John M. Skelly

Issues in scaling tree size and age responses to ozone : A review

Ozone is probably the most important regional air pollutant currently affecting forest trees. The vast majority of information regarding ozone effects on trees has come from experiments with seedlings, where controlled concentrations of ozone were administered in indoor or outdoor chambers for periods lasting from several days to one or more growing seasons. However, it is difficult to extrapolate, or scale, results from experiments on seedlings to larger forest trees. Mature trees typically differ from seedlings in morphological, phenological, and physiological characteristics that may profoundly influence response to ozone exposure. Also, it is possible that ozone exposure dynamics may differ for seedlings growing near the ground compared to exposure within the forest canopy. Complicating the ability to scale ozone responses from seedlings to canopy trees are differing interpretations of what is meant by ozone sensitivity. Differences in ozone sensitivity between mature trees and seedlings may occur because of differences in: ozone uptake (avoidance), compensation for injured tissues, internal properties that oppose the production of tissue injury (defense), and repair of tissue injury. Of these mechanisms, avoidance is commonly measured in scaling studies whereas compensation, defense, and repair are not. A review of studies that have compared stomatal conductance between trees of different size and age showed that large trees typically have lower stomatal conductance than seedlings, suggesting greater avoidance of ozone uptake by large trees, but there are notable exceptions to this apparent trend. For tree species where response to ozone and stomatal conductance has been compared between large and small trees, the tree size class with the greatest stomatal conductance showed the greatest detrimental leaf physiological response to ozone. This finding supports the hypothesis that differences in ozone response between different-sized trees of the same species occurs, at least in part, because of differences in ozone uptake. For most of these species (Picea rubens, Pinus ponderosa, Prunus serotina, Sequoiadendron giganteum), large or old trees had lower stomatal conductance and lower ozone foliar injury than small or young trees, whereas for Quercus rubra, large trees had greater stomatal conductance and greater ozone foliar injury than small trees. Drawing firm conclusions from published scaling studies is complicated by wide variation in study methodology and how ‘seedling’ and ‘mature tree’ are defined. To facilitate synthesis and improve prediction of ozone impacts on trees, we recommend that future ozone scaling research examine the occurrence and effectiveness of avoidance, compensation, defense, and repair in trees of different sizes with consistent methodology on a suite of species that vary in ecological and physiological characteristics. We also recommend that future research examine the possible consequences of these mechanisms to long-term ecological success for trees of different sizes in the presence of other biotic and abiotic stresses.

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.

Observation and Confirmation of Foliar Ozone Symptoms of Native Plant Species of Switzerland and Southern Spain

Tropospheric ozone is considered as the major pollutant of concern to the health and productivity of forests in the eastern United States and has more recently become of increasing concern within the forests of southern Europe. Recent observations have clearly demonstrated foliar injury symptoms to be occurring on many tree and native plant species within remote forested areas. Several plant genera (and a few species within genera) found in both the forests of Switzerland and the southern coastal region of Spain exhibit field symptoms typical of ambient ozone exposures. Ozone exposures for many species have been conducted under controlled CSTR conditions and within open-top chambers within the study areas. Results have confirmed that the O3-like foliar symptoms as observed under natural forest and open grown conditions for many native tree, shrub, and herbaceous species in Spain and Switzerland are caused by exposures to ambient O3.

Physiology, morphology, and ozone uptake of leaves of black cherry seedlings, saplings, and canopy trees.

Patterns of ozone uptake were related to physiological, morphological, and phenological characteristics of different-sized black cherry trees (Prunus serotina Ehrh.) at a site in central Pennsylvania. Calculated ozone uptake differed among open-grown seedlings, forest gap saplings, and canopy trees and between leaves in the upper and lower crown of saplings and canopy trees. On an instantaneous basis, seedling leaves had the greatest ozone uptake rates of all tree size classes due to greater stomatal conductance and higher concentrations of ozone in their local environment. A pattern of higher stomatal conductance of seedlings was consistent with higher incident photosynthetically-active radiation, stomatal density, and predawn xylem water potentials for seedlings relative to larger trees. However, seedlings displayed an indeterminate pattern of shoot growth, with the majority of their leaves produced after shoot growth had ceased for canopy and sapling trees. Full leaf expansion occurred by mid-June for sapling and canopy trees. Because many of their leaves were exposed to ozone for only part of the growing season, seedlings had a lower relative exposure over the course of the growing season, and subsequently lower cumulative uptake, of ozone than canopy trees and a level of uptake similar to upper canopy leaves of saplings. Visible injury symptoms were not always correlated with patterns in ozone uptake. Visible symptoms were more apparent on seedling leaves in concurrence with their high instantaneous uptake rates. However, visible injury was more prevalent on leaves in the lower versus upper crown of canopy trees and saplings, even though lower crown leaves had less ozone uptake. Lower crown leaves may be more sensitive to ozone per unit uptake than upper crown leaves because of their morphology. In addition, the lower net carbon uptake of lower crown leaves may limit repair and anti-oxidant defense processes.

Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings

Two black cherry families differing in sensitivity to ozone (O(3)) were used to test the hypothesis that leaf morphology is related to foliar sensitivity to O(3). Two uninjured sections of leaf tissue were sampled from a single leaf collected from each of 12 open-grown O(3)-tolerant and 12 O(3)-sensitive seedlings. Standard histological techniques and light microscopy were used to examine 11 morphological characteristics. The O(3)-sensitive genotype had significantly greater stomatal density, thinner palisade mesophyll layer and thicker spongy mesophyll layer, lower ratio of palisade to spongy mesophyll, greater leaf weight and leaf area. In addition, total leaf thickness, guard cell length, and specific leaf mass were also slightly greater for the O(3)-sensitive genotype.

Size-mediated foliar response to ozone in black cherry trees.

Local ozone concentration and visible foliar injury were measured over the 1994 growing season on open-grown black cherry (Prunus serotina Ehrh.) trees of varying size (age) within forest stands and adjacent openings at a site in north-central Pennsylvania. Relationships were determined between visible ozone injury and ozone exposure, as well as calculated between injury and ozone uptake expressed as the product of stomatal conductance and ozone concentration. In addition, simultaneous measurements of visible symptoms and leaf gas exchange were also conducted to determine the correlation between visible and physiological injury and ozone exposure. By September, the amount of leaf area affected by visible foliar ozone injury was greatest for seedlings (46%), followed by canopy trees (20%) and saplings (15%). A large amount of variability in foliar ozone symptom expression was observed among trees within a size class. Sum40 and Sum60 (ozone concentration > 40 and > 60 nl liter(-1)) cumulative exposure statistics were the most meaningful indices for interpretation of foliar injury response. Seedlings were apparently more sensitive to ozone injury than larger trees because their higher rates of stomatal conductance resulted in higher rates of ozone uptake. Seedlings also had higher rates of early leaf abscission than larger trees with an average of nearly 30% of the leaves on a shoot abscised by 1 September compared to approximately 5% for larger trees. However, per unit ozone uptake into the leaf, larger trees exhibited larger amounts of foliar injury. The amount of visible foliar injury was negatively correlated (r(2) = 0.82) with net photosynthetic rates, but was not related to stomatal conductance. Net photosynthesis and stomatal conductance thus became uncoupled at high levels of visible foliar injury.

Response of native plants of northeastern United States and southern Spain to ozone exposures; determining exposure/response relationships

Tropospheric ozone has been identified as the most important regional scale air pollutant across much of eastern United States of America and many areas of Mediterranean climes in southern Europe. Recent field surveys in the northeastern USA and in southeastern Spain have revealed many additional plant species that exhibit symptoms typical of ozone-induced injuries. Objectives of this study were to confirm ozone as the cause of the observed foliar symptoms, determine ozone induced exposure/response relationships, and identify possible bio-indicator species. Thirteen native species of northeastern USA and 27 native species of southeastern Spain were selected for study. Plant species were exposed to ozone within 16 CSTR chambers in a greenhouse during the summer seasons of 2000 and 2001; ozone exposures of 30, 60, 90, and 120 ppb were delivered for 7 h/day, 5 days/week. Results have confirmed that with few exceptions, symptoms observed in the field were induced by exposures to ambient ozone. Species differed significantly in terms of the exposures required for the initiation of visible symptoms and subsequent injury progression.

Assessment of ozone visible symptoms in the field: perspectives of quality control

The second UN/ECE ICP-Forests Intercalibration Course on the Assessment of Ozone Injury on European Tree Species was carried out in August 2001 at Lattecaldo (Canton Ticino, CH) and Moggio (Lombardy, I). Forty-eight experts from several European countries participated in the exercises and assessed visible symptoms of ozone injury both in open-top chambers (OTC) (Lattecaldo) and under open field (Moggio) conditions. Evaluation of the results indicated a large variability among the teams and call for adequate training of the observers prior to symptom assessment for quality assurance purposes. Highest variability was found for the species developing unclear symptoms which could be confused with senescence processes; such species should not be used in the field. The authors provide suggestions to improve the reliability of the ozone injury assessment on forest plant species.

Physiological and foliar injury responses of Prunus serotina, Fraxinus americana, and Acer rubrum seedlings to varying soil moisture and ozone

Sixteen black cherry (Prunus serotina, Ehrh.), 10 white ash (Fraxinus americana, L.) and 10 red maple (Acer rubrum, L.) 1-year old seedlings were planted per plot in 1997 on a former nursery bed within 12 open-top chambers and six open plots. Seedlings were exposed to three different ozone scenarios (ambient air: 100% O3; non-filtered air: 98% ambient O3; charcoal-filtered air: 50% ambient O3) within each of two different water regimes (nine plots irrigated, nine plots non-irrigated) during three growing seasons. During the 1998 and 1999 growing season, leaf gas exchange, plant water relations, and foliar injury were measured. Climatic data,ambient- and chamber-ozone-concentrations were monitored. We found that seedlings grown under irrigated conditions had similar (in 1998) but significantly higher gas exchange rates (in 1999) than seedlings grown within non-irrigated plots among similar ozone exposures. Cherry and ash had similar ozone uptake but cherry developed more ozone-induced injury (< 34% affected leaf area, LAA) than ash (<5% LAA), while maple rarely showed foliar injury, indicating the species differed in ozone sensitivity. Significantly more severe injury on seedlings grown under irrigated conditions than seedlings grown under non-irrigated conditions demonstrated that soil moisture altered seedling responses to ambient ozone exposures.

Foliar sensitivity of eight eastern hardwood tree species to ozone

As part of a larger 3-yr study, container-grown seedlings of black cherry (Prunus serotina) red maple (Acer rubrum), red oak (Ouercus rubra), sweetgum (Liquidambar styraciflua), white ash (Fraxinus americana), white oak (Ouercus alba), yellow-poplar (Liriodendron tulipifera), and yellow birch (Betula allegheniensis) were exposed to 0,0.075, or 0.15 μL L-1 O3 in laboratory controlled-environment chambers for 6 hr d−1 on 2 consecutive days for 12 weeks. On the third consecutive day of each week, plants were treated for 45 min with precipitation at pH 3.0 or 4.2. The only significant foliar symptoms were induced by the O3 treatments, and the severity of symptoms was not influenced by precipitation pH. The most common symptom was a dark, adaxial stipple which was most severe on the oldest leaves. Equations were developed to express the influence of leaf position on percent leaf injury following 4, 8, and 12 weeks of treatment. Based on percent leaf tissue showing stipple and defoliation following exposure to 0.15 μL L−1 O3, the most sensitive species to O3 was black cherry, followed by sweetgum, yellow-poplar, white ash, red maple and yellow birch. Red oak and white oak foliage did not exhibit stipple.