Evaluation of Possible Causes for the Decline of Japanese Cedar

The decline of Japanese cedar (Cryptomeria japonica) has been observed mainly in the groves of shrines, temples, and residences located in inland area...
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Environ. Sci. Technol. 1996, 30, 2376-2381

Evaluation of Possible Causes for the Decline of Japanese Cedar (Cryptomeria japonica) Based on Elemental Composition and δ13C of Needles MASAHIRO SAKATA* Komae Research Laboratory, Central Research Institute of Electric Power Industry (CRIEPI), 2-11-1 Iwato-kita, Komae-shi, Tokyo 201, Japan

The decline of Japanese cedar (Cryptomeria japonica) has been observed mainly in the groves of shrines, temples, and residences located in inland areas of the Kanto Plain, Japan, since the 1960s. I evaluated possible causes for the decline such as soil acidification and/or water stress based on the concentration of nutrient elements and Al and δ13C of needles. Needles from declining trees did not exhibit the concentration of these elements that would be expected if the trees were affected by soil acidification. On the other hand, higher levels of δ13C were observed in needles from sites with a high level of decline and especially in needles from the upper crown of declining trees. These results tend to support the hypothesis that the main cause of decline is due to water stress related to dry atmospheric conditions and possibly ambient ozone exposure. Also, the results suggests that the δ13C of needles from the upper crown is useful as a sensitive indicator of the degree of water stress experienced by trees.

Introduction The decline of Japanese cedar (Cryptomeria japonica) has been observed mainly in the groves of shrines, temples, and residences located in a wide swath stretching toward the northwest inland from Tokyo Bay in the Kanto Plain of Japan since the 1960s (1-3), as shown in Figure 1. The decline begins with needle loss in the upper crown, and dieback progresses slowly down the trunk. Trees on the grove edges, isolated trees, and trees projecting out of the grove canopy are most likely to decline (3). Healthy big trees with more than 90 cm of DBH (diameter at breast height) are fewer in declining areas (Figure 1). The causes for decline remain unclear, although several hypotheses have been proposed to account for the observed decline (1, 3, 4). Exposure experiments with simulated acid rain (pH 2.0, 3.0, and 4.0) have been carried out for 3-year-old seedlings of conifer trees such as Japanese cedar grown in pots (5). * E-mail address: [email protected]; fax: 81-3-3480-1942.

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FIGURE 1. Distribution of declining groves and location of study groves in the Kanto Plain. Decline index (DI) indicates the average value for trees ranked at each site on the basis of needle loss and degree of dieback as follows: healthy, 1; more than 30% needle loss, 2; more than 30% needle loss and severe damage to the crown, 3; crown dead, 4 (3).

According to the results, Japanese cedar did not show any visible symptoms and growth reduction when treated at pH 3.0 or 4.0 for 23 months. On the other hand, reddishbrown necrosis in needles was clearly observed at pH 2.0. The pH of rain monitored in the Kanto Plain is generally higher than 4.0. These results suggest that current levels of acid rain are not related to direct and significant effect on the decline of Japanese cedar. Around the roots of declining trees, the leaching of nutrient elements from soils by soil acidification with subsequent enrichment of toxic soluble Al has been observed (6, 7). Soil acidification has been proposed as a major mechanism leading to forest decline in Europe and North America (8). Japanese cedar has a very low degree of water stress tolerance because of large leaf conductance and total resistance to water flow relative to other tree species (4). Also, meteorological data indicate that the atmospheric water vapor saturation deficit is higher in declining areas (Figure 1) and has gradually increased since the 1950s (4). These results provided the basis for the hypothesis that the main cause of decline of Japanese cedar is due to water stress related to dry atmospheric conditions in recent years (4). In this study, I evaluated possible causes for the decline such as soil acidification and/or water stress based on concentration of nutrient elements and Al and δ13C of needles.

Experimental Section Sampling. Based on a previous survey of cedar groves in the Kanto Plain (3), I selected the Washinomiya and

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TABLE 1

Description of Sites and Trees Studied site

area (ha)

DIa

Washinomiya Shrine

2.7

2.6

Mizunuma Shrine Ooto Shrine

ca. 0.5 0.52

3.4 1.1

Mibashira Shrine

0.13

a

Decline index: See legend of Figure 1.

1.0 b

trees studied

sampling date

no.

DBHb (mean)

height (mean)

July 7, 1994 May 9, 1995 Oct 16, 1994 Sep 28, 1994 May 23, 1995 May 8, 1994

3 5 4 4 4 4

50-65 cm (58 cm) 58-93 cm (69 cm) 40-71 cm (56 cm) 46-71 cm (59 cm) 46-71 cm (60 cm) 29-46 cm (38 cm)

ca. 20-25 m (ca. 22 m) 25-30 m (28 m) ca. 18-20 m (ca. 20 m) ca 25-30 m (ca. 28 m) 26-33 m (29 m) ca. 14-15 m (ca. 15 m)

Diameter at breast height.

Mizunuma Shrines as declining sites and the Ooto and Mibashira Shrines as healthy sites. Figure 1 shows the location of the sites and also the decline level of their groves. Descriptions of the sites and trees studied are given in Table 1. Needle loss was observed in the upper crown of study trees from declining sites. Sampling of needles was carried out at the above four shrines during 1994. A few twigs were taken by hand from upper (15-20 m above the ground), middle (10-15 m), and lower parts (∼5 m) of the crown at the Washinomiya Shrine and only from the lower part (∼5 m) of the crown at the other shrines. In addition, the samples for determination of vertical distribution of δ13C were taken at Washinomiya and Ooto Shrines in May 1995. At the same time as sampling, the height of the sampled twigs above the ground was measured. The twig samples were washed carefully with distilled water in an ultrasonic cleaner and cut into current year and 1-year-old needles. Only 1-yearold needles were taken for Mibashira Shrine in 1994 and for Washinomiya and Ooto Shrines in 1995. These needles with little visible injury were dried at 60 °C for 24 h and then ground using a ball mill for analysis. Analytical Procedures. Analyses of K, Mg, and Ca were carried out on bulk sample (0.5 g) using ICP (Mg and Ca) and AAS (K) after dry ashing at 450 °C for 24 h followed by dissolution of ash into 6 M HCl. For Al and Fe, the contents in the 0.1 M HCl-soluble fraction of needles were determined by ICP after selective leaching treatment of 0.5 g of bulk sample with 20 mL of 0.1 M HCl solution at room temperature for 24 h. This procedure was used because a significant portion of these elements are present in the form of soil particles, which cannot be physically separated for analysis (10). The elemental contents were normalized to dry-sample weight. The δ13C of the needles was measured by the following method. A total of 4-5 mg of a ground sample was combusted together with 2 g of CuO as an oxidizing agent in a sealed quartz tube at 850 °C for 2 h. The resulting CO2 was purified and then analyzed by a Finigan MAT mass spectrometer delta S. The δ13C values were calculated with respect to the PDB standard. The standard deviation in the δ13C measurements was 0.2‰.

Results and Discussion Evaluation Based on Elemental Composition of Needles. First, I evaluated the contribution of soil acidification to the decline of Japanese cedar based on elemental composition of needles. Kohno et al. (9) investigated the effects of Al on the growth and nutrient uptake for 2-year-old seedlings in 1/5 Hoagland’s no. 2 nutrient culture solution containing 0.5-20 mM of Al for 4 months. The results

showed clear increases in Al concentration and Al/Fe ratio and decreases in Ca and Mg concentration in needles with increasing Al concentration in the solution. Also, I examined the relationship of elemental concentration between current year and 1-year-old needles from mature trees (10). K and Mg were enriched in current year needles relative to 1-year-old needles, which was opposite of the trend for Ca, Al, and Fe. Based on these results, I propose the following evaluation methods using the concentration of two elemental groups in current year and 1-year-old needles. (i) K and Mg: Both lower concentration in 1-year-old needles and higher concentration ratio of current year needles against 1-year-old needles are observed in cases strongly affected by soil acidification. This is due to the supply of the amount of elements required for growth of current year needles by retranslocation from 1-year-old needles to compensate for the low uptake from transpiration stream in such cases. (ii) Ca, Al, and Fe: Lower Ca concentration and higher 0.1 M HCl-soluble Al concentration and also Al/Fe ratio in both current year and 1-year-old needles are observed in cases strongly affected by soil acidification. The reasons are leaching of Ca from soils and enrichment of Al, but not Fe in soil solution results from soil acidification. Also, these elements are not retranslocated in quantity from old needles. The above evaluation methods were applied to needles taken from declining trees in Washinomiya and Mizunuma Shrines and from healthy trees in Ooto Shrine. Table 2 gives pH (H2O), base saturation, and exchangeable cation contents of soils (all Andosol) around the roots of trees in the study sites (unpublished data by Nashimoto et al.). There are significant differences (P < 0.01 ty t-test) in acidity, base saturation, and exchangeable cation contents of soils between the declining (n ) 8) and healthy sites (n ) 7). Figure 2 shows that the concentration of K and Mg in 1-year-old needles varies considerably, independent of site and needle position in the crown. And the ratio of concentration between current year and 1-year-old needles is almost constant (∼1) in the higher concentration range of 1-year-old needles and then increases linearly with a decrease in the concentration of 1-year-old needles by retranslocation. On the other hand, the concentration of Ca and 0.1 M HCl-soluble Al in needles also differs considerably, showing a correlation between the concentration in current year and 1-year-old needles (Figure 3). Thus, needles from declining sites and even from upper crowns with needle loss at the Washinomiya Shrine did not exhibit the concentration of nutrient elements and Al that would be expected if the trees were affected by soil acidification. Also, no significant differences in the concentration of these

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TABLE 2

pH (H2O), Base Saturation, and Exchangeable Cation Contents of Soils from Study Sitesa exchangeable cation (mequiv/100 g) site

pH (H2O)

BSb (%)

Al

Ca

Mg

K

Washinomiya Shrine Mizunuma Shrine Ooto Shrine Mibashira Shrine

3.9 (3.8-4.0) 4.2 (4.0-4.3) 4.9 (4.7-5.1) 4.9 (4.7-5.0)

5(1 20 ( 4 24 ( 9 33 ( 4

7.5 ( 1.1 4.8 ( 0.9 2.6 ( 0.9 2.5 ( 0.6

1.4 ( 0.5 2.2 ( 0.4 4.2 ( 2.9 10.3 ( 2.4

0.3 ( 0.1 0.4 ( 0.1 1.3 ( 0.6 3.2 ( 0.7

0.4 ( 0.1 0.3 ( 0.1 1.0 ( 0.3 0.5 ( 0.1

a Average value and standard deviation (range for pH) of three or four soils (all Andosol) around the roots of trees in each site (Nashimoto et al., unpublished data). The soils were taken from the layer 5-10 cm deep (A horizon), because surface soils may have been disturbed by human activity. b Base saturation.

FIGURE 2. Relationship between concentration of 1-year-old needles [(E)1] and concentration ratio of current year needles against 1-year-old needles [(E)0/(E)1] for K and Mg. Arrow indicates the direction of the relationship changing in cases strongly affected by soil acidification (same manner for Figures 3 and 4).

FIGURE 3. Relationship of Ca and 0.1 M HCl-soluble Al concentration between current year and 1-year-old needles. The symbols are the same as in Figure 2.

elements were observed between declining and healthy trees (P < 0.05 by t-test). In addition, the Al/Fe ratio of 0.1 M HCl-soluble fraction of needles without soil particles was almost constant and independent of the degree of decline of trees as illustrated in Figure 4. Soils around the roots of declining trees from Washinomiya and Mizunuma Shrines tended to have relatively high acidity and low nutrient cation contents compared to 18 other declining sites with black soils (Andosol) (6). These results suggest that soil acidification is not a major

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FIGURE 4. Relationship between 0.1 M HCl-soluble Al and Fe contents in needles (1-year-old). The symbols are the same as in Figure 2.

mechanism leading to the decline of Japanese cedar at other sites as well as at the Washinomiya and Mizunuma Shrines. It was reported that only a small hemisphere around the roots of trees was strongly affected by soil acidification at some declining sites (7). Also, the maximum concentration of aqueous Al was 0.74 mM (Al/Ca molar ratio: 0.37) in soil

FIGURE 5. δ13C of needles (1-year-old).

solution at those sites (7). These Al concentrations probably have not affected the growth and nutrient uptake of trees. This is inferred from growth experiments that showed the significant effects at higher than 2 mM (Al/Ca molar ratio: 2.5) (9). Analyses of needles (n ) 364) from healthy and declining sites in nine suburban areas of Japan also showed no evidence that nutrient concentration is reduced by soil acidification (11). Evaluation Based on δ13C of Needles. During photosynthetic CO2 assimilation, plants have a smaller δ13C than atmospheric CO2 as a result of the discrimination of 13CO2 in favor of 12CO2. Farquhar et al. (12) proposed a carbon isotope fractionation model for C3 plants that predicts that this discrimination will negtively correlate with water-use efficiency (WUE). This has been confirmed by measurements of δ13C of dry matter or leaves and WUE for many plants (e.g. refs 13 and 14). This also suggests that the δ13C of dry matter or leaves is useful as an indicator of the degree of water stress experienced by plants. One example is the work by Takahashi (15). He demonstrated that the δ13C of leaves from seedlings of tree species such as Zelkowa serrata and Cinnamomum camphora grown in pots show an increase of 2.1-3.8‰ when treated with drought conditions (pF of soils: 2.8) compared to well-watered conditions (pF of soils: 1.4). Also, he observed lower intercellular CO2 concentration in leaves of seedling treated to drought conditions due to stomatal closure caused by water stress. Thus, if the δ13C and concentration of atmospheric CO2 does not significantly differ among the study sites, higher δ13C of needles would be observed at sites with trees strongly affected by water stress. In order to evaluate the contribution of water stress to the decline of Japanese cedar, the δ13C of needles was measured. The results for needles taken during 1994 are shown in Figure 5. Comparison of δ13C in needles from the lower crown (∼5 m above the ground) among four shrines indicated that the average values decrease according to the

order of Mizunuma (-26.7‰) > Washinomiya (-27.0‰) > Ooto (-27.4‰) > Mibashira (-28.6‰), which is consistent with the order of DI for the groves of these shrines (Table 1). There was also a significant difference (P < 0.01 by t-test) of the average δ13C of needles between all declining (-26.8‰, n ) 7) and healthy trees (-28.0‰, n ) 8). The difference of the average δ13C of needles among the study sites cannot be explained by a decrease in δ13C of atmospheric CO2 due to the contamination of 13C-depleted CO2 from fossil fuel combustion. The concentration of NO2 and SO2 derived mainly from fossil fuel combustion at the study sites increases roughly in the order of Ooto < Mibashira ∼ Mizunuma < Washinomiya (Table 3). This should lead to a decrease in δ13C of needles converse to the above order, which is quite different from the actual order of δ13C. Air pollutants such as O3 and SO2 are also known to cause an increase in the δ13C of leaves probably by stomatal closure (16-18). Table 3 indicates the relatively low levels of air pollutants at the study sites, and there are no significant differences (P < 0.05 by t-test) in the SO2 and oxidant levels between declining and healthy sites. Stomatal closure was reported with higher exposure of these air pollutants in controlled studies for Japanese cedar seedlings (19). I believe that air pollution stress probably made a minor contribution to the increase in δ13C of needles from Japanese cedar. However, there is increasing evidence of ozone-induced water stress for other tree species at ambient levels (20-22), as described later. Both the air temperature and the supply of nutrients may also affect the δ13C of needles via effects on photosynthesis rates (23, 24). The declining sites of the Washinomiya and Mizunuma Shrines had a slightly higher average temperature (0.5-1 °C) than the healthy sites of the Ooto and Mibashira Shrines during the growing season (MaySeptember) for the 1990-1994 period (Figure 7). Kitagawa and Matsumoto (25) obtained a negative δ13C versus temperature coefficient (-0.29‰/°C) based on the measurement of δ13C records of annual growth rings of Japanese cedars from Yakushima Island, southern Japan. It would be expected that more negative δ13C values would be observed for needles from the declining sites than the healthy sites, which is opposite of the observed δ13C values. On the other hand, there were no significant differences (P < 0.05 by t-test) in the average concentration of K, Mg, Ca, P, and N of needles between declining (n ) 13) and healthy sites (n ) 8) in this study (10). Thus, the difference in δ13C of needles among the study sites cannot be explained by differences in the air temperature and/or the supply of nutrients. It was reported that Japanese cedars have a very low degree of water stress tolerance because of large leaf conductance and total resistance to water flow relative to

TABLE 3

Concentration of Air Pollutants (µL/L) at Study Sitesa site

SO2

NO2

oxidants

Washinomiya Shrine Mizunuma Shrine Ooto Shrine Mibashira Shrine

0.006 ( 0.002 0.004 ( 0.002 0.003 ( 0.001 0.005 ( 0.001

0.019 ( 0.001 0.017 ( 0.001 0.005 ( 0.001 0.014 ( 0.001

0.028 ( 0.006 0.037 ( 0.008 0.034 ( 0.004 0.022 ( 0.002

a Average concentration and standard deviation during the growing season (May-September) for the 1989-1993 period at the nearest pollution monitoring station (26) to each study site. Oxidant data are based on hourly concentrations during the daytime (5:00-20:00).

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FIGURE 6. Vertical distribution of δ13C of needles (1-year-old) in crown of declining (n ) 5) and healthy trees (n ) 4). Needles from a height of 26-30 m above the ground had been lost by declining trees at Washinomiya Shrine.

other tree species (4). Stomatal closure caused by the low water potential of needles in the daytime was indeed observed even for mature healthy tree (4). It is likely that the needles from sites with a high level of decline have relatively large increases in the δ13C of needles due to stomatal closure caused by water stress. In addition, Figure 5 shows higher levels of δ13C in needles from the upper crown (15-20 m above the ground) of declining trees in Washinomiya Shrine. The vertical distribution of δ13C of needles in the crown between declining and healthy trees is compared in Figure 6. The δ13C values of needles increase with the height of needle position in both the crown of declining and healthy trees. However, the rate of increase with height in declining trees is much larger than for healthy trees. This leads to the larger difference in δ13C of needles from the upper crown between declining and healthy trees. Thus, needles from the upper crown of declining trees are strongly affected by water stress relative to those from the lower crown, which induces needle loss and dieback in the upper crown. This is supported by the fact that larger amounts of water are transpired by needles from the upper crown due to higher atmospheric water vapor saturation deficit, wind speed, solar radiation, temperature, etc. Water stress for plants is induced by differences in the balance between supply and demand for water, which is frequently caused by the meteorological changes. Figure 7 illustrates average air temperature, precipitation, and atmospheric water vapor saturation deficit during the growing season (May-September) for the 1990-1994 period. Atmospheric water vapor saturation deficit is indicative of dry atmospheric conditions.

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FIGURE 7. Average air temperature (A), precipitation (B), and atmospheric water vapor saturation deficit (C) during the growing season (May-September) for the 1990-1994 period (27). Isoclines were roughly drawn based on the values at meteorological observatories.

cedar remains unknown; however, there is the possibility of ozone-induced water stress due to the similar levels of ozone exposure in the Kanto Plain. In summary, the results presented here tend to support the hypothesis that the main cause of decline of Japanese cedar in the Kanto Plain is due to water stress related to dry atmospheric conditions and possibly ambient ozone exposure. Also, the results suggest that the δ13C of needles from the upper crown is useful as a sensitive indicator of the degree of water stress experienced by trees.

Acknowledgments I thank M. Nashimoto (CRIEPI), K. Takahashi (Toyota Motor Co.), and Y. Matsuura (Forestry and Forest Products Research Institute) for helpful advice and information and R. K. Kawaratani (Nihon Tetra Pak K. K.) for critically reading the manuscript. Also, I would like to express my appreciation for the skillful performance of the carbon isotope analyses by K. Yamada of Tokyo Metropolitan University.

Literature Cited

FIGURE 8. Changes in annual average atmospheric water vapor saturation deficit during the growing season (May-September) since 1951 (27).

Air temperature and atmospheric water vapor saturation deficit are higher in the central areas of the Kanto Plain, which coincide with the areas where the decline of Japanese cedar has been observed (Figure 1). The average temperature increase was 0.8-1 °C at Tokyo, Kumagaya, and Maebashi located in those areas and -0.1-0.3 °C at Chichibu, Mito, and Choshi located in areas without notable decline for the 1951-1994 period. As shown in Figure 8, a higher increase in atmospheric water vapor saturation deficit was also observed at Tokyo, Kumagaya, and Maebashi relative to other observatories for the 1951-1994 period. These increases in air temperature and atmospheric water vapor saturation deficit are thought to be mainly due to thermal pollution and urban development in recent years. Figure 7 also shows that areas with precipitation less than 700 mm increased in the eastern Kanto Plain. A significant change in annual precipitation (decrease or increase) was not observed at all observatories during the 1951-1994 period (P < 0.05 by t-test). Thus, it is likely that water stress for Japanese cedar in the Kanto Plain is caused by dry atmospheric conditions. On the other hand, there is increasing evidence that ozone at ambient levels can increase water loss of spruce trees during the drought period (20, 21). In addition, McLaughlin and Downing (22) reported that ozone exposures at >0.04 µL/L interacted with low soil moisture and high air temperature to reduce short-term rates of stem expansion of mature loblolly pine trees. Annual growth was also inversely related to seasonal ozone exposure and soil moisture stress. Whether this is the case for Japanese

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Received for review November 16, 1995. Revised manuscript received March 1, 1996. Accepted March 6, 1996.X ES950865Q X

Abstract published in Advance ACS Abstracts, May 1, 1996.

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