AIR P O L L U T I O N - - E F F E C T S ON THE STRUCTURE A N D FUNCTION OF THE TEMPERATE FOREST ECOSYSTEM

WILLIAM H. SMITH

Department of Forest Pathology, School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut06511, USA ABSTRACT Air pollution has had, is having, and will continue to have an influence on forest ecosystems throughout the temperate regions of the world. The nature of this relationship can be divided into three classes. Under conditions of low dosage--Class I relationship--the vegetation and soils of forest ecosystems presumably function as a very important sink for air contaminants. When exposed to intermediate dosage-Class H relationship--individual tree species or individual members of a given species may be adversely and subtly affected by nutrient stress, reduced photosynthetic or reproductive rate, predisposition to entomological or microbial stress, or direct disease induction. Exposure to high dosage--Class III relationship--may induce acute morbidity or mortalio' of specific trees. The ecosystem impact of these various relationships wouM be very variable. In the Class I relationship, pollutants wouM be transferred from the atmospheric compartment to the biotic (organic) or available nutrient compartments. Depending on the nature of the pollutant, the ecosystem impact of this transfer couM be undetectable (innocuous effect ?) or stimulatory (fertilising effect). If the effect of air pollution exposure on some component of the ecosystem biota is inimical then a Class H relationship is established. The ecosystem impact in this case could include reduced productivity or biomass, shifts in species composition, increased secondary effects, such as insect outbreaks or disease epidemics, or increased morbidity and reduced vigour. The ecosystem impacts of Class II relationships are extraordinarily important because of their potentially widespread significance. In the presence of high air pollution dosage--Class III relationship-impact on the structure of the ecosystem may be gross simplification, and disturbances to the function of the ecosystem mar' include basic changes in hydrology, nutrient cycling, erosion, microclimate and overall stability. While these numerous ecosystem impacts, resulting from air pollution stress, have been identified, few have been quantified in the field. We are especially deficient in our ability generally to assess Class I and H relationships. This hiatus of knowledge
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is due to several factors in addition to the obvious difficulty of making accurate measurements of subtle processes in expansive andfrequently remote forest ecosys terns. Among the most important factors are: (1) the extraordinarily variable response different plant species and individuals within species have to individual air pollutants, (2) the strong controlling influence that local edaphic, topographical and meteorological conditions exert on plant response to air contaminants, (3) the fact that numerous tree species and most forest shrub and herb species have not been evaluated in regard to response to air pollutants, (4) the realisation that most of our data stem from studies with a very few pollutants reacted singly and that some gaseous and particulate contaminants and mixtures of pollutants have received little research attention, (5) that much of the research has been conducted employing air pollution dosages in considerable excess of ambient forest levels, and that (6) most of the investigations have been carried out under highly controlled--and hence artificial--environments. These six difficulties must be taken into consideration in future research. This research shouM concentrate on Class 1 and 11 relationships as these are considerably more significant than Class I l l situations. With the recognised deficiencies in our information we can speculate on the total impact of a i r pollution on forest ecosystems, but at present we cannot model or quantify it. Research to determine the relationships between air pollution and forest ecosystems must be given high priority because of the size and significance of these ecosystems in temperate regions and the numerous potentially-damaging interactions that have been identified.

INTRODUCTION

This is a very difficult topic to review because of the varied nature and sources of air contaminants and the diverse structure and complex function of temperate forest ecosystems. The topic has been included in the subject of excellent previous reviews (Treshow, 1968; Parmeter & Cobb, 1972; Babich & Stotzky, 1972) and I will concentrate on the most recent advancements. My comments will primarily assess the impact of air pollution on the vegetative component of forest ecosystems. I am restricted by competence to the plants but perhaps justified when one considers their role as primary producers and their dominant influence on the forest ecosystem function. The indirect influence air pollution may have on forests by affecting climate will not be considered as this is another large and complex topic which has been recently reviewed (Wenger et al., 1971). Although our knowledge is incomplete, we have sufficient information to divide the influence of air pollution on forest vegetation into three classes. Under conditions of low pollution load, designated Class I, the response of individual trees is undetectable and may involve no, or minimal, physiological alteration because the forest acts as a sink for air contaminants. The impact on the ecosystem, under these conditions, is to transfer the air pollutants from the atmospheric compartment

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to the organic or available nutrient compartments. If the air pollution load is increased to an intermediate level and when some threshold of tolerance, varying with different species and pollutants, is exceeded, then Class II responses occur, causing significant direct or indirect physiological impairment to individual members of the biota with reduced growth, reduced reproduction or increased morbidity, The impact on the ecosystem under Class I[ conditions may be reduced productivity or biomass, insect infestations, disease epidemics, reduced vigour and changes in species composition. High air pollution loads elicit Class III reactions which may include acute morbidity or mortality on the part of individual trees and simplification at the ecosystem level, perhaps along with nutrient loss, erosion, microclimatic and hydrological alteration and reduced stability. These classes are conceptual rather than actual and it must be realised that plant influence from air pollution occurs along a gradient that varies in regard to the orientation and strength of the source.

CLASS I RELATIONSHIP~ LOW POLLUTION LOAD--ECOSYSTEM ACTS AS A SINK

Numerous particulate and gaseous materials classified as air pollutants have natural origins. Carbon monoxide, H 2 S , N H 3 , oxides of nitrogen and hydrocarbons derived from natural sources greatly exceed the emission of these gases from manmade sources (Robinson & Robbins, 1968; Weinstock & Niki, 1972). The annual, global contribution of hydrocarbons by forests is i 75 x 106 metric tons of reactive hydrocarbons from tree foliage. This is six times larger than the emission level from man-made sources (Rasmussen, 1972). On the average, 70 ~o of the tree species of United States forest regions release appreciable quantities of volatile organic substances to the atmosphere (Rasmussen, 1972). One of the most abundant monoterpenes released by forests is ~t-pinene (Rasmussen, 1972), which has been suggested to be reactive in natural forest air (Westberg & Rasmussen, 1972) and capable, under laboratory conditions, of participating in the generation of ozone (Ripperton & Lillian, 1971). Since plants have evolved in the presence of numerous materials usually considered to be air pollutants, and since vegetation covers 90 ~o of the land area in the United States, it is reasonable to hypothesise that terrestrial ecosystems act as important sinks for air contaminants. If plant tolerance is great enough, the sinkfunction may extend to low pollution loads generated by man. Vegetation has been suggested as an important sink for N H 3 , HF, SO2, Cl2, N O 2, O 3 and, to a lesser extent, PAN during the growing season (H'ill, 1971; Hutchinson et al., 1972; Porter et al., 1972). Alfalfa data indicate that this plant could theoretically remove S O 2 from the atmosphere at a rate of 1.27 x 106 kg k m - 2 y - I [7"25 106 lb m i - Z y - l ] a n d N O E a t a r a t e o f 3 . 5 8 1 0 4 k g k m - E y - l [ 2 . 0 4 x l 0 5 1 b m i - z y -1] (Hill, 1971). Soybeans could r e m o v e NH 3 at a rate of 2.0 x l03 kg k m - 2 y - i

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TABLE 1
CALCULATED AIR POLLUTANT REMOVAL RATES FOR SELECTED ECOSYSTEM COMPONENTS

Ecosystem component

Pollutant

Annual removal rate kg k m 2 (Ibs mi- 2)

Reference

Alfalfa
Alfalfa

SO2 NH3 CO
NO2

Soybeans Soil

1-27 x l06 3"58 X 104 2.0 x 103 7.38 x 104

(7.25 x 106) (2"04 105) (l.14 X 104) (4"21 105)

Hill, 1971 Hill, 1971 Hutchinson etal., 1972 Inman et al., 1971

TABLE 2
CALCULATED* PARTICULATE METAL REMOVAL RATES FOR THE LEAVES AND CURRENT TWIGS OF A SINGLE, 3 0 CM (12 IN) DIAMETER URBAN SUGAR MAPLE (Acer saccharum MARSH) DURING THE COURSE OF A OROWING SEASON

Metal contaminant

Growing season removal rate mg tree 1 (oz tree 1)

Cadmium Chromium Lead Nickel

69 140 5,800 820

(0.092) (0.005) (0.20) (0-03)

* Calculated using sugar maple-dimension analysis data from Hubbard Brook Experimental Forest, New Hampshire, USA, and contamination data from New Haven, Connecticut, USA. [1"14 x 1041b mi -2 y - l ] (Hutchinson et al., 1972). The average capacity of temperate zone soils to remove CO from the atmosphere has been estimated to be 7-38 104 kg km -2 y-1.[4.21 l0 s lb mi-2 y - l ] (lnman et al., 1971) (Table 1). Soil may also be effective in removing ethylene, other hydrocarbons, SO2, and NO2 from the atmosphere (Abeles e t al., 1971). It has been widely suggested (Smith, 1970; Heggestad, 1972) that trees function efficiently to remove air pollutants from the atmosphere. Due to their size and abundance, trees may function more effectively than agricultural crops as filters (Keller, 1971). This hypothesis, however, is supported by very little direct evidence. Indirect calculations indicate that if a polluted air mass containing 0.15 ppm 03 stood over a forest of trees 4.6 m high for an hour, the air reaching the forest floor would have only 0.06-0.09 ppm 0 3 remaining and if the air mass stalled for eight hours, only 0.03 ppm 0 3 would reach the forest floor (Rich & Tomlinson, 1970). With regard to particulate subtraction from th e atmosphere via impaction on plant surfaces, trees may be quite efficient, due to tlae high surface to volume ratio of their foliage. Our data with heavy metals and urban trees suggest that the leaves and current twigs of a 30 cm diameter sugar maple remove from the atmosphere 60, 140, 5800 and 820 mg of cadmium, chromium, lead and nickel, respectively, during the course of a single growing season (Smith, 1973) (Table 2).

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What are the ecosystem consequences of the movement of air pollutants from the atmospheric to the vegetative and available nutrient compartments? The influence is variable and depends on the nature of the pollutant. In the case of exposure to very low levels of reactive materials such as 0 3 and PAN, the conversion to non-toxic, innocuous compounds is probably quite rapid with no detectable or significant ecosystem perturbation. In the case of SO2,-NO2 and NH 3, conversion may proceed to compounds useful as nutrient sources. If absorption is large enough, particularly with regard to nitrogenous gases and the nitrogen budget, the long-term impact on certain ecosystem components could be stimulatory (Hill, 1971 ; Hutchinson et al., 1972; Porter et al., 1972). The effect of this stimulation on overall ecosystem function is not clear but conceivably could be either advantageous or disadvantageous. With regard to accumulative and recalcitrant materials such as chloride, fluoride and heavy metals, even in the absence of direct vegetative injury, a damaging impact may be imposed on consuming organisms such as those insects that feed on leaves or twigs. Pollinators, cambium feeders and even predatory insects associated with fluoride-contaminated trees have been shown to have elevated fluoride levels (Carlson & Dewey, 1971). Once the threshold of deleterious effect on some component of the ecosystem biota is crossed, however, the ecosystem can no longer be considered an effective, long-term sink and a Class II relationship is established.

CLASS I1 RELATIONSHIP" INTERMEDIATE POLLUTION LOAD--ECOSYSTEM UNDERGOES SUBTLE, DETERIORATING ALTFRATION

The impact of intermediate pollution dosage on individual trees may range from reduced growth and reproduction through increased morbidity.
Reduced growth Air pollution may indirecl~ly depress growth by interfering with nutrient availability. Within the forest ecosystem, nutrients occur in one of four basic comparlments: (1) atmosphere, (2) living and dead organic matter, (3) available nutrients, and (4) primary and secondary minerals (soil and rock) (Likens & Bormann, 1971). Air pollution may influence nutrient cycling by altering amounts in, and rates of, flow between compartments (1), (2) and (3). The leaves and twigs of trees in and around urban (Smith, 1972, 1973; Stephens et al., 1972) and industrial (Little & Martin, 1972) locations can become contaminated with very high levels of heavy metals. The litter formed beneath such trees acts as a giant sink for these accumulated metals. With regard to the known microbial toxicity of heavy metals, especially the fungitoxicity (Horsfali, 1956), an hypothesis has been advanced (Tyler, 1972) that litter decomposition--and hence re-mobilisation of minerals--may be slower or less complete in forests subjected

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to heavy metal air pollution. Heavy metals have been shown to be capable of reducing soil respiration (Bhuija & Cornfield, 1972). The results of preliminary studies performed in a spruce forest ecosystem, situated close to a metal-emitting industry in central Sweden, suggested that the general litter decomposition rate was limited by increased concentration of heavy metal ions in those periods of the year when water or temperature were not limiting factors (Rfihling & Tyler, 1972). Within 2 km of a Pennsylvania zinc smelter dilution plate counts have shown that total numbers of actinomycetes, bacteria and fungi in an upper soil horizon were much lower than in similar soils 40 km from the smelter (Buchauer, 1973a). The increasing acidity of precipitation may also be altering the rates of nutrient flow. Water in the atmosphere in equilibrium with average CO2 pressures will form sufficient carbonic acid to produce a pH of 5-7. Increasing quantities of much stronger acids (most importantly sulphuric acid) in rain and snow has produced pH values between 3 and 5 in northern Europe (Od6n, 1968; Od6n & Ahl, 1970; Engstr6m, 1971) and in the northeastern areas of the United States (Johnson et al., 1972; Likens et al., 1972). Acid rain may alter leaching rates of nutrients from plant parts or ch/~nge leaching rates of soil nutrients. There is little evidence to support or reject either of these hypotheses. Overrein (1972) has demonstrated that the leaching of calcium in various forest soil types increases drastically when the acidity of the precipitation is increased. Leaching of inorganic and organic materials from trees by acid precipitation is "a very complex topic. Leaching can occur from the stems and branches--as well as from the foliage--and may proceed both during the growing and the dormant seasons (Tukey, 1971). In recent laboratory experiments with young sugar maple seedlings T. Wood & F. H. Bormann (pers. comm.) have found that simulated acid precipitation can cause significant increases in the loss of calcium, magnesium and potassium from foliage, but only at pH levels below those occurring at present in the northeastern United States. Alterations in tree leaching rates would not only influence the nutrient budget of the leached tree, but also the nutrient budgets of lesser vegetation, epiphytes, parasites and the soil biota. The authors of a recent paper have concluded that, in spite of the excess acid flux over New England, the rate of cationic denudation of upland forest watersheds remains relatively low (Johnson et al., 1972). Whether or not changes are occurring in leaching rates within forest ecosystems due to acid precipitation and whether or not these changes may be able to induce nutrient stress, remains to be clarified. Swedish investigators have concluded that acidified precipitation cannot be eliminated as a cause of reduced forest growth, especially on poor sites (Engstr6m, 1971 ; Jonsson & Sundberg, 1972). Wood & Bormann (pers. comm.) were able to reduce growth and induce acute injury symptoms in one to four-month-old yellow birch seedlings only after reducing the pH of artificial precipitation to below 3.0. A more positive case for reduced growth caused by air pollution can be made with regard to suppressed photosynthesis. In numerous agricultural plants the rate of

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net photosynthesis has been shown to be suppressed by ozone (Hill & Littlefield, 1969) and nitrogen oxides (Hill & Bennett, 1970). In several cases this suppression occurred at pollution dosages below those necessary to cause visible injury. With regard to trees, three-year-old ponderosa pine seedlings exhibited reduced rates of net photosynthesis when exposed to ozone in controlled environment chambers (Miller et al., 1969). The exposure of seedlings of four pine species, widely distributed in the southeastern United States, to ozone typically resulted in depressed photosynthesis and increased respiration (Barnes, 1972). Using our small chamber technique, we have demonstrated the ability of ozone to suppress the rate of net photosynthesis of five-year-old white pine saplings collected from suburban nurseries (Botkin et al., 1971, 1972). Our most recent field research has indicated that ozone has the capacity to reduce net photosynthetic rates of mature deciduous trees. Details of this work will be published. If photosynthetic suppression occurs under field conditions, and if this suppression is sustained, then growth suppression of the affected plants would be an inevitable response. Growth suppression of an impressive list of agricultural plants exposed to urban air pollution has been documented (Feder, 1970; Hill & Bennett, 1970; Heagle et al., 1972). Gradual reduction of growth of white oak in northern Illinois and Indiana in the 1940s, as indicated by analysis of ring-width development, may have been due to air pollution stress (Ashby & Fritts, 1972).
Reduced reproduction One of the most important, subtle impacts of air contaminants on plant development may be on reproductive processes. Reduced fruit yields of citrus trees occasioned by photochemical oxidants (Thompson & Taylor, 1969) and of strawberry plants occasioned by hydrogen fluoride (Pack, 1972) have been shown. Daily exposure of geranium and carnation cultivars to ozone over a growing season causes a retardation of floral initiation and a decrease in floral productivity (Feder & Campbell, 1968; Feder, 1970). Ozone-induced depressed frond multiplication and floral production have also been shown in duckweed (Feder & Sullivan, 1969). Reduced pollen germination has been described in tobacco and corn following ozone exposure (Feder, 1968; Mumford et al., 1972). None of this research has been specifically concerned with the influence of air pollution on the reproductive processes of forest trees. Mrkva (1969), however, has suggested that SO2 can decrease the cone and seed yield of Scots pine. It is not unreasonable to assume that other forest species may react similarly and that the reproductive potential of certain species may be altered. In a study of the vegetation impact of an iron-sintering plant in northern Ontario, new seedlings of white pine were not observed within 48 km upwind from the smelter, while those of white and black spruce and quaking aspen were not recorded within 24 km (Gordon & Gorham, 1963). Limestone dust accumulation on forest sites in southwestern Virginia has been sho~vn to decrease or entirely stop the reproduction of

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WILLIAM H. SMITH

certain tree species (Brandt & Rhoades, 1972). Buchauer (1973b) attributed the absence of reproductives of early and late successional tree species around a Pennsylvania smelter to the inhibition of seed germination and/or seedling growth by high soil zinc levels. The weight and number of seeds produced by certain understorey species of a Utah aspen community were reduced following ozone exposure (M. Treshow, pers. comm.). Reproduction can be altered by changes in pollinator populations. In the portion of the Flathead National Forest (Montana, USA) subject to fluoride pollution from an adjacent aluminium reduction plant, the following insect pollinators were shown to have elevated fluoride levels; bumblebee (two species), honey bee, sphinx moth, skipper butterfly and wood nymph butterfly (Carlson & Dewey, 1971). If the fluorides are shown to be capable of altering the pollinator complex, then changes in the reproductive potential of those plants dependent upon these insects for seed production would follow.

Morbidity The word morbidity, as employed in this paper, refers to those situations where the abnormal physiology or pathological state of the plant is indicated by obvious, external signs or symptoms. Air pollution is capable of producing morbid trees by predisposing them to entomological and microbial stress or direct disease induction. Considerable evidence has been accumulated indicating that atmospheric pollution injury predisposes conifers to bark beetle infestation (Bosener, 1969). Examination of forest stands in the San Bernardino Mountains of California has shown that trees exhibiting advanced symptoms of pollution injury were most frequently infested by the western pine beetle (Dendroctonus brevicomis) and the mountain pine beetle (D. ponderosae) (Stark et al., 1968). These two insects are undoubtedly the most destructive insect pests of pines in the western United States (Stark & Cobb, 1969). Apparently photochemical air contaminants reduce the exudation pressure, quantity, and rate of oleoresin flow; increase the propensity of oleoresin to crystallise; and reduce phleom and sapwood moisture content: all of which enhance successful establishment of bark beetles (Cobb et al., 1968). Studies of lodgepole and ponderosa pines in the Flathead National Forest adjacent to an aluminum reduction plant ihdicated that elevated fluoride levels in pine needles leads to a build-up of the pine needle, scale (Phenocaspis pinifoliae) (Carlson & Dewey, 1971). In this same area lodgepole pine may also be predisposed by fluoride injury to attacks by a pitch mass borer, a needle miner, a needle sheath miner and sugar pine tortrix (C. E. Carlson, pers. comm.). Trees under air'pollution stress may also be predisposed to infection by certain microbial pathogens (Parmeter & Cobb, 1972). Since many microbes gain ingress to healthy plants via stomatal pores, the increased stomatal aperture induced by SO2 and particulate exposure (William et al., 1971; Unsworth et aL, 1972) may facilitate infection. On dry or exposed sites, increased stomatal opening may

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also aggravate moisture stress. Sassafras and wild grape plants continuously exposed to emissions of limestone dust in southwestern Virginia were more susceptible to infection by Guignardia bidwellii and Gloeosporium sp., the causal agents of leaf spot disease (Manning, 1971). It has been suggested (Sinclair, 1969) that trees may be rendered more susceptible to infection by the important rootrotting fungus, Armillaria mellea, by air pollution exposure. No specific evidence is available to support this hypothesis, although it is well known that this fungus most efficiently invades trees under stress. The air pollution/plant pathogen interaction is confused by the facts that air pollution can be directly toxic to microbes themselves (Koeck, 1935 ; Heagle, 1970; Lighth art e t al., 197 l) and specific microbial response to individual air pollutants is highly variable (Hibben & Stotzky, 1969; Saunders, 1971). Heagle (1973) has intensively examined the influence of air pollutants on insects and microbes causing plant stress. His review suggests that while there are several cases where air pollution has initiated or worsened an insect or plant pathogen interaction, there are also many examples where air pollutants have adversely affected insects and oathogens and ameliorated the severity of the plant response. Babich & Stotzky 0972)have also recently documented variable air pollution influences on host-parasite interrelations. Considerably more research is needed before general conclusions are drawn in this important area. At sufficient dosage numerous air pollutants have been shown to be capable of directly causing disease in many tree species. This topic has been very adequately reviewed (for example, Daines et aL, 1967; Hansbrough, 1967; Hepting, 1968, 1971 ; Heggestad, 1968; Brandt & Heck, 1968). Dosages and resultant syndromes are well appreciated (Lacasse & Moroz, 1969; Jacobson & Hill, 1970). Our greatest understanding concerns the ability of SO2, fluoride, and photochemical products (most importantly O3) to cause disease in coniferous species. We know considerably less about the influence on tree health of particulates (including heavy metals) NOx, PAN, NH3, Cl2, hydrocarbons and hydrogen chloride-cyanide-sulphide, among others. Since most research has concentrated on conifers, our knowledge of air pollution-induced disease in angiosperms is relatively deficient. Nevertheless, several generalisations concerning morbidity due to air pollution can be made. Two or more pollutants may concurrently interact with a plant and cause an additive (Matsushima & Brewer, 1972), antagonistic (Mansfield & Majernik, 1970; Majernik & Mansfield, 1972), or synergistic (Tingey et aL, 1971) response. The latter may be particularly significant and synergism has been documented when trees have been exposed to SO2 and oxidants (Dochinger et al., 1970; Banfield, 1972; Kress, 1972; Costonis, 1973). The gaseous pollutants enter the leaves through the stomates and, initially at least, cause symptoms and abnormal physiology in foliar tissue. Because of their high surface-to-volume ratio, leaves are also the site of primary interception (impaction) of particulate pollutants. The symptoms produced by air contaminants, while very well described (for example, Richards

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et al., 1968; Treshow, 1970), are not unlike symptoms produced by numerous other stress factors and field diagnosis is best accomplished by a plant pathologist familiar with both the tree species and the locality. In the case of gaseous contaminants, induced disease tends to be aggravated by any factor causing the stomates to open wider or remain open longer. Good general health and favourable site conditions such as abundant nutrients and soil moisture, therefore function to predispose susceptible trees to greater damage. Ecosystem impact Under Class II conditions the reaction of the forest ecosystem to air pollution stress is variable, depending on the individual responses of component trees. If the dominant response of one or more vegetative components is reduced growth caused by nutrient stress (reduced availability), reduced photosynthetic rate or increased respiration (or an interaction of all three), then the ecosystem will be characterised by reduced productivity and, ultimately, lessened biomass. Sustained alteration of reproductive potential or competitive advantage on the part of a~y species will ultimately lead to changes in species composition and community structure. Contamination of a Virginia hardwood forest with limestone dust has significantly reduced the lateral (wood) growth of red oak, red maple and chestnut oak and increased the growth of yellow-poplar over uncontaminated controls (Brandt & Rhoades, 1973). The writers speculated that the enhanced growth of yellow-poplar, which is apparently more tolerant of dust exposure than its associated species, was due to an attenuation of the coml~etitive pressure from the trees with limited tolerance. Air pollution predisposition to insect attack or microbial infection may lead to local or regional insect outbreaks or disease epidemics. Foliar tissue disruption directly caused by air pollution exposure would also reduce productivity and generally decrease stand vigour. Growth (diameter increment) of conifers, with foliar symptoms induced by SO2 from smelters at Trail, British Columbia, was markedly reduced for many kilometres downwind (Lathe & McCallum, 1939). Recent modelling of growth of the northern hardwood forest has suggested that stress may favour short-lived, shade-intolerant species and slow down the process of succession (Botkin, in press). Because Class H relationships are so varied, because they may interact synergistically on the forest, because they may occur at pollution dosages approximating ambient levels at present occurring in several forest areas, and because of their clandestine character, they must be considered to have extraordinary potential importance.

CLASS III RELATIONSHIP: HIGH POLLUTION LOAD---ECOSYSTEM IS SIMPLIFIED

When an air pollution dosage is sufficiently high to cause extensive damage (that is a high proportion of the foliage is symptomatic), acute morbidity results and

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mortality may follow. Acute morbidity and mortality of vegetation in forest ecosystems have been and are prevalent in specific regions generally adjacent to industrial, power-generating or urban concentrations. At the turn of the century, smelters at Cop.per Hill, Tennessee, destroyed 2833 ha of deciduous forest and replaced an additional 4047 ha with grass species (Hedgcock, 1914). An aluminumreduction plant near Spokane, Washington, has caused acute morbidity and mortality of ponderosa pine over a 130 km 2 area (Adams et al., 1952). Mortality of 81 ha of Douglas fir has been documented adjacent to a phosphate reduction plant in Georgetown Canyon, Idaho (Treshow et al., 1967). At Wawa, in northern Ontario, air pollution from an iron-sintering plant has caused extensive damage to vegetation northeast from the source due to strongly prevailing southwest winds. Arboreal damage was 'very severe' up to approximately 8 km from the source (Gordon & Gorham, 1963). In another area of Ontario--the Sudbury smelter district--three large smelters are causing severe tree injury from SO 2 emissions over a 1865 km 2 area (Linzon, 1971). Within this area the annual loss of white pine alone has been valued at $117,000. Oxidants, primarily 03, are seriously damaging trees in the Angeles, San Bernardino and Cleveland National Forests in southern California (Miller & Millecan, 1971). In the San Bernardino National Forest alone oxidants from urban concentrations are at present influencing 1.3 million trees on an area covering more than 40,469 ha (Wert, 1969; Wert et al., 1970). Acute morbidity and mortality of ponderosa pine due to direct air pollution and bark beetle impact has been high for at least twelve years and many of the more susceptible trees were killed prior to 1966 (Cobb & Stark, 1970). A comprehensive list of examples (e.g. Miller, 1972) of Class III relationships for the temperate forests of the world would be of a very impressive length! When the air pollution influence on component vegetation is severe, as in the case of Class III relationships, the ecosystem impact is also acute and dramatic. Woodwell (1970) has very succinctly reviewed the impact of acute pollution stress on the structure and function of ecosystems. With regard to structure, pollution induces simplification. Irrespective of the specific pollutant, forest communities react, first, by losing sensitive species; secondly, by losing the tree canopy, and thirdly, by maintaining cover in resistant shrubs and herbs widely recognised as seral or successional species. The acute impact of air contaminants on forests is consistent with this generalisation. In the Cooper Basin area of Tennessee the forest was eliminated, and in certain areas replaced, with a grassland ecosystem. In Wawa, Ontario, the forest was damaged layer by layer as proximity to the ironsintering plant was increased. Furthest from the plant the tree layer was destroyed, then, as one approached the smelter, the shrub layer and, finally, the herb layer, were killed. In the San Bernardino National Forest, if air pollution from the Los Angeles basin continues unabated, ponderosa pine may all but be eliminated as a species and well stocked stands will be converted to poorly stocked stands vegetated

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by more resistant species such as sugar pine, incense cedar and white fir. On exposed ridge crests, conditions will probably favour natural regeneration of shrub species rather than of other conifers (Miller, in press). Alteration of species composition of the above-ground ecosystem will be accompanied by alteration in the flora and fauna of the below-ground ecosystem. Bassus (1968) has recorded changes in species composition of the nematode population in German pine forests stressed by industrial air pollution. In addition to the simplification of forest ecosystem structure, loss of important ecosystem function occurs under conditions of Class II[ influence. The critical role of the forest in nutrient cycling, soil stabilisation and climatic and hydrologic regulation may be altered. Biomass reduction results in a corresponding reduction in the total inventory of nutrient elements held within the system and loss of the dominant vegetation destroys cycling pathways and mechanisms of nutrient conservation. Research at the Hubbard Brook Experimental Forest in New Hampshire has clearly demonstrated that retention of nutrients within a forest ecosystem is dependent on constant and efficient cycling between the various components of the intrasystem cycle and that deforestation impairs this retention (Likens & Bormann, 1971). Extensive nutrient loss could result in depauperisation of a site and have long-term consequences with regard to future plant-growth potential. Increase in soil instability and erosion would follow extensive mortality of the dominant vegetation, particularly in regions with steep or unstable slopes. Increased erodibility was found to follow deforestation at Hubbard Brook (Bormann et al., 1969). This mature forest ecosystem, when undisturbed, was little affected by erosion, with an average annual particulate matter export of only 2.5 metric tons km- 2 y - 1. Deforestation and repression of growth for three years increased export to a maximum of 38 metric tons km- 2 y - 1 (Bormann et al., in press). Soil erosion has been extensive at both Copper Hill, Tennessee (Hepting, 1971) and at Wawa, Ontario (Gordon & Gorham, 1963). Since forests have a regulating influence on local microclimate (Geiger, 1965), drastic alterations of forest structure may influence local meteorology. In the denuded zone at Copper Hill, relative to the contiguous intact forest, the summer air temperature averages 1-2C higher, while the winter air temperature averages 0.3-1C lower; the soil temperature is 1 iC higher in the summer; the wind velocities are five to fifteen times higher and rainfall is consistently lower (Hepting, 1971). In those areas subject to fire stress, for example southern California, an increase in the abundance of dead trees and increased shrub cover would act to increase the fire hazard. Fire incidence has become more frequent in a coastal western hemlock forest severely stressed by SO2 from a copper smelter in Anyox, British Columbia (Errington & Thirgood, 1971). In general, since diversity is directly correlated with stability (Odum, 1971) ecosystem simplification occasioned by air pollution stress would tend to increase the instability of the ecosystem and render it more vulnerable to damage from other stresses.

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CONCLUSIONS

Air pollution has had, is having, and will continue to have an influence on forest ecosystems throughout the temperate regions of the world. Under conditions of low dosage, the vegetation and soils of these ecosystems presumably function as a very important sink for air contaminants. With intermediate and high dosages of air pollutants and in the absence of sufficient time to accomplish evolutionary adjustments, certain tree species--and the ecosystem of which they are a part-are adversely influenced. The response of individual trees may range from reduced growth and reproduction through morbidity and death. The reaction of the ecosystem may range from reduced productivity with shifts in species composition to simplification with altered function and stability. Specific and quantified estimates of the extent of the various relationships betweerl air pollutants and forests are not possible, for several reasons. Some of the most important of these reasons are: 1. The inherent response of individual trees within a single species and the response of various species to individual pollutants is highly variable (Rohmeder & von Schonborn, 1965; Gerhold & Palpant, 1968; Heggestad & Heck, 1971 ; and H. D. Gerhold, pers. comm.). 2. The response of plants to air contaminants is largely regulated by environmental conditions (Rohmeder & v o n Schonborn, 1965; Heck & Dunning, 1967; Heck, 1968; Heggestad & Heck, 1971). Plant reaction in the field would be strongly influenced by local edaphic, topographical and meteorological conditions. 3. Most of our information concerning tree response to air pollution stems from research with conifers, mostly pines. Deciduous trees have received less interest and shrub and herb components of forest communities have received almost no attention. (Lichens and mosses have received considerable attention (e.g. Gilbert, 1968; Skye, 1968; LeBlanc, 1969; Saunders, 1970) and are obviously reliable indicators of certain pollutants. Their role in ecosystem structure and function, however, is not clear at the present time.) Pioneering research to establish 03 injury threshold values for plants indigenous to grassland, oak, aspen and conifer ecosystems in Utah has been initiated (M. Treshow, pers. comm.). 4. Most of our data regarding tree response to air pollution have resulted from investigations with two gases--SO2 and O3--generally applied to the plant singly. Limited information is available concerning plant reaction to numerous other air contaminants. This is especially critical as there is increasing evidence for interactive response involving additive, synergistic or antagonistic reaction when plants are exposed to more than one pollutant concurrently (Heggestad, 1972).

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WILLIAM H. SMITH 5. M u c h o f the research reported concerns experiments where plants have been exposed to air pollution dosages exceeding those characteristic o f most natural environments, either in a m o u n t o f pollutant employed or in duration o f exposure. 6. Most research data regarding air pollution and trees have resulted from studies of small trees under highly controlled and artificial conditions. Little has been documented concerning the reaction of large trees in their natural habitat.

TABLE 3
INFLUENCE OF AIR POLLUTION ON TEMPERATE FOREST ECOSYSTEMS

Designation

Air pollution load

Response of vegetation

Impact on ecosystem

Class I

Low

Class II

Intermediate

Class IIl

High

1. Pollutants shifted from atmospheric to organic or available nutrient compartment 2. Undetectable influence, 2. No or minimal physiological fertilising effect alteration I. Reduced productivity, 1. Reduced growth lessened biomass (a) detruded nutrient availability (i) depressed litter decomposition (ii) acid rain leaching (b) suppressed photosynthesis, enhanced respiration 2. Reduced reproduction 2. Altered species composition (a) pollinator interference (b) abnormal pollen, flower, seed, or seeding development 3. Increased morbidity 3. Increased insect outbreaks, (a) predisposition to entomologi- microbial epidemics cal or microbial stress Reduced vigour (b) direct disease induction 1. Acute morbidity 1. Simplification; increased erodibility, nutrient attrition, altered microclimate and hydrology 2. Mortality 2. Reduced stability

1. Act as a sink for contaminants

To summarise our awareness of the influence of air pollution on forest ecosystems (Table 3) we see that Class I relationships (sink function) are based on calculation, not on direct measurement, that Class II relationships (subtle, deleterious effects) are based primarily on extrapolation from controlled laboratory and greenhouse experiments, frequently with non-forest plant species, and, finally, that only Class I I I relationships (acute damage, destruction) h~ive been documented directly in the field. Research priority must, therefore, obviously be given to studies involving Class I and I I relationships. The potential magnitude of significance of the sink function and the subtle ecosystem impact is infinitely greater than acute damage. Inventory

AIR POLLUTION EFFECTSON TEMPERATEFOREST ECOSYSTEMS

125

of stress c o n d i t i o n s in A m e r i c a n forests is b e g i n n i n g to include air pollution (US Forest Service, 1971). This inclusion, however, only covers extreme Class II a n d Class I I I relationships. N o q u a n t i t a t i v e field e s t i m a t i o n of the bulk of Class II relationships is possible at present. This precludes the use of models to estimate regional or n a t i o n a l significance of subtle air pollution impact a n d inhibits a suggestion o f relative i m p o r t a n c e of the various relationships. Research to determ i n e the relationships between air p o l l u t i o n a n d forest ecosystems m u s t be given high priority because of the size a n d significance of these ecosystems in temperate regions a n d the n u m e r o u s p o t e n t i a l l y - d a m a g i n g interactions that have been identified.

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