.3 ± 21 71 83 90 Mammoth Lakes, CA 2,395 92 20 30 40 50 46.6 ± 16 60 70 70 Monterey, CA 23 86 10 10 20 30 27.3 ± 12 30 40 50 Ojao, CA 233 87 10 10 20 40 42.3 ± 26 60 80 90 Pasadena, CA 255 89 0 0 10 20 47.8 ± 58 70 130 170 Pinnacles NM, CA 355 66 10 16 26 41 42.8 ± 22 58 72 80 Redwood NP, CA 233 49 8 10 15 22 22.0 ± 0.09 28 34 39 San Bernardino, CA 320 80 0 0 0 30 50.2 ± 57 80 140 170 Santa Barbara, CA 25 96 0 10 20 30 32.2 ± 19 40 60 60 Santa Barbara County, CA 12 96 0 10 20 30 31.5 ± 20 40 60 70 Santa Monica Mountains, CA 191 55 0 2 10 30 39.6 ± 35 59 86 110 Scotts Valley, CA 171 79 0 0 10 20 22.4 ± 18 30 50 50 South Lake Tahoe, CA 1,907 88 10 20 20 40 37.8 ± 17 50 60 60 Ventura County, CA 1,600 83 0 10 20 40 36.2 ± 22 50 60 70 Wawona Valley, CA 1,280 66 9 15 27 42 44.0 ± 23 61 76 83 

5-197
Table 5-34 (cont’d). Growing Season (May Through October) Summary Statistics for Ozo

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 t

Elevation

(m)

Percent

Data

Capture

Percentiles (ppb) 

Siteb 5 10 25 50 Mean ± SDc 75 90 95

Yreka, CA 809 80 0 0 10 20 25.9 ± 18 40 50 60 Clackamas County, OR 174 94 4 8 14 23 25.3 ± 16 33 45 55 Columbia County, OR 6 88 1 4 11 20 21.3 ± 14 29 39 46 Crook County, OR 1,372 90 20 25 30 35 36.5 ± 0.09 40 50 55 Eugene, OR 187 77 1 3 9 18 21.4 ± 17 30 42 52 Marion County, OR 102 94 1 1 7 18 20.3 ± 16 30 41 50 Medford, OR 503 93 1 3 9 22 24.8 ± 18 37 50 59 Cedar River, WA 210 82 11 14 19 28 31.4 ± 17 39 53 64 King County, WA 22 90 0 0 0 10 14.9 ± 17 20 40 50 Olympic NP, WA (DOE) 100 85 0 0 10 20 16.3 ± 11 20 30 40 Olympic NP, WA (NPS) 125 26 0 1 1 2 4.8 ± 0.07 3 17 23 

Pack Forest, WA 24 80 10 10 20 30 30.0 ± 18 40 50 70 Pierce County, WA 14 85 0 0 0 10 15.1 ± 16 20 40 40 Port Angeles, WA 30 71 0 0 1 2 8.4 ± 10 10 20 30 Snohomish County, WA 120 83 0 0 0 10 17.0 ± 15 30 40 40 Spokane, WA 584 74 0 0 10 20 20.9 ± 16 30 40 50 Stampede Pass, WA 1,217 80 20 20 30 30 35.2 ± 14 40 50 60 Apache-Sitgreaves, AZ 2,462 94 25 30 35 40 42.3 ± 12 50 60 65 Cochise County, AZ 1,401 56 13 17 26 37 37.4 ± 15 49 58 63 Flagstaff, AZ 2,117 77 17 24 34 44 43.7 ± 15 53 62 67 Grand Canyon NP, AZ 2,073 56 17 20 23 27 29.4 ± 0.09 33 43 46 Pima County, AZ 695 86 1 2 10 28 29.8 ± 22 46 60 68 Prescott, AZ 1,673 69 5 9 16 30 29.9 ± 16 43 52 55 Saguaro NM, AZ 933 66 19 22 30 38 38.8 ± 14 47 57 63 Douglas County, NV 1,951 60 6 11 20 35 35.5 ± 19 49 62 69 Reno, NV 1,280 92 0 0 10 30 28.4 ± 20 40 50 60 Boulder County, CO 1,635 95 8 14 24 35 36.0 ± 18 47 60 69 

Colorado Springs, CO 1,842 88

0 2 10 25 26.3 ± 18 40 51 57

5-198
Table 5-34 (cont’d). Growing Season (May Through October) Summary Statistics for Ozo

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 t

Elevation

(m)

Percent

Data

Capture

Percentiles (ppb) 

Siteb 5 10 25 50 Mean ± SDc 75 90 95

Colordao NM, CO 1,750 30 30 32 37 42 44.1 ± 14 48 54 57 Denver, CO 1,591 96 0 2 7 19 21.9 ± 18 33 47 55 Great Sand Dunes, CO 2,487 54 24 27 33 39 38.4 ± 0.09 44 49 52 Larimer Country, CO 1,522 90 1 4 14 27 27.9 ± 18 40 52 59 Rocky Mountains NP, CO 2,743 49 25 31 38 46 46.0 ± 12 54 60 65 Arches NP, UT 1,567 32 28 31 36 43 42.8 ± 0.09 49 54 58 Bountiful, UT 1,335 87 8 14 25 38 38.3 ± 20 49 62 72 Logan, UT 1,382 45 8 12 20 32 32.5 ± 15 45 52 58 Ogden, UT 1,314 97 0 1 9 30 29.8 ± 22 46 58 65 Provo, UT 1,402 72 2 5 14 29 32.1 ± 22 49 62 68 Salt Lake, UT 1,305 87 2 4 11 28 30.4 ± 22 45 59 70 Albuquerque, NM 1,585 89 1 5 15 29 29.8 ± 19 43 55 61 

Yellowstone NP, WY 2,484 58 15 19 27 36 35.4 ± 12 44 51 55 

aPercent hours are normalized to represent the average occurrence of ozone levels during May through October. Percent data captu

hours/4,416 × 100, where 4,416 is the total number of hours during the period May through October.

bSite abbreviations: NPS = National Park Service, NM = National Monument, DOE = Department of Energy.cSD = Standard deviation.Source: Modified from Böhm (1992).

5-199
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.

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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 × 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 × 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 macrocarpa) 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-canyon 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
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 styraciflua), 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 exposureresponse 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]).

5-204
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).

5-205
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 longterm 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 (Al3+), 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 × 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).

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. sativa) 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 11C-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 Ectomycorrhizaea

Host Plant Mycorrhizae Exposure Conditions Effect of O3 on Mycorrhiza Loblolly pine Pisolithus tinctorius OTC, field Reduced root infection Adams 

Not stated OTC, field, 3 years Reduced root infection EdwarNot stated CEC No effect MahonNot stated CSTR Reduced root infection Meier 

Scots pine Ten species Open air, field, 3 years No significant effects Shaw eWhite pine Pisolithus tinctorius CEC Reduced root infection Stroo eNorway spruce Six species Open air, field, 3 years No significant effects Shaw e

Four species CEC No consistent effects Blasch

Paper birch Pisolithus tinctorius CEC No effects Keane 

Red oak Not stated CEC and OTC Significant increase Reich 

aSee Appendix A for abbreviations and acronyms.

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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 hostfungus 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 successional patterns are poorly understood. Shaw et al. (1992), using an openfield 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 carbonpools 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

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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,

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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 growthrelated 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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Figure 5-34. Carbon uptake through photosynthesis is made available to a general pool of carbohydrates us

maintenance of various tissues. Carbohydrates may be shifted from one category to aenvironmental conditions.

Source: Waring and Schlesinger (1985).

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Figure 5-35. Organizational levels at which air pollutants have been shown to affect the growth-related 

Source: McLaughlin (1994).

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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 1. Altered species composition

2. Forest nutrient cycling, alteration

a. Reduced litter decomposition

b. Increased plant and soil leaching and soil

weathering

c. Disturbance of microbial symbioses

2. Reduced growth, less biomass

3. Forest metabolism

a. Decreased photosynthesis

b. Increased respiration

c. Altered carbon allocation

3. Reduced growth, less biomass

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

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

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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 Leaf area and distribution

Biomass and allometry

Photosynthesis, respiration

Nutrient uptake and release

Carbon allocation

Population Age and size structure

Population density

Genetic composition

Spatial distribution

Dispersion (spatial pattern)

Natality (reproduction,

mortality)

Competition

Productivity

Community Species composition

(diversity)

Trophic levels and food

webs

Physical structure (leaf-area

index)

Redundancy and resilience

Succession (the integration

of all species processes

such as competition and

predation)

Ecosystem Biomass

Element pools

Soil properties

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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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 "selfmaintaining" 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;

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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

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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 interdependencies

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 

Model Features Results (Annual 19

Study Region Pollutant and Concentration

Price

Changes

Output

Substitutions

Input

Substitutions

Quality

Changes Crops

Consumer

Benefits

Garcia et al.(1986)

Illinois Ozone, 10% increase from

46.5 ppbb

No Yes Yes No Corn, soybeans None 

Adams et al.(1986a)d

U.S. Ozone, 25% reduction from 1980

level for each statea

Yes Yes Yes No Corn, soybeans,

cotton, wheat,sorghum, barley

$1,160 × 10

Kopp et al.(1985)d

U.S. Ozone, universal reduction from

53 to 40 ppbb

Yes Yes Yes No Corn, soybean, wheat,

cotton, peanuts

Not reported 

Shortle et al.(1988)

U.S. Ozone, universal reduction from

53 to 49 ppba

Yes No No Yes Soybeans $880 × 106 

Adams et al.(1986b)

U.S. Acid deposition, 50% reduction in

wet acidic deposition

Yes Yes Yes No Soybeans $172 × 106 

Kopp andKrupnick (1987)

U.S. Ozone, 10% reduction from annual

levels (1986 to 1990) for ruralareas. Includes adjustments for1985 Farm Bill.

Yes Yes Yes No Corn, cotton,

soybeans, wheat

NA 

Adams et al.(1989)

U.S. Ozone, seasonal standard of 50 ppb

with 95% compliancec; includesadjustments for 1985 Farm Bill.

Yes Yes Yes No Corn, soybeans,

cotton, wheat,sorghum, rice, hay,barley

$905 × 106 

Adams and Rowe(1990)

U.S. Increased UV-B radiation and

associated increase of troposphericO3 (of 16%)

Yes Yes Yes No Soybeans (for UV-B)

and all crops inAdams et al. (1989)for tropospheric O3

NA 

aAll studies except Garcia et al. (1986) use NCLAN data to generate yield changes due to ozone; see Appendix A for abbreviations and acronyms.bSeven-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 

not to be exceeded more than once a year Heck et al. (1982).

cSeven 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).

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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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Table 5-39. Studies of the Economic Effects of Ozone and

Other Pollutants on Forests

Study Pollutant/Coverage

Response and Air Quality

Data Economic Model

Annual Damages

or Benefits of

Control

(billions of

dollars)

Callaway

et al.

(1985)

All pollutants. Forest

products (hardwood

and softwood) in the

eastern United States.

Assumes three arbitrary

growth reductions (10, 15,

and 20%) for hardwood

and softwood tree species.

Spatial equilibrium

models of softwood

and hardwood

stumpage and forest

products industries

in the United States.

−270 to 563

damage in 1984

dollars for

assumed

reductions in

growth levels

Crocker

(1980)

Acid deposition.

Forest products and

forest ecosystem

service flows for

eastern United States.

Assumes a 5% reduction

in products due to acid

deposition: assumes a

pristine background pH of

approximately 5.2

Naive; assumed

changes in output

multiplied by

average value of

those goods or

services.

−1,750 damage in

1978 dollars from

current levels of

acid deposition

Crocker

and

Forster

(1985)

Acid deposition.

Forest products and

forest ecosystem

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

and

Adams

(1992)

Air pollutants,

including acid

precipitation. Losses

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 stateof-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 largetree 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 peakweighted, 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., SUM00). 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

SUM00 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., exposureresponse 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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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 N-phenyl-N -isopropyl-p-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

(cis-polyisoprene and cis-polybutadiene) containing N,N -di-(1-methylheptyl)-pphenylenediamine 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

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Figure 5-38. Reaction of anthraquinone dyes with ozone and with nitrogen oxides.

Source: Haylock 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.

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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 × 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

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Table 5-40. Laboratory and Field Studies on Effects of Ozone on Elastomer

Conditions

Material/

Product Pollutant

Concentration,

(ppm) Exposure

Environmental

Variables

Dose,

(ppm-h) Effects Com

Laboratory/field

Automotivetires

Ozone 0.25 to 0.5 NA Tires under stress

— Cracking of white

side wall.

Purpose was to and field tests. time, detailed pmeasurements, analyses were 

Ambient air 0.04

(annualaverage)

>1 year Los Angeles

environment;actual service use

>350 Positive

correlationbetween laboratoryand ambient airtests.

Laboratory Vulcanized

rubber strips

Ozone 0.02 to 0.46,

20,000

3 to 65 min Physical stress ~0.02 to 0.03 Surface cracking. Test was desig

dose/response O3-sensitive ru

an analytical m

Field Rubber tires

and variouspolymers

Ambient air 0.023 to

0.048

150 to 700 h Physical stress

and ambientenvironment

9 to 20 Time of cracking. Cracking occur

broad range of related to stres

Laboratory SBR: Plysar S

and PlysarKrylene, withand withoutantiozonants

Ozone 0.25 19 to 51 h 120 °F,

100% strain

4.75 to 12.75 Percent

antiozonant wasrelatedto cracking depthrate.

Demonstrated linear relations

unprotected rub

Laboratory White sidewall

tire specimens

Ozone 0.05 to 0.5 250 to 1,000 h 10 and 20%

strain

20 to 500 Mean cracking

rates weredetermined fordifferent stress andO3 levels.

Detailed data nverify author’s 2 to 5 years of conditions werO3 cracks to pedepth.

Laboratory Polyisoprene Ozone 0 to 1.8 2 h 22 °C Up to 3.6 Cracking and

stress relaxation.

Rate of attack proportional toO3 concentratio

5-258
Table 5-40 (cont’d). Laboratory and Field Studies on Effects of Ozone on Elasto

Conditions

Material/

Product Pollutant

Concentration

(ppm) Exposure

Environmental

Variables

Dose

(ppm-h) Effects 

Laboratory Ten different NR,

SBR, and CRformulations withand withoutprotection

Ozone 0.5 Up to 300 h 30 °C Up to 50 Time to 10 to 20%

relaxation.

Both fprotectrelaxat

Laboratory Natural rubber,

epoxidised rubber,and copolymers

Ozone 0.05 to 1,000 To 16 h −20 to 70 °C,

10 to 100% strain

0 to 240 Time to first cracking. Tempe

dependantiozo

Laboratory Several NR/SBR

blends, with andwithout protection

Ozone 0.05 to 0.15 ~3 to 16 h Sunlight, humidity ~0.15 to 2.4 Interply adhesion

affected at 0.05 ppm andabove.

Both wantiozoprotectsunligh

Laboratory Tire cords

(66 nylon; Dacronpolyester; Kevlararamid)

Ozone 0 to 1.5 0 to 48 h UV light; heat

(100 °C); RH(20 to 90%); NO2

Up to 72 RFL adhesion loss

occurred primarily during6-h exposure to high RHand 0.2 ppm O3.

Synergand RHdeterioat surf

aSee Appendix A for abbreviations and acronyms.

5-259
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 μg/m3) and 0.5 ppm

(1,000 μg/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 μg/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
Figure 5-39. Relative decrease in stress (∆ρ) with time as a function of ozone

concentration for polyisoprene vulcanizate.

Source: Razumovskii et al. (1988).

Table 5-41. Protection of Tested Rubber Materialsa

Protected

Rubber Formulation Mixtures Unprotected Wax Antiozonant

GL 2073 (NR) B, C

D

G

X

X

X

X

SS 200 (NR) A, C

B X

X X

SS 202 (SBR) A

B

X

X X

SS 203 (CR) X

a

See Appendix A for abbreviations and acronyms.

Source: Ganslandt and Svensson (1980).

5-261
Figure 5-40. Relaxation of rubber compounds in ozone (O3) is affected by the combination

of rubber formulation and type of O3 protection. Compounds SS 202B (A)

and SS 200C (B) were tested at an O3 concentration of 0.5 ppm, a

temperature of 30 °C, and elongation of 50%. The vertical lines at the end

of curves mean total failure, and vertical axes represents relaxation, where

FO is the initial force, and Ft is the force after time t.

Source: Ganslandt and Svensson (1980).

5-262
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

Final Adhesionc

Compound

Initial

Adhesion

0.15 ppm O3

(294 μg/m3),

30% RH

0.25 ppm O3

(490 μg/m3),

30% RH

0.15 ppm O3

(294 μg/m3),

60% RH

NR 5 2 to 3 1 1

IR 5 4 to 5 2 to 1 1

SBR 5 4 to 5 3 to 4 3 to 4

a

Adhesion is rated from 1 (bad) to 5 (excellent), based on visual scale standardized by the authors.

b

See Appendix A for abbreviations and acronyms.

c

All 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 μg/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 Fad

Dye Fabric

Concentration

(ppm) Exposure

Environmental

Variables Effects Comm

Blue and red Drapery 0.1

—

— Both dyes were markedly

bleached. No fadingoccurred when antioxidantswere added.

Insufficient ddose-responsdeterminationstudy followestudy showinoxidants otheNOx caused 

DisperseDirect, fiber

reactive vat,sulfur, azo

DisperseDisperse, basicDisperse, acidDirectPremetolized, acid

Cellulose acetateCottonPolyesterOrlonNylon taffetaViscoseWool

Laboratory0.02 to 0.55;field exposureconcentrationsnot reported

54 h3 mo

Light-proof cabinets,11 rural and urbansites

Photochemical agentscaused more fading thannonradiated samples.Urban locations producedmore fading, andtemperature and humidityare not the primary causesof fading.

Both laboratofield measureReported labO3 concentra

questionable. was also prelaboratory ex

Direct red 1Reactive red 2Sulfur green 2Azoicb red

Direct red 1Acid red 151Acid yellow 65Acid violet 1Basic red 14Basic yellow 11Acid orange 45Disperse blue 3Disperse blue 3Disperse blue 3Disperse blue 27Disperse blue 27AATCC O3 ribbon

CottonCottonCottonCottonRayonWoolWoolWoolAcrylicAcrylicNylonNylonCelluloseAcetateAcetatePolyesterAcetate

0.050.5

12 weeks Temperature = 55 °F,

90 °FRH = 50%, 90%

Induced fading at bothlevels, but at a nonlinearrate. Both temperature andhumidity increased fadingrate, and RH was moreimportant. Eight of thetested fabric-dyecombinations fadedmeasurably in response toO3. Only trace amounts of

fading occurred in theremaining fabrics.

Insufficient dshow detailed response relaAlthough samwere measurthroughout thexposure, on12-week data presented.

5-265
Table 5-43 (cont’d). Laboratory and Field Studies of the Effects of Ozone on Dye 

Dye Fabric

Concentration

(ppm) Exposure

Environmental

Variables Effects Comm

Olive I and IIDisperse blue

3 and 7

Nylon fibersNylon fibers

0.20.9

1 to >6 h RH = 70 to 90%

Temperature = 40 °C

Visible fading inOlive I after 16 h at70% RH; same effectafter 4 h at 90% RH.Linear increase infading at 0.9 ppm O3.

Both RH and Oconcentration afading and in a linear fashion. form was moresusceptible thaform. Haylock (1976) found t(1) increased fratio reduced f(2) increased htemperature infading; and incfiber surface aincreased fadin

Disperse blue dye in

an avocado greenmixture

Nylon 6 yarn 0.5 — RH = 85%

Temperature = 40 °C

Fading was closelycorrelated with fibersurface area (diameter).

Insufficient daresponse relatideterminations

2 Disperse dyes and

2 acid dyes

Nylon 6 and Nylon 66carpet

3 mo to 3 years 28 homes in different parts

of the country

Geographic andseasonal variation infading.

Field study. 

Disperse blue 3 Nylon 6 yarn 0.2 2 to 120 h RH = 65%, 85%, and 90%

Temperature = 40 °C

Nearly linear increasein fading with time.RH had a majorinfluence on fadingrate.

This study focon mechanism

fading than on response relati

Disperse, basicDisperseDirect vat, sulfur,

fiber reactive

DisperseDisperse, acidDirectAcid, mordant

AcrylicCellulose acetateCottonPolyesterNylonViscose rayonWool

— 2 years in 3-mo

blocks

Light-proof cabinets,eight rural and urban sites

Two-thirds of samplesexhibited substantialfading, O3 was

significant foreight fabric/dyecombinations.

Field study. 

5-266
Table 5-43 (cont’d). Laboratory and Field Studies of the Effects of Ozone on Dye 

Dye Fabric

Concentration

(ppm) Exposure

Environmental

Variables Effects Comm

Disperse blue 3Acid blue 25Acid blue 40Acid blue 45Acid blue 80Acid blue 127

Nylon 6 yarnNylon 66 yarn

0.2 0 to 96 h RH = 85%

Temperature = 40 °C

Fading proceededconsistent withdiffusion of dye to fibersurface.

Study of mecof O3 fading, 

on the Kama(1983).

Royal blueRedPlum

Drapery fabricRayon acetateRayon acetateCotton duck

0.5 and 1.0 250 to 1,000 h 50 and 90% RH, NO2

and SO2.

O3 was not astatistically significantcause of fading.

Laboratory s

aSee Appendix A for abbreviations and acronyms.bCoupling component 2, azoic diazo component 32.

5-267
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 urbanrural 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 onethird 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 plumcolored 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,

5-268
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.

5-269
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 μm 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 substantial. 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

5-270
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 coworkers 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

5-271
Table 5-44. Laboratory and Field Studies of the Effects of Ozone on Fibers

Fiber

Concentration

(ppm) Exposure

Environmental

Variables Effects 

Cotton 0.02 and 0.06 50 days Cloth, both wet and dry

O3-exposed wetted samples had 20% loss of breakingstrength.

Cotton 0.5 50 days 21 °C, 72% RH No loss of breaking strength. Cotton 1.0 60 days 25 °C, periodic washing or

wetting

Washed O3-exposed fabrics had 18% loss of breaking

strength.

Modacrylic,Acrylic,Nylon 66,Polyester

0.2 7 days 48 °C, 39% RH,

atificial sunlight, wetting

No effect on modacrylic and polyester. Slightly reducedbreaking strength in acrylic and nylon.

Nylon 0.03 Up to 445 days Exposed in industrial warehouse Loss of dyeability. 

aSee Appendix A for abbreviations and acronyms.

5-272
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 (DraegerTM 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 μm/year. At an average annual O3 level of 0.05 ppm, this regression

predicts that a 20-μm-thick coating would last over 80 years.

In a comprehensive study by Campbell et al. (1974), panels painted with different

exterior paints (automotive refinish, 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 Coatingsa

Paint/Coating Type Substrate

Concentration

(ppm) Exposure

Environmental

Variables Effects Comments 

Latex house paintOil house paintVinyl coil coatingAcrylic coil coating

Aluminum

panels

0.05 and 0.5 To 1,000 h Chamber exposures with SO2,

NO2, and O3; 50 and 90% RH;

13 and 35 °C; and artificialdew and sunlight cycles.

Very slow erosion of coilcoatings.

Automotive refinishLatexCoil coatingIndustrial maintenancecoatingOil house paint

Stainless

steel panels

0.1 and 1.0 To 1,000 h

To 24 mo

Chamber study with SO2, 70 to100% RH, 50 to 65 °C, andartificial dew and sunlightcycles.Field studies in four sites, ruralto industrial.

Although 1 ppm O3produced significantchanges in finishes,0.1 ppm O3 did not produce

statistically increasederosion.Erosion greater in urbanareas.

No environmentalmeasurements conducted.

Latex house paintOil house paint

Stainless

steel

0.006 to 0.055 3 to 30 mo Field study. Effects of O3 not

independently statisticallysignificant.

Nine sites around St. Louis. 

aSee Appendix A for abbreviations and acronyms.

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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 

Pigment Types Substrate Concentration Exposure

Environmental

Variables Effects Com

17 Artists’watercolorpigments

Paper 0.4 ppm 95 days 23 °C

47% RH

Alizarin-basedwatercolors werevery sensitive;other pigmentsshowed lesserdegrees of fading.

Alsoinvestigfading oJapanese block pr

Alizarin,Alizarin crimson,anthraquinone

Silica gelcellulose—Teflon

0.4 ppm0.4 ppm—10 ppm

95 days95 days

—

18-80 h

22 °C50% RH—24 °C≤40% RH

Each pigmenttested faded on allsubstrates.

Presentepossible mechaniproducts

16 Traditionalorganic colorants

Paper 0.4 ppm 12 weeks 23 °C

50% RH

Eleven colorantswere reactive withO3, three were

possibly reactive.

Indigo,dibromoindigo,thioindigo,tetrachlorothioindigo

Teflon 10 ppm 4 days 24 °C

5% RH

All indigo,dibromoindigoconsumed.Thioindigo andtetrachlorothioindigo were muchless reactive andstill retained muchcolor.

Presentepossible mechani

Curcumin Cellulose,

watercolorPaper, silica gel—Teflon

0.4 ppm0.4 ppm—10 ppm

95 days95 days

—

4 days

25 °C50% RH—24 °C≤20% RH

Faded rapidly onall substrates,producing colorlessproducts.

Somewhslower fwatercolpaper.

5-277
Table 5-46 (cont’d). Laboratory Studies of the Effects of Ozone on Artists’ Pigments 

Pigment Types Substrate Concentration Exposure

Environmental

Variables Effects Comm

TraditionalJapanese colorantsand dyes

Paper, silk cloth 0.4 ppm 12 weeks 22 °C

50% RH

Several organicand one inorganicpigment fadedsignificantly.

Also investfading on cJapanesewoodblock 

Triphenylmethanecolorants

Teflon 10 ppm 4 days 24 °C

≤20% RH

Found that, althoughsome are notaffected, thosecolorants withunsaturated C-Cbonds may fade.

Presented preactionmechanism

Alizarin crimson Watercolor paper 0.4 ppm 7 days 22 °C

50% RH

Severe fading. Framed sam

behind glasexhibited vno fading.

Various artists’colorants

Watercolor paperCellulose

Mixture0.2 ppm O30.01 ppm PAN0.08 ppm NO2

12 weeks 16 to 26 °C

46 to 83% RH

11 colorants,negligible changes;12 colorants,small changes;3 colorants,modest changes;9 colorants,substantial changes.

aSee Appendix A for abbreviations and acronyms.

5-278
virtually completely consumed, producing colorless reaction products. Cass et al. (1991)

noted that O3 damage to artwork is proportional to the O3 exposure (C × 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)a

Materials Costs

Study Elastomers/Plastics Fabric/Dye All

Barrett and Waddell

(1973)

ND (260) (3,878)

Mueller and

Stickney (1970)

500.0

(1,500)

ND ND

Salmon (1970) 295.2

(915)

358.4

(1,111)

653.6

(2,026)

Salvin (1970) ND 83.5

(259)

ND

Waddell (1974) ND ND 900.0

(2,790)

Yocom and

Grappone (1976)

ND ND 572.0

(1,773)

Freeman (1979) ND ND 505.0

(1,566)

a

ND = 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 paintdamaging 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

5-283
sampling and extrapolation. And we have learned that a mere costaccounting 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."

5-284
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5-349
#

Appendix A

Abbreviations and Acronyms

#&1/ #EKF&GRQUKVKQPCPF1ZKFCPV/QFGN

#). #DQXGITQWPFNGXGN

#+45 #GTQOGVTKE+PHQTOCVKQP4GVTKGXCN5[UVGO

#/ #NXGQNCTOCETQRJCIG

#3%& #KT3WCNKV[%TKVGTKC&QEWOGPV

#3%4 #KT3WCNKV[%QPVTQN4GIKQP

#752': #VOQURJGTKE7VKNKV[5KIPCVWTGU2TGFKEVKQPUCPF'ZRGTKOGPVU

% %CTDQP

% %QPEGPVTCVKQP

%# %JTQOQVTQRKECEKF

%## %NGCP#KT#EV

%### %NGCP#KT#EV#OGPFOGPVUQH

%#.4#/5 %QCUVCPF.CMG4GIKQPCN#VOQURJGTKE/QFGNKPI5[UVGO

%#4 %GPVTKCEKPCTTGIKQP

%#5#% %NGCP#KT5EKGPVKHKE#FXKUQT[%QOOKVVGG

%$/ %CTDQPDQPFOGEJCPKUO

%%/ %QOOWPKV[%NKOCVG/QFGN

%(% %JNQTQHNWQTQECTDQP

%* 1* /GVJCPQN 

%* /GVJCPG

%+ %JGOKECNKQPK\CVKQP

%+6 %CNKHQTPKC+PUVKVWVGQH6GEJPQNQI[

%. %JGOKNWOKPGUEGPEG

%/$ %JGOKECNOCUUDCNCPEG

%0) %QORTGUUGFPCVWTCNICU

%1 %CTDQPOQPQZKFG

%1 %CTDQPFKQZKFG 

%69/ %QORNGZ6GTTCKP9KPF/QFGN

&+#. &KHHGTGPVKCNCDUQTRVKQPNKFCT
#

&02* &KPKVTQRJGP[NJ[FTC\KPG

&1#5 &KHHGTGPVKCNQRVKECNCDUQTRVKQPURGEVTQOGVT[

&9/ &KCIPQUVKE9KPF/QFGN

'%& 'NGEVTQPECRVWTGFGVGEVKQP

'-/# 'ORKTKECN-KPGVKE/QFGNKPI#RRTQCEJ

'/5 'OKUUKQPU/QFGNKPI5[UVGO

'2# 75'PXKTQPOGPVCN2TQVGEVKQP#IGPE[

'2'/ 'XGPV2TQDCDKNKV['ZRQUWTG/QFGN

'24+ 'NGEVTKE2QYGT4GUGCTEJ+PUVKVWVG

'25 'OKUUKQPU2TGRTQEGUUQT5[UVGO

'4#35 'CUVGTP4GIKQPCN#KT3WCNKV[5VWF[

'6$' 'VJ[NVGTVKCT[DWV[NGVJGT

'V1* 'VJCPQN

(&&# (QWTFKOGPUKQPCNFCVCCUUKOKNCVKQP

(G51 (GTTQWUUWNHCVG 

('8 (QTEGFGZRKTCVQT[XQNWOGKPU 

(8% (QTEGFXKVCNECRCEKV[

(+& (NCOGKQPK\CVKQPFGVGEVKQP

(6+4 (QWTKGTVTCPUHQTOKPHTCTGFCDUQTRVKQPURGEVTQUEQR[

)% )CUEJTQOCVQITCRJ[

)/'2 )GQEQFGF/QFGNQH'OKUUKQPUCPF2TQLGEVKQPU

)26 )CURJCUGVKVTCVKQP

* *[FTQIGPKQP 


*% *[FTQECTDQP

*%(% *[FTQEJNQTQHNWQTQECTDQP

*%*1 (QTOCNFGJ[FG

*01 0KVTQWUCEKF 

*01 0KVTKECEKF 

*1 *[FTQRGTQZ[N 

* 1 *[FTQIGPRGTQZKFG  

*2.% *KIJRGTHQTOCPEGNKSWKFEJTQOCVQITCRJ[

* 51 5WNHWTKECEKF  

+% +QPEJTQOCVQITCRJ[

+& +FGPVKHKECVKQPPWODGT

+1 +PFQQTQWVFQQT
#

+4 +PHTCTGFTCFKCVKQP

+4 +PETGOGPVCNTGCEVKXKV[

./15 .CMG/KEJKICP1ZKFCPV5VWF[

.2) .KSWKHKGFRGVTQNGWOICU

/$6* /GVJ[NDGP\QVJKC\QNQPGJ[FTC\QPG

/%%2 /QWPVCKP%NQWF%JGOKUVT[2TQITCO

//// /GUQUECNG/QFGNXGTUKQPUCPF

/1$+.' 75'PXKTQPOGPVCN2TQVGEVKQP#IGPE[GOKUUKQPUOQFGNHQTOQDKNG

UQWTEGU

/1&'.5 /QFGNKPIHTCOGYQTMVJCVEQPUQNKFCVGUCNNQHVJG75'PXKTQPOGPVCN

2TQVGEVKQP#IGPE[	UVJTGGFKOGPUKQPCNRJQVQEJGOKECNCKT

SWCNKV[OQFGNU

/2#0 2GTQZ[OGVJCET[NQ[NPKVTCVG

/5# /GVTQRQNKVCP5VCVKUVKECN#TGC

/5%'6 /QPVJCPFUVCVGEWTTGPVGOKUUKQPUVTGPFU

/6$' /GVJ[NVGTVKCT[DWV[NGVJGT

0# 0QVCXCKNCDNG

0##35 0CVKQPCN#ODKGPV#KT3WCNKV[5VCPFCTFU

0#&2 0CVKQPCN#VOQURJGTKE&GRQUKVKQP2TQITCO

0#/5 0CVKQPCN#KT/QPKVQTKPI5VCVKQP

0#2#2 0CVKQPCN#EKF2TGEKRKVCVKQP#UUGUUOGPV2TQITCO

0#2$0 9GUVGTP0CVKQPCN#KT2QNNWVKQP$CEMITQWPF0GVYQTM

0#5 0CVKQPCN#ECFGO[QH5EKGPEGU

0$-+ 0GWVTCNDWHHGTGFRQVCUUKWOKQFKFG

0$5 0CVKQPCN$WTGCWQH5VCPFCTFUPQY0CVKQPCN+PUVKVWVGQH

5VCPFCTFUCPF6GEJPQNQI[

0%#4 0CVKQPCN%GPVGTHQT#VOQURJGTKE4GUGCTEJ

0%.#0 0CVKQPCN%TQR.QUU#UUGUUOGPV0GVYQTM

0&&0 0CVKQPCN&T[&GRQUKVKQP0GVYQTM

0'/ 0CVKQPCN#KT3WCNKV[5VCPFCTFU'ZRQUWTG/QFGN

0( 0CVKQPCNHQTGUV

0* #OOQPKC 

0* *51 #OOQPKWODKUWNHCVG  

0* 1* #OOQPKWOJ[FTQZKFG 


0*  51 #OOQPKWOUWNHCVG  
#

0+56 0CVKQPCN+PUVKVWVGQH5VCPFCTFUCPF6GEJPQNQI[

0/ 0CVKQPCNOQPWOGPV

0/*% 0QPOGVJCPGJ[FTQECTDQP

0/1% 0QPOGVJCPGQTICPKEEQORQWPF

01 0KVTKEQZKFG

01 0KVTQIGPFKQZKFG 

0 1 0KVTQWUQZKFG 

01 0KVTCVG 



01 0KVTQIGPQZKFGU Z

02 0CVKQPCNRCTM

020 PRTQR[NPKVTCVG

062 0CVKQPCN6QZKEQNQI[2TQITCO

1 1\QPG 

1#325 1HHKEGQH#KT3WCNKV[2NCPPKPICPF5VCPFCTFU

1DU 1DUGTXCVKQPU

1* *[FTQZ[N

1*$# *[FTQZ[DGP\QKECEKF

2#/5 2JQVQEJGOKECN#GTQOGVTKE/QPKVQTKPI5[UVGO

2#0 2GTQZ[CEGV[NPKVTCVG

2#0U 2GTQZ[CE[NPKVTCVGU

2#4 2TQZKOCNCNXGQNCTTGIKQP

2$. 2NCPGVCT[DQWPFCT[NC[GT

2$\0 2GTQZ[DGP\Q[NPKVTCVG

2&(+& %T[QIGPKERTGEQPEGPVTCVKQPFKTGEVHNCOGKQPK\CVKQPFGVGEVKQP

2(62.+( 2JQVQHTCIOGPVCVKQPVYQRJQVQPNCUGTKPFWEGFHNWQTGUEGPEG

R* *[FTQIGPKQPEQPEGPVTCVKQP

2. .KSWKFRJCUGXCRQTRTGUUWTG

2.#04 2TCEVKEGHQT.QYEQUV#RRNKECVKQPKP0QPCVVCKPOGPV4GIKQPU

2/0 2QN[OQTRJQPWENGCTNGWMQE[VGCNUQECNNGFPGWVTQRJKN

RRO% 2CTVURGTOKNNKQPECTDQP

220 2GTQZ[RTQRKQP[NPKVTCVG

25& 2CUUKXGUCORNKPIFGXKEG

281% 2QNCTXQNCVKNGQTICPKEEQORQWPF

3 .CVGPVJGCVHNWZ '

3 *GCVHNWZ *

T .KPGCTTGITGUUKQPEQTTGNCVKQPEQGHHKEKGPV
#

4 /WNVKRNGEQTTGNCVKQPEQGHHKEKGPV 

4#&/ 4GIKQPCN#EKF&GRQUKVKQP/QFGN

4#25 4GIKQPCN#KT2QNNWVKQP5VWF[

4'*': 4GIKQPCN*WOCP'ZRQUWTG/QFGN

4/5& 4QQVOGCPUSWCTGFKHHGTGPEG

41) 4GCEVKXGQTICPKEICU

41/ 4GIKQPCN1ZKFCPV/QFGN

41/0'6 4GIKQPCN1\QPG/QFGNKPIHQT0QTVJGCUV6TCPURQTVRTQITCO

46 4GURKTCVQT[VTCEV

5#$ 5EKGPEG#FXKUQT[$QCTF

5#+ 5[UVGOU#RRNKECVKQPU+PVGTPCVKQPCN

5#24% 5VCVGYKFG#KT2QNNWVKQP4GUGCTEJ%GPVGT7PKXGTUKV[

QH%CNKHQTPKC4KXGTUKFG

5#4/#2 5CP,QCSWKP8CNNG[#KT3WCNKV[5VWF[5,8#35#VOQURJGTKE7VKNKV[

5KIPCVWTGU2TGFKEVKQPUCPF'ZRGTKOGPVU#752':4GIKQPCN

/QFGN#FCRVCVKQP2TQLGEV

5#41#& 5VQTCIGCPF4GVTKGXCNQH#GTQOGVTKE&CVC75'PXKTQPOGPVCN

2TQVGEVKQP#IGPE[EGPVTCNK\GFFCVCDCUGUWRGTUGFGFD[

#GTQOGVTKE+PHQTOCVKQP4GVTKGXCN5[UVGO=#+45?

5%#35 5QWVJ%QCUV#KT3WCNKV[5VWF[%CNKHQTPKC

5+2 5VCVG+ORNGOGPVCVKQP2NCP

5.#/5 5VCVGCPF.QECN#KT/QPKVQTKPI5VCVKQP

5,8#35 5CP,QCSWKP8CNNG[#KT3WCNKV[5VWF[

51 5WNHWTFKQZKFG 

51 5WNHCVG 



515 5QWVJGTP1ZKFCPV5VWF[

54/ 5VCPFCTFTGHGTGPEGOCVGTKCN

542 5VCPFCTFTGHGTGPEGRJQVQOGVGT

56'/++ 5WNHWT6TCPURQTV'WNGTKCP/QFGNXGTUKQP++

57/ 5GCUQPCNUWOQHCNNJQWTN[CXGTCIGEQPEGPVTCVKQPURRO

57/ 5GCUQPCNUWOQHCNNJQWTN[CXGTCIGEQPEGPVTCVKQPURRO

57/ 5GCUQPCNUWOQHCNNJQWTN[CXGTCIGEQPEGPVTCVKQPURRO

574' 5WNHCVG4GIKQPCN'ZRGTKOGPV2TQITCO

6 6GORGTCVWTG

6#/5 6QZKE#KT/QPKVQTKPI5VWF[75'PXKTQPOGPVCN2TQVGEVKQP#IGPE[

6&.#5 6WPCDNGFKQFGNCUGTCDUQTRVKQPURGEVTQUEQR[
8

#

6'# 6TKGVJCPQNCOKPG

6I 6GTCITCO

6)62 6JG)NQDCN6JKPMKPI2TQLGEV

60/*% 6QVCNPQPOGVJCPGJ[FTQECTDQPU

62.+( 6YQRJQVQPNCUGTKPFWEGFHNWQTGUEGPEG

66(/5 6YQVQPGHTGSWGPE[OQFWNCVGFURGEVTQUEQR[

7#/ 7TDCP#KTUJGF/QFGN

78 7NVTCXKQNGV

78$ 7NVTCXKQNGVTCFKCVKQPQHYCXGNGPIVJUVQPO

8/6 8GJKENGOKNGUVTCXGNGF

81% 8QNCVKNGQTICPKEEQORQWPF

' /KPWVGXGPVKNCVKQPGZRKTGFXQNWOGRGTOKPWVG

9(/ 9JKVG(CEG/QWPVCKP

9/170'2 9QTNF/GVGQTQNQIKECN1TICPK\CVKQP7PKVGF0CVKQPU'PXKTQPOGPV

2TQITCO

9 %WOWNCVKXGKPVGITCVGFGZRQUWTGKPFGZYKVJCUKIOQKFCNYGKIJVKPI

HWPEVKQP
B-1

Appendix B

Colloquial and Latin Names

#NFGT #NPWUUGTTWNCVC#KVQP9KNNFGPQY

#NFGTTGF #NPWUTWDTC$QPI

#NFGTURGEMNGF #NPWUKPECPC./QGPEJ

#NHCNHC /GFKECIQUCVKXC.

#NOQPF 2TWPWUCO[IFCNWU$CVUEJEX0QPRCTKGN

#RRNG /CNWUURR

#RTKEQV 2TWPWUCTOGPKCEC.

#UJITGGP (TCZKPWURGPPU[NXCPKEC/CTUJ

#UJYJKVG (TCZKPWUCOGTKECPC.

#URGPVTGODNKPI 2QRWNWUVTGOWNQKFGU.

#XQECFQ 2GTUGCCOGTKECPC/KNN

#\CNGC 4JQFQFGPFTQPURR

$CTNG[URTKPI *QTFGWOXWNICTG.

$CUUYQQFNKPFGP 6KNKCCOGTKECPC.

$GCPDTQCF 8KEKCHCDC.

$GCPDWUJ 2JCUGQNWUXWNICTKU.XCTJWOWNKU#NGH

$GCPMKFPG[RKPVQUPCRYJKVG 2JCUGQNWUXWNICTKU.

$GGEJ'WTQRGCP (CIWUU[NXCVKEC.

$GGVUWICT $GVCXWNICTKU.

$GIQPKC $GIQPKCUR

$GIQPKCDGFFKPI $GIQPKCUGORGTHNQTGPU.KPM1VVQ

$GPVITCUU #ITQUVKUECRKNNCTKU.

$KTEJ'WTQRGCPYJKVG $GVWNCRGPFWNC4QVJ

$KTEJFQYP[ $GVWNCRWDGUEGPU'JTD

$KTEJRCRGT $GVWNCRCR[TKHGTC/CTUJ

$NCEMDGTT[EQOOQP 4WDWUCNNGIJGPKGPUKU2QTVGT

$NCEMITCO 8KIPCOWPIQ.

$NWGITCUU-GPVWEM[
B-2

2QCRTCGVGPUKU.

$WEMJQTP 2NCPVCIQNCPEGQNCVC.

%CDDCIG $TCUUKECQNGTCEGCECRKVCVC.

%CORKQPDNCFFGT 5KNGPGEWECDCNWU9KDGN

%CORKQPOQUU 5KNGPGCECWNKU.

%CTPCVKQP &KCPVJWUECT[QRJ[NNWU.

%GFCTKPEGPUG .KDQEGFTWUFGEWTTGPU6QTT

%CNQEGFTWUFGEWTTGPU=6QTT?(NQTKP

%GFCTYGUVGTPTGF 6JWLCRNKECVC&QPPGZ&&QP

%GNGT[ #RKWOITCXGQNGPU.XCTFWNEG2GTU

%JGUVPWV#OGTKECP%CUVGPGCFGPVCVC/CTUJ$QTMJ

%JGTT[DNCEM 2TWPWUUGTQVKPC'JTJ

%JKEMRGC %KEGTCTKGVKPWO.

%NQXGTNCFKPQYJKVG 6TKHQNKWOTGRGPU.

%NQXGTTGF 6TKHQNKWORTCVGPUG.

%QTP <GCOC[U.

%QVVQP )QUU[RKWOJKTUWVWO.

%QVVQPYQQFRQRNCT 2QRWNWUFGNVQKFGU/CTUJ

%TGUUICTFGP .GRKFKWOUCVKXWO.

%WEWODGT %WEWOKUUCVKXWU.

&QEM 4WOGZQDVWUKHQNKWU.

(GPWITGGM 6TKIQPGNNCHQGPWOITCGEWO.

(GUEWGVCNN (GUVWECGNCVKQT.(GUVWECRTCGVGPUKU*WFU

(KTDCNUCO #DKGUDCNUCOGC./KNN

(KT&QWINCU 2UGWFQVUWICOGP\KGUKK/KTD(TCPEQ

(KT&QWINCUDKIEQPG2UGWFQVUWICOCETQECTRC8CUG[/C[T

(KT(TCUGT #DKGUDCNUCOGC.HTCUGTK2WTUJ2QKT

(KTUKNXGT #DKGUCNDC/KNN

(KTYJKVG #DKGUEQPEQNQT.KPFN

)GTCPKWO 2GNCTIQPKWOZJQTVQTWO$CKNG[

)QNFGPTCKP -QGNTGWVGTKCRCPKEWNCVC.CZO

)TCRG8KVKUNCDTWUECPC$CKNG[

)TCRGYKNF 8KVKUURRB-3

)TCRGHTWKV4WD[4GF %KVTWURCTCFKUK.

)TCUUEQNQPKCNDGPV #ITQUVKUVGPWKU5KDVJQTR

)TCUUQTEJCTF &CEV[NKUINQOGTCVC.

)TCUUTGF (GUVWECTWDTC)CWF

)TCUUT[G .QNKWORGTGPPG.

)WOUYGGV .KSWKFCODCTUV[TCEKHNWC.

*GONQEMGCUVGTP

6UWICECPCFGPUKU.%CTT

*GONQEMYGUVGTP 6UWICJGVGTQRJ[NNC4CH5CTI

+X[ *GFGTCJGNKZ.

-GPCH *KDKUEWUECPPCDKPWU.

,WPKRGTUJQTG ,WPKRGTWUEQPHGTVC2CTN

.GOQP8QNMCOGT %KVTWUXQNMCOGTKCPC  6GP2CUS

.GVVWEG .CEVWECUCVKXC.

.KEJGP .QDCTKCURR

.KEJGPRCTOGNKC (NCXQRCTOGNKCECRGTCVC

.KEJGPWODKNKECN 7ODKNKECTKCOCOOWNCVC

.KNCE 5[TKPICXWNICTKU.

.QEWUVDNCEM 4QDKPKCRUGWFQCECEKC.

.QEWUVJQPG[ )NGFKVUKCVTKCECPVJQU.

.WRKPG .WRKPWUDKEQNQT.KPFN

/CPIGN $GVCXWNICTKU.

/CRNGTGF #EGTTWDTWO.

/CRNGUWICT #EGTUCEEJCTWO/CTUJ

/KNMYGGF #UENGRKCUU[TKCEC.

/KNMYGGF #UENGRKCUUR

/KPV /GPVJCRKRGTKVC.

1CM%CNKHQTPKCDNCEM 3WGTEWUMGNNQIIKK0GYD

1CM%CP[QPNKXG3WGTEWUEJT[UQNGRKU.KGDO

1CMTGF 3WGTEWUTWDTC.

1CMYJKVG 3WGTEWUCNDC.

1CVU #XGPCUCVKXC.
B-4

1PKQP #NNKWOEGRC.

1TCPIG %KVTWUUKPGPUKU.1UDGEM

2GC 2KUWOUCVKXWO.

2GCEJ 2TWPWURGTUKEC.$CVUEJEX*CNHQTF

2GRRGT %CRUKEWOCPPWWO.

2GCT 2[TWUR[TKHQNKC4JFEXVJ%GPVWT[

2GVWPKC 2GVWPKCJ[DTKFC8KNO

2KPGGCUVGTPYJKVG 2KPWUUVTQDWU.

2KPG%QWNVGT 2KPWUEQWNVGTK&&QP

2KPG,GHHTG[ 2KPWULGHHTG[K)TGX$CNH

2KPGNQDNQNN[ 2KPWUVCGFC.

2KPGRKVEJ 2KPWUTKIKFC/KNN

2KPGRQPFGTQUC 2KPWURQPFGTQUC.CYU

2KPG5EQVU 2KPWUU[NXGUVTKU.

2KPGUJQTVNGCH 2KPWUGEJKPCVC/KNN

2KPG5KGTTCNQFIGRQNG 2KPWUEQPVQTVCXCTOWTTC[CPC)TGX$CNH

'PIGNO

2KPGUNCUJ 2KPWUGNNKQVVK'PINGOGZ8CUG[

2KPGUWICT 2KPWUNCODGTVKCPC&QWIN

2KPG6CDNG/QWPVCKP 2KPWURWPIGPU.COD

2KPG8KTIKPKC 2KPWUXKTIKPKCPC/KNN

2NCPG.QPFQP 2NCVCPWUZCEGTKHQNKC#KV9KNNF

2NCPVCKPRNCPVCIQEQOOQP 2NCPVCIQOCLQT.

2NWO 2TWPWUFQOGUVKEC.

2QKPUGVVKC 'WRJQTDKCRWNEJGTTKOC9KNNF

2QRNCTJ[DTKF 2QRWNWUOCZKOQYKE\KKZ2VTKEJQECTRC

2QRNCT[GNNQYQTVWNKR .KTKQFGPFTQPVWNKRKHGTC.

2QVCVQ 5QNCPWOVWDGTQUWO.

4CFKUJ 4CRJCPWUUCVKXWU.

4CFKUJ 4CRJCPWUUCVKXWU.EX%JGTT[$GNN

4CRGURTKPI $TCUUKECPCRWU.XCTPCRWU

4JQFQFGPFTQPC\CNGC 4JQFQFGPFTQPQDVWUWO.KPFN2NCPEJ

4KEGFQOGUVKE 1T[\CUCVKXC.

5CUUCHTCU 5CUUCHTCUCNDKFWO=0WVV?0GGU

5GSWQKCIKCPV 5GSWQKCFGPFTQPIKICPVGWO$WEJJQN\
B-5

5QTIJWOJ[DTKF 5QTIJWODKEQNQT./QGPEJZ5QTIJWOZ

FTWOOQPFKK5VGWFGN/KNNUR%JCUG

5Q[DGCP )N[EKPGOCZ./GTT

5RKPCEJ 5RKPCEGCQNGTCEGC.

5RTWEG0QTYC[ 2KEGCCDKGU.-CTUV

5RTWEGTGF 2KEGCTWDGPU5CTI

5RTWEGUKVMC 2KEGCUKVEJGPUKU$QPI%CTT

5VTCYDGTT[EWNVKXCVGF (TCICTKCZCPCPCUUC&WEJ

5VTCYDGTT[YKNF (TCICTKCXKTIKPKCPC&WEJ

5WPHNQYGT *GNKCPVJWUCPPWWU.

5MWPMDWUJ 4JWUVTKNQDCVC0WVV

5[ECOQTG 2NCVCPWUQEEKFGPVCNKU.

6KOQVJ[ 2JNGWORTCVGPUG.

6QDCEEQ 0KEQVKCPCVCDCEWO.

6QOCVQ .[EQRGTKEQPGUEWNGPVWO/KNN

8KTIKP	U$QYGT %NGOCVKUXKTIKPKCPC.

9CVGTOGNQP %KVTWNNWUNCPCVWU6JWPD/CUVUWO0CMCK

9JGCV 6TKVKEWOCGUVKXWO.