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Effects of Ozone on Forest Trees in the Southern Appalachians

An Assessment of the Current State of Knowledge

Prepared for the Southern Appalachian Mountain Initiative (SAMI)

October 28, 1996

Arthur H. Chappelka and Lisa J. Samuelson

School of Forestry

Auburn University

Auburn, Alabama 36849-5418


John M. Skelly

Department of Plant Pathology

Pennsylvania State University

University Park, Pennsylvania 16802-4507


Allen S. Lefohn

ASL & Associates

Helena, Montana 59601-4144

EXECUTIVE SUMMARY

The Southern Appalachian Mountain Initiative (SAMI) is a multi-institutional cooperative established in response to concerns over the potential adverse effects of air pollutants on terrestrial and aquatic ecosystems in the southern Appalachian region. The main focus of this project is to provide a balanced and unbiased assessment of the effects of tropospheric ozone on forest trees. Primary emphasis is on Class I areas in the Appalachian regions of Alabama, Georgia, Kentucky, North Carolina, South Carolina, Virginia, and West Virginia. Key indicators used in the evaluation of ozone effects on forest trees are: visible foliar injury, growth and productivity, and physiological function. The major objectives of this report are:

1. Summarize the existing state of knowledge on the effects of ozone on forest trees in the SAMI region.

2. Evaluate the use of available assessment methodologies for predicting future changes in ozone effects to forest trees in the SAMI region.

The major findings are:

Visible Injury

* Tropospheric ozone air pollution has repeatedly been shown to cause foliar injury on sensitive vegetation throughout much of the SAMI region. On broadleaf species, foliar injury has been observed as a mid- to late-season adaxial stipple, leaf reddening, and early leaf senescence. Under ambient ozone exposures, symptoms on conifers are less evident due to many mimicking symptoms, but have been noted to involve season long chlorotic spotting and mottle. A few observations of an early summer uniform tipburn of newly emerging needles have been reported.


* Foliar injury has been induced following exposures to ozone delivered within laboratory, greenhouse and field open-top chamber conditions of fumigation. However, very few exposure/foliar symptom responses are defined for subsequent use under field conditions.

* Open-top chambers have been used under natural field conditions for the protection of forest species from ambient ozone exposures on a season-long basis. Clear differences in symptom expression are consistently observed following such treatments.

* With the exception of one preliminary study, no clearly defined association has been demonstrated between foliar injury and growth under natural growing conditions. Such relationships have been recently observed for measured physiological changes in leaf performance.

Growth and Physiological Function

* Growth and physiological responses to ozone have been reported for individual trees that occur in the SAMI region. Most of these are with individual seedlings (< two yrs in age) under controlled conditions (CSTRs or open-top chambers). The majority of these investigations were short-term (< one year), and were with potted seedlings. At least one study regarding growth effects due to ozone has been reported for 11 different coniferous species and 17 hardwood species that occur in the SAMI region. Of the conifers, the vast majority (>95%) of research was conducted on loblolly pine (majority of all research regarding ozone effects) and red spruce. Yellow-poplar, northern red oak and black cherry were by far, the most investigated hardwood species.

* Mature tree responses in the SAMI region have been reported for six species: black cherry, red maple, eastern white pine, loblolly pine, northern red oak and loblolly pine. Three of the studies were correlative and uncontrolled. Only research with northern red oak was controlled (cause-effect) in nature.

* Ranking of species sensitivity to ozone (growth, physiology and visible injury) is hindered by variation in environmental conditions, ozone exposures, study duration and objectives, tree age and differential genetic sensitivity within a species. Of the five species most intensively studied, black cherry and loblolly pine appear the most sensitive, yellow-poplar and northern red oak intermediate to tolerant, and red spruce very tolerant to ozone. Results were quite variable, for the above-mentioned reasons. Eliciting a statistically significant growth response at ambient ozone levels is very difficult. This may be the result of several factors; the trees exposed are not sensitive under most ambient concentrations, not enough replication to detect statistical differences, the short-term nature of most studies (generally less than 5% of a tree's lifespan), variability in ozone exposure regimes (temporally and spatially) and differential sensitivity within the species exposed (Chappelka and Chevone 1992, Teskey 1995).

* No conclusions can be made at present regarding the effects of ozone on growth and productivity of the forests in the SAMI region. There are only two reports of ozone effects to mature tree growth growing in a forest situation. One is a preliminary report with yellow-poplar and black cherry and the other with loblolly pine. There are simply not enough data to make any "broad" statements regarding growth and productivity.

* Ozone effects can be altered by other environmental and biotic factors such as water status, temperature, light, relative humidity, insects and diseases. Given the interaction between ozone and these factors, it is unknown if any reductions in ozone levels (10-20%) will result in subsequent, measurable increases in growth and physiological function of forest trees in the SAMI region.

Exposure-Response

* For the years 1983 through 1990, the ozone exposure kriging estimates resulted in most of the grid cells falling between 23.8-66.5 ppm-h for the W126 index. In 1988, 11 of the 120 cells had W126 estimates greater than 66.5 ppm-h. Three cells in 1986 and 1989, and one cell in 1990 had a W126 estimate of 5.9-23.7 ppm-h. No cells were classified as having less than 5.9 ppm-h.

* An important observation is that usually, within the Southern Appalachian area boundary, ozone monitors experienced fewer than 40 hours in which the hourly average ozone concentration was � 0.10 ppm (1983-1990). The only year that deviated from this pattern was 1988 when 11 of the 15 ozone monitors in the area had greater than 50 hours in which the hourly average ozone concentration was � 0.10 ppm.

* The combination of the Palmer hydrologic index and the ozone exposure results indicate that soil moisture conditions may alter tree growth response to ozone exposures (Lefohn et al. 1997). Combining exposure information with moisture availability and experimental exposure-response data has identified possible areas that may have the greatest potential for possible vegetation effects.

Models

* Several models have been used to simulate growth and/or physiological responses to ozone for trees in the SAMI region. These include a single tree model (TREGRO), several canopy models on ozone uptake and carbon fixation, a forest succession model (FORET) and a loblolly pine management model (AIRPTAEDA). These models all provide some information on ozone effects to species commonly found in the SAMI region. Each model has advantages and disadvantages, and they vary in their level of complexity. TREGRO provides good information on ozone effects for a single, open-grown tree. It, however, does not provide information regarding forest stand growth. Accurate ozone dose-response functions are needed to model tree responses using TREGRO. While these functions are available for some tree species at the seedling level, they are not available for mature trees. Given the paucity of mature tree studies, model predictions using experimental growth responses are not easily validated. In addition, the model (TREGRO) requires detailed ozone exposure, environmental and physiological data. These data are not presently available for many species. The canopy models all provide good information on ozone uptake and carbon fixation. They do not provide information on whole-tree responses (root growth, etc.). In addition, all assume that ozone levels and ozone responses are equal within a crown. This may produce error in the model. The FORET model provides some extremely useful information on ozone effects to a forest stand. It can provide information on changes in growth and productivity over time. This simulator needs to be reparameterized specifically for ozone. It originally was parameterized for air pollution effects in general, and this assumption needs to be modified specifically for ozone. Also, the model assumes ozone effects to be equal within a species, and error could result due to this assumption. AIRPTAEDA has limited use for an assessment of the trees within the SAMI region at present, since loblolly pine is a minor component within the forests of the SAMI region. Also, this model is based on a growth and yield model for plantation-grown trees. It does, however, account for differential genetic variability within a species to ozone.

Assessment Methodologies

* Three assessment methodologies have been used to detect risk due to ozone for different forest types in the SAMI region. The method proposed by Lefohn and co-workers (1997) provides information of areas that are possibly at risk. The methodology uses exposure-response information with ozone kriging information and the Palmer hydrologic index to create "areas of concern maps" for ozone. This methodology is empirically driven and is based on the assumption that moisture stress in conjunction with ozone causes a reduction in ozone-induced growth effects. Limited exposure-response data were available from which the investigators could choose. More realistic exposure-response experiments with deciduous tree species experiments would be helpful. The second risk assessment was conducted by Hogsett et al. (1993). There appears to be several layers of parameterization necessary (model linkages) for the assessment to be operational. Forest growth scenarios are based on individual seedling data from only a small number of studies (similar to the ones used by Lefohn et al. (1997), mostly with seedlings growing in pots, in open-top chambers. Other concerns are with the error associated with the estimation of ozone exposures and species distribution. Similar to the limitations of the work described by Lefohn et al. (1997), there is little ozone monitoring data available. Hogsett et al. (1993) estimate ozone values for the region using actual data, NOx emissions information, and meteorological data. The uncertainty in using county-based emissions information as a predictor of ozone formation can lead to potential errors in the determination of exposure values. Regarding species distribution and amounts, the inventory of particular species may not be up-to-date. The third methodology, proposed by Luxmoore (1992) although a very valid technique is probably not feasible in its current form (assessment only for loblolly pine). However, it may be possible to modify this technique in the future to encompass the major tree species growing in the SAMI region.

Recommendations

It is our opinion that any of the three aforementioned assessment methodologies have merit, but it is up to SAMI to choose which one (or a modification of them) that best suits its purpose. It is imperative, however, when conducting assessment exercises, that we must constantly keep in mind the tremendous variability that exists within natural systems. Therefore, to "model" ozone induced exposure/responses across the geographic range of a species (even within the limited range of the SAMI region) poses a formidable task. At this time, we would consider the influence of micro-site factors to be most important in controlling responses to altering the potential for ozone induced exposures. Available soil moisture appears at present to be of greatest single importance in controlling ozone uptake, and subsequent effects, through its influence on stomatal function at the leaf level. Therefore scaling of this single site/physiological response phenomenon from seedling research to mature canopy responses continues to hold a significant position of need in future research efforts. Such forest-based research is necessary in support of the assessment efforts at determining region-wide ozone impacts when these are suggested to be occurring as larger scale forest responses.

In addition, assessments must also take into account the relative influences of insect pests, biotic pathogens and abiotic stressors (other than ozone) and inter and intra species competition for resources in contributing to the measured/ modeled changes in forest health and/or productivity. Very careful diagnostics must first take place at the specific sites and for the species of interest before an ozone-induced response may be held accountable at that specific site, or even for selected species at that site. Scaling responses across broad regions (i.e., SAMI) for the purpose of determining ozone-induced effects without regard to gaining a clear understanding of the influence of many other stress-inducing factors would possibly present a skewed and, therefore, unrealistic scenario of the relative importance of ambient ozone exposures to forests in the SAMI region.

TABLE OF CONTENTS

Executive Summary

I. INTRODUCTION

The Southern Appalachian Mountain Initiative (SAMI) is a multi-institutional cooperative established in response to concerns over the potential adverse effects of air pollutants on terrestrial and aquatic ecosystems in the southern Appalachian region. The mission of SAMI is "through a cooperative effort, to identify and recommend reasonable measures to remedy existing and to prevent future adverse effects from human-induced air pollution on the air quality-related values (AQRV's) of the southern Appalachians, primarily those of Class I parks and wilderness areas."

Ozone is considered as one of the most important air pollutants affecting vegetation in the SAMI area (U.S. EPA 1986, 1996). Therefore, assessing the impact of this pollutant on terrestrial ecosystems occurring within the region is critical. The main focus of this project is to provide a balanced and unbiased assessment of the effects of tropospheric ozone on forest trees. Primary emphasis of this assessment is on Class I areas in the Appalachian regions of Alabama, Georgia, Kentucky, North Carolina, South Carolina, Virginia, and West Virginia (Figure 1). Key indicators of ozone effects to be evaluated are: visible foliar injury, growth and productivity, and physiological functions of forest vegetation.

Class I Areas

The Clean Air Act, enacted in 1970, was amended in 1977 to establish Class I areas as national parks and wilderness areas greater than 2,400 and 2,000 hectares in size, respectively. These areas are afforded the greatest degree of air quality protection under the Clean Air Act. Air pollution is not acceptable in resources in Class I areas if it 1) diminishes the national significance of the area, 2) impairs the quality of the visitor experience, or 3) impairs the structure and function of the ecosystem (USDA DOI, 1982). Federal land managers are required to detect air quality in Class I areas and assess possible impacts of air pollutants on resources (AQRVs) within these designated areas. Of the Class I areas shown in Figure 1, The Shenandoah National Park and Great Smoky Mountains National Park are by far the largest areas that are potentially at risk in the SAMI region.

Forest Resources

The forested areas within the SAMI region cover more than 50% of the land area and are very diverse in nature. Most of the tree species in the region are deciduous hardwoods with various species of oak, hickories, maples and yellow-poplar (Liriodendron tulipifera) as the predominant species. Many other species of hardwoods do commonly occur in the region. Although not as prevalent as hardwoods (< 30% of the total wood volume) several different coniferous species can commonly be found in the SAMI region. These include eastern hemlock, Fraser fir, red spruce, pitch pine, Virginia pine and loblolly pine. A more detailed description of the forested resources in the region is presented in The South's Fourth Forest: Alternatives for the Future (USDA Forest Service 1988).

Natural Stressors

Besides air pollutants, many other stresses affect forests in the SAMI region. These can be found in any forest in the world and include abiotic agents such as moisture and nutrient deficiencies (Dougherty 1995) and biotic stresses such as insects and diseases (Hepting 1971, Skelly et al. 1987).

Commonly found insects include the balsam wooly adelgid (Adelges piceae), gypsy moth (Pothetria dispar), several bark beetles (primarily Ips spp.) inclusive of the southern pine beetle (Dendroctonus frontalis), and diseases such as sycamore anthracnose (Gnomonia veneta), Armillaria root rot (Armillaria spp.), numerous cankers, fusiform rust (Cronartium quercuum f. sp. fusiforme), littleleaf syndrome (Phytophthora cinnamomi), and annosum root rot (Heterobasidion annosum). Although primarily endemic in nature, insect attacks and diseases can reach epidemic proportions in the SAMI region as evidenced by the balsam wooly adelgid, gypsy moth, and the fungi which cause chestnut blight [Cryphonectria (Endothia) parasitica], dogwood anthracnose (Discula destructiva) and butternut canker (Sirococcus clavigignenti-juglandacearum). Wildlife activities also cause serious losses in the forest with particular concern for damage to regeneration by the whitetail deer. In addition, numerous abiotic stressors inclusive of local and/or regional scale major and minor periods of drought, rime ice and more heavy accumulations of ice leading to top breakage, freezing temperatures leading to winter injury, flooding, and of course fire are all present within the forests of the SAMI region. Moisture and nutrient stresses can be limiting factors in both the productivity and species composition of the various forest types in the SAMI region.

The interrelationships of ambient ozone exposure with all of these natural stressors remains virtually unknown. Introduced insects and pathogens usually need only a susceptible host specie(s) and favorable growing conditions for rapid speed and reproduction into epizootic/epidemic proportions. More is known about other abiotic stressors such as with drought and/or other pollutant interactions as reviewed later in this document. These naturally occurring and introduced stressors as may be found throughout the SAMI region are described in more detail by Skelly et al. (1987), Meadows and Hodges (1995) and Tainter and Baker (1996).

Objectives

The synthesis document will use information obtained from the annotated bibliography (already submitted to SAMI) to assess the scientific evidence concerning ozone effects on forest trees (primarily Class I areas) in the SAMI region. The primary emphasis of the document includes seven items: 1) evaluation of ozone effects on visible injury, growth and productivity, and physiological function; 2) review and classify historic trends, status and contribution of ozone to these trends in the SAMI region; 3) evaluate ozone exposure-response relationships derived from both greenhouse and field studies; 4) critique existing ozone exposure data sets applicably to Class I areas and their potential for use in assessing status of Class I areas; 5) evaluate other abiotic and biotic factors that may influence forest response to ozone and assess the potential influence of ozone compared with other environmental and plant factors; 6) review alternative interpretations of existing data; and 7) identify information gaps that limit assessment of current and future status of forest resources in the SAMI region. Recommendations from this assessment will be used by SAMI to address three policy questions:

1. What is the current status of the resources relative to ozone effects on vegetation?

2. What is the relationship between ozone exposures and vegetation response?

3. What changes in resource status are projected to occur from changes in exposures due to implementation of the 1990 Clean Air Act Amendments or other emission management options being considered by SAMI's Policy Committee?

II. VISIBLE FOLIAR SYMPTOMS

This introductory section, as adapted in large measure from Skelly et al. (1987), will present descriptive information on the visible foliar injuries as induced by exposures to ambient ozone under natural field conditions within the SAMI region. It is recognized that pre-visual physiological changes are induced before the manifestation of such visible symptoms. Growth and/or productivity changes may also precede or follow visible symptoms. Please refer to the respective sections that review these forms of pre-visual and productivity changes.

Visible symptoms resulting from ozone exposure are generally recognized as resulting from either acute or chronic exposures as manifested on the foliage of sensitive plants. Injury from acute [unusually high concentrations (generally >0.10 ppm in the SAMI region), short-term (generally <24 hr)] exposures normally involves the death of cells and develops within a few hours or days following exposure. Injury is expressed as tissue bleaching, leading to bifacial necrosis (fleck), and may follow exposure to unusually high ozone concentrations. Acute ozone exposures rarely occur in nature.

Foliar injury resulting from chronic exposures [lower concentrations (generally < 0.100 ppm in the SAMI region), longer-term (generally days, weeks, or months)] may be manifested as chlorosis, pigmentation (stippling), general leaf reddening and/or premature or enhanced senescence. Both types of symptoms (resulting from acute or chronic exposures), particularly those from chronic exposures, may be confused with symptoms of other conditions, such as normal senescence, nutritional disorders, other environmental stresses, biotic pathogens, or insect infestation (Skelly et al. 1987).

Description of Symptoms

Broadleaf Species

Under conditions of ambient ozone exposures several specific symptoms appear on broadleaf species in the field, the most common of which is stipple, defined as discrete areas of pigmentation restricted to the adaxial leaf surface. The upper leaf surface of sensitive plants may have a tan, red, brown, purple, or black stippling (as if pepper had adhered to the upper leaf surface) that may appear uniformly over the leaf surface, or restricted to certain areas of the leaf, or discrete dot-like lesions. The lower leaf surface usually remains uninjured, with only the palisade cells underlying the upper epidermis affected. Veins and veinlets are usually not involved, and small veinlets often bound the injured areas, producing angular sections of affected tissue. Sometimes stippling is best observed by holding the leaf toward the sun; symptoms are often more intense on leaves exposed to direct light. Recent evidence suggests that shaded leaves may be more sensitive earlier in the growing season and exhibit the earliest symptoms (Fredricksen et al. 1995).

Stippling has been described as the classic symptom of ozone injury on broadleaf trees. The coloration of stippling is usually characteristic for a species, but can vary with environmental or physiological conditions. The youngest fully expanded leaves are normally the most sensitive, although all but the youngest leaves may be affected. On young leaves, symptoms tend to develop at the tips, on older leaves, toward the base. The entire surface of older leaves may exhibit symptoms when exposed to ozone periodically during the growing season. Although stippling is usually interveinal, following repeated and continually higher ozone exposures, extensive injury may also occur to the leaf veins themselves resulting in generalized chlorosis. In some species, especially sycamore, stippling tends to appear adjacent to the larger veins. Chlorosis, or loss of chlorophyll, may occur as a generalized condition similar to senescence, in discrete patches called mottle, or in patterns similar to stippling. Chlorosis is often more prevalent on the upper leaf surface of species that have palisade cells. On plants with pinnately compound leaves, such as ash, hickory, and tree-of-heaven, only some leaflets at certain positions along the petiole may be affected. Because stippling is a photosensitive response, overlapping leaflets or leaves may create a sharp line of demarcation between injured and uninjured (shaded) tissue.

On broadleaf species that are very sensitive to ozone, injury is usually expressed as a fleck characterized by small, discrete areas of dead cells-usually palisade parenchyma and sometimes associated epidermal tissues-leading to the formation of irregular lesions that although first evident on the adaxial leaf surface injury quickly become evident on both leaf surfaces. The lesions are often bleached (unpigmented) but can be colored as in stippling, and the affected areas may be slightly sunken. Bifacial necrosis results when the tissues connecting the upper and lower leaf surfaces are killed. The tissue coloration ranges from white to red-orange to black and is often characteristics of a specific tree species. Small veins are usually included in the necrotic tissue, but larger veins often remain alive. The area of dead cells collapses, and the upper and lower leaf surfaces adhere together to form a papery lesion.

In bifacial necrosis, the leaf margins are sometimes the most severely injured. Prolonged exposures to even low ozone concentrations may cause coalescence of chlorotic tissues, light stippling, and/or production of a bronzed appearance, especially on ozone-sensitive tree species.

Season-long exposures to ambient ozone may further result in premature or enhanced senescence of the older leaves on sensitive species. This may be a classic symptom of cumulative ozone exposures for many species, but remains elusive of description due to lack of filtered air controls for purposes of phenological comparisons. For sensitive species such as black cherry, notable stippling and general leaf reddening of the older leaves has been observed, with defoliation occurring several weeks before more tolerant individuals on the same site (Skelly, personal communication). For other sensitive individuals within species such as yellow-poplar (Liriodendron tulipifera, L.), white ash (Fraxinus americana, L.), or sassafras (Sassafras albidum L.) premature senescence is characterized more simply by the yellowing and dropping of the older leaves. When defoliation is severe, leaves with ozone-induced stipple may commonly be found on the forest floor below sensitive individuals several weeks before full autumn coloration.

Conifer Species

Foliar injuries on conifers as may be induced by ambient ozone exposures are far more difficult to identify in comparison to the more distinctive symptoms induced on broadleaf species. Although ozone induced symptoms were once thought to be easily diagnosed, recent controversies (Skelly, personal communication ) about the causes of several needle anomalies have added to the confusion of proper diagnosis, especially under ambient forest conditions and following ambient ozone exposures. So many other causes may be involved in inducing the symptoms described below that determination of cause/effect relationships during field surveys may prove difficult.

Usually, on conifer species the two most common needle symptoms are chlorotic mottle and tipburn (Skelly et al. 1987). Overall, mottle of young and older needles may be induced by low ozone exposures, while tipburn of young needles may be produced by higher, early season exposures. There is, however, considerable difference in symptom expression depending on species, within-species variation, timing of exposures, and environmental conditions. Chronic symptoms usually only develop during the late summer or early fall on the current year needles with chlorotic mottle and/or spotting developing as small patches of yellow tissue interspersed with green areas (mottle), or as discrete yellow spots surrounded by apparently healthy tissue. Chronic symptoms in two, three and older-year needles simply intensify with coalescing of symptomatic areas leading to more general needle chlorosis and early senescence. Loss of second and third-year needles on eastern white pine (Pinus strobus, L.) and loblolly pine (Pinus taeda, L.) following advancing chlorotic mottle, spotting, and general chlorosis has been reported (Skelly et al. 1987, Chappelka and Chevone 1992).

Symptoms on most conifer species occurring as the result of acute exposures are rare and usually occur following episodic events to ambient ozone early in the growing season. If an ozone episode were to occur at this sensitive time of needle growth, that portion exposed to the higher ozone concentrations may subsequently develop necrotic needle tips resulting in tip dieback or necrotic banding. Tip necrosis is characterized with a pink to reddish coloration that fades brown with age. Towards the end of the growing season, these necrotic tips may break off, making affected needles appear much shorter. The tipburn symptom, especially in eastern white pine, usually affects all needles in a fascicle equally following an exposure to episodic ozone in the spring portion of the growing season. Severely affected individuals are evident within populations due to their off-color for much of the growing season.

On eastern white pine, a late season phenomenon of banding in the mid-portions of individual needles within the current year fascicles has also been attributed to episodic ozone exposures immediately before symptom expressions. Although shown to be induced by high ozone exposures under controlled conditions, additional controversy as to the role of fungi in causing this symptom leads to a less clear decision of determining this symptom as solely being due to ambient ozone exposures under forest conditions (Skelly, personal communication). Young, rapidly growing needles that are directly exposed to sunlight are the most sensitive, but older needles can exhibit mottle and premature senescence from prolonged, chronic exposures. Similar to broadleaf species, symptoms on plants within a single conifer species can vary considerably.

Bioindicator Species

Some particularly sensitive broadleaf tree species include black cherry, white ash, yellow poplar, and sassafras have become recognized as very useful bioindicators of ozone exposure because of a distinctive upper surface stipple, leaf reddening, and a large portion of the population appearing as sensitive under varied conditions of exposure and environments (Chappelka et al. 1992). Clonal lines of eastern white pine have been suggested for use as bioindicators of ambient ozone exposures, but as described above the general use of this species under field conditions may pose difficulties in determining cause/effect relationships. Other forest species that may serve as bioindicators of ozone pollution are blackberry, milkweed, dogbane, big-leaf aster and poison-ivy. Blackberry and poison-ivy exhibit a dark purple-red stippling of the upper leaf surface that often coalesces over most of the leaf surface. The symptom on milkweed is similar to that on blackberry, except that the coloration is purple-black. Milkweed has been reported as a common bioindicator of ozone (Duchelle and Skelly 1981).

Visible Foliar Ozone Symptoms: Tree Species in the SAMI Region

Current knowledge of visible foliar symptoms on forest tree species growing in the SAMI region is limited to only a few species of hardwoods and conifers. Only those species that have had symptoms confirmed from laboratory studies (for example, CSTRs) or studies with open-top chambers using charcoal-filtered air controls (CF) will be discussed. For purposes of this section only open-top chamber studies and field surveys will be reviewed.

Aspen (Populus tremuloides):

In a controlled study using open�top chambers in Switzerland, Keller (1988) observed no visible symptoms but premature defoliation occurred when ozone was greater than 20 ug/m3-h for sensitive clones and greater than 60 ug/m3-h for tolerant clones. In a more recent study of aspen by Karnosky et al. (1992), symptoms appeared as upper leaf surface stipple, bifacial necrosis, and premature leaf abscission. Foliar injury began to occur by late July and more than 50% of leaves of sensitive and intermediate clones had symptoms by the end of August. Open�top chambers were used, with cumulative ozone concentrations of 5.0, 10.0, 19.4 ppm�hr (1988) and 7.7, 15.4, 26.4 ppm�hr (1989) for 6hr/d, 3d/wk during both years. Trees were also grown in ambient air.

Black cherry (Prunus serotina):

Black cherry develops very distinctive symptoms in the presence of elevated ambient ozone exposures. Very sensitive individuals rapidly develop an upper surface (adaxial) stipple followed by leaf reddening and early leaf senescence. In a screening study by Davis and Skelly (1992a) the predominant foliar symptom observed consisted of a dark adaxial stipple of the oldest leaves; premature senescence occurred following exposures of 12 weeks. Ozone concentrations were 0.01, 0.075, and 0.150 ppm for 6 hr/d, 2 d/wk/12 wks. Dark adaxial stipple on oldest leaves was observed with concentrations of 0.040 or 0.080 ppm ozone from 0830�1530 h / 5 d/wk for 8 or 12 wks.

In a field study by Fredericksen et al. (1995) injury on black cherry foliage was greatest on seedlings, followed by saplings, with least injury noted on mature trees. In larger trees, symptoms were more prevalent in the lower crown.

Symptoms of red/black adaxial stipple and leaf abscission were positively correlated with ozone exposure in a study by Neufeld and Renfro (1993). Necrosis of older leaves was also observed by August. In a study in TN (Samuelson 1994a) exposed seedlings to ozone in open�top chambers with CF, 1.0, 1.5, 2.0 AA exposure treatments. A dark adaxial stippling, characteristic of ozone injury occurred on the oldest leaves of black cherry exposed to 2.0X AA from April � August 1993.

In two separate field surveys during the late summer seasons of 1991, 1992, and 1993, foliar symptoms on black cherry were observed at sites of three different elevations each in Shenandoah National Park, Va. and Great Smoky Mountains National Park, respectively. Black, red/black, and red/purple stipple was observed on black cherry foliage; symptoms were observed to have increased with increasing ozone concentration and with increasing elevation. (Chappelka et al. 1992, Hildebrand et al. 1996). Subsequent regression analysis showed symptoms to be positively correlated with SUM06 and W126 ozone concentrations, ie., the higher ozone concentrations were related to the greatest amount of visible foliar injury. (Hildebrand et al. 1996).

Black locust (Robinia pseudoacacia):

During a late season survey of several species for responses to ambient ozone exposures, significant positive correlations were shown between foliar injury (upper surface stipple), typical of ozone symptoms for this species (Duchelle et al. 1992), and elevation in field surveys in Shenandoah National Park, VA. by Winner et al. (1989).

Honeylocust (Gleditsia triacanthos):

Symptoms were observed from June through September, 1981 on honeylocust seedlings grown in open plots under conditions of ambient ozone exposures in New Jersey. Symptoms included upper leaf surface stipple, chlorosis, and premature leaf drop. There was considerable variation in response among pre determined, ozone- sensitive and tolerant selections, with ozone- tolerant trees remaining green and full�crowned throughout the growing season (Smith and Brennan 1984).

Hybrid poplar (Populus maximowizii x trichocarpa):

Davis and McClenahen (1993) reported that more ozone-induced injury (stippling) was observed on hybrid poplars established along ridge top than in lower elevation plots. Seedlings were planted in open plots near coal�fired power plants. More necrosis occurred in crosswind plots and injury incidence was positively correlated with the number of days when ozone was greater than 0.040 ppm. Hourly means were 0.040 � 0.050 ppm throughout the summer. There were 36 hrs with ozone concentrations greater than 0.080 ppm in June and July at one site, more than 98 hours at another site. The maximum concentration at the four sites ranged from 0.124 � 0.155 ppm.

Red maple (Acer rubrum):

In an early study, Townsend and Dochinger (1974) reported red maple to exhibit pale green to yellowish-white chlorotic areas within the interveinal leaf tissues. Ozone fumigations were very high at 0.750 ppm for 7 hr/d, 3d/wk. There was more foliar injury in younger than in older seedlings, and more injury in seedlings from PA and MN stocks. The least injury was reported for seedlings grown from AL sources. In a later controlled CSTR study, Davis and Skelly (1992a) reported chlorosis within four weeks when wild-type PA red maple seedlings were exposed to 0.150 ppb. Ozone concentrations in all treatments were 0.0, 0.075, and 0.150 ppm for 6 hr/d, 2 d/wk for 12 wks. Samuelson (1994a) also observed ozone-induced injury on red maple as chlorosis, with more injury in the lower portions of the crown. Seedling plants were exposed to 2.0 X AA, with cumulative concentrations of 29, 38,41, 33, 32 ppm�h for April � August.

Northern red oak (Quercus rubra):

Samuelson and Edwards (1993) reported that no visible injury was observed on mature trees or seedlings in open�top chambers with ozone concentrations of 18, 45, 87 ppm�h, or 34, 79, 147 ppm�hr and/or at 37, 95, 188 ppm�hr (0.03, 0.060, 0.0 90, 0.120 ppm for 7 hr/d/5 d/wk for 6, 8,10 wks).

Similarly, red oak was the only one of eight tree species showing no visible symptoms of ozone injury when fumigated in CSTRs at 0.010, 0.075, and 0.150 ppm 6 hr/da, 2 consecutive. da/wk for 12 wks as reported by Davis and Skelly (1992a).

Sassafras (Sassafras albidum):

Symptoms on sassafras were observed in a field survey in Jefferson National Forest in VA. by Andersen et. al. (1987). Chappelka et al. (1992) reported increasing symptoms with increasing ozone exposure and increasing elevation in a field survey in Great Smoky Mts. National Park. Symptoms generally appeared as red to red/brown stipples on the adaxial leaf surface.

Sweetgum (Liquidambar styraciflua):

Sweetgum exhibits a combination of symptoms including adaxial stipple and general leaf reddening. Kress and Skelly (1982) reported that adaxial black stipple increased with increased ozone concentration in CSTR chambers when ozone exposures were 0, 0.050, 0.100, 0.150 ppm for 6 hr/d for 28 consecutive days. Typical symptoms were also reported by Showman (1991) on sweetgum during a field survey conducted in Indiana in 1989. Although ozone concentrations were higher in 1988, no symptoms were noted due to the extreme drought also realized during 1988 (Showman 1991). In a controlled CSTR study, Davis and Skelly (1992a) reported a dark adaxial stipple when seedling sweetgum were exposed to 0.075 ppm after 8 wks. Plants were exposed to concentrations of 0, 0.075, 0.150 ppm for 6 hr/d for 2 consecutive days/wk for 12 wks.

Sycamore (Platanus occidentalis):

Kress and Skelly (1982) reported adaxial stipple, and some necrosis and leaf abscission for sycamores following exposure to ozone up to 0.150 ppm for 6 hr/d for 28 consecutive days within CSTR chambers. Foliar injury increased with increasing exposures.

White ash (Fraxinus americana), Green ash (F. pennsylvanica):

In an early investigation, Steiner and Davis (1979) observed chlorotic mottling, tan to buff colored stipple, and dark red/black stipple on white and green ash, with more injury on white ash; total leaf surface injured was 2.5 � 40%. Ozone concentrations were excessively high at 0.250 ppm for 6 hr.

In a study also conducted at excessively high ozone exposures (ozone concentrations were 0.50 ppm for 7.5 hr for 5 � 6 consecutive da, then 2 consecutive da 2 months later in CSTRs), Karnosky and Steiner (1981) reported purple or black upper leaf surface stipple, bifacial necrotic stipple, leaflet curling, and premature senescence. Total leaf surface injured was 0 � 40%. An increase in stipple as seen with increased ozone concentrations has been reported by Kress and Skelly (1982). In an open�top chamber study in New Jersey using FF, NF, and AA, 2 green ash seedlings had dark stippling late in the season (Elliott et al. 1987). No other symptoms were observed.

Field surveys have also demonstrated the sensitivity of these ash species to season-long ambient ozone exposures. Typical injury was seen in a field survey in Ohio in 1989. Although ozone concentrations were much higher in 1988 no significant symptoms were reported due to the extreme drought conditions which accompanied the weather systems of the 1988 vs the wetter 1989 growing season (Showman 1991). Visible injury has been observed by Bennett et al. (1992) in a field survey in forests of southern Indiana and southern New York in 1981, 1982, and 1986. In an intensive field survey, symptoms were observed at three sites of differing elevations in the Shenandoah National Park, VA. Symptoms increased with increasing ozone concentration and increasing elevation (Hildebrand et al. 1996). Symptoms were reported as a black to purple/black adaxial stipple in both 1991 and 1992.

Yellow-poplar (Liriodendron tulipifera):

In a forest survey, Andersen et al. (1987) observed dark adaxial stippling of yellow-poplar foliage in the Jefferson National Forest, VA; 59% per cent of the yellow�poplar surveyed exhibited symptoms of ozone injury. Higher cumulative ozone concentrations were observed with an increase in elevation. However, Winner et al. (1989) did not observe increasing injury on yellow�poplar with increasing elevation in Shenandoah National Park, VA. Typical injury was observed in a field survey in Indiana in 1989. Ozone concentrations were higher in 1988, however, due to a severe drought no symptoms were observed (Showman 1991).

Davis and Skelly (1992a) reported that older leaves were more sensitive than younger leaves when exposed to ozone; ozone concentrations of 0.075 and 0.150 ppm 6 hr, 2 da/wk, for 12 wks were employed in a CSTR chamber investigation (Davis and Skelly 1992a). In a second study, dark adaxial stipple appeared on oldest leaves when exposed to ozone concentrations of 0.040 or 0.080 ppm from 0830�1530 h / 5 da/wk for 8 or 12 wks (Davis and Skelly 1992b).

In two field surveys, symptoms were observed at sites of different elevations in Shenandoah National Park, Va. and Great Smoky Mountains National Park. Symptoms increased with increasing ozone concentration and increasing elevation at GRSM but not at SHEN (Chappelka et al. 1992). Brown/black to brown adaxial stipple was observed on yellow-poplar foliage in 1991, 1992, and 1993 in Shenandoah National Park, Va. at three sites of differing elevations. In contrast to other studies showing increasing injury at higher elevations and ozone exposures, symptoms were most common at the low elevation and low ozone exposure site (Hildebrand et al.,1996). The yellow-poplar at the low elevation site were growing on a fairly wet site whereas those at the higher elevation were situated on a dry west-facing slope near the ridge top.

In contrast, one study (Endress et al. 1991) reported that no symptoms were induced on yellow-poplar exposed to ozone concentrations of 0.036, 0.108, or 0.172 ppm for 70 hrs with peaks of 0.085, 0.152, or 0.211 ppm.

Understory Species Sensitivities

During a vegetation survey by Anderson et al. (1987), ozone induced foliar symptoms were commonly seen on sassafras, blackberry, dogwood, poison ivy, milkweed, and wild grape in Jefferson National Forest, VA. Ozone symptoms has also been observed on black locust, Clematis spp. and Vitis spp. in Shenandoah National Park, Va. with increasing injury with increasing elevation and ozone exposures reported by Winner et al. (1989). As presented above, ozone injury was light in 1988 due to drought conditions with high ozone but in 1989 ozone induced injury was widespread on blackberry, sweetgum, yellow�poplar, wild grape (Indiana) and white ash, wild grape, and blackberry (Ohio) (Showman 1991).

When fumigated with CF, 1.0, 1.5, and 2.0X AA ozone concentrations, 25 of 28 species shown to have field injury due to ozone showed symptoms. Of 39 species fumigated, 1/3 were sensitive, 1/3 were moderately sensitive, 1/3 exhibited no symptoms (Neufeld et al. 1992).

In a study conducted within CSTR chambers, Davis and Skelly (1992a) concluded that the observed order of ozone sensitivity from most to least sensitive tree species was observed to be black cherry, sweetgum, yellow�poplar, and white ash; symptoms were expressed on these most sensitive species as an adaxial stipple. Trees were exposed to 0.01, 0.075, 0.150 ppb ozone for 6 hr/da 2da/wk/12 wks). Within this same study, red maple and yellow birch only exhibited chlorosis while northern red oak showed no visible injury.

Conifers

Jack pine (Pinus banksiana), Eastern white pine (P. strobus):

Low amounts of chlorotic mottle increased with an increasing ozone gradient on seven populations of jack pine and eastern white pine were reported following an Indiana field survey conducted by Armentano and Menges (1987). Greatest injury was seen on juvenile trees and several site factors caused other interactions.

Tipburn and chlorotic mottling were seen in 23% of sampled eastern white pine stands in a field survey of 6 southeastern states. More injury occurred on plantation trees than those in natural stands, and more injury occurred on trees growing on southwest facing slopes. Highest incidence of injury occurred in Kentucky, and least in Georgia (Andersen et al. 1988). Due to numerous suspected causes, the foliar injury symptoms on eastern white pine have become very confusing (Skelly, personal communication ). Thus, we have not included other citations at this time.

Loblolly pine (P. taeda):

Meier et al. (1990) reported chlorotic mottling and flecking at 0.10 � 0.150 ppm ozone exposures within the first week, increasing in intensity and area with time. No symptoms appeared when plants were exposed to 0 or 0.050 ppm for 6 or 12 weeks. Symptoms of banded chlorosis, tipburn, and premature senescence were observed (after 3 wks in high exposures of 0.320 ppm ozone and 6 wks in 0.160 ppm ozone (Wiselogel et al. 1991).

In a study by Shafer et al. (1987) open�top chambers were used and loblolly pine seedlings were exposed to AA, CF, NF, 1.25,1.5, 1.75, 2.0 X AA ozone concentrations (Shafer et al. 1987). Chlorotic mottle, tipburn, necrosis, and needle abscission from lower stem occurred in plots exposed to all concentrations, but were more pronounced for plants exposed to greater than ambient ozone concentrations.

In a later study, Shafer and Heagle (1989) exposed loblolly pine in open-top chambers with 0.022 to 0.092 ppm seasonal mean ozone concentrations; ozone exposures were delivered at CF, NF, 1.33, 1.67, 2.0, and 3.0X AA in 1988, 1989, and 1990. Symptoms observed included chlorosis and needle necrosis which increased with increased ozone beginning at 0.06 ppm. No changes in growth occurred. Symptoms were seen in the top half of each plant. All elevated ozone treatments caused decreased foliar retention, especially after exposure to130 � 220 ppm�hr ozone. The longer seedlings stayed in CF chambers, significantly greater needle retention in 3rd growing season resulted (Stow et al. 1992).

Pitch pine (P. rigida):

Scherzer and McClenahen (1989) observed visible injury after 4 days with fumigations of 0.30 ppm ozone. After the second fumigation at 0.20 and 0.30 ppm ozone, injury appeared as chlorotic mottle and tip burn, especially on the oldest leaves. Symptoms induced by 0.40 ppm ozone were tan flecking, mottling, and tip necrosis.

McQuattie and Schier (1993) observed chlorotic tip and curvature of midsection needle portions on 20 � 25% of exposed pitch pine needles beginning with 0.10 ppm ozone exposure. No symptoms were induced at 0.050 ppm ozone, but there were 50% chlorotic needles with high exposures of 0.20 ppm ozone concentrations.

Red spruce (Picea rubens):

Fincher et al. (1992), in an open-top chamber study, demonstrated that trees with winter injury had increased injury with increasing ozone concentration. Exposures were CF, NF, 2.0, 3.0, and 4.0X AA. with mean ambient ozone concentrations (NF) of 0.029 and 0.040 ppm for 24-hr and 7-hr-day, respectively. Browning of sensitive trees in spring increased with the increased ozone treatments.

No symptoms of ozone injury were observed on red spruce seedlings at Whitetop Mt, VA, when grown in exclusion chambers or in ambient air. (Thornton et al. 1990). Flecking increased with needle age and on two mountains increased with elevation in a field survey in Great Smoky Mountains National Park. However, ozone was not monitored (Andersen et al. 1991).

General Conclusions

Tropospheric ozone air pollution has repeatedly been shown to cause foliar injury on sensitive species throughout much of the SAMI region. On broadleaf species, foliar injury has been observed as a mid- to late-season adaxial stipple, leaf reddening, and early leaf senescence. Under ambient exposures, symptoms on conifers are less evident due to many mimicking symptoms. Ozone injury has been confirmed only on a few species of trees and understory vegetation in the SAMI region. More research is need in this area.

Foliar ozone injury has been induced following exposures within laboratory, greenhouse and field open-top chamber conditions of fumigation. Open-top chambers have been used under natural field conditions for the protection of forest species from ambient ozone exposures on a season-long basis. Clear differences in symptom expression have consistently been noted following such treatments.

III. INTERACTIONS OF O3 AND OTHER STRESS FACTORS

Trees grow in a dynamic environment, and are continuously exposed to a wide variety of climatic and edaphic conditions. Plant response can be altered by various abiotic and biotic factors, and O3 can predispose plants to various pests and pathogens.

Abiotic factors such as temperature, moisture, solar radiation and nutrition can all have a significant influence on tree response to ozone (Chappelka and Chevone 1992, Chappelka and Freer-Smith 1995, McLaughlin and Downing 1995). In addition, ozone, alone or in combination with other air-borne contaminants in various physical forms (aerosols, gases or precipitation), has been observed to alter tree response (Chappelka and Chevone 1992, Chappelka et al. 1985, Mahoney et al. 1984).

Biotic factors can influence tree response to ozone. Trees can be weakened by ozone and predisposed to other stresses, such as insects and plant pathogens. In addition, other factors, including symbiotic relationships (mycorrhizae) can be affected (Meier et al. 1990, Chappelka and Chevone 1992).

Most recent interest regarding pollutant interactions has centered on the combinations of ozone and acidic precipitation, as would be expected to occur under ambient conditions and forest situations. It is important to note that the majority of these have reported interactive effects when either the ozone exposures and/or the pH of treatment rainfalls were extreme. Lee et al. (1990b) demonstrated that branch water potential in red spruce was reduced following exposures to 0.100 ppm ozone and rainfall pH of 3.0 as compared to red spruce exposed to 0.025 ppm ozone and rainfall pH of 5.6; no interactive effects on growth were reported for either treatment scenario.

Several studies on hardwood tree species of the SAMI region yielded similar results. Cannon (1993) reported that the lowest relative growth rate (RGR) was seen in exposures of white oak seedlings to 0.15 ppm ozone and rainfall pH of 4.2 as compared to CF air and rainfall pH of 4.2 which had the highest RGR. In contrast within the same study, red oak had the highest RGR following exposures to CF air and rainfall pH of 3.0. Jensen and Patton (1990) studied effects of combinations of ozone and acidic precipitation on seedling yellow-poplar and reported that dry weight and RGR decreased linearly following exposures to 0.05 and 0.100 ppm ozone and decreasing pH treatments. They reported increased swelling of the mesophyll area of leaves with increasing ozone and decreasing pH, ie., air space in the mesophyll region was reduced. Increasing ozone exposures and lower pH of delivered precipitation also resulted in decreased height, and leaf and new growth dry weights. White ash seedlings were exposed by Chappelka and Chevone (1986) to ozone exposures of 0, 0.050, 0.100, and 0.150 ppm for 5 d/wk, for 5 wks with varying pHs of delivered rainfall. Visible foliar injury expressed as an adaxial purple-white stipple was observed only following the highest ozone exposure (0.150 ppm ozone) treatments; symptomatic areas eventually coalesced with necrotic lesions on 61% of the seedlings. Ozone exposures at 0.150 ppm and pH rainfall treatments at 3.0 resulted in less injury, but still 54 % of the exposed white ash seedlings developed necrotic lesions.

Several studies (eg. Kress et al. 1982, Chappelka et al. 1985, Winner et al. 1987) have been conducted with forest tree species indigenous to the SAMI region with the goal of understanding the potential interactions of gaseous pollutants in combination on forest tree seedling exposure/responses. Unfortunately, for a variety of reasons (square-wave fumigations, simultaneous exposures, high concentrations, etc.), all of these studies have been conducted at unrealistic pollutant exposures. Although these studies have been placed in the annotated bibliography, due to their non-applicability to ambient conditions within the SAMI region, they will not be further discussed in this report.

Similarly, several reports of potential interactions of ozone exposures with biotic pests and pathogens have been included in the annotated bibliography, but due to effects only being observed at extreme ozone exposures in most of the controlled studies, little relevance to natural conditions must be concluded (Endress et al. 1991, Carey and Kelley 1994). A few studies of abiotic stressors such as increasing frost damage to red spruce with increasing ozone exposures (Fincher et al. 1989), and interactions with drought conditions leading to less effect (Showman 1991) suggest numerous possible interactive effects with of ambient ozone with additional environmental factors.

Hildebrand et al. (1996) reported microsite differences in response of yellow-poplar to ozone within the Shenandoah National Park, especially in relation to soil moisture availability and its direct influence on foliar symptom development even at relatively low ozone exposures. Lefohn et al. (1996) used analytical procedures that combined experimental ozone exposure response data with ambient ozone exposure data and soil moisture indices. They found that potential areas of greatest ozone impact (possible reductions in growth) in the SAMI region could be altered depending on soil moisture conditions. This approach is discussed in detail later in this report (sections VI and VII)). McLaughlin and Downing (1995) reported relationships between ozone, moisture stress and radial growth of loblolly pine growing in eastern TN. The interaction of increased soil moisture deficit with increased ozone concentrations resulted in a decrease in annual radial growth rates. Reductions in growth were predicted to vary from 7% in a relatively wet year to 30% in a relatively drier year. This report was controversial in nature and is discussed in detail in a later section (section V) of this document.

General Conclusions

The ambient environment exerts a profound influence on the physiological status of a plant and, therefore, its response to ozone. No studies to date have examined the effects of changing environmental conditions on tree growth, using ambient or near-ambient ozone concentrations. Results demonstrate that moisture stress can have a profound effect on tree response to ozone. It is clear from the evidence presented that visible injury is less under conditions of extreme moisture stress (Showman 1991, Hildebrand et al. 1996). Results are not as clear regarding growth effects (McLaughlin and Downing 1995, Lefohn et al. 1996). More research, under controlled field conditions with several different tree species is needed to confirm these findings.

Biotic factors can influence tree response to ozone. Tree sensitivity to other stresses, such as insects and biotic plant pathogens, can be altered by exposure to ozone (Chappelka and Chevone 1992). However, knowledge is limited to only a few stress-tree systems under very controlled conditions. Research needs to be expanded to encompass a greater variety of interactions in more realistic field conditions. In addition, very little research has been conducted on mechanisms influencing these systems. The establishment of either a biochemical or physiological basis for the alteration of insect/pathogen success on trees is needed.

IV. PHYSIOLOGICAL EFFECTS

Mechanisms of Ozone Toxicity

Ozone enters the leaf mainly through the stomata and once inside the leaf may form hydrogen peroxide, superoxide anions and hydroxyl and organic free radicals. These chemical species possess a high oxidizing potential and may attack various cellular sites (Pell 1987). Ozone may reduce carbon fixation directly by affecting steps in the carbon fixation process or indirectly by reducing stomatal opening and subsequent diffusion of CO2 into the leaf (Heath 1994). Ozone stress may reduce carbon fixation, increase respirational demands, alter the partitioning of carbon into different chemical forms, and disrupt the allocation or flow of carbon among plant tissues (Laurence et al. 1994, Samuelson and Kelly 1996). Shifts in plant nutritional status may occur from ozone-induced changes in carbon metabolism, tissue growth and leaf senescence (Baker et al. 1994). These changes in carbon dynamics may reduce total plant growth and affect the growth of specific plant organs. A decline in root growth is a widely cited response to ozone-induced changes in carbon metabolism (Pell et al. 1994). Winner (1994) suggests that to some extent, changes in carbon allocation and partitioning may be viewed as compensatory responses that enable plants to maintain growth during stress. Reductions in carbon allocation to roots and reduced root-to-shoot ratios may maintain above-ground structures and photosynthesis during stress for short periods of time. However, in long-lived trees exposed to a multiple stress environment, the long-term impact of ozone-induced changes in carbon metabolism on growth is unknown.

Tree Physiological Response to Ozone: Tree Species in the SAMI Region

Current knowledge of physiological ozone sensitivity in forest trees growing throughout the SAMI region is limited to six broadleaf and five coniferous species. These are yellow-poplar (Liriodendron tulipifera), sugar maple (Acer saccharum), red maple (Acer rubrum), black cherry (Prunus serotina), northern red oak (Quercus rubra), white oak (Quercus alba), red spruce (Picea rubens), Fraser fir (Abies fraseri), loblolly pine (Pinus taeda), shortleaf pine (Pinus echinata), and eastern white pine (Pinus strobus). This review will focus on the influence of ozone on the most studied physiological processes; net photosynthesis, stomatal conductance, carbon allocation or partitioning, and nutrient allocation. Unless mentioned, plants were exposed to ozone in controlled environmental chambers or continuously stirred reactors. Only open-top chamber studies conducted in the SAMI region were included, because these studies provided more realistic experimental environments and ozone exposures than open-top chamber studies conducted outside the SAMI region.

Yellow-poplar

Studies with yellow-poplar seedlings report little physiological ozone sensitivity, defined by changes in carbon assimilation, carbon partitioning or nutrient allocation (Table 1). An exception was observed by Chappelka et al. (1988) who detected a 15% reduction in stomatal conductance in response to 6 weeks (4 hr/day, 5 day/week) of exposure to 0.10 ppm ozone, but net photosynthesis was unaffected by ozone exposure. In contrast, a 24% reduction in net photosynthesis was reported from exposure to 0.10 ppm ozone for 8 hr/day, 3 day/week for 3 months (Roberts 1990). However, seedlings exposed to ambient + 60 ppm concentrations of ozone for five months in open-top chambers in Oak Ridge, TN exhibited no change in net photosynthesis or stomatal conductance.

Northern red oak and white oak

Northern red oak and white oak are components of many forest cover types in the SAMI region. An open-top chamber study conducted in Norris, TN reported little influence of ambient and twice ambient ozone concentrations on net photosynthesis and stomatal conductance of northern red oak seedlings after two growing seasons of ozone exposure (Samuelson and Edwards 1993; Hanson et al. 1994). In contrast, Reich et al. (1986) observed a 20% reduction in net photosynthesis of northern red oak seedlings in response to fumigation with 0.12 ppm ozone for 7 hr/day, 5 day/week for 10 weeks (Table 1). For mature trees, photosynthetic response to ozone was linear and could be predicted using cumulative ozone uptake or the SUM0 index (Hanson et al. 1994). They (Hanson et al. 1994 ) reported that 32-year-old northern red oak trees exhibited a 25% and 50% reduction in net photosynthesis in response to ambient and twice ambient ozone concentrations, respectively. In addition, carbon partitioning and allocation, and nutritional status of mature trees were more affected by ozone exposure than seedlings (Samuelson and Kelly 1996, Samuelson et al. 1996). However, photosynthetic reductions of up to 50% and changes in carbon dynamics in mature trees in response to twice ambient ozone concentrations were not accompanied by growth reductions. A companion field study of ozone uptake in northern red oak seedlings and mature forest trees growing in the Great Smoky Mountains National Park observed similar ozone uptake rates as in the controlled study (Samuelson and Kelly 1997).

The one study that examined white oak response to ozone reported no influence of two seasons of exposure to above ambient ozone concentrations on seedling net photosynthesis and stomatal conductance (Foster et al. 1990).

Black cherry

Black cherry has been suggested as an indicator species because of the high incidence of visible foliar injury reported by field foliar surveys of the SAMI region (Chappelka et al. 1992). Reductions in carbon uptake have been documented for leaves showing visible injury. For example, after one growing season of fumigation with twice ambient concentrations of ozone in shaded open-top chambers in Norris, TN, black cherry seedlings exhibited a 23% reduction in net photosynthesis of leaves with visible injury scores of 1-6% (Table 1) (Samuelson 1994a). In an uncontrolled field study conducted in north-central Pennsylvania, Fredericksen et al. (1996) observed negative correlations between visible foliar injury and net photosynthesis in seedling, sapling and mature tree leaves. These data suggest that for black cherry, visible injury may be related to reductions in leaf physiological rates.

Sugar maple and red maple

Reductions in leaf physiological function because of ozone exposure have been reported for sugar maple and red maple (Table 1). Reich et al. (1986) observed a 30% decline in net photosynthesis of sugar maple seedlings exposed to 0.12 ppm ozone concentrations for 7 hr/day, 5 day/week for 10 weeks. An ozone concentration of 0.10 ppm delivered continuously for 74 days reduced the photosynthetic capacity of sugar maple seedlings only when seedlings were grown under 7% of full sunlight (Volin et al. 1993). In an open-top chamber study in the SAMI region (Norris, TN), a 23% reduction in net photosynthesis of shaded red maple seedlings was detected in response to ambient concentrations of ozone after one season of exposure (Samuelson 1994a).

Red spruce and Fraser fir

Red spruce has received much research attention because of reported declines in growth in the SAMI region (McLaughlin and Kohut 1992). The majority of ozone research, however, indicates that red spruce is relatively insensitive to ozone. For example, six studies relevant to the SAMI region report no influence of ozone on net photosynthesis, stomatal conductance, or carbon partitioning and allocation patterns (Table 1). Thornton et al. (1994) summarized three years of collaborative research on the impact of ozone on red spruce growing on Whitetop Mountain, VA. The influence of controlled ozone exposure on seedlings and mature tree branches, and uncontrolled ambient ozone exposure on seedlings, saplings and mature trees was evaluated. The authors concluded that ambient ozone concentrations at Whitetop Mountain had little influence on red spruce physiological function.

Similarly, two reports of Fraser fir found no influence of ozone on foliar physiological function. For example, exposure to 0.10 ppm ozone for 4 h/day and 3 day/week had no influence on net photosynthesis and stomatal conductance of Fraser fir seedlings (Tseng et al. 1988). Likewise, Fraser fir seedlings subjected to a total of five accelerated 10-week growth cycles and exposed to ozone concentrations as high as 0.15 ppm during each cycle exhibited no change in net photosynthesis or stomatal conductance (Seiler et al. 1994).

Loblolly and shortleaf pine

Because loblolly pine is the most important commercial timber species in the southern United States, considerable effort has been devoted to the assessment of loblolly pine response to air pollution. Kelly et al. (1993) summarized three years of data gathered by the multidisciplinary research program, Response of Plants to Interacting Stress (ROPIS), that investigated loblolly pine response to ozone (Table 1). This open-top chamber field study was conducted in the SAMI region (Oak Ridge, TN). Seedlings exposed to twice ambient ozone concentrations exhibited increases in compensatory photosynthesis and respiratory losses, changes in the allocation and partitioning of carbon, and shifts in nutritional status. However, the magnitude and occurrence of these responses varied over the three growing seasons.

Sasek and Flagler (1995) reviewed research, conducted mainly outside the SAMI region (most studies were conducted in SAMI states, however), on loblolly pine physiological response to ozone and concluded that "exposure-response relationships for loblolly pine (seedling) photosynthesis suggest that these ambient exposures (100 to 150 ppm-h, 12-h summation during the growing season) could decrease instantaneous photosynthesis compared to 'clean air,' leading to less total carbon fixation during a needle's functional life span."

The one open-top chamber study of shortleaf pine response to ozone near the SAMI region (Piedmont of South Carolina) reported alterations in seedling carbon partitioning from two years of exposure to 2.5 times ambient ozone concentrations (Paynter et al. 1992).

Eastern white pine

Early research with white pine conducted in the 1970's reported photosynthetic reductions in seedlings exposed to high concentrations of ozone for short durations (Botkin et al. 1972). More recent work (Table 1) observed a 20% decline in net photosynthesis in sensitive clones after 50 days of fumigation for 4 h/day with 0.10 ppm ozone (Yang et al. 1983). Similarly, Boyer et al. (1986) reported varying photosynthetic sensitivity to ozone in different white pine clones. Alterations in seedling nutritional status and a 20% reduction in needle photosynthesis was observed in response to an ozone exposure of 0.14 ppm for 7 h/day, 3 d/week for 4 months (Reich et al. 1987, 1988). An uncontrolled field study conducted in the SAMI region (Oak Ridge, TN) reported changes in carbon allocation and increased foliar respiration in 25-yr-old white pine trees ranked as ozone sensitive based on length, color and longevity of needles (McLaughlin et al. 1982).

Ozone-Environment Interactions

Very few experiments investigated the influence of ozone in combination with other environmental stresses, and the majority of these studies were conducted outside the SAMI region. Existing data are limited to short-term seedling responses and to 2-way interactions between ozone and either water stress, fertility or light. Physiological response to ozone and water stress was examined in yellow-poplar, loblolly pine and Fraser fir. Although water stress reduced photosynthesis of yellow-poplar, ozone exposure in combination with drought did not result in larger reductions in photosynthesis (Cannon et al. 1993, Roberts 1990). However, Lee et al. (1990b) reported greater photosynthetic sensitivity to water stress in loblolly pine seedlings exposed to 0.10 ppm ozone for 4 h/day, 3 day/week for 10 weeks. In contrast, no interaction between water stress and ozone exposure of 0.15 ppm for 5 hr/day, 5 day/week for 12 weeks was reported for loblolly pine seedlings by Meier et al. (1990). Similarly, the influence of ozone on photosynthesis was not dependent on the degree of water stress in Fraser fir seedlings (Tseng et al. 1988). Differences in the duration and magnitude of water stress among these studies limit our understanding of water stress and ozone interactions. The level of water stress that reduces ozone uptake and the ability of a tree to tolerate reductions in photosynthesis during drought varies by species, stress history, environmental conditions, leaf age and tree size.

The interactive influence of ozone and plant nutrition was examined in red spruce, white pine, loblolly pine and yellow-poplar. For example, ozone exposure in combination with varying leaf nitrogen levels did not affect foliar carbohydrates in 20-yr-old red spruce saplings (Amundson et al. 1995). Likewise, soil type did not influence ozone-induced photosynthetic decline in white pine seedlings (Reich et al. 1987). Similarly, no interactive influence of ozone and soil nitrogen on photosynthesis of loblolly pine or yellow-poplar seedlings was detected (Tjoelker et al. 1991). Although these results suggest that nutrition does not influence physiological ozone sensitivity, the positive relationship between leaf nitrogen concentration and stomatal conductance (Field 1991) suggests that foliar nitrogen plays an important role in regulating ozone uptake.

Volin et al. (1993) examined the influence of light on ozone sensitivity in sugar maple seedlings and noted that photosynthesis was more sensitive to ozone in seedlings grown under low irradiance. Conversely, ozone-induced reductions in photosynthesis were greater in hybrid poplar when seedlings were grown under high irradiance (Volin et al. 1993). In contrast, northern red oak seedlings grown under a 80% reduction of ambient light exhibited the same photosynthetic sensitivity to ozone as did seedlings grown in the full sun (Samuelson 1994b). Because the majority of ozone exposure research with species in the SAMI region was conducted in controlled environmental chambers, growth chambers or continuously stirred reactors that typically provide low light levels during ozone exposure, ozone uptake and subsequent physiological responses are likely confounded by variation in light levels among studies.

Ozone Uptake

Ozone dose or uptake by the leaf is considered physiologically more relevant to the plant than external ozone exposure. Diffusion of ozone into the leaf is dependent on the concentration of ozone surrounding the leaf, resistance to diffusion at the leaf surface and leaf interior, stomatal density, degree of stomatal opening, and ozone deposition on exterior and interior leaf surfaces (Taylor et al. 1988). Reich (1987) concluded that the influence of ozone on net photosynthesis of different plant species could be quantified using stomatal conductance and ozone uptake. The effective ozone dose is usually calculated using the product of ozone concentration and stomatal conductance to water vapor, adjusted for the diffusivity of ozone in air (Hanson et al. 1994). Stomatal opening and hence leaf ozone uptake is controlled by complex interactions between the environment and plant. In general, environmental conditions that accompany high ozone concentrations such as high temperature, high vapor pressure deficit and low soil water reduce stomatal opening and ozone flux into the leaf (Wieser and Havranek 1995). However, stomatal response to the environment may vary depending on the species, age of the tree, leaf phenology, leaf nutrients and time of year (Teskey 1995). In addition, ozone-induced reductions in photosynthesis may reduce stomatal conductance and limit further ozone uptake (Weber et al. 1993).

Using estimates of ozone uptake and seedling physiological response to ozone in controlled studies, Reich (1987) concluded that hardwood species are more sensitive to ozone than coniferous species due to greater stomatal conductance in hardwood leaves. For mature forest trees, ozone uptake and dose-response functions are difficult to estimate given the variation in ozone concentration, microclimate and stomatal conductance within complex, mature tree canopies. In addition, physiological and morphological differences between different size trees may affect ozone uptake and physiological ozone sensitivity (Samuelson and Edwards 1993). Studies of ozone uptake in mature tree species relevant to the SAMI region indicate that ozone uptake rates vary among different size trees. Fredericksen et al. (1995) report greater ozone uptake rates in leaves of black cherry seedlings than in leaves of mature forest trees, but cumulative ozone doses calculated on a whole plant basis were lower for seedlings due to indeterminant shoot growth. Greater cumulative doses and physiological sensitivity to ozone were documented for mature northern red oak trees than for seedlings due to greater stomatal conductance, ozone uptake and total leaf area in mature trees (Samuelson and Edwards 1993, Hanson et al. 1994, Samuelson and Kelly 1996). In an uncontrolled field study conducted in the Great Smoky Mountains National Park, mature black cherry, red maple, and northern red oak trees had greater stomatal conductance and ozone uptake than understory seedlings and saplings (Samuelson and Kelly 1997). Diurnal patterns of stomatal conductance and ozone uptake differ between seedlings and mature loblolly pine trees (Sasek and Flagler 1995). For red spruce, ozone uptake was as much as two-fold greater in seedling scions than mature tree scions and larger ozone-induced reductions in photosynthesis were detected in mature tree scions (Rebbeck et al. 1993). These studies indicate the need for mature tree research and scaling studies.

General Conclusions

Physiological studies of ozone impacts to trees dominant in the SAMI region are limited to 11 species. The usefulness of continuously stirred tank reactors (CSTRs) and controlled environmental chamber studies in the assessment of forest tree response to ozone is limited by the lack of natural experimental environments and realistic ozone exposures. In addition, our ability to detect a small but biologically significant ozone response is hindered by low replication both within and between studies, and by short exposure duration. For some species such as white oak, only one report of ozone sensitivity exists. Three growing seasons, which is an extremely short time relative to a 300-year lifespan of a late-successional tree species, is the longest study duration reported by this review. While studies spanning the entire life of a tree are unfeasible, research is needed to understand the integration of ozone damage in long-lived species. The use of existing seedling literature in the assessment of forest tree response to ozone is further limited by interactions among ozone exposure and leaf area dynamics. The majority of reviewed reports examined physiological ozone sensitivity in one leaf age class, usually a recently expanded leaf. Because most tree species express multiple flushing, indeterminant leaf growth or free growth in the seedling stage, ozone impacts on whole seedling photosynthetic function are not well understood.

Seedling pot studies conducted under optimum conditions will not likely predict mature forest tree responses given the potential for interactions between ozone and other environmental stresses, and age or size dependent variation in ozone sensitivity. Scaling studies with northern red oak and black cherry indicate that general species level assessments may not accurately describe sensitivity of different developmental stages. Research is needed to understand interactions among ozone exposures, tree age or size and location in the canopy, leaf area dynamics, and co-occurring environmental and competitive stresses. Quantification of whole tree photosynthetic response to ozone will likely require the use of process-based models. Given that physiological changes often do not result in growth reductions, the impact of ozone-induced declines in physiological function on tree and forest productivity is unknown.

Finally, genetic variation in physiological sensitivity to ozone complicates the assessment of species sensitivity to ozone. Taylor (1994) suggests that genetic variation in ozone resistance may be identifiable by family differences in stomatal physiology and hence ozone uptake. For small trees, stomatal physiology may be a potentially useful tool in the identification of genetic variation in ozone sensitivity.

V. GROWTH RESPONSES

Ozone effects originate with initial injury at the biochemical level and can potentially manifest themselves as reductions in growth. Early literature concerning ozone effects on plants reported response based on visible foliar injury (Davis and Wilhour, 1976). Foliar injury, in general, is not directly related to growth reductions in trees exposed to long-term, ambient or near-ambient concentrations of ozone (Chappelka and Chevone 1992, Flagler and Chappelka 1995). Visible foliar injury generally indicates lost photosynthetic area following a failure of cellular homeostasis. Relatively low concentrations of ozone can reduce photosynthetic efficiency and increase respiration without the loss of homeostasis. Because short-duration, low concentration exposures of ozone cause minimal effects on photosynthesis, subtle injuries are observed as a cumulative result of longer-term exposures. Since trees are perennials, and are exposed to some amount of ozone continuously, primary interest has involved the study of alterations in growth and productivity under chronic ozone exposure regimes, irrespective of visible symptom expression.

The majority of research regarding growth effects in the SAMI region, is with young trees in pots, and the primary species studied is loblolly pine. This is mainly due to the large amount of funding devoted to research on this species as part of the National Atmospheric Precipitation Program (NAPAP) effort (Fox and Mickler 1995). Loblolly pine is a minor component in the Class I areas, but is common in the SAMI region, and therefore, will be included in the assessment.

The purpose of this section will be to assess major findings critically, identify knowledge gaps and make recommendations for future research. To facilitate discussion, this section will be divided into several subsections: Greenhouse studies, controlled field studies, uncontrolled field studies, modeling, conclusions and recommendations for future research.

Greenhouse Studies

The major portion of research on tree response to ozone has been conducted in greenhouse experiments with seedlings. The reasons for this are obvious; seedlings are easy to manage, adapted for pot studies, and can be used in indoor fumigation facilities, such as continuously stirred tank reactors (CSTRs). Results from greenhouse studies need to be interpreted with caution, however. Plants differ morphologically and physiologically from those grown in the field, and pollutant response can be altered (Lewis and Brennan, 1977). Several factors that make it difficult to relate laboratory studies to field situations include: soil nutrient status, water availability, tree age, temperature, and duration and fluctuations in ozone concentrations under ambient conditions.

Eastern Hardwoods

Kress and Skelly (1982a) exposed 2-4-week-old seedlings of 10 eastern forest species 6 hours per day for 28 consecutive days to ozone to various square-wave ozone concentrations (0.0-0.15 ppm) in CSTRs. Loblolly pine (wild-type) and American sycamore exhibited the greatest depressions in growth (linear with concentration), and this reduction became evident at the 0.05 ppm treatment. Pitch pine, sweetgum and green ash exhibited effects between 0.06 and 0.100 ppm, and yellow-poplar and sugar maple growth reductions manifested themselves between 0.100 and 0.150 ppm. Yellow-poplar and white ash exhibited large amounts of visible symptoms to ozone, but were intermediate to tolerant in growth response, indicating that visible and growth suppressions are not necessarily correlated with each other. This research stimulated much interest in ozone effects studies on southern trees.

Jensen and Dochinger (1989) exposed 10 different eastern hardwood species common to the SAMI region 8 hours per day, 3 days per week for 16 weeks in CSTRs to different combinations of ozone (0.070 and 0.150 ppm), sulfur dioxide and acidic precipitation. Based on growth and visible injury responses, they divided the groups into two sensitivity groups. White ash, yellow birch, sweetgum, red maple, sugar maple and yellow-poplar were considered relatively sensitive to ozone. Sugar maple exhibited no visible symptoms, but did express growth reductions. All other species exhibited both visible symptoms and decreases in growth with increasing concentrations of ozone. The tolerant group included both American and European beech, shagbark hickory and white oak.

Reich et al. (1986) observed similar responses when fumigating sugar maple and northern red oak to ozone at various concentrations ranging from 0.02-0.12 ppm seven hours per day, five days per week for up to ten weeks. Northern red oak was tolerant to ozone, but exposure of sugar maple to this pollutant did result in a 9% decrease in plant dry weight and a 13% decrease in leaf area at the highest concentration.

Based on the studies above, Davis and Skelly (1992b) exposed in CSTRs four species of eastern hardwoods, black cherry, red maple, northern red oak and yellow-poplar to various levels of ozone (0.040 or 0.080 ppm), sulfur dioxide and acidic precipitation for 5 hours per week for either 8 or 12 weeks. Black cherry was the most sensitive regarding growth and biomass reductions of elevated ozone (0.080) across all other treatments. Red oak was the least sensitive and the other two species (yellow-poplar and red maple) intermediate in sensitivity.

Chappelka and coworkers (Chappelka et al. 1985, Chappelka and Chevone 1986, Chappelka et al. 1988a, 1988b) conducted a series of laboratory experiments (CSTRs) to determine the sensitivity of yellow-poplar, green ash and white ash to ozone alone or in combination to other pollutants including sulfur dioxide and acidic precipitation. Yellow-poplar was intermediate to tolerant to ozone alone, but this response was exacerbated in combination with other pollutants (Chappelka et al. 1985, 1988a). White ash, however, was reported to be sensitive (linear decreases in growth) to increasing concentrations of ozone (0.025-0.15 ppm), with the greatest response occurring with decreases in root growth (Chappelka and Chevone 1986, Chappelka et al. 1988b). The only growth component affected by ozone regarding green ash, was shoot elongation, which was significantly decreased at the highest (0.10 ppm) ozone treatment (Chappelka et al. 1988b).

Coniferous species

In a study to determine if differential genetic sensitivity to ozone exists, Kress et al. (1982) fumigated (CSTRs) seedlings of 18 full sibling families of loblolly pine to increasing ozone levels (0.00-0.20 ppm). They found a wide variation in foliar sensitivity to ozone exposures, indicating some genetic control in ozone sensitivity. These results were confirmed in a series of studies using over 100 open-pollinated half-sibling families of loblolly pine grown throughout the southern pine (including the SAMI region) region (McLaughlin et al. 1993, Shafer et al. 1993, Wiselogel et al. 1991). Ozone levels > 0.160 ppm produced visible injury in all families. Reductions in growth, however, were not directly correlated with visible injury, with certain families exhibiting greater suppressions in growth than others. These results were confirmed in an independent study by Winner et al. (1987).

Several studies have reported decreased biomass production of loblolly pine with increased ozone exposure (Horton et al. 1990, McLaughlin et al. 1993, Shafer et al. 1993, Wiselogel et al. 1991). All plant component parts examined (roots, foliage, stems) exhibited deceases in growth. Results were variable depending on family and exposure concentrations used. These results are summarized in more detail in Flagler and Chappelka (1995).

Horton et al. (1990) found that potting media had a large influence on loblolly pine response to ozone. They found that root biomass was decreased more than above-ground biomass in response to ozone exposures of 0.320 ppm, 6 hours per day, four days per week for two months, but the response varied with the growing media used. The decrease in root biomass was greater when the seedlings were grown in a peat-vermiculite commercial growth media than in mineral soil. The decrease in above-ground biomass was not significantly affected by the growing media used.

Pitch pine was moderately sensitive to ozone with the greatest reductions in growth occurring at the highest ozone concentrations (0.20-0.30 ppm) (Scherzer and McClenahen 1989, Schier et al. (1990). A differential sensitivity to ozone among different half-sibling families was observed (Scherzer and McClenahen 1989) and ozone interacted to causes a significant decrease in root weight was observed at high levels of aluminum and ozone (Schier et al. 1989).

Other coniferous species exposed to elevated ozone concentrations exhibited little if any growth responses. These species include red spruce ( Lee et al. 1990, Taylor et al. 1987), white pine (Reich et al. 1987) and Fraser fir (Seiler et al. 1994, Tseng et al. 1988).

Summary

Growth responses to ozone have been reported for individual trees that occur in the SAMI region. Most of these studies are, however, with individual seedlings (< 2 yrs in age) under controlled conditions (CSTRs). Most studies were short-term (< one year), and were with potted seedlings. Major findings regarding O3 effects on biomass production and growth from controlled fumigation studies are shown in Table 2. The greatest reductions in growth were observed at the highest ozone concentrations. The majority of these levels do not currently occur in the field at the present time. Growth response to ozone was not necessarily correlated with visible injury, and different genotypes within a species exhibited differential responses to ozone exposure. Results are limited regarding the number of species exposed, but certain species such as black cherry, loblolly pine, white ash, American sycamore and yellow-poplar appear to be intermediate to sensitive in growth responses to ozone. Response was quite variable, however, and was influenced by many factors, including environmental conditions before, during and after fumigation, and seedling genotype.

Controlled Field Exposures

Eastern Hardwoods

In an early investigation in the Shenandoah Mountains of Virginia, Duchelle et al. (1982) exposed eight tree species to ambient and sub-ambient levels of ozone in open-top chambers for two years. Tree species exposed included: Liriodendron tulipifera, Liquidambar styraciflua, Fraxinus pennsylvanica, Robinia pseudoacaica, P. pungens, P. strobus, P. virgininana and Tsuga canadensis. All species exhibited reduced height growth in ambient air compared with those grown in sub-ambient levels of ozone. Reductions in growth, however, were not necessarily correlated with visible foliar symptoms of ozone injury.

Neufeld et al. (1992) exposed 39 different plant and tree species native to Great Smoky Mountains National Park (GSMNP) to concentrations ranging from 0.5X ambient to 2X ambient in open-top chambers. They reported that approximately 33% of the species fumigated were classified as sensitive to ozone, regarding visible foliar injury. Some of these species also exhibited reductions in growth and biomass. However, other species demonstrated these reductions without visible injury. Based on this initial study, Neufeld et al. (1995) exposed two different sets of black cherry seedlings growing in pots in a commercial potting mixture to increasing ozone concentrations (CF-2X ambient) for one growing season each. Exposures occurred in open-top chambers in GSMNP near Gatinburg, TN. At the end of each growing season plants were harvested and growth was measured. A decrease in total, leaf, root and stem + root biomass, and the number of leaves present at 2X ambient was observed both years of the study. Using a combined data set (1989 and 19992) data set a Weibull model was used to determine exposure-response relationships. Based on the model, leaf parameters were identified as the most severely impacted plant component, followed by root weight. Seasonal growth losses ranged from 1-2% when NF-treated plants were compared with controls for all plant components. The SUM06 and AOT40 indices showed the best fits of the data to the model and SUM00 the least fit.

Samuelson (1994a) exposed black cherry (Prunus serotina) and red maple (Acer rubrum) seedlings to sub-ambient, ambient and twice ambient concentrations of ozone in open-top chambers for one growing season. Seedlings were grown in pots in native soil and in reduced light (25% ambient) to simulate regeneration in the understory of mature trees. No reductions in height growth of red maple were observed, however net photosynthesis was decreased and visible foliar injury observed at the highest ozone levels. Black cherry exhibited reduced height growth, decreased photosynthesis and increased visible foliar injury as ozone concentrations increased from subambient to 2X ambient.

To determine if results obtained from seedling studies can be compared with those from large trees several studies were conducted with northern red oak (Quercus rubra) in Tennessee (Edwards et al. 1994, Samuelson 1994b, Samuelson and Edwards 1993). Individual, 30-year-old red oak trees were grown in large open-top chambers (Edwards et al. 1994) and exposed to sub-ambient, ambient and twice ambient concentrations of ozone. Northern red oak seedlings, in pots, growing in native soil from the same location were exposed simultaneously to the same concentrations of ozone in smaller open-top chambers. After two years exposure the large trees exhibited decreases in leaf dry weight and decreased net photosynthesis in the twice- ambient ozone chambers. Growth and biomass of the seedlings were unaffected by any ozone treatment (Samuelson and Edwards 1993). Although direct comparisons could not be made, these results indicate that ozone may be affecting trees and seedlings differently.

Samuelson (1994a) placed northern red oak seedlings in different canopy positions in the large trees to determine reasons behind these differences in response to ozone, and allowed them to be exposed to the same ozone treatments for one growing season. Microclimate influenced the growth and physiology of the seedlings, but no differences in response to ozone were observed. Trees were more responsive to ozone exposures than seedlings. These results indicate that other physiological and biochemical factors may be more important in determining differences in response between seedlings and mature trees than microclimate.

Kelting et al. (1995) examined the effects of ozone on root production and turnover for the same red oak trees discussed in the above studies. They found that fine root production and biomass was decreased in the 2X treatments relative to ambient treatments, and the magnitude of the decrease was much greater for the mature trees relative to seedlings. These results support the findings of Samuelson and Edwards (1993) regarding above-ground effects. These results are not surprising, since below-ground processes have been reported in the literature as a sensitive indicator of ozone stress (Chappelka and Chevone 1992). The absolute values for seedling root growth and production compared with those for mature trees is not comparable, however, due to the fact the seedlings were grown in pots and trees in native (in the ground) conditions.

In a study to detect ozone effects on tree growth under different nitrogen regimes, Tjoelker and Luxmoore (1991) exposed loblolly pine and yellow-poplar seedlings to different levels of ozone and N in open-top chambers for one year in eastern Tennessee. For yellow-poplar, elevated ozone resulted in a significant increase in leaf abscission and leaf turnover, but does not decrease in biomass. These factors could be a compensatory response in reaction to the stress induced by ozone. Loblolly pine exhibited significant reductions in needle biomass when exposed to elevated levels of ozone and high levels of N.

Pine

Since the early 1980s many studies have been conducted using open-top chambers to establish a cause-effect relationship between ozone exposure and individual tree growth. The majority of which have been conducted with southern pines within the framework of large multi-institutional cooperative studies (refer to Flagler 1992, Kelly et al. 1993, Flagler and Chappelka 1995 for more details) under ideal growing conditions, i.e., adequate moisture and free from competition with other plants.

Kelly et al. (1993) summarized published results from a multi-disciplinary research program whose overall goal was to determine the response of loblolly pine to ozone, acidic deposition and soil Mg. The studies were conducted in open-top chambers using loblolly pine seedlings grown in large pots in native soil with either adequate or deficient amounts of Mg in the soil. Plants were exposed to sub-ambient, ambient and twice ambient levels of ozone and were also exposed to different rain acidities. Rain acidity and/or soil Mg status did not affect loblolly pine growth in these studies. Regarding ozone, there were no significant differences in diameter and height growth detected among treatments after three years, although family responses were different (Adams et al. (1990a). Biomass did decrease with increasing ozone levels during each of the three years of study (Kelly et al. 1993). The largest decreases observed were in fine root biomass. This correlated with carbon allocation patterns (Adams et al. 1990b, Edwards et al. 1992) in which allocation of photosynthate to fine roots was reduced in the presence of elevated ozone (2X).

In a long-term study with loblolly pine in North Carolina (Shafer et al. 1987, Shafer and Heagle, 1989) loblolly pine exhibited decreasing growth and biomass production as ozone concentrations increased. Response varied by family and reductions in growth were not correlated with foliar symptoms of ozone exposure.

Through the auspices of the Southern Commercial Forest Research Cooperative (Fox et al. 1992, Fox and Mickler 1995) a series of studies were developed to determine the effects of acidic precipitation and/or ozone on the growth and productivity of three commercially grown southern pine species: loblolly pine, slash pine and shortleaf (P. echinata) pine. To provide a regional perspective, five intensive field sites were located at different locations throughout the range of southern pines, including four in the SAMI states (Alabama, Georgia, North Carolina and South Carolina). Trees were grown in situ in native soils and exposed to varying concentrations of ozone and acidic rain for three years.

Results from these studies are summarized in Flagler (1992) and Flagler and Chappelka (1995). In general, increasing ozone concentrations resulted in decreases in height and diameter growth for all three species investigated. The greatest responses were found at levels above-ambient, although some responses were observed at ambient levels. Response varied by species, genotype, levels of ozone exposures and location. Height growth response was more variable and less consistent decreases in growth were observed than with diameter growth.

Premature senescence of foliage with increasing ozone concentrations (CF-3X ambient) was the most commonly observed response (Allen et al. 1992, Stow et al. 1992). This resulted in decreases in foliage area with increasing ozone levels in all three of the southern pine species investigated (Allen et al. 1992, Boutton and Flagler 1990, Byres et al. 1992). The greatest impacts of foliage loss were in the above-ambient ozone treatments.

Since trees were grown directly in the ground determination of below-ground responses to ozone was difficult (root excavation). Root data was, however, obtained from two studies. Faulkner et al. (1991) using soil cores, found a 50% decrease in root biomass of loblolly pine after two years of exposure to 3 X ambient ozone in North Carolina. No differences were observed with any other exposure level. Qiu et al. (1992) grew loblolly pine in the ground in root exclusion tubes and exposed them for one year to different concentrations of ozone. They found no differences in root biomass among ozone treatments, but a significant linear decrease in root surface area with increasing ozone levels in the ozone-sensitive genotype. No differences in growth were observed with an ozone-tolerant family.

In an attempt to determine if ozone was affecting pine growth across the region, Flagler et al. (1992) reported on data combined by genotype and species and analyzed for growth and biomass responses from all five open-top chamber studies. The most severe decreases observed were with foliage biomass. At ambient levels of ozone, relative to sub-ambient (charcoal-filtered) levels, there were 7.5%, 1.5% and 1% decreases observed in foliage and stem biomass and diameter growth, respectively. These findings were reported using an exposure-response equations comparing the various growth variables to SUM00. Other exposures indices were not used in this study.

Based on these and other results from the SCFRC, Teskey (1995) reported that growth losses to ozone at ambient levels are probably occurring, and that the annual reductions in growth are small (2-5%). These conclusions were based on findings with seedling studies. Growth reductions appear to be less for mature trees (1-3%), based on model predictions (Dougherty et al. 1992).

In an attempt to gain a better understanding of the response of loblolly pine to ozone in a competitive environment, Barbo et al. (1995) exposed one-year-old seedlings grown in native soil in open-top chambers to varying concentrations of ozone throughout the growing season. Competing plants were not removed and understory vegetation was allowed to regenerate and grow naturally in competition for resources. First year results suggested that seedlings exposed to twice ambient ozone exhibited reductions in height and diameter growth, however, trees grown in sub-ambient levels of ozone exhibited similar decreases in growth. These reductions were attributed to the severe competition for resources with understory vegetation in the charcoal-filtered (sub-ambient) chambers, demonstrated by increased number of understory species and increased percent cover in these chambers. Unpublished results for the second year (Chappelka and Barbo unpublished) tend to verify these results. This is the only known study in the SAMI region were trees are grown in a competitive environment and exposed to ozone.

Other Coniferous Species

Controlled field studies with other species of conifers is limited (Duchelle et al. 1982, Nuefeld et al. 1992), except red spruce regarding growth responses in the field due to ozone.

Thorton et al. (1994) provided a synopsis of three years research conducted at Whitetop Mountain, Virginia with red spruce growing in modified open-top chambers and mature trees with branches exposed to ambient levels of ozone. No growth effects regarding ozone were observed. Kohut et al. (1990) observed similar results with red spruce exposed to various levels of ozone for 2 growing seasons in Ithaca, New York. No effects on any growth variable were observed.

Summary

Results from controlled-field studies with eastern tree species common to the SAMI region indicate that exposure to high levels of ozone can injure foliage, modify physiology and affect productivity of individual trees of many different species. Ozone alters the transport of carbon to the roots and root growth is a very sensitive indicator of ozone stress. Within a species there is differential genetic sensitivity regarding ozone effects, with some genotypes being very sensitive (ambient responses) and others tolerant. The vast majority of these studies are with individual seedlings, not mature trees, and seedlings were not exposed to ozone in competitive environments.

The majority of statistically significant responses observed occurred at concentrations above-ambient ozone levels for any given location. However, a large number of the trees exposed exhibited linear decreases in growth with increasing levels of ozone exposure using statistical techniques (regression analysis, trend analysis). These results indicated the possibility of subtle decreases in growth at ambient levels of ozone.

It is very difficult to elicit a statistically significant growth response at ambient ozone levels. This may be the result of several factors; the trees exposed are not sensitive at ambient concentrations, not enough replication to detect statistical differences, the short-term nature of most studies (generally less than 5% of a tree's lifespan), variability in ozone exposure regimes (temporally and spatially) and differential sensitivity within the species exposed (Chappelka and Chevone 1992, Teskey 1996).

Uncontrolled Field Studies

Since ozone is ubiquitous and tree response is altered by many other factors (light, nutrition, moisture), it has proven difficult to determine whether ozone significantly affects tree growth and productivity in the field. At present there is little research on ozone effects to forested ecosystems. The majority of published research is correlative and based on visible symptoms of foliar ozone injury.

Anderson et al. (1988) conducted a survey of eastern white pine growing at more than 200 sites in the SAMI region (South Carolina, Tennessee, Virginia, North Carolina, Kentucky and Georgia) for symptoms of visible injury due to ozone. The diameter (dbh) of each tree was also measured. Of the stands sampled, injury was found in 23% of the stands. Symptomatic trees had 49% less mean volume than non-symptomatic trees. However, other factors, e.g., tree age, soil types, or other biotic or abiotic factors may have been involved in the decreases in growth that were observed.

The effect of oxidant air pollution on the radial growth of eastern white pine (Pinus strobus L.) in the Blue Ridge Mountains of Virginia, differing in ozone sensitivity (visible symptoms) was evaluated (Benoit et al. 1983). Reduced radial growth was observed for trees in all sensitivity classes during the period from 1955-1978. Mean annual growth was significantly less for the ozone-sensitive trees compared with those exhibiting no visible symptoms.

Swank and Vose (1991) observed chlorotic mottling and tip burn on white pine in a 13.4 ha watershed located in the southern Appalachian Mountains after several unusually high ozone episodes (0.08-0.120 ppm) during the 1984 growing season. They observed premature senescence of foliage, small increases in NO3-N and K and reduced basal area increment and related this to the unusually high ozone levels observed. This growth depression was short-term in nature and tree growth recovered after a couple of years.

The response of mature loblolly pine growing in eastern TN to ambient ozone and moisture stress was reported by McLaughlin and Downing (1995). Radial growth measurements at dbh (dendrometer bands) were made between 12-37 times per year over a five year period (1988-1992) for 34 trees (approx. 60-years-old), of which 16 were located on a relative xeric site and 18 located on a more mesic, fertile area. Using statistical techniques, relationships between ozone, moisture stress and radial growth were determined. Ozone exposures >0.039 ppm interacting with high temperatures and low soil moisture resulted in a short-term depression in radial growth. The interaction of increased soil moisture deficit with increased ozone concentrations resulted in a decrease in annual radial growth rates. Reductions in growth were predicted to vary from 7% in a relatively wet year to 30% in a relatively drier year.

Recently, this report (McLaughlin and Downing 1995) has been questioned regarding the statistical treatment of the data (Reams et al. 1995). Reams et al. (1995) perceive that the majority of the within-year variation observed is explained by natural variations in growth leaving little variability to be explained by environmental variables, including ozone and moisture stress. In reply, the authors' (McLaughlin and Downing) defend their analysis and state that the discrepancy between their analysis and the one conducted by Reams et al. (1995) is that Reams et al. (1995) only examined the variability of the most ozone-tolerant tree. Both groups, however, feel that this is an important topic and more research is needed in this area.

Based on a study where visible symptoms of ozone injury were characterized on large, mature yellow-poplar and black cherry trees in Great Smoky Mountains National Park, Somers et al. (1997) compared radial growth differences among trees classified as sensitive or tolerant based on the severity of ozone symptoms observed over a three year period. Twenty-five tolerant and 26 sensitive yellow-poplar and 23 tolerant or sensitive black cherry were cored and patterns of radial growth determined for the last 5 (1990-1994) and 10 years (1985-1994). Various indices were to used to eliminate variables (competition, etc.) that maybe confounding factors. Although the results are unpublished and preliminary, Somers et al. (1997) observed significantly more radial growth for both the last 5 and 10 years for the yellow-poplar trees identified as tolerant based on visible injury. This relationship was not observed with black cherry. Since this was not a controlled experiment and was limited in the number of trees used, there is no way to prove a cause-effect relationship between visible symptoms and radial growth. However, these results do indicate the need for further research.

Summary

Although several studies have implicated ozone as a potential contributing factor to decreases in radial growth of a few forest tree species no conclusions can be made at present regarding the effects of ambient levels of ozone on growth and productivity of the forests in the Class I areas of the SAMI region. There is simply not enough data to make any "broad" statements. Given the interaction among ozone and other environmental factors, it is unknown that any reductions in ozone levels will result in subsequent increases in growth and physiological function of forest trees.

General Conclusions

The critical assessment of ozone effects to forest tree growth in the SAMI region is very difficult for several reasons:

1. Ozone research is relatively new and the majority of early experiments (1960-1970's used unrealistic concentrations and instrument calibration was difficult (Matyssek et al. 1995).

2. The numbers of species exposed in controlled studies to ambient or near ambient ozone exposures in the SAMI region is limited, especially regarding deciduous tree species.

3. Generally, studies are short-term in nature (< 1 year) and in artificial growing media. This discounts the cumulative nature of ozone effects (Reich 1987, Chappelka and Chevone 1992).

4. There is a paucity of data regarding growth effects on large trees and forest stands (Matyssek et al. 1995, Chappelka and Chevone 1992). Northern red oak is the only species where large, mature trees were exposed to ozone under controlled conditions (Samuelson and Edwards 1993). All controlled exposure studies, except one preliminary study with loblolly pine (Barbo et al. 1995) are with individual trees in a noncompetitive situation. There are no growth studies regarding ozone effects to mature eastern hardwoods, except one unpublished, uncontrolled field study with black cherry and yellow-poplar.

VI. EXPOSURE-RESPONSE

Ozone is a naturally occurring chemical in both the upper atmosphere and at surface levels. Ozone is considered the pollutant of greatest concern with respect to potential regional impacts to trees in North America (U.S. EPA 1986, 1996, National Acid Precipitation Assessment Program 1991). Ozone is an omnipresent air pollutant that has caused foliar injury to agricultural crops and trees (U.S. EPA 1986, Chevone and Linzon 1988, Krupa and Manning 1988, Pye 1988, Swank and Vose 1991, Chappelka and Chevone 1992). The effects of ozone on individual plants and the factors that modify plant response to ozone are complex and vary with species, environmental conditions, and soil and nutrient conditions. Factors such as genetic susceptibility, light, temperature, relative humidity, soil nutrients, and soil moisture influence the uptake of ozone.

Unfortunately, not enough data are available to quantify the relationship between dose and vegetation effects (Fredericksen et al. 1996). Furthermore, the link between exposure and dosage are not strong. Alternatively, researchers have focused on describing the relationships between exposure characteristics and plant response, recognizing that exposure is not necessarily an adequate surrogate for dose (Lefohn 1992, U.S. EPA 1996). Although it would be helpful if one could use actual ozone dose measurements to predict cause-and-effect relationships, the current state-of-science is limited mostly to relating ozone exposure measurements to vegetation effects. Until further information is available on actual dosages received by vegetation and their resulting effects, the focus will continue to be on exposure.

Air pollution specialists have used exposure indices as surrogates for dose (Oshima 1975, Lefohn and Benedict 1982, Lefohn et al.1988a, Lee et al.1988, Hogsett et al. 1988, Lee et al. 1991, Lefohn 1992, U.S. EPA 1986, 1992, 1996). For selecting a set of exposure indices to relate to internal dose, some important concerns that need to be addressed are:

� What is the effect we are trying to prevent?

� Are there sufficient experimental data to link "dose" with exposure?

� What is the sensitivity variation among species and/or cultivars? What are the causes of these variations?

� Is there a specific time of day or specific month that vegetation is most sensitive?

� Is there a specific threshold or range of thresholds below which no effects occur?

� For assessing effects, should all concentrations be treated in an equivalent fashion? Are some concentrations more important than others?

� Is concentration more important than the length of exposure or amount of exposure?

� What are the specific exposure regimes responsible for affecting vegetation?

� What are the important components of those regimes responsible for the observed effects?

� Are the concentration regimes used in research experiments mimicking those regimes experienced under ambient conditions?

Several different types of ozone exposure indices have been proposed as surrogates for dose, and are summarized as follows (adapted from Lee et al. 1989):

� One Event: the second highest daily maximum 1-h concentration (HDM2), the maximum of 7-h (P7) and 1-h (P1) maximum daily averages, and the 90th (PER90), 95th (PER95), and 99th (PER99) percentiles of hourly distribution;

� Mean: the seasonal mean of 7-h daily means (M7), the seasonal mean of 1-h daily peaks (M1), and the effect mean (EFFMEAN) (Larsen and Heck 1984);

� Cumulative: the seasonal sum of hourly concentrations (i.e., total exposure (TOTDOSE). This is sometimes referred to as SUM0;

� Concentration Weighting: the seasonal sum of hourly concentrations at or above 0.06 ppm (SUM06), 0.07 ppm (SUM07), 0.08 ppm (SUM08), 0.10 ppm (SUM10); the seasonal censored sum of hourly concentrations at or above 0.08 ppm (AOT08) or 0.10 ppm (AOT10); the total impact (TIMPACT) (Larsen et al. 1983); the ALLOMETRIC in which the hourly concentrations were raised to a power and summed; SIGMOID or W126 in which the hourly concentration was variably weighted using a sigmoid function and summed (see Lee et al. 1989, Lefohn et al. 1988a); total hours with concentrations at or above 0.08 ppm (HRS08), or 0.10 ppm (HRS10); the number of episodes (an episode was defined as an event with hourly O3 concentrations above a threshold level) of threshold 0.08 ppm (NUMEP08), or 0.10 ppm (NUMEP10); and the average episode length with threshold 0.08 ppm (AVGEP08), or 0.10 ppm (AVGEP10);

� Multicomponent: indices that incorporate several characteristics of exposure, including the phenologically weighted cumulative impact indices (PWCI) (Lee et al. 1987).

A possible disadvantage of applying an integrated exposure index, such as the SUM06, is that the use of an artificial threshold concentration as a cutoff point eliminates any possible contribution of the lower concentrations to vegetation effects. Recognizing this, Lefohn and Runeckles (1987) suggested a modification to the Lefohn and Benedict (1982) exposure index by weighting individual hourly mean concentrations of ozone and summing over time. Lefohn and Runeckles (1987) proposed a sigmoidal weighting function that was used in developing a cumulative integrated exposure index. The sigmoid function was of the form:

here: M and A are positive arbitrary constants

wi = weighting factor for concentration I

ci = concentration I

Lefohn et al. (1988a) reported the use of the sigmoidally weighted index with constants, M and A, 4403 and 126 ppm-1, respectively. The authors referred to the index as W126. The values were subjectively determined to develop a weighting function that 1) included hourly average concentrations as low as 0.04 ppm, 2) had an inflection point near 0.065 ppm, and 3) had an equal weighting of 1 for hourly average concentrations at approximately 0.10 ppm and above. To determine the value of the index, the sigmoidal weighting function at ci was multiplied by the hourly average concentration, ci, and summed over all relevant hours. The index included the lower, less biologically effective concentrations in the integrated exposure summation.

Using various indices, several investigators have described ozone exposures in the SAMI region (e.g., Pinkerton and Lefohn 1986, 1987, Lefohn and Pinkerton 1988, Lefohn et al. 1988b, Winner et al. 1989, Lefohn and Lucier 1991, Aneja et al. 1992, 1994, Lefohn 1992, Gilliam and Turrill 1995).

Lefohn et al. (1997) collected hourly average ozone concentration data from the U.S. Environmental Protection Agency (EPA) Aerometric Information Retrieval System (AIRS) database and from the data in the National Dry Deposition Network program for the period 1983-1990. Using a 24-h period, the W126 cumulative exposure index was calculated for each monitoring site. The 7-month (April-October) W126 exposure index value was kriged for each �� by �� cell in Alabama, Georgia, South Carolina, North Carolina, West Virginia, Tennessee, Kentucky, and Virginia for each year. At this time, there is insufficient information available regarding optimum growth periods for trees to limit the daily integrated exposure period to a minimum of 12 hours (e.g., 0800-1959h) or a 3-month growth period. It was decided to integrate over the full 24 hours, recognizing that in most cases, the low-elevation sites would experience their highest hourly average concentrations during the daylight hours (i.e., greater than 12 hours but less than 24 hours). Therefore, at these sites the contribution to the W126 magnitude would mostly consist of hourly average values experienced during the daylight hours. Lefohn et al. (1997) selected the 7-month time period because of growth patterns associated with most trees. Lefohn et al. (1987) and Lefohn et al. (1992a) have discussed the approach used for kriging ozone. Figures 2-9 illustrate the W126 exposures for the area during the time period (1983-1990).

General Conclusions

Many different indices have been used as surrogates for ozone dose in exposure-response models. A possible disadvantage of applying an integrated exposure index, such as the SUM06, is that the use of an artificial threshold concentration as a cutoff point eliminates any possible contribution of the lower concentrations to vegetation effects. Recognizing this, Lefohn and Runeckles (1987) suggested a modification to the Lefohn and Benedict (1982) exposure index by weighting individual hourly mean concentrations of ozone and summing over time (W126).

For the years 1983 through 1990, the ozone exposure kriging estimates resulted in most of the grid cells falling between 23.8-66.5 ppm-h for the W126 index. In 1988, 11 of the 120 cells had W126 estimates greater than 66.5 ppm-h. Three cells in 1986 and 1989, and one cell in 1990 had a W126 estimate of 5.9-23.7 ppm-h. No cells were classified as having less than 5.9 ppm-h.

Generally, within the Southern Appalachian area boundary, ozone monitors experienced fewer than 40 hours in which the hourly average ozone concentration was � 0.10 ppm (1983-1990). The only year that deviated from this pattern was 1988 when 11 of the 15 ozone monitors in the area had greater than 50 hours in which the hourly average ozone concentration was � 0.10 ppm.

The combination of the Palmer hydrologic index and the ozone exposure results indicate that soil moisture conditions may alter tree growth response to ozone exposures (Lefohn et al. 1997). By combining exposure information with moisture availability and experimental exposure-response data possible areas that may have the greatest potential for possible vegetation effects may be identified.

VII. MODELS

As stated in the above sections, the majority of the reported growth and physiological responses due to ozone are for individual trees, primarily in the seedling or sapling stage of development, and in greenhouses or open-top chambers. The lack of information concerning tree response under field conditions presents difficulty in extrapolating ozone effects to a forest stand or region-wide assessment. One way to attempt to use these laboratory data is through the use of models. Several models used with trees species common to the SAMI region are described in this section.

It is imperative when conducting modeling exercises, that forest biologists must constantly keep in mind the tremendous variability that exists within natural systems. To "model" ozone induced exposure/responses across the geographic range of a species (even within the limited range of the SAMI region) poses a formidable task. At this time, we consider the influence of micro-site factors to be most important in altering the potential for ozone-induced exposures. Available soil moisture appears at the present time to be of greatest single importance in controlling ozone uptake through its influence on stomatal function at the leaf level (Showman 1991, Lefohn et al. 1997). Scaling of this single site/physiological response phenomenon from seedling to mature canopy responses continues to necessitate future research. Such research is necessary in support of the modelling attempts at determining region-wide ozone impacts.

Modeling efforts must also take into account the relative influences of insect pests, biotic pathogens and abiotic stressors (other than ozone) in contributing to the measured (modelled) changes in forest health and/or productivity. Very careful diagnostics must first take place at the specific sites and for the species of interest before an "ozone- induced response" may be held accountable at that specific site, or even for selected species at that site. Scaling responses across broad regions (i.e., SAMI) for the purpose of determining ozone-induced effects without regard to gaining a clear understanding of the influence of many other stress-inducing factors would possibly present a skewed and, therefore, unrealistic senario of the relative importance of ambient ozone exposures to forests in the SAMI region.

Models can be for individual trees, forest stands or regions. Several examples of each will be included. This review will not be exhaustive in nature regarding the mechanics of the models. For a detailed description of this the reader is referred to the critical review of Kickert and Krupa (1991).

Individual Tree Models

A model has recently been developed (TREGRO) to derive the impact of ozone on individual whole-tree processes (Weinstein et al. 1991, Weinstein and Yanai 1994). This simulation model calculates the flow of water, carbon and nutrients through a plant and the influences of limitations of each on carbon assimilation, allocation and use. A tree is divided into the canopy, branches, stem and coarse and fine roots. The model then calculates photosynthesis, daily carbon distribution within the plant, and losses of carbon due to respiration and senescence. The model was originally developed to simulate the response of individual, open-grown red spruce trees to ozone stress, with or without nutrient stress over a 10-year period (Weinstein et al. 1991, Laurence et al. 1993, Weinstein and Yanai 1994 ). A 20% and 40% reduction in nutrients induced a 19% and 28% decrease, respectively, in growth after 10 years of simulation. Nutrient stress resulted in a shift in carbon allocation from above to below-ground plant parts. Elevated ozone (2X) caused a simulated reduction in above-ground and below-ground growth by approximately 18% and 20%, respectively, after 10 years (Weinstein et al. 1991). Laurence et al. (1993) compared simulated results with actual responses in field-grown red spruce (1993). Results from the simulation model parrelled the experimental findings. Simulated seedling weight was within 8% of the actual weight of the experimental trees. Over 3-4 years of simulation cumulative photosynthesis was decreased by 8% and total biomass by 6% in the 3X ambient ozone treatments.

Summary

Accurate ozone dose-response functions are needed to model tree responses using TREGRO. While these functions are available for some tree species at the seedling level they are not available for mature trees. Given the paucity of mature tree studies, model predictions using experimental growth responses are not easily validated. In addition, the model (TREGRO) requires detailed ozone exposure, environmental and physiological data. These are not presently available for many species.

Canopy Models

A simulation model of ozone impacts on photosynthetic carbon gain at the canopy level was described by Reich et al. (1990). Leaf and canopy-level CO2 exchange rates of several forest tree types were predicted using ozone concentration, leaf N concentration, leaf weight/area, light intensity, VPD and water potential as the driving variables. The data used for the model were collected from a mixed oak-maple forest. The model was developed from a software package called STELLA (High Performance Systems, Lyons, NH). Simulated ozone concentrations used in the model were 0.35, 0.50, 0.65 or 0.80 ppm, 12 hr/d, for 90 consecutive days. The tree canopy was divided into four sections, understory, lower, middle, and upper canopy. Ozone concentrations could be simulated to be the same or variable among canopy layers. Ozone effects on the mature tree canopy carbon balance resulted from effects on primarily the upper and middle canopy positions. Eighty-six percent of the total carbon gain occurred in the top two layers of the canopy. Ozone, however, was found to affect carbon balance of plants in the lower canopy or understory positions.

A model developed to predict the flux of carbon from tree crowns within a forest canopy (MAESTRO, Wang and Jarvis 1991) was used to assess the effects of ozone on carbon gain of mature loblolly pine (Dougherty et al. 1992). The model focuses on a single tree canopy or a group of canopies from neighboring trees. Photosynthetically active radiation and vapor pressure deficit were the driving variables. Ozone concentrations were assumed to be constant throughout a tree crown. Ozone effects on carbon gain were incorporated into the model by modifying mesophyll conductance as a function of cumulative ozone exposure. The modeling data were closely linked to the experimental results where loblolly pine branches were exposed to ozone at several levels using branch chambers (Teskey et al. 1991). From the model it was determined that ozone can affect annual net carbon fixation from approximately 2-9% for tolerant or sensitive trees, respectively compared with trees exposed to carbon-filtered air. If ozone concentrations were doubled the amount of carbon fixed per year would decrease by approximately a range from 5-22%.

Another canopy-level model for eastern hardwood tree species has been developed using ozone as a predictor variable (Amthor et al. 1994). The model is based on the "big-leaf" model (Sinclair et al. 1976), where a canopy can be considered analogous to a single, large leaf. Amthor et al. (1994) found a positive correlation (r= 0.76) between predicted and measured ozone uptake rates for a mature, mixed oak-maple stand in Massachusetts. The model more accurately predicted uptake during the morning hours compared with afternoon, indicating that the model over predicted stomatal conductance. The model could be adapted for predictions of carbon gain in relation to ozone exposure and uptake.

Summary

All of the models (canopy-level) provide interesting results regarding ozone uptake and carbon fixation within the canopy of tree species common to the SAMI region. These models if combined with stand-level models can potentially provide information on carbon fixation and growth at a tree and/or stand level.

The models, in present form, all have similar assumptions that could cause error in the results. All assumed that foliage response in all canopy positions would be equal. Recent reports (Tjoelker et al. 1993, Fredrickson et al. 1995, Samuelson and Edwards 1994, Chappelka unpublished) with several hardwood species have indicated that this may not be a valid assumption. It appears that foliage growing in the lower canopy may be more sensitivive to ozone injury that "sun leaves" growing in the upper canopy. This would cause a greater reduction in carbon fixation than previously estimated.

Another factor that influences ozone uptake and subsequently carbon fixation is the fluctuation in ozone distribution within the canopy. All of the models assumed that ozone concentrations did not fluctuate within a forest canopy. Ozone concentrations do, however, vary depending on canopy position (Nuefeld et al. 1992, Fredrickson et al. 1995, Samuelson et al. 1996) and whether or not the canopy is closed or open (Neufeld et al. 1992).

Stand Models

Individual tree and canopy-level models provide valuable information on tree response to ozone, however, translation of these models to the stand level is very difficult without appraisement of the complex nature of the system. Consideration has to be given to intra and interspecific competition, differential sensitivity to ozone and differences in growth habits and form of the many different species comprising the forests of the SAMI region. Reviewed below are two models (one for hardwoods and one for conifers that have been used to explore the response of forest trees found in the SAMI region to ozone.

Hardwoods

West et al. (1980) utilized the simulation model FORET (Shugart and West 1977) to study the long-term effects of air pollution on forest community growth and dynamics. The FORET model is a stochastic simulation model that grows a forest and follows stand dynamics through time (successional model). The model (West et al. 1980) evaluated 32 forest tree species native to the southern Appalachian (SAMI) region and simulated the growth of individual trees on a circular 1/12-ha plot. Annual growth rates vary with degree days, total leaf area of the dominant trees, and the number and size of trees per plot. The establishment and growth of each species are then determined by its silvicultural characteristics. A schematic diagram of the model is shown in Figure 10. For a more detailed description of the model characteristics the reader is referred to Shugart and West (1977).

To evaluate air pollution stress on the forest, relative species sensitivity rankings were developed used existing literature (up to 1980). The rankings were based on visible injury to sulfur dioxide and/or photochemical oxidants. They were not specific to any one pollutant. Resistant species identified were red maple, sugar maple, bitternut hickory, pignut hickory, shagbark hickory, mockernut hickory, dogwood, persimmon, American beech, white ash, red cedar, black gum, sourwood, white oak, chestnut oak and post oak (16 species). Intermediate tree species were buckeye, redbud, sweet gum, yellow-poplar, scarlet oak, southern red oak, northern red oak, black oak, sassafras, and basswood (10 species). Sensitive species included black walnut, shortleaf pine, white pine, Virginia pine, black cherry and black locust (6 species). The authors assumed that reductions in physiological function and growth would parrell visible injury effects. Forest responses were examined by imposing varying degrees of stress on the trees based on their sensitivity ranking. Two levels of stress were imposed: high (20%, 10%, 0%) and low (10%, 5%,0%) for sensitive, intermediate and resistant trees, respectively. No differential sensitivity within a species was assumed. The simulated forest was grown up to 400 years. Air pollution stress was imposed at various times during the simulation (age 0, 50 and 400).

The model showed that response to the stress varied by species and by the time when the stress was imposed. Several species based on their growth characteristics "took advantage" of the stress and grew at more rapid rates than other species in the same sensitivity category. Yellow-poplar and black oak were both classified as intermediate, however, yellow-poplar grew better over time and black oak grew less under 10% stress. This is due to their silivicultural characteristics such as growth rates, tolerance to light, etc. Black cherry was the most sensitive species observed. Under 20% stress the species almost disappeared in older stands (>100 years old). Biomass production in the forest stand was reduced under the high stress level, with the maximum reduction occurring at 200 years.

Summary

Although the model provides an interesting tool to study air pollution effects over the life-span of a forest stand several of the assumptions need to be reevaluated to make the model more amenable to ozone effects to forests in the SAMI region.

1. The relative sensitivies of the various species that were grown needs to be up dated and based on growth reductions. The correlation between visible injury and growth reductions is week at best. Sensitivity ranking need to be specific to ozone.

2. Differential sensitivity to ozone within a species is a reality. This may be very difficult to simulate.

3. Is constant addition of a stress appropriate? Variable additions may provide more meaningful results.

Loblolly Pine

An individual tree, distance-dependent model (AIRPTAEDA) that accounts for stand competition and mortality was developed for loblolly pine (Webb and Burkhart 1988, Webb et al. 1992). The model was adapted from a growth and yield model for loblolly pine (PTAEDA2) developed by Burkhart et al. (1987). The model includes one basic assumption: ozone impact to trees within a stand is not uniform. Based on this assumption, the simulator generates one of two scenarios: sensitive trees are chosen at random, or the tallest trees are considered the most sensitive. The population of trees is then further divided into three sensitivity categories (low, medium, or high). The proportion of individuals "falling" in each category can be varied. Ozone effects can only be simulated starting with the ninth growing season, based on the inherent nature of the original model, PTAEDA2 (Burkhart et al. 1977). The model simulates growth for 30 years, which is an average rotation age for most southern pines. Different growth rate reduction scenarios were used, based on experimental data (Shafer and Heagle 1989, Stow et al. 1991, Dougherty et al. 1992).

Growth loss at the stand level was dependent on several factors: 1) The severity of the growth loss. The more severe the growth loss the greater the reduction in stand volume. 2) The relative frequency of trees in the various sensitivity categories. The greater the proportion of trees in the insensitive category the greater the growth reduction needs to be to elicit an effect. 3) Randomness in sensitivity. When simulations were conducted with randomly selected trees compared to tall trees being the most sensitive, stands where the later scenario was chosen exhibited lesser growth than when trees were selected at random.

Average annual reductions averaged from approximately 1-2% per year to 10-20% per year based on the input variables. The most severe case was based on reductions in crown volume rather than decreases in height or diameter growth.

Summary

This simulation model provides some interesting information on ozone effects to loblolly pine stands. It accounts for differential sensitivity within a species. The input variables and sensitivity rankings, however, are driven by experimental data. This model is adapted for a single species, loblolly pine, growing in an even-aged, plantation situation. The model also runs for only 30 years, and does not begin introduction of the various ozone scenarios until age nine. Its utility in an assessment of mixed hardwood-coniferous stands and early successional stages of forest development, therefore, is limited.

General Conclusions

Several models have been used to simulate growth and/or physiological responses to ozone. These include a single tree model (TREGRO), several canopy models on ozone uptake and carbon fixation, a forest succession model (FORET) and a loblolly pine management model (AIRPTAEDA).All of these models provide some information on ozone effects to species commonly found in the SAMI region. Each model has advantages and disadvantages, and they vary in their level of complexity. TREGRO provides good information on ozone effects to a single, open-grown tree. It however, does not provide information regarding forest stand growth. Accurate ozone dose-response functions are needed to model tree responses using TREGRO. While these functions are available for some tree species at the seedling level they are not available for mature trees. Given the paucity of mature tree studies, model predictions using experimental growth responses are not easily validated. In addition, the model (TREGRO) requires detailed ozone exposure, environmental and physiological data that are not presently available for many species.

The canopy models all provide good information on ozone uptake and carbon fixation. They do not provide information on whole-tree responses (root growth, etc.). In addition, all of the canopy models assume that ozone levels and leaf responses are equal within a crown. This may produce error in the model.

The FORET model provides some extremely useful information on ozone effects to a forest stand. It can provide information on changes in growth and productivity over time. This simulator needs to be reparameterized specifically for ozone. It originally was parameterized for air pollution effects in general, and this assumption needs to be modified. Also, the model ozone effects to be equal within a species, and error could ensue due to this assumption. AIRPTAEDA has limited use for an assessment of the trees within the SAMI region, since loblolly pine is a minor component. Also this model is based on a growth and yield model for plantation-grown trees. It does, however, account for differential genetic variability within a species to ozone. This technique may be able to be modified and used in conjunction with other models in an assessment framework.

VII. METHODOLOGIES USED IN ASSESSING OZONE EFFECTS

Establishing the risk to forests in the SAMI region from tropospheric ozone is a difficult task. It requires approaches that utilize existing databases on the forest resources, ozone monitoring information, realistic ozone exposure-tree response experiments, modeling information to predict changes over a spatial and temporal scale, and integration of social values.

In this section three different assessment methodologies will be discussed. All three methods have been utilized for tree species growing in the SAMI region. The first methodology involved the use of kriging (ozone concentrations) combined with data obtained from experimental results for four tree species, black cherry, northern red oak and yellow-poplar, growing in the SAMI region to determine areas of possible concern (Lefohn et al. 1997). Since environmental factors such as soil moisture availability may potentially influence tree response to ozone, the Palmer hydrologic index (Palmer 1965, 1967) was used to further subdivide these areas of concern.

Even though not applied, Hogsett et al. (1993) in the second approach discussed the use of GIS in combination with experimental data and individual and stand-level models to determine potential growth losses of several major tree species due to ozone. At risk areas could then be identified. The investigators combined exposure-response models derived from data collected in open-top chambers with predicted ozone exposures to predict growth losses.

A third proposed approach used in risk assessment was developed by Luxmoore (1992). This approach is being developed for the assessment of regional responses of loblolly pine to ozone and other climatic factors (variation in rainfall) scaling up from seedlings to forest stands using various physiologically-based simulation models.

Applying Exposure Information for Identifying Areas of Concern - Lefohn et al. (1997)

Lefohn et al. (1997) described the protocols for the identification of vegetation areas that may be at risk, which involved combining experimental exposure-response effects data for deciduous and coniferous seedlings and trees with 1) kriged characterized O3 ambient exposure data mentioned previously and 2) soil moisture. The conclusions of Musselman et al. (1994) and others (see U.S. EPA 1996), that all hourly average concentrations have the potential for impacting vegetation, but that the higher values should be given a greater weighting than the mid- and low-levels, were used in the methodology described by Lefohn et al. (1997). Recent work by Karnosky et al. (1996) appears to reinforce the importance of high hourly average concentrations. The cumulative-type exposure index performs adequately in relating growth reduction to vegetation and ozone exposures occurring with single experiments (U.S. EPA 1992, 1996, Lee et al. 1991, Lefohn 1992). However, when attempting to relate a particular set of exposure-response results to ambient conditions or other experimental results, single-parameter cumulative indices should be combined with some measure of the high hourly average values (e.g., values � 0.10 ppm), which occurred in many of the open-top experiments (Lefohn and Foley 1992, 1993, Lefohn et al. 1992b, Lefohn 1992).

In their analysis, the 24-h sigmoidally weighted exposure index (Lefohn and Runeckles 1987), W126, was used over the April-October period for the reasons described above. Alternatively, a 24-h SUM06 (the sum of all hourly average concentrations � 0.06 ppm) exposure index could have been used. Both the W126 and the SUM06 are highly correlated and provide similar exposure-response results in effects modeling efforts (U.S. EPA 1996). The W126 was selected, however, because it does not use a subjectively determined threshold of 0.06 ppm, which cannot be biologically substantiated at this time. The index includes the lower, less biologically effective concentrations. The W126 cumulative index was integrated over a 24-h period.

For estimating the exposure regimes that relate to growth reduction of various deciduous and coniferous tree species grown in the Southern Appalachian region, Lefohn et al. (1997) characterized ozone exposures from biological experiments. The initial review of the literature associated with this research effort focused on exposure-response information for the following species: black cherry; yellow-poplar, Virginia pine; red maple, eastern white pine, slash pine, pitch pine, loblolly pine, northern red oak, white oak, sycamore, shagbark hickory, American beech, white ash, and green ash.

Using the experimental results, four broad sensitivity categories were developed [i.e., 1) minimal, 2) level 1 (black cherry), 3) level 2 (yellow-poplar), and 4) level 3 (northern red oak, Virginia pine, loblolly pine, eastern white pine, white oak, sugar maple, red maple, American beech, and shagbark hickory] were defined. For assigning the response categories, focus was on only those studies where growth effects were noted. The minimal category was defined as a level where exposures were less than those which cause damage to black cherry or where moisture conditions were not favorable for ozone uptake.

The initial approach assumed that the 1) environmental conditions were favorable for ozone to enter the leaf and 2) total cumulative exposure would result in a growth loss. However, as mentioned above, it is necessary to consider conditions that affect a plant's sensitivity. The experimental studies used seedling and tree plants which were grown under optimum conditions (e.g., adequate moisture and nutrients). Showman (1991), Jackson et al. (1992) and Kouterick (1995) have observed significantly fewer ozone symptoms on sensitive species during periods of drought than during years when the growing season had adequate rainfall. Unfortunately, at this time, little experimental information is available relating ozone exposure, drought conditions, and tree growth reduction.

Each �� by �� grid cell in the Southern Appalachian area was assigned one of four categories (Table 3) mentioned above. Because the criteria listed in Table 3 requires that both the W126 and number of hours � 0.10 ppm be met, it was necessary to predict the number of occurrences of high hourly average concentrations. There is a paucity of air quality monitoring data which makes it difficult, at this time, to spatially predict the number of hourly average concentrations � 0.10 ppm accurately. However, the authors found that it was possible to separate the area into broad exposure categories due to the occurrences of hourly average concentrations � 0.10 ppm during "high" and "low" ozone exposure years. For example, in 1983-1986 and 1989-1990, the number of hourly average concentrations � 0.10 ppm at all sites in the geographic area was less than 51, which is below the Level 2 sensitivity category. In 1987, there was only one site that experienced greater than 51 occurrences � 0.10 ppm. In 1988, the high exposure year, 11 of 15 monitoring sites experienced 51 or more hourly occurrences � 0.10 ppm. Subjectively, it was decided that grids which had two or more ozone monitors were classified using the highest value; cells which did not have a monitor were classified by examining the pattern from monitors surrounding the cell and selecting a site whose value was the second highest number of hours � 0.10 ppm.

The Palmer hydrologic index was selected as an indicator of soil moisture (Palmer 1965, 1967). Because Palmer hydrologic index data were available for the period 1983-1990, the study was limited to this time frame. The index is a monthly value, computed for a climatic division, which indicates the severity of a wet or dry spell.

Combining the Palmer hydrologic index and ozone exposures allowed Lefohn and co-workers (1996) to identify those areas within the region where 1) soil moisture may have been adequate in the area and 2) ambient exposure regimes closely matched those experiments where growth losses were observed. Areas which were classified as experiencing a drought were assigned the minimal category; otherwise the sensitivity category value remained the same after applying the criteria previously mentioned.

Using available monitoring data for 1983-1990 and exposure-response data based on seedlings and trees, Lefohn et al. (1997) identified geographic regions within the area that may have experienced ozone exposures, which include high cumulative values as well as the presence of sufficient numbers of high concentrations, coupled with sufficient soil moisture, that have the potential for inhibiting vegetation growth. As indicated earlier, current ozone exposures are causing visible symptoms on the foliage of sensitive species and injury has been documented in numerous locations throughout the Southern Appalachian area. Their results indicated that in a small number of areas within the region, ozone exposures and soil moisture availability might be sufficient to cause growth losses to some sensitive species. The number of hectares where vegetation may be affected by exposures may represent an overestimate due to the optimum growth conditions experienced in the experimental open-top chambers and the manner in which the investigators characterized the ambient ozone data (i.e., over a 7-month period). In addition, two other items are important: 1) the growing range of each species and amounts of species in each cell were not used in our analysis; and 2) the resolution of the Palmer hydrologic index is at the climatic division for each month and, depending upon the variability of soils in the climatic area, the index may provide less than optimum predictions. It is clear that there still needs to be verification of actual growth losses for the areas of concern.

Risk Characterization - Hogsett et al. (1993)

To assess potential risk of sensitive tree species to ozone, Hogsett et al. (1993) applied an assessment methodology based on the use of a Geographical Information System (GIS) combined with estimated ozone exposures, simulation models and experimental data. To test this method, they used the eastern US, including the SAMI region as the study area. For the purposes of this initial, preliminary assessment eight tree species were used: quaking aspen, black cherry, yellow-poplar, sugar maple, red maple, loblolly pine, Virginia pine, and eastern white pine. All species occur in the SAMI region, however, quaking aspen and loblolly pine are minor components of the forest types commonly found in this region.

To characterize risk of these forests to ozone, Hogsett et al. (1993) attempted to integrate four elements to form the data base that comprised the two major components of the assessment (exposure characterization and characterization of ecological effects). These four elements are:

1. Ozone exposures for the region.

2. Spatial distribution of the resources. The degree of interest can be at the species, community or ecosystem level.

3. The spatial distribution of other abiotic or biotic factors that may influence tree response to ozone. Included in this is environmental factors and exposure dynamics.

4. Exposure-response functions for the selected measurement endpoints.

The framework of this assessment is illustrated in Figure 11. (Hogsett et al. 1993). Information used to develop the response functions (ecological effects) are enclosed within the circles. These data are derived through experimental data or literature, then simulated over time by using simulation, process-level models. Models were used because all of the data used in the preliminary assessment was from individual tree seedling data gathered over a short duration (generally one year or less). These results (response functions) were then integrated with ozone exposure information, species distributions and other environmental factors using GIS to derive the final risk characterization, ie., the likelihood of the occurrence of adverse effects (biomass reductions, etc.) with ozone exposure (Figure 11).

Since ozone monitoring data are limited, ozone exposures were estimated for areas without monitors using a method developed by Hogsett and Herstrom (1991, Hogsett et al. 1993). The method uses GIS to generate potential ozone exposures based on ozone precursors (NOx), solar radiation, stagnating air masses and wind direction. The ozone exposure statistic used was the maximum 3-month SUM06 value. Exposure-response information was developed from open-top fumigation experiments.

The results of this preliminary assessment (Hogsett et al. 1993) indicated a wide range of annual biomass losses (0-33%) depending on species and ozone exposures. The two most sensitive species were black cherry and aspen with annual predicted growth losses over 20% for greater than 50% of their range. Yellow-poplar, loblolly pine, sugar maple and white pine had between 5-12% annual biomass losses with a large portion or their range experiencing these losses.

As mentioned by the authors (Hogsett et al. 1993) this assessment was preliminary in nature and subject to several sources of error. These include uncertainty associated with the use of seedling data to estimate mature forest response, climate data, estimation of ozone exposures, and species distribution. The authors do feel, however, that this is a valid technique and deserves further refinement. One key difference between that by Hogsett et al. (1993) and Lefohn et al. (1997) is that Hogsett et al. (1993) did not focus on the presence of high hourly average concentrations (i.e., � 0.10 ppm), while Lefohn et al. (1996) did. As discussed in Lefohn et al. (1997), many of the experiments used to develop the exposure-response information by Hogsett et al. (1993) were based on NCLAN-type exposures, which experience numerous occurrences � 0.10 ppm in the experimental treatments where effects were observed. Ignoring the presence of the high hourly average concentrations, may lead to overestimates of growth reduction. In addition, Hogsett et al. (1993) used a 92-day SUM06 exposure index. The rationale for using a this exposure period is unclear. The growing season for most tree species is generally greater than this three-month period.

Scaling Up Physiological Responses to Ozone - Luxmoore (1992)

Another potential assessment methodology to consider is one proposed by Luxmoore (1992) where the response of loblolly pine variations in rainfall and ozone exposures would be scaled-up from a seedling to a forest stand and long-term effects on loblolly pine productivity would be assessed. The framework for this proposed methodology is shown in Figure 4.

Input variables are first entered into a physiologically-based model [Unified Transport Model (UTM)]. This model consists of five linked models that provide data at an hourly basis on carbon, nutrients, water and pollutant fluxes to trees in a uniform stand. Data are then incorporated in the FORET model (previously described) and trees grown over time. This in turn is linked to PTAEDA2 to provide different management options and stand manipulations. These are then incorporated with different policy options with different pollution and climate change scenarios (Figure 12).

This assessment technique is still in the development stages, ie., it has been tested on only one tree species (loblolly pine). It, however, allows for the incorporation of policy options to a physiologically-based process model. The model allows for the manipulation of various edaphic and climatic variables, as well as ozone and carbon dioxide levels.

General Conclusions

All three methodologies provide information that can be used in an assessment framework. Each of these has advantages and disadvantages or limitations. Each method is potentially applicable to a regional assessment.

The first method by described by Lefohn et al. (1997) affords a technique where areas of potential risk can be identified for several different tree species. Many different ozone-exposure statistics can be used, although the authors for reasons mentioned above, prefer the W126 accumulated over a 24-h, 7-month period. It also provides a way to combine ozone data with other environmental variables, ie., water availability that are believed to be important in physiological function and growth response to ozone.

There are several limitations that need to be recognized. The experimental data used were limited because of data availability and primarily was for seedling response to ozone. Because ozone monitoring information is limited, kriging was used as a surrogate to ozone monitoring data in many areas. The errors associated with using kriging to estimate ozone exposures was determined for each cell. The Palmer hydrologic index many not represent a true account of whether or not a particular species is under water stress. Some species are more adapted to xeric conditions than others. In addition, a recent report by McLaughlin et al. (1995) suggests the possibility of growth response of loblolly pine to ozone being enhanced by drought. This contrary to the hypothesis proposed by Lefohn et al. (1997) and cited in the U.S. EPA Criteria Document (U.S. EPA 1996), and deserves further exploration.

Hogsett et al. (1993) proposed a methodology for the regional risk assessment of forest response due to ozone exposure for similar tree species as described by Lefohn et al. (1997) growing in the SAMI region. This method takes advantage of the new technology associated with GIS and simulation models, and provides information on the areas within a species range that are potentially at more risk than others. There appears to be several layers of parameritization necessary (model linkages) for the assessment to be operational. Forest growth scenarios are based on individual seedling data from only a small number of studies, mostly with seedlings growing in pots, in open-top chambers (Hogsett et al. 1993, Neufeld 1993, Karnosky 1993, Karnosky et al. 1993, Lefohn et al. 1992, Qiu et al. 1992). Other concerns are with the error associated with the estimation of ozone exposures and species distribution. Because there is little ozone monitoring data available, the exposures are estimated using emissions data. This can lead to error in determination of exposure values (Hogsett et al. 1993). Regarding species distribution, the inventory of a particular species may not be up-to-date.

The third proposed assessment technique (Luxmoore 1992) may not be applicable at present for an assessment of multiple tree species that occur in the SAMI region. This method was developed for a single species, loblolly pine, and would have to be reparameterized for an assessment including multiple species. This technique relies heavily on physiologically-based process-level models and a great deal of parameteritization and computer-time would be required.

VIII. OVERALL CONCLUSIONS AND RECOMMENDATIONS

Conclusions

1. Growth and physiological responses to ozone have been reported for individual trees that occur in the SAMI region. Most of these studies are, however, with individual seedlings (< 2 yrs in age) under controlled conditions (CSTRs or open-top chambers). Most studies were short-term (< one year), and were with potted seedlings. At least one study regarding growth effects due to ozone has been reported for 11 different coniferous species and 17 hardwood species that occur in the SAMI region. Of the conifers, the vast majority of research was conducted on loblolly pine (majority of all research regarding ozone effects) and red spruce. Yellow-poplar, northern red oak and black cherry were by far, the most studied hardwoods. Other species occurring within the region need to be more intensively examined, regarding ozone effects.

2. Mature tree growth and/or physiological responses to ozone in the SAMI region have been reported for six species: black cherry, red maple, white pine, loblolly pine, northern red oak and yellow-poplar. Two of the studies were correlative and uncontrolled. Only research with northern red oak was controlled (cause-effect) in nature. An intensified research effort in this area is needed.

3. Ranking of species sensitivity to ozone (growth, physiology and visible injury) is hindered by variation in environmental conditions, ozone exposures, study duration and study objectives, tree age and differential genetic sensitivity within a species. Of the five species most intensively studied, black cherry and loblolly pine appear the most sensitive, yellow-poplar and northern red oak intermediate to tolerant, and red spruce very tolerant to ozone. Results were quite variable, for the above-mentioned reasons.

4. No conclusions can be made at present regarding the effects of ozone on growth and productivity of the forests in the SAMI region. There are only two reports of ozone effects to mature trees growing in a forest situation. One is a preliminary report with yellow-poplar and black cherry and the other with loblolly pine. There is simply not enough data to make any "broad" statements regarding growth and productivity, ie., there is simply not enough data to make recommendations as to whether or not a 10-20% reduction in ozone would affect tree growth and/or productivity. However, visible injury has been observed at ambient levels in both "high" and "low" ozone years on mature trees and seedlings in a forest situation. Without a clear understanding of the interaction between ozone and other environmental factors it is uncertain that a 10-20% reduction in ozone levels would affect visible injury.

5. Tropospheric ozone air pollution has repeatedly been shown to cause foliar injury on sensitive species throughout much of the SAMI region. On broadleaf species, foliar injury has been observed as a mid- to late-season adaxial stipple, leaf reddening, and early leaf senescence. Under forest conditions of exposure, symptoms on conifers are less clearly evident due to numerous mimicking symptoms but have been noted to involve season long chlorotic spotting and mottle. A few observations of an early summer uniform tipburn of newly emerging needles have been reported.

6. Foliar ozone injury, as described above, has been induced following exposures to ozone delivered within laboratory, greenhouse and field open-top chamber conditions of fumigation. However, very few exposure/foliar symptom responses have been clearly defined for subsequent use under field conditions.

7. Open-top chambers have been used under natural field conditions for the protection of forest species from ambient ozone exposures on a season-long basis. Clear differences in symptom expression have consistently been noted following such treatments; foliar injury was minimal in the CF treatments and was evident in NF-treated air.

8. No clearly defined relationships have been demonstrated under natural growing conditions between foliar ozone injury and growth, although preliminary data indicate that a relationship may exists for some species. Such relationships have, however, been recently shown for measured physiological changes in leaf performance.

9. Ozone effects can be altered by other environmental and biotic factors, e.g., water status, temperature, light, relative humidity, insects and diseases. Given the interaction among ozone and these factors, it is unknown that any reductions in ozone levels (10-20%) will result in subsequent increases in growth and physiological function, or decreases in visible injury of forest trees in the SAMI region. More research is needed, especially regarding eastern hardwoods and mature trees.

10. For the years 1983 through 1990, the ozone exposure kriging estimates resulted in most of the grid cells falling between 23.8-66.5 ppm-h for the W126 index. In 1988, 11 of the 120 cells had W126 estimates greater than 66.5 ppm-h. Three cells in 1986 and 1989, and one cell in 1990 had a W126 estimate of 5.9-23.7 ppm-h. No cells were classified as having less than 5.9 ppm-h.

11. An important observation is that usually, within the Southern Appalachian area boundary, ozone monitors experienced fewer than 40 hours in which the hourly average ozone concentration was � 0.10 ppm (1983-1990). The only year that deviated from this pattern was 1988; 11 of the 15 ozone monitors in the area had greater than 50 hours in which the hourly average ozone concentration was � 0.10 ppm. Although Lefohn et al. (1997) kriged ozone data for the period 1983-1993, only the 1983-1990 period was used in their analysis due to Palmer hydrologic data not being available for the remaining three years. Our findings from this assessment indicate the need for more ozone monitoring stations along with meteorological information to develop more accurate exposure-response models in the SAMI region.

12. The combination of the Palmer hydrologic index and the ozone exposure results indicate that soil moisture conditions may alter tree growth response (lessen the effect) to ozone exposures (Lefohn et al.1997). Other information indicates that these two stress factors may act synergistically to reduce tree growth (McLaughlin and Downing 1995). Combining exposure information with moisture availability and experimental exposure-response data has identified possible areas that may have the greatest potential for possible vegetation effects and more investigation is warranted in this area.

13. Several models have been used to simulate growth and/or physiological responses to ozone. These include a single tree model (TREGRO), several canopy models on ozone uptake and carbon fixation, a forest succession model (FORET) and a loblolly pine management model (AIRPTAEDA). These models all provide some information on ozone effects to species commonly found in the SAMI region. Each model has advantages and disadvantages, and they vary in their level of complexity. TREGRO provides good information on ozone effects to a single, open-grown tree, it however, does not provide information regarding forest stand growth. Accurate ozone dose-response functions are needed to model tree responses using TREGRO. While these functions are available for some tree species at the seedling level they are not available for mature trees. Given the paucity of mature tree studies, model predictions using experimental growth responses are not easily validated. In addition, the model (TREGRO) requires detailed ozone exposure, environmental and physiological data. These are not presently available for many species. The canopy models all provide information on ozone uptake and carbon fixation. They do not supply data regarding whole-tree responses (root growth, etc.). In addition, all assume that ozone levels and ozone responses are equal within a crown. This may produce error in the model. The FORET model provides some extremely useful information on ozone effects to a forest stand. It can provide data on changes in growth and productivity over time. This simulator needs to be reparameterized specifically for ozone. It originally was parameterized for air pollution effects in general, and this assumption needs to be modified. Also, the model ozone effects to be equal within a species, and error could ensue due to this assumption. AIRPTAEDA has limited use for an assessment of the trees within the SAMI region, since loblolly pine is a minor component. Also this model is based on a growth and yield model for plantation-grown trees. It does, however, account for differential genetic variability within a species to ozone. This technique may be able to be modified and used in other models.

14. Three assessment methodologies have been used to determine ozone risk to different forest types in the region. All three have advantages and disadvantages. It will be up to SAMI to determine which one if any (or a modification of them) bests suits their needs. The method proposed by Lefohn et al. (1997) provides information on areas that are possibly at risk by using ozone kriging information combined with the Palmer hydrologic index to create "hazard maps" for ozone. This methodology is empirically driven and is based on the assumption that moisture stress in conjunction with ozone stress cause a reduction in ozone-induced growth effects. It is difficult, however, to distinguish between ozone effects and/or drought effects using this method, and due to a lack of ozone monitoring data values are kriged. The second risk assessment was conducted by Hogsett et al. (1993). The advantage of this technique is that it combines the use of simulation models, such as TREGRO and GIS technology to provide a regional assessment. There appears to be several layers of parameritization necessary (model linkages), however, for the assessment to be operational. As with the previous technique (Lefohn et al. 1997), forest growth scenarios are mainly based on individual tree data from only a small number of studies, mostly with seedlings growing in pots, in open-top chambers. Other concerns are with the error associated with the estimation of ozone exposures and species distribution. There is little ozone monitoring data available and the exposures are estimated using emissions data. The third methodology proposed by Luxmoore (1992) although a very valid technique is probably not feasible at present for an overall assessment of multiple trees species occurring in the SAMI region regarding ozone effects in its current form.

15. Research needs to be performed using ambient-type exposure patterns instead of applying exposure regimes that exhibit numerous high hourly average concentrations that do not occur under ambient conditions.

16. Additional monitoring stations should be established in rural areas at both high and low elevations.

Recommendations

It is our opinion that any of the three aforementioned assessment methodologies have merit, but it is up to SAMI to choose which one (or a modification of them) best suits its purpose. It is imperative, however, when conducting assessment exercises, that we must constantly keep in mind the tremendous variability that exists within natural systems. Therefore, to "model" ozone induced exposure/responses across the geographic range of a species (even within the 'limited' range of the SAMI region) poses a formidable task. At this time, we would consider the influence of micro-site factors to be most important in controlling responses to altering the potential for ozone induced exposures; available soil moisture appears at the present time to be of greatest single importance in controlling ozone uptake through its influence on stomatal function at the leaf level. Scaling of this single site/physiological response phenomenon from seedling research to mature canopy responses continues to hold a significant position of need in future research efforts. Such forest-based research is necessary in support of the assessment efforts at determining region-wide ozone impacts when these are suggested to be occurring as larger scale forest responses.

In addition, assessments must also take into account the relative influences of insect pests, biotic pathogens and abiotic stressors (other than ozone) and inter and intra species competition for resources in contributing to the measured/ modeled changes in forest health and/or productivity. Very careful diagnostics must first take place at the specific sites and for the species of interest before an ozone-induced response may be held accountable at that specific site, or even for selected species at that site. Scaling responses across broad regions (i.e., SAMI) for the purpose of determining ozone-induced effects without regard to gaining a clear understanding of the influence of many other stress-inducing factors would possibly present a skewed and, therefore, unrealistic scenario of the relative importance of ambient ozone exposures to forests in the SAMI region.

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U.S. Environmental Protection Agency. 1992. Summary of selected new information on effects of ozone on health and vegetation: Draft supplement to air quality criteria for ozone and other photochemical oxidants. Environmental Protection Agency, Office of Health and Environmental Assessment, Washington, DC. U.S.; EPA report no. EPA-600/8-88/105A. Available from NTIS, Springfield, VA.

U.S. Environmental Protection Agency. 1996. Air quality criteria for ozone and related photochemical oxidants. Environmental Protection Agency, Office of Air Quality Planning and Standards, Research Triangle Park, NC. U.S.; EPA report no. EPA/600/P-93/004bF.

Volin, J.C., Tjoelker, M.G., Oleksyn, J. and Reich, P.B. 1993. Light environment alters response to ozone stress in seedlings of Acer saccharum Marsh and hybrid Populus L.: 2. diagnostic gas exchange and leaf chemistry. New Phytol. 124:637-646.

Wang, Y.P. and Jarvis, P.G. 1990. Description and validation of an array model MAESTRO. Agr. For. Meterol. 54:257-280.

Webb, C.D. and Burkhart, H.E. 1988. Modelling the effects of air pollution on forest productivity: a sensitivity analysis using PTAEDA. P. 530-537 In: A.R. Ek, S.R. Shifley and T.E. Burk (eds.). Forest Growth Modelling and Prediction (Volume 1). Proc. of the IUFRO Conference, August 23-27, 1987, Minneapolis, MN. USDA Forest Service, North Central Forest Experiment Station, St. Paul, MN, General Technical Report NC-120.

Webb, C.D., Burkhart, H.E. and Amateis, R.L. 1992. An approach to scaling up physiological responses of forests to air pollutants. P. 287-302 In: R.B. Flagler (ed.). Transactions: The Response of Southern Commercial Forests to Air Pollution. Air and Waste Mange. Assoc., Pittsburgh, PA.

Weber, J.A., Clark, C.S. and Hogsett, W.E. 1993. Analysis of the relationships among O3 uptake, conductance, and photosynthesis in needles of Pinus ponderosa. Tree Physiol. 13:157-172.

Weinstein, D.A. and Yanai, R.D. 1994. Integrating the effects of simultaneous multiple stresses on plants using the simulation model TREGRO. J. Environ. Qual. 23:418-428.

Weinstein, D.A., Beloin, R.M. and Yanai, R.D. 1991. Modeling changes in red spruce carbon balance and allocation in response to interacting ozone and nutrient stresses. Tree Physiol. 9:127-146.

West, D.C., McLaughlin, S.B. and Shugart, H.H. 1980. Simulated forest response to chronic air pollution stress. J. Environ. Qual. 9:43-49.

Wieser, G. and Havranek, W.M. 1995. Environmental control of ozone uptake in Larix decidua Mill.: A comparison between different altitudes. Tree Physiol. 15:253-258.

Winner, W.E. 1994. Mechanistic analysis of plant responses to air pollution. Ecol. Appl. 4:651-661.

Winner, W.E., Lefohn, A.S., Cotter, I.S., Greitner, C.S., Nellessen, J., McEvoy, L.R. Jr., Olson, R.L., Atkinson, C.J. and Moore, L.D. 1989. Plant responses to elevational gradients of O3 exposures in Virginia. Proc. Natl. Acad. Sci. U.S.A. 86: 8828�8832.

Winner, W.E., Cotter, I.S., Powers, H.R. Jr. and Skelly, J.M. 1987. Screening loblolly pine seedling responses to SO2 and O3: Analysis of families differing in resistance to fusiform rust disease. Environ. Pollut. 47:205-220.

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X. LIST OF FIGURES

1. The SAMI region, including Class I areas.

2. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1983

3. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1984

4. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1985

5. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1986

6. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1987

7. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1988

8. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1989

9. Kriged ozone exposures using the 7-month (April-October), 24-h, W126 index for the Southern Appalachian Mountain Region, 1990

10. Input parameters and relationship to the simulated forest stand for the FORET model (modified from West et al. 1980).

11. Proposed risk assessment framework modified from Hogsett et al. (1993).

12. Proposed risk assessment framework modified from Luxmoore (1992).

Table 1. Summary of ozone effects on light-saturated net photosynthesis (Pn) and stomatal conductance (gs), carbon partitioning or allocation, or nutrient status in species found in the SAMI region. Ozone exposures were delivered using CSTRs (continuously stirred reactors), CECs (controlled environmental chambers) or OTCs (open-top chambers). Only OTC field studies located in the SAMI region were included. Unless noted, studies were conducted on seedlings.


Tree species
Exposure duration
Exposure facility
Ozone concentrations
Physiological response
Reference

Abies fraseri
4 h/day, 3 d/week, 10 weeks
CSTR
<0.02, 0.05, 0.10 ppm
no effect on Pn, no water stress interaction
Tseng et al. 1988


4 h/day, 3 d/week, 10 week growth cycles
CSTR
0.025, 0.070, 0.150 ppm
no effect on Pn, gs
Seiler et al. 1994

Acer rubrum
1 growing season
OTC, Norris, TN
CF (SUM00=35 ppm-h), AA (SUM00=89 ppm-h), AA x 2 (SUM00=173 ppm-h)
AA x 2 reduced Pn by 25%
Samuelson 1994a

Acer saccharum
74 days
CEC
0.008, 0.099 ppm
reduced Pn by 60% only in shaded seedlings
Volin et al. 1993


17 h/day, 5 d/week, 10 weeks
CEC
0.03, 0.06, 0.09, 0.12 ppm
0.12 ppm reduced Pn by 30%
Reich et al. 1986

Quercus alba
2 growing seasons
CSTR
CF, > AA
no effect on Pn, gs
Foster et al. 1990

Quercus rubra
2 growing seasons
OTC, Norris, TN
CF (SUM00=35 ppm-h), AA (SUM00=100 ppm-h), AA x 2 (SUM00=190 ppm-h)
no effect on Pn, gs of seedlings; Pn reduced by 25% in AA and 50% in AA x 2 in mature trees
Hanson et al. 1994


3 growing seasons
OTC, Norris, TN
CF, AA, AA x 2
greater influence of ozone on carbon allocation and partitioning , and nutrition of mature trees than seedlings.
Samuelson et al. 1996; Samuelson 1996


7 h/day, 5 d/week, 10 weeks
CEC
0.03, 0.06, 0.09, 0.12 ppm
0.12 ppm reduced Pn by 20%
Reich et al. 1986

Liriodendron tulipifera
6 h/day, 1 month
CSTR
CF, 0.07,

0.15 ppm


no effect on Pn, gs
Cannon et al. 1993


4 h/day, 5 d/week, 6 weeks
CSTR
<0.02, 0.05, 0.10, 0.15 ppm
0.10 ppm reduced gs by 15%
Chappelka et al. 1988


8 h/day, 3 d/week, 5 months
CSTR
0, 0.05, 0.10,

0.20 ppm


no effect on Pn or root starch
Jensen et al. 1990


8 h/day, 3 d/week, 3 months
CSTR
0, 0.05, 0.10,

0.20 ppm


0.10 ppm reduced Pn by 24%
Roberts 1990


8 h/day, 3 d/week, 20 weeks
CSTR
0, 0.05, 0.10,

0.20 ppm


0.20 ppm increased foliar Mn and Fe
Schier 1990


18 weeks
OTC, Oak Ridge, TN
CF, AA, AA + 60 ppm
no effect on Pn, gs; no interaction between O3 and soil nitrogen
Tjoelker and Luxmoore 1991

Picea rubens
4 h/day, 3 d/week, 10 weeks
CSTR
<0.25, 0.10 ppm
no effect on Pn, gs
Lee et al. 1990a


6 h - 24 h/day, 28 weeks
CSTR
CF, 0.15 ppm for 6 h/day, 0.15 ppm for 6/h day + 0.07 ppm for 18/h day
greatest ozone exposure reduced sugar in needles and roots
Patton et al. 1991


2 growing seasons
OTC, Whitetop MT., VA
AA x 0.5, AA
no effect on Pn
Pier et al. 1992


4 h/day, 2 d/week, 16 weeks
CSTR
CF, 0.12 ppm
no effect on leaf or whole seedling Pn
Taylor et al. 1986


1 growing season
OTC, Whitetop MT., VA
CF, AA
no effect on Pn
Thornton et al. 1990


3 growing seasons
OTC, Whitetop MT, VA
CF, AA
no effect on Pn, seedling nutrition
Thornton et al. 1992

Prunus serotina
1 growing season
uncontrolled field, central PA
ambient
foliar injury related to Pn
Fredericksen et al. 1996


1 growing season
OTC, Norris, TN
CF (SUM00=35 ppm-h), AA (SUM00=89 ppm-h), AA x 2 (SUM00=173 ppm-h)
AA x 2 reduced Pn by 23%
Samuelson 1994

Pinus strobus
7 h/day, 3 d/week, 4 months
CEC
0.02, 0.06, 0.10, 0.14 ppm
linear increase in foliar K, decrease in root Ca
Reich et al. 1988


7 h/day, 3 d/week, 4 months
CEC
0.02, 0.06, 0.10, 0.14 ppm
linear reduction in Pn, 20% decline in Pn in 0.14 ppm
Reich et al. 1987


1 growing season
uncontrolled field, Oak Ridge, TN
ambient
25-yr-old trees with greater visible injury had greater foliar respiration
McLaughlin et al. 1982


4 h/day, 50 days
CSTR
0, 0.10, 0.20, 0.30 ppm
photosynthetic reduction dependent on clone and exposure duration
Yang et al. 1983

Pinus taeda
12 weeks
OTC, Oak Ridge, TN
CF, AA + 0.08 ppm, AA + 0.16 ppm
AA + 0.16 ppm reduced coarse root starch
Adams and O'Neill 1991


2 growing seasons
OTC, Oak Ridge, TN
CF, AA, AA x 2
AA x 2 increased foliar N, P
Edwards et al. 1991


2 growing seasons
OTC, Oak Ridge, TN
CF, AA, AA x 2
no effect on carbon allocation
Edwards et al. 1992


3 growing season
OTC, Oak Ridge, TN
CF, AA, AA x 2
AA x 2 affected carbon allocation & partitioning
Friend and Tomlinson 1992


7 h/day, 5 d/week, 13 weeks
OTC, Oak Ridge, TN
0.014, 0.170 ppm
reduced Pn by 25%
Hanson et al. 1988


4 h/day, 3 d/week, 10 weeks
CSTR
CF, 0.10 ppm
ozone induced greater sensitivity to water stress
Lee et al. 1990b


5 h/day, 5 d/week, 12 weeks
CSTR
CF, 0.05, 0.10, 0.15 ppm
linear reductions in foliar starch and total plant carbohydrates
Meier et al. 1990


1 growing season
OTC, Oak Ridge, TN
CF, AA, AA x 2
no effect on seedling nutrition
Simmons and Kelly 1989


18 weeks
OTC, Oak Ridge, TN
CF, AA, AA + 60 ppm
AA + 60 reduced gs 35%, no interaction of O3 with soil nitrogen
Tjoelker and Luxmoore 1991

Table 2. Summary of ozone effects on growth and biomass production of selected tree species found in the SAMI region. Ozone exposures were delivered using CSTRs (continuously stirred tank reactors), CECs (controlled environment chambers) or OTCs (open-top chambers). Only OTC field studies located in the SAMI region were included. Unless noted, studies were conducted with seedlings.


Tree species
Exposure duration
Exposure facility
Ozone concentration
Growth response
Reference

Abies fraseri
4 h/d, 3 d/wk, 10 wks
CSTR
<0.02, 0.05, 0.10 ppm
No effect on any growth variable measured
Tseng et al. 1988


4 h/wk, 3d/wk, 10 wk growth cycles
CSTR
0.025, 0.70, 0.15 ppm
No effect on any growth variable measured
Seiler et al. 1994

Acer rubrum
1 growing season
OTC (trees in pots) - Norris, TN
CF, NF, NFX2
No effect on any growth variable measured
Samuelson 1994a


8 h/d, 3 d/wk for 16 weeks
CSTR
0.0, 0.07, 0.15 ppm
Slight decrease (4%) in leaf dry weight at 0.15 ppm
Jensen and Dochinger 1989


7 h/d, 5 d/wk for 8 or 12 wks
CSTR
0.04 or 0.08 ppm
Sig. decreases in stem dia., twig dia., and stem biomass; 18%, 18% and 34%, respec. At 0.08 ppm compared with 0.04 ppm
Davis & Skelly 1992b


1 growing season
OTC (trees in pots) - Great Smoky Mount. Nat. Park
CF, NF, NFX1.5, NFX 2, 24 h/d
Sig decrease in root biomass (29%) and total biomass (15%) at 2X compared with ambient. No effect on ht & dia
Nuefeld et al. 1992

Acer saccharum
8 h/d, 3 d/wk for 16 weeks
CSTR
0.0, 0.07, 0.15 ppm
Slight decrease (4%) in new growth biomass at 0.15 ppm
Jensen and Dochinger 1989


6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
12%, 42%, 31% and 41% decrease in height, top wt., root wt., and total biomass at 0.15 ppm compared with 0.0 ppm. Only sig. treat. effect
Kress & Skelly 1982

Fraxinus americana
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
Sig. decreases in top, root and total biomass (9%, 8%, 13%) beginning at 0.1 ppm
Kress & Skelly 1982


4 h/d, 5 d/wk for 5 wks
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
Sig. linear decrease in root, leaf and total biomass, total height and root/shoot ratio with increasing ozone conc.
Chappelka & Chevone 1986


4 h/d, 5 d/wk for 6 wks
CSTR
0.025 or 0.1 ppm
Sig. decrease in leaf area (18%) and total biomass (14%) at high conc.
Chappelka et al. 1988

F. pennsylvanica
4 h/d, 5 d/wk for 6 wks
CSTR
0.025 or 0.1 ppm
Sig. decrease in ht growth (15%) at 0.1 ppm
Chappelka et al. 1988


6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
A 24% decrease in ht growth at 0.1 ppm
Kress & Skelly 1982


2 growing seasons
OTC (trees in pots) - Shenandoah Nat. Park, VA
CF, NF, AA
67% decrease in ht growth in NF compared with CF
Duchelle et al. 1982

Liquidambar styraciflua
8 h/d, 3 d/wk for 16 weeks
CSTR
0.0, 0.07, 0.15 ppm
At 0.15 ppm trees had a slight reduc. in leaf dry wt, leaf area and ht (4-7%)
Jensen and Dochinger 1989


6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
Reduc. in ht and biomass occurred at 0.1ppm. Root biomass was the most sensitive variable with a 48% decrease at 0.15 ppm
Kress & Skelly 1982

Liriodendron tulipifera
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
No sig. effect compared with controls for growth variables
Kress & Skelly 1982


7 h/d, 5 d/wk for 8 or 12 wks
CSTR
0.04 or 0.08 ppm
A 20%, 35% decrease in twig dia and leaf wt. and 30% increase in defoliation at elevated ozone level
Davis & Skelly 1982b


8 h/d, 3 d/wk for 16 weeks
CSTR
0.0, 0.07, 0.15 ppm
No sig. effect on ht growth or biomass
Jensen and Dochinger 1989


4 h/d, 5 d/wk for 6 wks
CSTR
0.025 or 0.1 ppm
No sig. diff. in plant growth
Chappelka et al. 1985


4 h/d, 5 d/wk for 6 wks
CSTR
<0.02, 0.05, 0.1 or 0.15 ppm
No sig. diff. in plant growth
Chappelka et al. 1988


6 h/d, 7 d/wk for 5 wks
CSTR
0.0 or 0.07 ppm
No sig. diff. in plant growth
Mahoney et al. 1984


2 growing seasons
OTC (trees in ground) - Shenandoah Nat. Park
CF, NF, AA
41% decrease in ht growth in NF compared with CF
Duchelle et al. 1982

Picea rubens
4 h/d, 2 d/wk for 4 months
CSTRs
CF or 0.12 ppm
No effects for any variable measured
Taylor et al. 1986


1 growing season
OTC (trees in pots) - Whitetop MT, VA
CF, NF
No effects for any variable measured
Thornton et al. 1990


3 growing seasons
OTC (trees in pots) - Whitetop MT, VA
CF, NF
No effects for any variable measured
Thornton et al. 1992

Platanus occidentalis
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
A linear decrease in root wt. and total wt. with increasing conc. Total biomass decreased by 69% at 0.15 ppm compared with 0.0 ppm
Kress & Skelly 1982


1 growing season
OTC (trees in pots) - Great Smoky Mount. Nat. Park
CF, NF, NFX1.5, NFX 2, 24 h/d
Increase in leaf drop and production at NFX2. Root and leaf biomass decreased with increasing ozone conc. Total biomass reduced 9% from CF to NF
Nuefeld et al. 1992

Pinus echinata
ozone added 12 h/d for 28 months
OTC (trees in ground) - Clemson, SC
CF, NF, NFX1.7 and NFX2.5
Sig. effects only observed at NFX2.5. Leaf area reduc 35% and leaf biomass decrease 30% from CF
Shelburne et al. 1993

P. pungens
1 growing season each for 3 consec growing seasons
OTC (trees in pots) - Great Smoky Mount. Nat. Park
CF, NF, NFX1.5, NFX 2, 24 h/d
No effect on growth or total biomass production
Nuefeld et al. 1992


2 growing seasons
OTC (trees in ground) - Shenandoah Nat. Park
CF, NF, AA
A 12% decrease in ht growth at NF compared with CF
Duchelle et al. 1982

P. rigida
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
Ozone effects observed beginning at 0.10 ppm. Total biomass reduced 24% at 0.15 ppm
Kress & Skelly 1982


8 h/d for 13 wks
CEC
0, 0.05, 0.1, and 0.2 ppm
Increasing ozone caused decreases in needle, stem and root dry wt. Greatest effect at 0.2 ppm
Schier et al. 1990


Variable, 2 4 h fumg. or 6 h/d, 3 d/wk for 5 wks
CEC
0, 0.08, 0.1, 0.2 or 0.3 ppm
No effects within families, but diff. in sensitivity among families
Scherzer & McClenehen 1989

P. strobus
7 h/d, 3 d/wk for 4 months
CEC
0.02, 0.06, 0.1 or 0.014 ppm
No effect on seedling biomass
Reich et al. 1987


2 growing seasons
OTC (trees in ground) - Shenandoah Nat. Park, VA
CF, NF, AA
A 20% decrease in ht growth at NF compared with CF
Duchelle et al. 1982

P. taeda
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
Differential sensitivity in response. "Wild-type" seedlings more sensitive than a full-sib family
Kress & Skelly 1982


3 growing seasons
OTP (trees in pots) - Oak Ridge, TN
CF, NF, NF+0.06 ppm
No effects on any growth variable measured
Adams et al. 1990


2 growing seasons
OTP (trees in pots) - Oak Ridge, TN
CF, NF, NFX2
Ht growth lowest in NF. Increasing ozone exposures resulted in decreased biomass of all plant components after 2 yrs
Edwards et al. 1991


3 growing seasons
OTP (trees in pots) - Oak Ridge, TN
CF, NF, NFX2
Ht growth lowest in NF. Dia growth greatest in CF. Relative wood density decreased with elevated ozone. Increasing ozone exposures resulted in decreased biomass of all plant components (8% decrease in total biomass) after 3 yrs
Edwards et al. 1992


2 growing seasons
OTP (trees in ground) - Durham, NC
CF, NF, NFX1.5, NFX2.25, NFX3
Foliage retention decreased with increased ozone. Family diff. observed
Kress et al. 1992


6 h/d, 4 d/wk for 12 weeks
OTC (trees in pots) - Oak Ridge, TN
CF, NF, NFX0.53, NFX1.1, NFX1.58, NFX2.15
NF treatment resulted in a 26% decreased in ht and 5% decease in dia compared with CF. Response to elevated conc highly variable; dependent on family
McLaughlin et al. 1994


2 growing seasons
OTC (trees in ground) - Durham, NC
CF, NF, NFX1.5, NFX2.25, NFX3
Shoot and fascicle elongation longer in CF compared with NFX3. No effect at intermediate levels
Mudano et al. 1992


3 growing seasons
OTC (trees in ground) - Raleigh, NC
CF, NF, AA, NFX1.25, NFX1.5, NFX1.75, NFX2
Differential sensitivity in response observed. Visible injury not correlated with growth.

Exposure-response models predicted above-ground reductions in biomass at ambient ozone from 0-19% after two yrs.

After 3 yrs growth loss was 13% for most sensitive family


Shafer & Heagle 1989


6 h/d, 4 d/wk, for 12 wks
CSTR
0, 0.08, 0.16, 0.24, 0.32 ppm
Differential sensitivity in response observed. Using a regression model total dry wt was reduced 25% at 0.32 ppm compared with controls
Shafer et al. 1993

P. virginiana
6 h/d for 28 consec. d
CSTR
0.0, 0.05, 0.1, and 0.15 ppm
No sig. effects for any growth variable measured
Kress & Skelly 1982


2 growing seasons
OTC (trees in ground) - Shenandoah Nat. Park, VA
CF, NF, AA
A 22% decrease in ht growth at NF compared with CF
Duchelle et al. 1982

Prunus serotina
7 h/d, 5 d/wk for 8 or 12 wks
CSTR
0.04 or 0.08 ppm
A 43%, 37%, 62%, 45%, 47% and 54% decrease in ht, twig dia, stem dry wt, root dry wt, leaf dry wt and leaves produced at 0.08 ppm compared with 0.04 ppm
Davis & Skelly 1982b


1 growing season
OTC (in pots) - Norris, TN
CF, NF, NFX2
A 29% and 14% decrease in ht and root/shoot ratio and 18% increase in branch wt at 2X
Samuelson 1994a


1 growing season each repeated for 2 yrs
OTC (in pots) - Great Smoky Mts. Nat. Park
CF, NF, AA, NFX1.5, NFX2
In both yrs the NFX2 caused a reduc in total, leaf, root and stem+root biomass, and present defol. Using combined data, growth losses ranged from 1-2% in NF vs. CF
Neufeld et al. 1995

Quercus rubra
7 h/d, 5 d/wk for 8 or 12 wks
CSTR
0.04 or 0.08 ppm
A 20% decrease occurred in root dry wt and a 6% increase in defoliation at 0.08 ppm
Davis & Skelly 1982b


1 growing season
OTC (trees in ground, seedlings in pots) - Norris, TN
CF, NF, NFX2
No effect on seedling ht or biomass, canopy leaf dry wt was decreased at NFX2 for mature trees
Samuelson & Edwards 1993


3 growing seasons
OTC (trees in ground, seedlings in pots) - Norris, TN
CF, NF, NFX2
Seedling ht increased at NFX2. No effect on biomass or dia. No effects on foliar biomass or canopy stem growth for mature trees
Samuelson et al. 1996

Robinia pseudoacacia
2 growing seasons
OTC (in ground) - Shenandoah Nat. Park, VA
CF, NF, AA
An 18% decrease in ht growth at NF compared with CF
Duchelle et al. 1982

Table 3. Ozone exposure levels as a function of tree response category.


Tree Response Category


Exposure




W126

(ppm-h)



Hours � 0.10 ppm


Minimal
�0


and


�0

Level 1 (only high sensitive species affected (e.g., black cherry)
�5.9


and


�6

Level 2 (moderately sensitive species affected (e.g., yellow- poplar)
�23.8


and


�51

Level 3 (all species affected, even those naturally nonsensitive (e.g., red oak)
�66.6


and


�135