Environmental Pollution 68 (1990) 453478
The Hohenheim Long-term Experiment: A North American Perspective Sagar V. K r u p a Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, USA
ABSTRACT
The Hohenheim experiment represents afire year multi-disciplinary study of tree sapling responses to 0 3, SO 2 and simulated acidic rain singly or in combination in modified open-top chambers. There are no comparable studies in North America which have been brought to completion at the present time. However, many of the results obtained in the Hohenheim study can be examined in the context of North American research. Independent of the differences in the methodology, the experimental conditions and the tree species used, many results are quite comparable between the Hohenheim study and the findings o f North American research. However, since comparisons were made with studies in chambers of various types, caution must be used in extrapolating the results in addressing questions in the chamberless ambient conditions.
INTRODUCTION The impacts of air pollutants on tree species and forest ecosystems are of much concern in North America (Linzon & Chevone, 1988; Manning, 1989; de Bauer & Krupa, 1990). In North America there are numerous studies in progress at the present time, and the reader is referred to Davis et al. (1983), Tingey (1984), Kozlowski & Constantinidou (1986a, b), US EPA (1986), Mayo (1987), US NAPAP (1987), Pye (1988), Proc. US/FRG Research Symposium (1988), Olson & Lefohn (1989) and Krupa & Kickert (1989) for details. In the following sections an attempt is made to discuss the North American research (as shown by the coverage of the literature) in the context of the Hohenheim long-term experiment. No attempt is made to review the 453 Environ. Pollut. 0269-7491/90/$03.50 © 1990 Elsevier Science Publishers Ltd, England. Printed in Great Britain
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European literature, since this subject has been addressed by other authors in this volume.
A BRIEF HISTORICAL PERSPECTIVE During the first half of the past 50 years much of the air pollution-vegetation effects research both in the Federal Republic of Germany (FRG) and in North America had been directed to point sources and primary pollutants (van Haut & Stratmann, 1970; US National Academy of Sciences, 1971; Guderian, 1977; US National Research Council, 1978). With the demonstration of the phytotoxic properties of ozone (03) by Richards et al. (1958) and Heggestad & Middleton (1959) and the recognition of the regional scale nature of 03 in the US (US National Academy of Sciences, 1977), significant research effort was shifted to the study of the effects of O3 on crops and trees in North America. Primary pollutants such as sulphur dioxide (SO2) and hydrogen fluoride (HF) became problems of specific local concern. The US EPA (Environmental Protection Agency) established one of the most comprehensive research programs to study the effects of 03 and other photochemical oxidants on forest ecosystems in the San Bernardino Mountains of southern California (Miller & Elderman, 1977). During this period open-top chambers were developed to study the effects of air pollutants on crop productivity (Heagle et al., 1973; Mandl et al., 1973). Using this approach, reports of air pollutant (primarily O3)-induced crop losses began to appear from various parts of the US (US National Academy of Sciences, 1977). In response to these reports, and the need to obtain data for establishing a secondary ambient 03 standard, the US EPA established the National Crop Loss Assessment Network (NCLAN) (Heck et al., 1982, 1984). In the middle to late 1970s scientific, public and political concern began to increase rapidly regarding the occurrence of 'acidic precipitation' (Bolin et al., 1971; Likens & Bormann, 1974). A total of some 106 scientific, public and political meetings, conferences and symposia were held during 1980 in North America to discuss the adverse effects of acidic precipitation on the environment (Krupa, unpublished). By this time the US EPA San Bernardino project was terminated before achieving its full scientific potential. Scientists in the US and in Canada were examining the effects of simulated acidic rain (SAR) on crops (Irving, 1983) and tree species (Jacobson, 1984). In these studies investigators were finding it difficult to demonstrate consistent results between experiments, between plant species and even between cultivars or provenances of a given species.
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During this period, observations of widespread tree decline (Waldsterben) became a major concern in the F R G (Schutt & Cowling, 1985). By this time scientists in the F R G had become fully aware of O a as a major atmospheric problem in that geographic region (Guderian, 1985). Air pollution was implicated as a major cause of tree decline. Acidic precipitation, 0 3, SO 2, oxides of nitrogen (NOx), peroxyacetyl nitrate (PAN), unknown organic compounds and heavy metals were all suspected (Cowling, 1986). As concern for tree decline reached major proportions in the FRG0 reports of tree decline in various parts of North America began to appear (Linzo n & Chevone, 1988). Scientists and others from North America began to travel to the F R G to observe 'Waldsterben' and to exchange information with the local counterparts. The US Department of Agriculture/Forest Service established a major thrust of forest response research under the US NAPAP (National Acid Precipitation Assessment Program). Six different forest response research cooperatives were established (Proc. US/FRG Research Symp., 1988). Bilateral agreements of information exchange and cooperative research were developed between the agencies within US NAPAP and the corresponding agencies in the FRG. Similar plans were established between the governments of Canada and the FRG. As studies continued to provide less than dramatic direct, short-term effects with SAR, research was directed toward the joint effects of O 3 and SAR on tree species (Lefohn & Krupa, 1988). In this context, many scientists in the US at the present time consider SO2 itself to be only a local vegetation effects problem in the vicinity of certain point sources. Nevertheless, Hogsett et al. (1989) have examined the sensitivity of western conifers to SO 2 and seasonal interaction of acidic fog and O a. Similarly scientists at the Pennsylvania State University for example, are examining the joint effects of O 3 and sulphate in precipitation on tree species (refer to Peterson et al., 1989). In contract to these studies, the Hohenheim experiment (initiated in 1981) included O 3, SO 2 and SAR. Arndt (this volume) notes that NO x was not included in the Hohenheim experiment. In North America the studies of Kress et al. (1982) may be the only one with O3, NO2 and/or SO2 and tree species. In this case, where N O 2 w a s included, SAR was not. Where SAR was i n c l u d e d , NO 2 was not. Ambient pollutant-plant response relationships are inherently stochastic in nature (Krupa & Teng, 1982). There is a significant spatial and temporal variability in pollutant occurrences and exposure profiles (Knapp et al., 1987; Legge & Krupa, 1990). Given these complexities, it is technically and financially unrealistic to expect the inclusion of every air pollutant in an open-top chamber study and to mimic the ambient pollutant exposure profiles in a given geographic area. At least some scientists in North America have raised concerns about the
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use of open-top chambers and the modified versions thereof and the consequent experimental designs (Howell et al., 1979; Olszyk et al., 1980; Krupa & Manning, 1988; Krupa & Nosal, 1989; Lefohn et al., 1989; Olszyk et al., 1989; Manning & Krupa, in press). Nevertheless, Manning & Krupa (in press) concluded that open-top chamber studies have value, as long as the limitations of the method are clearly understood and the results obtained from such studies are not inappropriately extrapolated to other situations. For that matter this is true for all methods. Modified open-top chambers were used in the Hohenheim experiment (Arndt et al., 1987). Arndt (this volume) and J~.ger et al. (1988) have discussed the advantages and limitations of the approach. The objective of the Hohenheim experiment was to evaluate the role of chemical climatology or key air pollutants as a major independent variable in causing adverse tree responses (Arndt, this volume). According to the Hohenheim investigators effort was made to maintain the air pollutant exposures to be somewhat analogous to the ambient in the study region. To my knowledge, the Hohenheim experiment represents the longest study of its kind that has been completed so far. Its strength lies in the fact that it is truly a multidisciplinary biological simulation-explanatory study. Many of the results would be highly valuable in developing further insights into cause-effects relationships under ambient conditions, if applied in the proper context. An interesting aspect of a comparison between the FRG and North America relates to the prevalence of air pollutant-induced visible foliar injury on native vegetation in the respective geographic regions. Certainly primary pollutant (SO2, HF, etc.)-induced foliar injury may be observed on sensitive plant species under appropriate conditions in the vicinity of certain point sources in both geographic regions. However, O3-induced symptoms of foliar injury on native tree species under ambient conditions have been reported from North America, but not from the FRG. Yet, sensitive, introduced, plant species used as biological indicators of 03 (Manning & Feder, 1980) show symptoms o f O 3 injury in the F R G (Knabe et al., 1973; Krupa, pers. observ, and comm. with U. Arndt, Hohenheim and G. H. M. Krause, Essen, FRG). de Bauer & Krupa (1990) have discussed some of the possible reasons for this, in the context of the photochemical oxidant problems in the Valley of Mexico.
PHYSIOLOGICAL A N D BIOCHEMICAL STUDIES In North America, as in the FRG, air pollution-tree response studies have been conducted under controlled environment conditions, in open-top chambers and in forest stands. No effort is made in the following sections to
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describe or discuss studies on specific forest stands or the modeling studies of forest stand growth and productivity. For information on these aspects, the reader may wish to consult among others, Legge et al. (1981), Johnson et al. (1982), Linthurst (1984), McLaughlin (1985), US EPA (1986), Mayo (1987), Proc. U S / F R G Research Symp. (1988), Pye (1988), Aber et al. (1989), Olson & Lefohn (1989) and Kickert & Krupa (in press). Because of the decline of certain tree species in certain geographic locations of North America (Linzon & Chevone, 1988), many air pollutiontree response studies in the US and in Canada have concentrated on growth and biomass effects. In my opinion plant process-related studies have received somewhat lesser attention. Nevertheless, Table 1 provides a listing of some pertinent studies in North America which are relevant to a discussion of the results of the Hohenheim long-term experiment. One aspect of plant response research both in the US and the F R G concerns the analysis of foliar photosynthetic and related pigments. In the US a reduction in chlorophyll concentrations due to 0 3 exposures has been reported for Ponderosa pine (Miller et al., 1963), grape (Thompson et al., 1969), pinto bean (Knudsen et al., 1977) and soybean (Pratt, 1980; Kromroy, 1982). Pratt (1982) and Brennan et al. (1987) have examined the relationship between foliar chlorophyll content and yield of soybean. Irving et al (1979) found a reduction in the soybean leaf chlorophyll content due to an exposure to varying concentrations of SO 2. Pratt (1980) and Kromroy (1982) found a more than additive reduction in the chlorophyll content of several cultivars of soybean exposed to a mixture of 0 3 and SO 2 in comparison to single (0 3 or SO2) pollutant treatments. Hoshizaki et al. (1988) measured the concentrations of chlorophyll and carotenoid pigments and computed their ratios in healthy and stressed red spruce (Picea rubrens) in Vermont, US. In the stressed trees the total chlorophyll concentrations were lower, chlorophyll (b) levels decreased more than chlorophyll (a) and the chlorophyll (a + b) concentrations were lower than the carotenoids. Similarly Cumming et aL (1988) observed a reduction in the concentrations of the photosynthetic pigments in red spruce seedlings exposed to 03. In comparison to the preceding discussion, in the Hohenheim long-term experiment, Siefermann-Harms (this volume), with Norway spruce (Picea abies) observed no differences in the chlorophyll (a) content for all three needle age classes in the control chambers (simulated acid rain, SAR treatments only at pH 5-0 or 4.0) and the chamber receiving 0 3 and rain treatment at pH 4.0. Also, no differences were noted in one year-old needles in the chambers with SO 2 and SAR at pH 4.0 and SO 2 + 0 3 with SAR at pH 4.0. Reductions of approximately 10 and 35% were measured in two yearold needles from the chambers with SO2 and SAR at pH 4.0 and SO2 + 03
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TABLE 1 Some Examples of Studies in North America on the Effects of Air Pollutants on Tree Species, Pollutant Exposures of 03, NO2, SO2 and SAR Singly and in Various Combinations and Plant Processes Studieda Growth/biomass
Adams et al. (1988) Benoit et al. (1982) Chappelka & Chevone (1986) Chappelka et al. (1985) Chappelka et al. (1988a,b) Chevone et al. (1983) Duchelle et al. (1982) Hogsett et al. (1985) Jensen (1979, 1981, 1983) Jensen & Masters (1975) Kress et al. (1982) Mahoney et al. (1984) McClenahen (1979) Miller et al. (1969) Peterson et al. (1987) Phillips et al. (1977a,b) Pye (1988) Reich & Lassoie (1985) Reich et al. (1986) Scherzer & McClenahen (1989) Stone & Skelly (1974) Seiler et al. (1988) Temple (1988) Tseng et al. (1988) Wilhour & Neely (1977) Screening f o r sensitivity
Berry (1971) Davis & Wood (1972) Davis & Coppolino (1974, 1976) Davis & Wilhour (1976) Davis et al. (1982) Jensen (1973) Karnosky & Steiner (1981) Kress & Skelley (1982a,b) Miller et al. (1983) Reinert et al. (1988) Winner et al. (1987) Gas e x c h a n g e a n d p h o t o s y n t h e s i s
Botkin et al. (1972) Boyer et al. (1986) Carlson (1979) Chevone et al. (1989) Coyne & Bingham (1981, 1982)
Jensen & Noble (1984) Jensen & Roberts (1986) Kohut et aL (1988) McLaughlin et al. (1982) Reich (1983) Reich & Amundson (1985) Reich & Lassoie (1984) Reich et aL (1986) Seiler et al. (1988) Taylor et al. (1986) Wilkinson & Barnes (1973) Yang et al. (1983a,b) Metabolites (pigments, carbohydrates, etc.)
selected enzymes,
Alscher et al. (1987) Barnes (1972) Constantinidou & Kozlowski (1979) Cumming et al. (1988) Elliott et al. (1987) Harvey & Legge (1979) Khan & Malhotra (1982) Reich (1983) Tingey et al. (1976) Interactions with the environment
Alscher et aL (1989) Davis & Wood (1973) Harkov & Brennan (1980) Norby & Kozlowski (1981a,b) Reich et al. (1987) Reproduction (pollen germination)
Benoit et al. (1983) Bruck & Shafer (1984) Luck (1980) Interactions with p a t h o g e n s a n d pests
Alstad et al. (1982) Chappelka & Kraemer (1988) Coleman & Jones (1988a,b) Costonis & Sinclair (1969, 1972) Dahlsten & Rowney (1980) James et al. (1980a,b) Jeffords & Endress (1984)
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TABLE l--contd. Interactions with pathogens and pests--contd.
Interactions with mycorrhizae
Jones & Coleman (1988) Lackner & Alexander (1983) Stark et al. (1968) Weidensaul & Darling (1979)
Mahoney et al. (1985) Manning & Keane (1988) McCool et al. (1979) Reich et al. (1985) Shafer et al. (1985) Stroo & Alexander [19851 Stroo et al. (1988)
a Given the nature of the Hohenheim experiment, literature on forest stands and the models of cause-effect relationships has been omitted from the compilation presented in the table.
with SAR at pH 4.0. The three year-old needles from these chambers had 40% lower chlorophyll (a) content compared to the control. No treatment effects were seen on the molar ratios of chlorophyll (b), the carotenes, lutein, neoxanthin, and the sum of carotenoids involved in the xanthophyll cycle, violaxanthin + antheraxanthin + zeaxanthin, to chlorophyll (a). The xanthophyll cycle, assayed in one year-old needles under defined light conditions (520/~E M - 2 s- 1, white light) was active in all samples. Needles from the control chambers and the chambers with SO2 and with 0 3 behaved similarly and differed from the SO2 + 03 treated needles by a 50% higher zeaxanthin content under light. Demmig et al. (1987) as cited by SiefermannHarms hypothesized that zeaxanthin plays a role in protecting the photosynthetic apparatus from destruction under excess light. In the Hohenheim experiment, the results of Siefermann-Harms were independently confirmed by Bermadinger et al. (this volume). Bermadinger et al. in the discussion of their results state: 'Alterations of photosynthetically active pigments mean alterations of photosynthetic processes, as a consequence of which disturbances of the anabolic metabolism of the plant may occur. However, a decrease in pigment content is an unspecific response to the impact of various stresses and therefore, alterations in the pigments are not stress-specific (Pfeifhofer & Grill, 1987), perhaps with the exception of photooxidatively induced stronger decrease of E-carotin as compared to ~carotin. Therefore, pigment analyses are useful for diagnostic assays only, in combination with other physiological examinations, i.e. content of anti-oxidants or enzyme activities (Pfeifhofer & Grill, 1987)'. Cumming et al. (1988) in their studies on red spruce and 0 3 exposures found that, changes in photosynthesis (on a g dry wt basis) and electron transport were not reflective of the changes in the chlorophyll content. Photosynthesis interpreted on a chlorophyll basis indicated that the
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photosynthetic activity of the remaining pigment is enhanced by the 0 3 treatment. A detectable decrease in the carotenoid content in the needles exposed to 0 3 was observed in the plant samples obtained in the fall. According to Cumming et al. (1988) the red spruce seedlings exposed to 03 exhibited decreased levels of photosynthetic pigments, perhaps as a consequence of oxidative action on the thylakoid membranes. Cumming et al. suggest that in the case of red spruce, the oxidative effect is potentiated by specific conditions of photoperiod and temperature, as the effect was detected after the normal period of dormancy induction. According to the authors, 0 3 itself might have affected the winter hardening process, in addition to the photoperiod and the temperature. In the Hohenheim experiment, Schweizer & Arndt (this volume) observed significant reductions in the photosynthetic activity of spruce exposed to 03 and SAR and 03, SO2 and SAR. In this case, transpiration was influenced only minimally. From the results obtained in CO 2 saturation studies, Schweizer and Arndt concluded that pollutant(s) effect was on the chloroplast and not so much on the stomata. In comparison to spruce, in the Hohenheim experiment fir (Abies alba) appeared to be more tolerant to 03. However, exposure to SO 2 alone and SO 2 and 03 resulted in distinct reductions in photosynthesis and transpiration. In the US Coyne & Bingham (1981, 1982) observed in Ponderosa pine (Pinus ponderosa) exposed to 0 3 that the losses in the photosynthetic capacity were greater than the reductions in the stomatal conductance, suggesting greater effects on the mesophyll components of the CO2 diffusion pathway than on the stomata. The studies of Chevone et al. (1989) with eastern white pine (Pinus strobus) confirm these observations. Chappelka & Chevone (in press) provide a critical analysis of this subject. The reader is also referred to Peterson et al. (1989) regarding the ongoing research in the US on tree seedling response to sulfur, nitrogen and associated pollutants. As opposed to this discussion of ozone, in North America Eckert & Houston (1980), Kelly et al. (1984) and Legge et al. (1988) have examined the effects of SO2, SAR and SO2 + H2S respectively on the net photosynthesis of conifer or hardwood species. While Eckert and Houston and Legge et al. found a reduction in the net photosynthesis, with SAR Kelly et al., were unable to show neither a reduction nor an enhancement. Norby et al. (1985) found an inhibition of photosynthesis in soybean exposed to 0 3 and SO2, but not with SAR alone. There is no doubt that different tree species respond differently to different air pollutants and their mixtures, to differences in the pollutant exposure dynamics and other environmental factors. McLaughlin et al. (1982) could not find differences in the photosynthetic capacity of O3-sensitive,
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intermediate and tolerant Pinus strobus and yet observed growth reduction in the sensitive populations. Legge et al. (1988) in their studies with SO 2 and H2S observed reductions in both photosynthesis and growth of Pinus contorta x P. banksiana. In the Hohenheim experiment Billen et al. (this volume) observed varying growth reductions, depending on the exposure treatment and the tree species involved (spruce, fir or beech, Fagus sylvatica). Mayo (1987) and Pye (1988) have reviewed the North American literature on the effects of 03 and other air pollutants on the photosynthesis, growth and productivity of tree species. An aspect immediately associated with photosynthesis is the carbon metabolism and carbon allocation. Hampp et al. (this volume) have addressed this issue in some detail. These authors made several very interesting observations with spruce: (1) a switch from anabolic to catabolic carbon metabolism in plants exposed to 0 3 alone and 03 and SO 2. However, in the latter case, there was some degree of compensation; and (2) an increase in A T P - A D P ratios and the redox ratios in plants exposed to O 3 and SO2, possibly due to increased metabolic turnover. The results in the Hohenheim experiment were qualitatively comparable to the results obtained from the Black Forest (southwest FRG). Hampp et al. interpret their Hohenheim results as being indicative of repair mechanisms and senescence being operative simultaneously, but to different degrees in different treatments. Plant health, growth and productivity may be viewed as a product of: [stress] - [normal maintenance + repair costs] (Kickert & Krupa, in press). Obviously, if stress effect exceeds maintenance and repair costs, adverse effects will occur. As opposed to Hampp et al. (this volume), Harvey & Legge (1979) found a definitive reduction in the needle ATP content of pine (Pinus contorta × P. baksiana) exposed to varying concentrations of a combination of SO 2 and H2S over many years. McLaughlin et al. (1982) found higher rates of respiration in the needles of sensitive Pinus strobus exposed to 03. These authors also found less transport of carbon from the foliage to the boles and the roots. Tingey et al. (1976) reported an increase in the concentrations of soluble sugars, starch and phenolic compounds in the shoots and a decrease in their concentrations in the roots of Ponderosa pine exposed to 0 3. Tingey et al. attributed their results to the alterations in carbon translocation from the shoot to the root. Obviously all these results represent various degrees of response to various forms of stress. Nevertheless, consequences of the findings of Hampp et al. (this volume) are discussed further in the following section on 'ectomycorrhizae'. Bermadinger et al. (this volume) and Bender et al. (this volume) have examined various asPects of tree species enzyme activities in the Hohenheim experiment. For many years, scientists in North America studied various
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enzyme activities in stressed or pollutant-exposed versus non-exposed trees with the objective of identifying specific biochemical responses to specific air pollutant exposures and their application in field diagnosis (Malhotra & Khan, 1984). The critical limitation of many of these efforts is the fact that many of the studies were conducted in controlled or partially controlled conditions with mostly the optimization of the influence of a single pollutant. Conversely, these types of mechanistic studies could be very useful, as long as they are not inappropriately extrapolated to the real world conditions. It is well known in the field of plant pathology and plant physiology that under natural conditions, biochemical responses are mostly non-specific in the context of cause-effect relationships. Bermadinger et al. (this volume) recognize this. This is also consistent with the ideas of Bender et al. (pers. comm.). The studies of Bermadinger et al. (this volume) and Bender et al. (this volume) in the Hohenheim experiment should be considered as mutually complementary. Bermadinger et al. examined: (a) the content of water soluble thiols; (b) content of ascorbic acid; (c) glutathione reductase activity; and (d) pigment content. In comparison, Bender et al. examined: (a) the peroxidase activity; (b) glutamate dehydrogenase activity; (c) glutamine synthetase activity; (d) foliage buffering capacity; and (e) soluble protein and nitrogen content. Bermadinger et al. report an increase in the thiol content of spruce foliage in response to SO2 exposure. Similarly Bender et al. observed an increase in the sulfur content of such foliage and a reduced buffering capacity. In North America Legge et al. (1988) found that the ratio of inorganic to organic foliar sulfur can be used as a useful indicator of sulfur loadings of forest ecosystems. In the Hohenheim experiment, in comparison to the SO2 exposures, spruce exposed to both SO2 and 03 exhibited a reduction in the accumulation of foliar sulfur. Similar results were previously obtained by Pratt et al. (1983) in their studies on soybean. Air pollutant mixtures can produce additive, more than additive or less than additive effects. However, the nature of the effect depends on the biological parameter examined, in addition to the pollutant(s) exposure dynamics. In the case of Pratt et al. the accumulation of foliar S in soybean was less in the SO2 + 03 treatment compared to the exposures of SO 2 alone. Yet, the amount of visible foliar injury was more than additive with the pollutant mixture, in comparison to the single pollutants. Similarly, in the Hohenheim experiment, while foliar S content of spruce was less in the S O / + 03 treatment compared to SO 2 alone, another biological variable, for example, ascorbic acid content in spruce foliage was much higher in the SO2 + 03 treatment compared to either pollutant alone (Bermadinger et al., this volume).
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In the Hohenheim experiment, the observations of Bender et al. and Bermadinger et al. (both in this volume) on the stimulation of peroxidase activity and the increases in the concentrations of ascorbic acid and glutathione, are very similar to the observations by North American scientists (Khan & Malhotra, 1982; Alscher et al. 1987; Barnes, 1972). The significance of all these results in the context of free radical scavenging and cellular repair and maintenance processes have been fully discussed by Alscher & Amthor (1988). Detailed plant and soil nutrient analyses were performed in the Hohenheim experiment (Sch/~tzle et al., this volume). The resulting data were used in computing nutrient flux from input to output (atmospheric contentplant content-soil content, lysimeters) (Seufert, this volume). I am not aware of similar results from North America using tree saplings and modified open-top chambers. However, using ambient study plots, Legge et al. (1988) observed a positive relationship between the proximity of the study plot to a long-term S gas emission source and increased soil acidification and nutrient leaching. At these study sites Legge et al. also observed increased concentrations of foliar (Pinus contorta x P. banksiana) S, A1, Fe, and Mn. These results are similar to those of Sch~itzle et al. and Seufert (this volume). Truog (1946) has presented a graphic representation of the element availability in soil as a function of pH. Reuss (1980) and Tabatabai (1985) have reviewed the literature on the effects of acidic rain on soils. While elements such as Fe and Mn will be solubilized by increasing soil acidification, in as much as they are available to the plant, they are also subject to leaching. Thus, the overall interaction between atmospheric input, plant nutrition and soil changes should be viewed as a dynamic function that is highly variable in time and space. Nevertheless, there are a number of reports both from Europe and from North America on nutrient imbalances in stressed trees and in the soil due to atmospheric deposition (consult among others Johnson et al., 1988; Mayo, 1987; Proc. Int. Congr. Forest Decline Res., 1989; Reuss & Johnson, 1986; Schulze, 1989; and Shortle & Stienen, 1988). ECTOMYCORRHIZAE One interesting aspect of the Hohenheim experiment concerns the findings of Blaschke (this volume) regarding ectomycorrhizae and the root biology of spruce. Ectomycorrhizae represent beneficial associations between secondary or non-woody feeder roots of trees and soil fungi (Harley & Smith, 1983). Ectomycorrhizae are obligatory for the survival of conifers under natural conditions. The tree provides the required carbon nutrition for the mycorrhizal fungi. Thus, there is a unidirectional flow of carbon from
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the higher (tree) to the lower (fungus) partner in the symbiosis (Harley & Smith, 1983). In return, among other benefits, ectomycorrhizal fungi promote the mineral nutrient availability and uptake by the trees. Blaschke (this volume) observed a reduction in the number of ectomycorrhizal feeder roots and an increase in the number of necrotic feeder roots in spruce exposed to 0 3 and SO 2. This is an important finding. According to Cooley & Manning (1987) the adverse effects of air pollutants on carbon allocation from shoots to the roots may be much more important than the direct, visible foliar injury. Hampp et al. (this volume) observed a switch from anabolic to catabolic carbohydrate metabolism in spruce exposed to 03 and SO 2. This again, is an important finding. Thus, the carbon flow required to sustain ectomycorrhizae appears to have been adversely modified or inhibited. In contrast to this discussion, Jfittner (this volume) found reduced concentrations of monoterpenes in the soil in the immediate vicinity of spruce exposed to 0 3 and SO2. Ji.ittner also reports a decrease in the number of basidiomycete soil fungi. Many ectomycorrhizal fungi associated with conifers belong to this taxonomic group. In passing, Jiittner cites the work of Krupa & Fries (1971) on axenic ectomycorrhizal root systems and monoterpenes in Scots pine (Pinus L~vlvestris). In these studies Krupa and Fries observed an increase in the concentrations of several terpenes in the ectomycorrhizal compared to the non-mycorrhizal root systems. Krupa & Fries also compared this qualitatively and favorably to mycorrhizal scots pine seedlings from a nursery. Subsequently Krupa et al. (1973) obtained similar results with short leaf pine (Pinus echinata). In their initial study, Krupa & Fries (1971) proposed that volatile organic compounds such as terpenes regulate the hostparasite interaction leading to symbiosis (reciprocal parasitism rather than pathogenesis). Melin & Krupa (1971) and Krupa & Nylund (1972) showed that monoterpenes in the gas phase act as fungistatic (not fungitoxic) compounds. These studies also showed that ectomycorrhizal fungi are more sensitive to the fungistatic effects of monoterpenes compared to root pathogenic fungi. In the light of this discussion, one might re-examine the results of Jfittner (this volume). Jiittner found a reduction in soil monoterpene concentrations in the vicinity of spruce exposed to 0 3 and SO2. This means there should be a decrease in the terpene mediated fungistasis and an increase in the numbers of soil fungi. Yet Jfittner reports a decrease in the number of soil basidiomycetes. Thus, in this context, the role of terpenes (given their fungistatic properties) appears untenable. To the contrary, the observations o f H a m p p et al. (this volume) might provide the explanation for the results of both Blaschke and Jiittner. As previously stated Hampp et al. observed a
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shift from anabolic to catabolic carbon metabolism in spruce exposed t o 0 3 and SO2. Tingey et al. (1976) reported an increase in the concentrations of soluble sugars, starch and phenolic compounds in the shoots and a decrease in their concentrations in the roots of Ponderosa pine (Pinus ponderosa) seedlings exposed to 0 3. Tingey et al. attributed their results to metabolite retention in the shoot and alteration in the transport of such metabolites to the roots. Similar results were obtained by McLaughlin et al. (1982). Chappelka & Chevone (1986) and Hogsett et al. (1985) have reported depression of root growth in comparison to the shoot growth in some tree species exposed to 0 3 and SAR or to 0 3 alone. These overall processes could explain the reduction in ectomycorrhizae and an increase in root necrosis. A related process must be a reduction in nutrient availability and uptake (for example N). N fertilization has been shown to increase tree terpene content (Pridham, 1967). Conversely N deficiency due to the lack or suppression of efficient ectomycorrhizae should result in decreased terpene content. The critical question here is: what is the order in which all the events occur and which processes are the causes as opposed to consequences? At the present time it is not possible to provide a satisfactory answer. In the Hohenheim experiment, Buffer et al. (this volume) obtained quantitative data on tissue monoterpene concentrations in Norway spruce. Buffer et al. were mainly interested in examining the possible differences in the composition of monoterpenes in saplings exposed to different pollutant treatments with the intent of using such results as biological indicators of pollutant stress. For the most recent North American literature on biological markers of forest stress, the reader should consult NAS (1989). Buffer et al. in the Hohenheim experiment concluded that there were no significant differences in the monoterpene content between the treatments. These results are in contrast to Jiittner (1988) who compared in a separate study healthy and chlorotic Norway spruce. These contradictory findings may be due to differences in the conditions of the study and the differences in the time point of chemical analyses in the varying time series of pollutant exposure and plant response. Both in parts of the F R G and in North America mature conifers known to have been subjected to long-term air pollution or other forms of stress have been shown to be vulnerable to bark beetle attack (Schutt & Cowling, 1985; Miller et al., 1982). Plant pheromones (modified terpenes) are attractants of bark beetles. Thus, mature conifers may be responding differently from the saplings studied in the Hohenheim experiment relative to their terpenoid metabolism. As opposed to the previous discussion on ectomycorrhizae, in the US, Shafer et al. (1985) have reported negative effects of SAR on ectomycorrhizae oflobolly pine (Pinus taeda). This study is interesting because SAR
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at pH 2-4 stimulated ectomycorrhizae, while SAR at pH 3.2 and 4.0 inhibited mycorrhizal development. Reich et al. (1984) and Keane & Manning (1988) have reported negative effects with SAR and 0 3. In contrast, Mahoney et al. (1985) did not find any adverse effect ofO 3 and SO2, singly or in combination on mycorrhizal formation in loblolly pine (Pinus taeda) seedlings. These conflicting results are most likely due to the differences in host pollutant sensitivity and stress compensation efficiency and differences in the pollutant exposure dynamics and exposure conditions. McCool (1988) has provided a brief review of the knowledge base on the effects of air pollutants on mycorrhizal development. Independent of the fact whether it is a cause or a consequence, adverse effects on ectomycorrhizal development and function will adversely affect mature tree or sapling growth and development. In addition to this discussion on ectomycorrhizae, Manning & Keane (1988) have published a review on the effects of air pollutants on the interactions between plants, insects and pathogens. A SUMMATION The Hohenheim experiment represents the first long-term (5 years) study to examine the effects of multiple pollutants on tree sapling response under partially controlled conditions. It is unique in the sense that investigators from some seven different institutions studied various aspects of plant biology within the same experiment. In North America somewhat similar studies are still in progress. There is much to be learned from the Hohenheim experiment. An important concept is, atmospheric processes and vegetation and edaphic responses must be studied in a common time and space. However, advantages and limitations of any experimental approach used must be viewed in the proper perspective in the context of stochastic ambient environment. Scientists have not fully addressed this issue. There are many similarities in the results obtained in the Hohenheim experiment and in North American research. Future air pollution-tree response research must consider the information presented in this volume and other similar works on an integrated basis, if they wish to understand cause-effect relationships fully. However, caution should be used in extrapolating results from artificial experimental conditions to real world situations. A C K N O W L E D G E M ENTS I am highly grateful to Dr Arthur Chappelka (Auburn University, US) for freely sharing with me information that was in press during the preparation
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o f this manuscript and for his constructive comments on the contents of this manuscript. I wish to acknowledge the assistance o f Leslie Johnson in the preparation of this manuscript.
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