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7 chronic exposure. The permanent-plot system used by Forest Inventory and Assessment personnel of the U. S. Forest Service and tree-ring analysis are particularly useful for integrating long-term effects of pollutant stresses on trees and forests. THE WORKSHOP The committee's workshop was held on April 25-27, 1 98S, at Little Switzerland, North Carolina. A fundamental question discussed at the workshop was whether there are any unequivocal markers of the effects of air pollution on trees. Can changes in the structure, color, metabolism, or reproductive success of trees and associated plants or changes in whole forest stands or systems unequivocally indicate effects of specific air pollutants not caused by any other factors? Or are the effects of individual pollutants so confounded with the effects of other stresses that they are impossible to identify without extensive experimentation? Introductory Papers Several papers at the workshop provided overviews of current programs for monitoring forest conditions and air-pollutant concentrations. Husar described a large-scale program for monitoring chemical air pollutants over North America and Europe. He provided, in effect, a distributional atlas of atmospheric pollutants, such as sulfur and nitrogen oxides, including their emissions, deposition, and concentra- tions. This atlas, which can be examined with microcomputers, is intended to reveal patterns of pollutant occurrence and of forest change. On a smaller scale, Mohnen examined elevational gradients of air pollutants based on data accumulated by the Mountain Cloud Chemistry Program (MCCP) in the eastern United States. At MCCP sites, chemical and physical measurement of selected acidic compounds and associated oxidants are being taken annually; the data will be useful for detecting attitudinal and latitudinal variations. Barnard reviewed the Forest Response Program of the National Vegetation Survey (NVS), a program begun in 1985 to determine the extent and magnitude of forest conditions in the United States. Several NVS projects, such as one on dendrochronology, give promise of a broad-scale monitoring program for the identifica- tion of visible symptoms in forest stands. In the southern United States, for example, a geographic information network will provide data on forest properties and on atmospheric deposition of pollutants. According to Cape, monitoring European forest conditions using routine visual assessments of leaf loss and discoloration has presented problems of interpretation. He suggested the use of alternative methods, such as comparison of visibly damaged versus undamaged trees, comparison of trees at different sites exposed to different pollution regimes, and controlled-exposure experiments intended to improve the validity of large-scale field surveys. Tingey examined general applications and constraints in the use of biologic markers for air pollution research. Because markers usually are relatively nonspecific indicators of a problem, they must be used with caution in drawing conclusions about cause-and-effect relationships. Ideally, markers are easily measurable, are responses to specific pollutants, and produce distinctive symptoms that are not confused with those caused by other environmental stresses. Sharpe and Spence examined several new and emerging technologies for potential use in the detection of responses to stress, including short-lived radioisotopes, nuclear magnetic resonance, infrared reflectance, fiber optics, and semiconductors. Successful implementation of these tools would not be easy or inexpensive, but preliminary information suggests that these new and emerging methods would be remarkably cost-effective, compared with traditional experimental protocols, for detecting some types of stress.

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8 Regional Applications of Biologic Markers The next group of papers covered the use of biologic markers at forest sites in different regions. A. H. Johnson reported on abiotic stresses and air pollution in the decline of northern Appalachian red spruce forests. Multiple stress factors in winter, coupled with pathogen and insect injuries, have been associated with declines in these forests. Air-pollution stress (e.g., related to ozone) might increase the effects of winter injury or affect energy balance as trees deplete resources in response to pathogens and insect attacks. Anderson reviewed surveys showing relationships between airborne pollutants and symptoms in several sensitive plants in southeastern U.S. forests: eastern white pine, milkweed, and lichens. The use of those plants as markers has provided information on extent of injury, type of associated pollutant, and temporal variations. However, limitations in their use were found to be related to mimicked symptoms and genetic, as well as climatic, variations. For western coniferous forests, Miller considered the relation of biologic markers at tissue and whole-tree levels to air-pollution exposure. An array of markers (foliage injury and changes in needle tissues and elemental contents of leaves) was found to be more effective than a single marker in suggesting the cause of observed effects. The evaluation of air-pollution effects is improved by measuring the concentration of suspected pollutants along gradients of decreasing pollutant deposition in combination with controlled exposures of seedlings or small trees in enclosures that compare ambient air with carbon-filtered air. More specific markers are needed to distinguish air-pollution effects from those of other abiotic stress factors. Schutt discussed some problems in understanding forest decline in Europe, such as the presence of multiple air pollutants and possible synergistic effects. The detection of reliable specific symptoms is complicated by the large number of tree species and wide-ranging variations in climate, soil, ecology, and altitude. The existence of all those variations and gaps in knowledge makes it difficult to determine whether different groups of scientists in different locations are working on similar or different sets of forest decline problems. Physiologic, Morphologic, and Ecologic Markers The authors of this group of papers examined physiologic processes and structural features as potentially useful markers of air pollution in trees. Waring focused on resource allocation in various parts of a tree as an aid to interpreting signals of environmental change. For example, nutritional imbalances brought about by environmen- tal changes can alter the ratios of essential minerals to one another in foliage and roots. Comparing changes in selected structural ratios (e.g., the leaf-to-bole ratio) might make it possible to distinguish specific causes of stress and to correlate them with changes in pollution loads on forests. D. W. Johnson, Van Miegroet, and Swank noted how air pollution might affect cycles of forest nutrients, particularly sulfates and nitrates in natural waters. Although nutrient pools might be affected by air pollution, their relatively large size makes them rather insensitive markers. Even so, well- documented long-term elemental budgets should be useful for determining changes in ecosystem nutrient pools caused by air pollution and other factors. Fry looked at the degree to which stable isotopes (in tree rings, lake sediments, and the atmosphere) can serve as historical tracers of anthropogenic pollutants. Large isotopic changes in sulfur were found in recent lake sediments in response to relatively large changes in sulfate loading. Historical elemental records were compared with records of regional and national emission patterns. Cook and Innes described the use of tree-ring analysis to assess the impact of air pollutants on forests and pointed out that anomalous tree-ring behavior could be important in understanding pollution effects on forests. However, inferring a causal link between air pollution and forest declines from tree-ring analyses alone requires

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9 a better understanding of air-pollution effects on tree growth under natural conditions. Richards evaluated root growth and function after pollution-caused reduction in carbon allocation. Four techniques showed particular promise for assessing root-system damage caused by air pollution. As pointed out in several other papers given at the workshop, the use of multiple measurements will yield more reliable information from biologic markers than will attempts to relate air pollution to tree damage on the basis of a single measurement. Rock, Vogelmann, and Defeo discussed the use of remote-sensing techniques for monitoring air-pollution effects in several forests. Remote sensing has shown changes in the health of portions of spruce-fir forests in the eastern United States that are too large to attribute to typical trends and natural variability. Some spectral signatures are characteristic of forest damage and can be used on a large scale to identify various specific symptoms of damage. Weinstein and Laurence evaluated the use of indigenous and cultivated plants as biologic indicators of air pollution. Carefully selected indicator species not only can identify some pollutants but also can provide estimates of pollutant distribution and a rough approximation of source strength. Of the many plant species that are sensitive to air pollution, a large number are low in cultivation cost, require little maintenance, and can be grown over wide geographic areas, including remote sites where the absence of electric power precludes many on-site measurements. Scott and Hutchinson explored the suitability of using epiphytic lichens at high altitudes as early indicators of forest decline. Preliminary work indicated that growth abnormalities and metal accumulation can be demonstrated in some lichens growing on healthy conifers. Although epiphytic lichens appear to have potential as biologic markers of forest decline, their use as early indicators requires the identification of specific structural and chemical predictors of severe tree dieback. Little-inves- tigated microbial markers were the subjects of papers by Marx and Shafer, who used fungal and bacterial symbiosis, and by Antibus and Linkens, who examined rhizosphere activities. In the absence of baseline data on and adequate techniques for assessing symbiosis in forests, it is doubtful whether microbial associations have potential as biologic markers of air-pollution effects in forests. Similarly, data are too sparse to suggest that any specific rhizosphere organisms or functions can serve as simple biologic markers of air-pollution effects. However, measurements of root and rhizosphere enzyme activities do offer a simple approach to the study of air-pollution effects on rhizosphere physiology. Biochemical, Cellular, and Tissue-Level Markers The final group of workshop papers focused on potential biologic markers at the biochemical, cell, and tissue levels. Norby concentrated on foliar nitrate reductase, an enzyme that responds to gaseous nitrogen pollutants, can be measured in the field, and thus might be a useful marker of the effects of nitrogen pollution on trees. Richardson, DiGiulio, and Tandy looked at the potential use of free-radical-mediated processes as early biologic markers of stress in trees. The authors established dose-response relationships between ozone and acid-rain exposures and growth, photosynthesis, and other biochemical activities in loblolly pines. Mechanisms of action and interspecific variations are poorly understood, but it appears that antioxidants can be used as early markers of oxidative stress in trees. Jones and Coleman also investigated the use of biochemical indicators to predict changes in secondary metabolites and nitrogen in leaves; their models, supported by preliminary data, indicate that two or more of these characteristics will help to identify air-pollution stress or damage in trees. Shortle was concerned with changing concentrations of metals in various tree tissues. Some soil-related effects of acidic deposition might be linked to specific

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10 adverse plant conditions (e.g., suppression of cambial growth). The mechanism is believed to involve the release of aluminum cations into solution in acidic soils (pH 3- 4.5) followed by the gradual replacement of essential metal cations, such as calcium and magnesium, with aluminum in the rooting zone of spruce-fir stands. Bondietti, Baes, and McLaughlin focused on changes in aluminum mobilization. The trend in Al:Ca cation ratios in a tree growing on a relatively undisturbed site is a sensitive marker of aluminum mobilization caused by atmospheric acid cleposition. The use of correlations between Al:Ca ratios and radial growth rates is a promising approach to evluating the linkage between aluminum mobilization (from atmospheric deposition) and growth-rate declines. McLaughlin examined the allocation and partitioning of carbon among various physiologic processes as indicators of pollutant impacts on forest trees. The use of carbon allocation pathways to identify and diagnose responses of trees to air pollutants can include (1) identification of stress-induced shifts in patterns of carbon production, storage, and use; (2) quantification of changes in the amount, timing, and distribution of growth; and (3) evaluation of alterations in susceptibility to other stresses. A whole-tree perspective is recommended as the best approach for detection of changes in carbon allocation. Winner dealt with the use of photosynthesis and transpiration changes as biologic indicators in forests. Although those processes are affected by pollutant exposures, nonpollution environmental factors, as well as seasonal variations, can produce similar effects or confounding problems. Luxmoore was concerned with nutrient-use efficiency (NUE) as a biologic indicator of air-pollution stress in trees. A review of reported experiments led Luxmoore to suggest that NUE can be an insensitive indicator of stress. He concluded that the use of NUE as an indicator of stress is impractical on a whole- plant basis and is not definitive on a tissue basis. The possibility of using changes in leaf cuticle structure as a marker of air pollution was discussed by Berg, who used field and laboratory studies to demonstrate pollution-caused changes in ultrastructure and physiologic properties. Alscher, Cumming, and Fincher focused on ozone effects in red spruce during different seasons. Results from a dose-response experiment on red spruce seedlings suggest that ozone exposure during the summer and fall leads to changes in carbohydrate metabolism associated with winter hardening and to cell damage during the late fall and indicator of leaf stress; the loss of chlorophyll from plants has long been used to assess injury induced by air pollutants. Changes in chlorophyll fluorescence kinetics, although indicative of pollutant injury, might not be specific to air-pollutant injury. Therefore, several markers should be correlated before air pollutants alone can be identified as causing stresses observed in plants. Tyree's paper discussed drought as a factor that might interact with or be confused with stresses from atmospheric pollutants. After reviewing the relevant literature on drought and related stress mechanisms, Tyree pointed out forest decline symptoms caused by drought that could be confused with symptoms caused by air pollutants. early winter. Heath examined the use of chlorophyll fluorescence as an early ESTABLISHING CAUSE- AND- EFFECT RELATIONSHIPS Where should researchers look to detect early stages of the effects of air pollution on forests and trees, and how might they address the classical problem of establishing relationships between causes and effects? The answers are complicated and somewhat unsatisfactory, but, in view of the importance of this issue for understanding and controlling air pollution in the United States and elsewhere, are worthy of review.