Ozone exposure thresholds and foliar injury on forest plants in Switzerland

Canton Ticino in southern Switzerland is exposed to some of the highest concentrations of tropospheric ozone in Europe. During recent field surveys in Canton Ticino, foliar symptoms identical to those caused by ozone have been documented on native tree and shrub species. In Europe, the critical ozone level for forest trees has been defined at an AOT40 of 10 ppm.h O3 (10 ppm.h accumulated exposure of ozone over a threshold of 40 ppb) during daylight hours over a six-month growing season. The objective of this study was to determine the amount of ambient ozone required to induce visible foliar symptoms on various forest plant species in southern Switzerland. Species were grown within eight open-top chambers and four open plots at the Vivaio Lattecaldo Cantonal Forest Nursery in Ticino, Switzerland. Species differed significantly in terms of the ppb.h exposures needed to cause visible symptoms. The most to least symptomatic species grown within open-plots in this study rank as Prunus serotina, Salix viminalis, Vibrnum lantana, Rhamnus cathartica, Betula pendula, Rumex obtusifolius, Sambucus racemosa, Morus nigra, Prunus avium, Fraxinus excelsior, Rhamnus frangula, Alnus viridis, Fagus sylvatica and Acer pseudoplatanus. Similar rankings were obtained in the non-filtered chamber plots. The ranking of species sensitivity closely follows AOT values for the occurrence of initial symptoms and symptom progression across the remainder of the exposure season. Species that first showed evidence of foliar injury also demonstrated the most sensitivity throughout the growing season, with symptoms rapidly advancing over ca. 25-30% of the total plant leaf surfaces by the end of the observation period. Conversely, those species that developed symptoms later in the season had far less total injury to plant foliage by the end of the observation period (1.5 to < 5% total leaf area injured). The current European ambient ozone standard may be insufficient to protect native plant species from visible foliar injury, and many more native species may be sensitive to ozone-induced foliar injury than are currently known.     

Ozone air pollution and foliar injury development on native plants of Switzerland

The objectives of this study were to examine the foliar sensitivity to ozone exposure of 12 tree, shrub, and herbaceous species native to southern Switzerland and determine the seasonal cumulative ozone exposures required to induce visible foliar injury. The study was conducted from the beginning of May through the end of August during 2000 and 2001 using an open-top chamber research facility located within the Lattecaldo Cantonal Forest Nursery in Canton Ticino, southern Switzerland (600 m asl). Plants were examined daily and dates of initial foliar injury were recorded in order to determine the cumulative AOT40 ppb h ozone exposure required to cause visible foliar injury. Plant responses to ozone varied significantly among species; 11 species exhibited visible symptoms typical of exposures to ambient ozone. The symptomatic species (from most to least sensitive) were Populus nigra, Viburnum lantana, Salix alba, Crataegus monogyna, Viburnum opulus, Tilia platyphyllos, Cornus alba, Prunus avium, Fraxinus excelsior, Ribes alpinum, and Tilia cordata; Clematis spp. did not show foliar symptoms. Of the 11 symptomatic species, five showed initial injury below the critical level AOT40 10 ppmh O3 in the 2001 season.     

Incidence of ozone symptoms on vegetation within a National Wildlife Refuge in New Jersey, USA

During 1993-1996 and 2001-2003, we evaluated the percentage of plants (incidence) exhibiting ozone-induced foliar symptoms on vegetation within a National Wildlife Refuge located along the Atlantic Ocean coast of New Jersey, USA. Incidence varied among plant species and years. Bioindicator plants most sensitive to ozone, across all years, included native common milkweed (Asclepias syriaca) and wild grape (Vitis spp.), as well as introduced tree-of-heaven (Ailanthus altissima). Less sensitive bioindicators included Virginia creeper (Parthenocissus quinquefolia) and winged sumac (Rhus coppolina). Black cherry (Prunus serotina) and sassafras (Sassafras albidum) were least sensitive. The greatest incidence of ozone symptoms, across all plant species, occurred in 1996, followed by 2001>1995>1994>1993>2003>2002. A model was developed that showed a statistically significant relationship between incidence of ozone symptoms and the following parameters: plant species, Palmer Drought Severity Index, and the interaction of W126 x N100 measures of ambient ozone.     

Differential response of buddleia (Buddleia davidii Franch.) to ozone

Five cultivars of buddleia, Buddleia davidii Franch., were exposed to sub-ambient, ambient, and twice-ambient levels of ozone in open-top chambers for 8 weeks (June-August) during 1995: Plants were evaluated for foliar injury, growth index, and inflorescence characteristics during and following exposure. Destructive harvests were conducted at the end of the exposure period to determine dry weights of both above- and below-ground plant components. All cultivars had symptoms of visible injury in the twice-ambient treatment at both three and eight weeks after exposures began. No visible symptoms were observed at ambient ozone concentrations. At three weeks of exposure, 'Pink Delight' had the highest percentage of the leaves injured (PLI), 46.2%, followed by 'Opera' with a PLI of 23.3%. The other three cultivars had similar PLIs of less than 15%. After eight weeks of exposure, visible injury was equally severe on all cultivars with a mean PLI of 50.2% and mean Horsfall-Barratt rating of 5.4, indicating 12 to 25% of the leaf area was injured. No ozone x cultivar interaction was found for any growth variable measured. Across cultivars, growth index was reduced by 6%, total dry weight by 35%, and the number of developing floral buds and inflorescences by 29% for plants in twice-ambient ozone concentrations compared to ambient ozone concentrations. Percent biomass allocated to inflorescences was significantly greater for plants exposed to sub-ambient levels compared to those exposed to ozone at either ambient or twice-ambient concentrations. Results indicate that ozone levels similar to those in large urban areas in the southeastern United States have the potential to reduce growth and flowering of this important landscape plant.     

Interpreting spatial variation in ozone symptoms shown by cutleaf cone flower,Rudbeckia laciniata L

Visible injury caused by ozone is recorded every year in native plant species growing in Great Smoky Mountains National Park (USA). One of the most sensitive species, cutleaf coneflower (Rudbeckia laciniata L.), shows great variation in symptoms between and within populations but the causes of this variation and its ecological significance are currently unknown. This paper presents data relating to genetic variation, ozone concentrations, stomatal conductance and light (PAR) within populations. The data show that populations differ in genetic diversity, one consisting of only three genets while another was very diverse. In the former population, symptoms varied greatly within a single genet, pointing to a large micro-environmental influence. Measurements of ozone, stomatal conductance and PAR within plant canopies suggest that variation in symptom expression is unlikely to be due to differences in ozone flux and more likely to be due to variation in light. The variation in visible symptoms raises the question of what bioindicators actually indicate, and it suggests that symptoms should be interpreted with great caution until the underlying causes of that variation are fully understood.     

The Characterization of Ozone Data for Sites Located in Forested Areas of the Eastern United States

Six years (1978-1983) of ozone monitoring data from sites located within six forested areas were examined. Areas that experienced the lowest to the highest ozone exposures were located in (1) northern New England/New York and upper Great Lakes, (2) New York/Pennsylvania/Maryland, (3) southeastern/southern, and (4) New Jersey pinelands. In general, higher ozone concentrations were observed in 1978, 1980 and 1983 as compared to the other three years examined. Ozone concentrations varied considerably within the areas. Recommendations for additional ozone monitoring sites are made. A concentrated effort should be made to examine ozone monitoring data from subsequent years (1984, 1985, and 1986) to explore whether the 6-year period 1978 through 1983 is representative of the annual variability of ozone concentrations over eastern forested areas. To better understand the relationship between ozone exposure and possible forest effects, we recommend that the temporal distributions of elevated ozone concentrations over a growing season be examined. The occurrence of elevated ozone levels during specific growth periods during a season may be an important aspect that biologists may wish to explore.     

Biochemical changes in needles of Pinus radiata D. Don trees in relationship to long-term ozone exposure indices

Ambient concentrations of ozone in Europe are high enough to cause negative effects on vegetation. Therefore, many efforts have been made to determine exposure indices and critical levels for protection of vegetation. In this context, the choice of a suitable attribute to determine the pollutant effect is of paramount importance. Until now, much of the work has been done with attributes such as biomass or growth. In the present work correlation factors have been established between biochemical parameters (peroxidase activity, ascorbate and sulfhydryl contents) of Pinus radiata trees and exposure indices of ozone. Our results show that peroxidase cannot be used as an indicator of effects of long-term exposure to ozone but still remains as an excellent indicator of short-term ozone fluctuations in the field. Ascorbate may act as an intermediate indicator responding to both short fluctuations and long-term exposures to ozone. Finally, sulfhydryl may be used as a long-term indicator in relation to the AOT (average over threshold) exposure index. Our results also point to the fact that Pinus radiata may be affected by ozone at AOT values lower than 10 ppm.h as already observed with other tree species.     

Sub-canopy deposition of ozone in a stand of cutleaf coneflower

Although there has been a great deal of research on ozone, interest in exposure of native, herbaceous species is relatively recent and it is still not clear what role the pollutant has in their ecological fitness. The ozone exposure of a plant is usually expressed in terms of the concentration above the canopy or as a time-weighted index. However, to understand the physiological effects of ozone it is necessary to quantify the ozone flux to individual leaves as they develop, which requires knowing the deposition velocity and concentration of the pollutant as a function of height throughout the plant canopy. We used a high-order closure model of sub-canopy turbulence to estimate ozone profiles in stands of cutleaf coneflower (Rudbeckia laciniata L.) located in the Great Smoky Mountains National Park, USA. The model was run for periods coinciding with a short field study, during which we measured vertical concentration profiles of ozone along with measurements of atmospheric turbulence and other meteorological and plant variables. Predictions of ozone profiles by the model are compared with observations throughout the canopy.     

Significance of Atmospheric Ozone as a Phytotoxicant

Since the recognition of ozone as a major phytotoxicant in crop plants in 1957, ozone type symptoms have been observed in a wide range of vegetation. These observations include leafy vegetables, field, forage, and textile crops, also shrubs, broad-leafed ornamental, fruit and forest trees, and various conifers. Fumigation experiments at various institutions have confirmed the etiological relation of ozone in many of these observations. Such visible injuries fail to provide a reliable index to the damaging impact of ozone on the numerous plants affected. Hidden injury or damage by ozone at sub-necrotic levels has been reported and experimentally established in a number of crop plants. Evidence is available which indicats that citrus varieties are so affected, and that much of the citrus decline in Southern California may be ozone induced. Photochemically induced ozone may prove to be the most persistent, if not the most difficult, of atmospheric phytotoxicants to control. Ozone type injury has been reported from eighteen different states, and from Canada to Japan.     

Ozone in the urban southeastern United States

Ozone measurements (daily maximum values) from the Aerometric Information Retrieval System database are analyzed for selected sites, during 1980 to 1988, in southeastern USA. Frequency distributions, for most sites during most years, show a typical bell-shaped curve with the higher frequency around the yearly daily maximum ozone mean of about 100 to about 110 microg m(-3) (50-55 ppbv). Abnormal years in ozone concentration may skew the distribution as the mean shifts. A correlation of daily maximum ozone concentrations above 140 microg m(-3) (70 ppbv) between sites shows a division between the sites in the northern protion of the region and those in the southern portion of the region. Variations in ozone levels are well correlated over distances of several hundred kilometers, suggesting that high values are associated with synoptic scale episodes. An ozone exposure analysis also shows higher ozone exposures (250-300 ppm days) in the northerly sites as compared to the southerly sites (150-170 ppm days).     

Surface ozone exposures measured at clean locations around the world

For assessing the effects of air pollution on vegetation, some researchers have used control chambers as the basis of comparison between crops and trees grown in contemporary polluted rural locations and those grown in a clean environment. There has been some concern whether the arbitrary ozone level of 0.025 ppm and below, often used in charcoal-filtration chambers to simulate the natural background concentration of ozone, is appropriate. Because of the many complex and man-made factors that influence ozone levels, it is difficult to determine natural background. To identify a range of ozone exposures that occur at 'clean' sites, we have calculated ozone exposures observed at a number of 'clean' monitoring sites located in the United States and Canada. We do not claim that these sites are totally free from human influence, but rather than the ozone concentrations observed at these 'clean' sites may be appropriate for use by vegetation researchers in control chambers as pragmatic and defensible surrogates for natural background. For comparison, we have also calculated ozone exposures observed at four 'clean' remote sites in the Northern and Southern Hemispheres and at two remote sites (Whiteface Mountain, NY and Hohenpeissenberg, FRG) that are considered to be more polluted. Exposure indices relevant for describing the relationship between ozone and vegetation effects were applied. For studying the effects of ozone on vegetation, the higher concentrations are of interest. The sigmoidally-weighted index appeared to best separate those sites that experienced frequent high concentration exposures from those that experienced few high concentrations. Although there was a consistent seasonal pattern for the National Oceanic and Atmospheric Administration (NOAA) Geophysical Monitoring for Climate Change (GMCC) sites indicating a winter/spring maximum, this was not the case for the other remote sites. Some sites in the continental United States and southern Canada experienced ozone exposures in the range between those values experienced at the South Pole and Mauna Loa NOAA GMCC sites. The 7-month average of the daily 7 h average ozone concentration at 'clean' sites located in the continental United States and southern Canada ranged from 0.028 to 0.050 ppm. Our analysis indicates that seasonal 7 h average values of 0.025 ppm and below, used by some vegetation researchers as a reference point, may be too low and that estimates of crop losses and tree damage in many locations may have been too high. Our analysis indicates that a more appropriate reference point in North America might be between 0.030 and 0.045 ppm. We have observed that the subtle effects of changing distribution patterns of hourly average ozone concentrations may be obscured with the use of exposure indices such as the monthly average. Future assessments of the effects associated with ground-level ozone should involve the use of exposure indices sensitive to changes in the distribution patterns of hourly average ozone concentrations.     

Seedling insensitivity to ozone for three conifer species native to Great Smoky Mountains National Park

Field symptoms typical of ozone injury have been observed on several conifer species in Great Smoky Mountains National Park, and tropospheric ozone levels in the Park can be high, suggesting that ozone may be causing growth impairment of these plants. The objective of this research was to test the ozone sensitivity of selected conifer species under controlled exposure conditions. Seedlings of three species of conifers, Table Mountain pine (Pinus pungens), Virginia pine (Pinus virginiana), and eastern hemlock (Tsuga canadensis), were exposed to various levels of ozone in open-top chambers for one to three seasons in Great Smoky Mountains National Park in Tennessee, USA. A combination of episodic profiles (1988) and modified ambient exposure regimes (1989-92) were used. Episodic profiles simulated an average 7-day period from a monitoring station in the Park. Treatments used in 1988 were: charcoal-filtered (CF), 1.0x ambient, 2.0x ambient, and ambient air-no chamber (AA). In 1989 a 1.5x ambient treatment was added, and in 1990, additional chambers were made available, allowing a 0.5x ambient treatment to be added. Height, diameter, and foliar injury were measured most years. Exposures were 3 years for Table Mountain pine (1988-90), 3 years for hemlock (1989-91), and 1 and 2 years for three different sets of Virginia pine (1990, 1990-91, and 1992). There were no significant (p<0.05) effects of ozone on any biomass fraction for any of the species, except for older needles in Table Mountain and Virginia pine, which decreased with ozone exposure. There were also no changes in biomass allocation patterns among species due to ozone exposure, except for Virginia pine in 1990, which showed an increase in the root:shoot ratio. There was foliar injury (chlorotic mottling) in the higher two treatments (1.0x and 2.0x for Table Mountain and 2.0x for Virginia pine), but high plant-to-plant variability obscured formal statistical significance in many cases. We conclude, at least for growth in the short-term, that seedlings of these three conifer species are insensitive to ambient and elevated levels of ozone, and that current levels of ozone in the Park are probably having minimal impacts on these particular species.     

Ozone Injury to Pinus Strobus

In a study of the ozone-induced needle blight of eastern white pine in central New York, acute injuries naturally induced on field trees during a year of relatively low ozone concentrations (1 966) were compared with injuries induced during a year of higher concentrations (1967). Injuries were more frequent and severe and were associated with higher mean ozone concentrations in 1967 than in 1966. Characteristic symptoms were induced on foliage of pine branches exposed to controlled doses of ozone as low as 7 ± 1 pphm for four hours or 3 ± 1 pphm for 48 hours. Such doses were equalled or exceeded two and four times, respectively, in the field during the 1 967 season. Ozone sensitivity of pine needle tissue was increased by fumigation in atmospheres containing water mist. High concentrations of ozone (40-60 pphm) caused general injury of foliage of both ozone-susceptible and resistant trees; the symptoms were unlike those found in the field or caused by fumigation with low concentrations of ozone.     

Bioindicator plants for ambient ozone in Central and Eastern Europe

Sixteen species of native detector plants for ambient ozone have been identified for use in Central and Eastern Europe. They include the forbs Alchemilla sp., Astrantia major, Centuarea nigra, Centauria scabiosa, Impatiens parviflora, Lapsana communis, Rumex acetosa and Senecio subalpinus; the shrubs Corylus avellana, Cornus sanguinea and Sambucus racemosa; the trees Alnus incana, Pinus cembra and Sorbus aucuparia; and the vines Humulus lupulus and Parthenocissus quinquefolia. Sensitivity to ozone and symptoms have been verified under controlled exposure conditions. Under these conditions, symptom incidence, intensity and appearance often changed with time after removal from exposure chambers. Ozone sensitivity for four species: Astrantia major, Centuarea nigra, C. scabiosa and Humulus lupulus are reported here for the first time. The other 12 species have also been confirmed by others in Western Europe. It is recommended that these detector bioindicator species be used in conjunction with ozone monitors and passive samplers so that injury symptoms incidence can be used to give biological significance to monitored ambient ozone data.     

Potential bioindicator plant species for ambient ozone in forested mountain areas of central Europe

From 1993 to 2000, trees, shrubs, forbs and vines were evaluated for symptoms of probable ozone injury in the vicinity of passive ozone samplers or active ozone monitors in forest condition assessment networks in mostly mountainous regions, principally the Carpathian Mountain Range, in the central European countries Czech Republic, Poland, Romania, Slovakia and Ukraine. Each country was visited at least twice during the time period. Over the course of eight seasons, 29 species of native plants were identified as potential bioindicators of ozone. This is the first report of probable ozone injury on native plants in central Europe. Forbs and shrubs made up the bulk of the species (21 of 29). Potential bioindicators that are widely distributed include the forbs Centaurea nigra. and Impatiens parviflora and the shrubs Alnus incana, Corylus avellana, and Sambucus racemosa. Ozone concentrations in forcsted areas of central Europe appear to be high enough and of sufficient duration to cause foliar injury on a wide variety of native plants.     

Acid mist and ozone effects on the leaf chemistry of two western conifer species

Seedlings of Jeffrey pine (Pinus jeffreyi) and giant sequoia (Sequoiadendron gigantea) were more susceptible to leaf chemical changes following exposure to acid mist (pH 3.4-2.0) or acid mist/ozone combinations, than to ozone alone (0.1-0.2 microl/litre), when plants were exposed to alternating doses of these pollutants for 6-9 weeks. Under acid mist treatment, leaves exhibited higher levels of nitrogen and sulfur, two elements applied in acid mist. In addition, levels of foliar sodium, and, in the case of giant sequia, potassium, as well, increased under acid mist treatment. Iron and manganese were also mobilized, resulting in significant increases in these elements in pine, and decreases in manganese in giant sequoia foliage. The acid treatment also reduced chlorophyll b concentrations in pine, and, to a less significant extent, in giant sequoia. Calcium, magnesium, barium and strontium were differentially accumulated in giant sequoia compared to Jeffrey pine. Under acid mist treatment, all of these elements (except strontium) declined in concentration in giant sequoia, with calcium showing the most significant trend. The more extensive changes in leaf chemistry induced by acid mist are consistent with earlier observations of significant changes in spectral reflectance of these seedlings after 3 weeks of fumigation. Limited foliage samples collected from these two species in 1985 and 1986 in Sequoia/Kings Canyon National Parks in the southern Sierra Nevada do not in themselves indicate any clearcut or severe effects of ozone alone on leaf chemistry of these species, but a mild influence of nitrate-laden acid deposition, possibly in combination with ozone, is consistent with the rise in nitrogen and lignin levels in Jeffrey pine on sites observed to have moderate visible injury symptoms. No firm conclusions about effects of pollutants on leaf chemistry in these field sites is possible without further study.     

Air Pollution Damage to the Forests of the Sierra Nevada Mountains of California

Numerous oxidant-injured ponderosa pine and other tree species have been detected in the lower elevation forests of the southern Sierra Nevada mountain range of California in the Sequoia National Forest, Sequoia-Kings Canyon National Parks, and on state and private lands. Affected pines were observed in a broad band following the many ridges that rise above the Central Valley floor to the 1900-2600 m elevation. Slight symptoms of ozone chlorotic mottle on ponderosa pine appeared from about 1000 m altitude, increased in severity as elevation increased and then diminished in severity above 2600 m. An apparent east to west gradient of disease was discovered; severity lessened as distance from the Central Valley increased. Atmospheric monitoring in three forested sites suggests that ozone occurs in doses sufficient to elicit symptoms of this widespread disease.     

Spatial pattern of ozone injury in Aleppo pine related to air pollution dynamics in a coastal-mountain region of eastern Spain

In eastern Spain, studies combining the tracking and meso-scale circulations of air pollutants with the evaluation of their effects on plants have been undertaken since 1994. Meso-scale processes are very important from the point of view of how and where forest ecosystems are affected by point sources and regional air pollution in the Mediterranean area. The first results of these field surveys show that in 1994, 1995 and 1996, the distribution pattern of ozone visual injury (chlorotic mottle) in Pinus halepensis correlated with the penetration of pollutants transported by the sea-breeze into coastal valleys of Castellón (eastern Spain). In this tree species, longer needles are associated with higher chlorotic mottle, and ozone injury seems to be among the factors affecting needle retention and crown transparency.     

Ozone-induced foliar injury in saplings of Psidium guajava 'Paluma' in São Paulo, Brazil

Psidium guajava 'Paluma' was evaluated under field conditions as a tropical bioindicator species of ozone (O(3)). Three exposures of 90 days each were performed (June 21, 2004-March 19, 2005). In each one of them, saplings of 'Paluma' (n=30) were exposed to ambient air at a site in S?o Paulo (Brazil) with high ozone concentrations, and in a greenhouse with charcoal-filtered air. Ozone-like visible foliar injuries were observed during the winter, spring and summer exposures, when AOT40 reached 6166ppbh, 3504ppbh and 4828ppbh, respectively. No injuries were observed in the plants kept under filtered air. The injuries consisted in red stippling on adaxial leaf surfaces. They did not cover the veins and appeared first in older leaves, becoming more intense as the exposure period increased. Injury incidence, severity, and the cumulative exposure threshold at injury onset varied among the exposure periods. AOT40 explained partly the incidence, severity and leaf injury index LII (r(2)=0.52, 0.39, 0.38, respectively, p=0.002). The results confirm the potential of the species as an O(3)-sensitive bioindicator.     

Responses of hybrid poplar clones and red maple seedlings to ambient O(3) under differing light within a mixed hardwood forest

The responses of ramets of hybrid poplar (Populus spp.) (HP) clones NE388 and NE359, and seedlings of red maple (Acer rubrum, L.) to ambient ozone (O(3)) were studied during May-September of 2000 and 2001 under natural forest conditions and differing natural sunlight exposures (sun, partial shade and full shade). Ambient O(3) concentrations at the study site reached hourly peaks of 109 and 98 ppb in 2000 and 2001, respectively. Monthly 12-h average O(3) concentrations ranged from 32.3 to 52.9 ppb. Weekly 12-h average photosynthetically active radiation (PAR) within the sun, partial shade and full shade plots ranged from 200 to 750, 50 to 180, and 25 to 75 micromol m(-2) s(-1), respectively. Ambient O(3) exposure induced visible foliar symptoms on HP NE388 and NE359 in both growing seasons, with more severe injury observed on NE388 than on NE359. Slight foliar symptoms were observed on red maple seedlings during the 2001 growing season. Percentage of total leaf area affected (%LAA) was positively correlated with cumulative O(3) exposures. More severe foliar injury was observed on plants grown within the full shade and partial shade plots than those observed on plants grown within the sun plot. Lower light availability within the partial shade and full shade plots significantly decreased net photosynthetic rate (Pn) and stomatal conductance (g(wv)). The reductions in Pn were greater than reductions in g(wv), which resulted in greater O(3) uptake per unit Pn in plants grown within the partial shade and full shade plots. Greater O(3) uptake per unit Pn was consistently associated with more severe visible foliar injury in all species and/or clones regardless of differences in shade tolerance. These studies suggest that plant physiological responses to O(3) exposure are likely complicated due to multiple factors under natural forest conditions.