Environ. Sci. Technol. 1988, 20, 1122-1125
Lytle, C. R.; Perdue, E. M. Environ. Sci. Technol. 1981, 15, 224-228.
Sowden, F. J.; Ivarson, K. C. Can. J. Soil Sci. 1966, 46, 109-120.
Hunter, J. V. In Organic Compounds in Aquatic Environments;Faust, S. D.; Hunter, J. V.; Eds.; Marcel Dekker: New York, 1965; pp 51-94. Langheld, K. Ber. Deutsch. Chem. Ges. 1909, 42, 392. Dakin, H. D. Biochem. J. 1916, 10, 319-323. Dakin, H. D. Biochem. J. 1917,11, 79-95. Goldschmidt, S.; Wiberg, E.; NageI, F.; Martin, K. Justus Liebigs Ann. Chem. 1927,456, 1-38. Friedman, A. H; Morgulis, S. J. Am. Chem. SOC.1936,58, 909-913.
Morris, J. C.; Ram, N.; Baum, B.; Wajon, D. “Formation and Significance of N-chloro Compounds in Water Supplies”;1980, EPA-600/2-80-031. Stanbro, W. D.; Smith,W. D. Enuiron. Sci. Technol. 1979, 13,446-451.
Burleson, J. L.; Peyton, G. R.; Glaze, W. H. Enuiron. Sci. Technol. 1980,14,1354-1359. Fox, S . W.; Bullock, M. W. J. Am. Chem. SOC.1951, 73, 2754-2755.
Isaac, R. A,; Morris, J. C. In Water Chlorination Enuironmental Impact and Health Effects;Jolley, R. L., Ed.; Ann Arbor Science: Ann Arbor, MI, 1980; Vol. 3, pp 183-191.
McKinny, J. D,; Maurer, R. R.; Haw, J. R.; Thomas, R. 0. In Identification and Analysis of Organic Pollutants in Water;Keith, L. H., Ed.; Ann Arbor Science: Ann Arbor, MI, 1976; pp 417-432. Keith, L. H.; Garrison, A. W.; Alien, F. R.; Carter, M. H.; Floyd, T. L.; Pope, J. D.; Thruston, A. D., Jr. In Identi-
fication and Analysis of Organic pollutants in Water; Keith, L. H., Ed.; Ann Arbor Science: Ann Arbor, MI, 1976; pp 329-373. (31) Simmon,V. F.; Kauhanen, K.; Tardiff, R. G. Dev. Toxicol. Environ. Sci. 1977, 2, 249-258. (32) Bull, R. J. In Water ChlorinationEnvironmental Impact and Health Effects;Jolley, R. L.; Brungs, W. A.; Cotruvo,
J. A.; Cumming, R. B.; Mattice, J. S.; Jacobs, V. A., Eds.; Ann Arbor $cience: Ann Arbor, MI, 1983; pp 1401-1415. (33) Bull, R. J.; Robinson, M. In Water Chlorination: Chemistry, Environmental Impact and Health Effects; Jolley, R. L.; Bull, R. J.; Davis, W. P.; Katz, S.; Roberts, M. H., Jr.; Jacobs, V. A., Eds.; Lewis Publishers: Chelsea, MI, 1985; V O ~5,. pp 221-228. (34) Mink, F. L.; Coleman, W. E.; Munch, J. W.; Kaylor, W. H.; Ringland, H. P. Bull. Environ. Contam. Toxicol. 1983,30, 394-399. (35) Palin, A. T. Water Water Eng. 1950, 53, 189-200. (36) Fed. Regist. Part VIII, Method 624, Friday Oct 26, 1984, Washington, DC, pp 141-152. (37) Standard Methods for the Examination of Water and Wastewater,16th ed.; American Public Health Association: Washington, DC, 1985. (38) Luknitskii, F. 1. Chem. Rev. 1975, 75, 259-289. (39) Morris, J. C. In Principles and Applications of Water Chemistry;Haust, S. D.; Hunter, J. W., Eds.; Wiley: New York, 1967; pp 23-53. (40) Stevens, A. J. Am. Water Works Assoc. 1976,68,615-620.
Received for review November 15, 1985. Revised manuscript received April 14,1986. Accepted May 12,1986. This work was supported by a grant from the U.S. Environmental Protection Agency under Contact 810973-01-0.
Regional Tree Growth Reductions due to Ambient Ozone: Evidence from Field Experiments Deane Wang” and F. Herbert Bormann Yale School of Forestry and Environmental Studies, New Haven, Connecticut 0651 1
David F. Karnosky School of Forestry, Michigan Technological Universlty, Houghton, Michigan 4993 1
rn Observations from extensive regions in Europe and North America suggest that many forests may be in early stages of ecosystem decline. We present experimental evidence from open-top chamber field studies indicating that ambient ozone at levels below the ambient air quality standard (235pg m-3) causes significant reductions (19%) in the growth of sapling poplars (hybrid Populus). While ozone-induced reductions in growth have been observed under laboratory and greenhouse conditions, demonstration of this effect under field conditions is critical to the establishment of ozone standards. Growth reductions for Populus deltoides and Robinia pseudoacacia were not significant (CY = 0.05). Reductions in productivity and height growth occurred without visible symptoms of foliar injury and at ozone concentrations below current standards. If this “invisible” injury is typical in other tree species, the extent of ozone-induced forest damage may presently be greatly underestimated. Additional field studies on a regional basis are needed. Introduction As attention on the causes of widespread forest decline *Address correspondence to this author at the Center for Urban Horticulture GF-15, University of Washington, Seattle, WA 98195. 1122 Environ. Scl. Technol., Vol. 20, No. 11, 1986
(1-5) shifts from SOz to NO, and its photochemical products such as ozone (6),it becomes increasingly important that scientific observations documenting ozone dose response be determined prior to undertaking major policy initiatives to deal with the problem. Field experiments have documented regional growth reductions in agricultural crops (IO),but forest tree responses to ambient ozone have not been adequately studied. Recent laboratory research (7) has provided one critical link connecting low, ambient levels of ozone and reduction of net photosynthesis in trees. Past work has shown important inconsistencies in pollutant dose response of plants under laboratory and greenhouse conditions as compared to response under field conditions (8, 9). Thus, field experiments are essential, providing realistic calibration points for dose-response functions which can be elucidated in more detail in the laboratory. Field research is limited by experimental artifacts including chamber effects and artificial plant assemblages. In addition, field trials have generally involved fumigations (10). These ozone additions have often been introduced abruptly, causing an initial rapid change in ozone concentrations. Also, fumigated chambers are subject to rapid wind-induced fluctuations in chamber concentrations (Figure 1). The effects of these conditions on dose re-
0013-936X/86/0920-1122$01.50/0
@ 1986 American Chemical Soclety
Table I. Results from Ambient-Open, Ambient-Chambered, a n d Filtered-Chambered Treatments on Saplings of Three Tree Species, September 1984” species/char
8
400-1
3j
I .
Windy
I
:2
0 0
.E
2%
1
0 0
5
10
15
20
25
30
1 3
Tim. (min)
Flgure 1. Short-term fluctuatlons in ozone concentration (pg m-3) in a fumigated open-top chamber in relatlon to wind speed (mph, measured at chamber helght 20 m from the chamber) on a calm and a windy day. Ozone flux into the chamber was constant. Thus, fluctuations represent dilution of added ozone by ingress of ambient air. Consecutive ozone readings are 30 s apart.
sponse have not been evaluated. The primary objective of our study was to measure growth responses of selected tree species to ozone pollution under realistic field conditions. Important considerations included environmental (soil, sunlight, climate, diurnal, and seasonal cycles) as well as ozone exposure conditions. Open-top chambers, field-grown saplings, and ambient vs. filtered air were important elements of the research design. Materials and Methods Field work was conducted at a rural location in Millbrook, NY (41’47’7’’ N, 70O44’18” W, elevation 126 m MSL). The nearest major urban center of Poughkeepsie, NY, is 20 km (12.4 miles) SW OI the site. We used open-top chambers (11)with charcoal-filtered (filtered-chambered) and nonfiltered (ambient-chambered) treatments to assess effects of ambient ozone on growth of a Populus hybrid (P. masimowiczii X trichocarpa, NE 388), Populus deltoides (eastern cottonwood), and Robinia pseudoacacia (black locust). These are commercially important species in world forestry (12,13)and are of ecological significance in many forest types. These field chambers have been well-studied (14-17l and are considered to proGide an effective method to kst responses of plants to gaseous air pollutants (10,18). Nonchambered open plots (ambient-open) were used to evaluate chamber effects on sapling g r w t h and development. Ten hybrid Populus, three P. deltoides, and three R. pseudoacacia saplings were planted in May 1984 in each experimental plot (3-m diameter). Hybrid Populus and P. deltoides were grown from single-clone cuttings established in pots during the previous winter. Robinia pseudoacacia plants were started from seed in tree tubes during the previous growing season. Plots were clustered into adjacent groups of three, each cluster with one nonfiltered chamber, one charcoal-filtered chamber, and one open plot (no chamber). Six replicate clusters, for a total of 18 plots,
hybrid poplar leaf weight, g stem weight, g total weight abovegrd, g height, cm diameter, mm no. of leaves per tree on main stem on lateral shoots total no. of leaves no. of lateral shoots cottonwood leaf weight, g stem weight, g total weight abovegrd, g height, cm diameter, mm no. of leaves per tree on main stern on lateral shoots total no. of leaves no. of lateral shoots black locust stem + leaf weight, g height, cm diameter, mm no. of leaves/tree (July 31, 84)
filteredambient- ambientchambered chambered open 34.la 49.9a 82.0a 189a 12.4a
41.4b 63.2b 103.2 b 208b 13.7b
50.9c** 78.6c** 126.9c** 231c** 14.6b
40.4a 16.6a 57.0a l.la
41.8a 30.0a 71.8a 3.7b
51.5b** 52.0b 103.5b** 7.9c**
107.6 86.0 193.6 162a 18.6
93.5 76.7 170.2 175ab 17.1
113.9 88.5 202.4 181b 17.8
31.8 183 214 22.9a
29.7 175 205 18.8b
33.6 192 226 20.3ab
106.5 94.1 14.6 54.la
76.2 113 12.0 36.5b
91.5 123 11.9 41.3b
‘All weights are oven-dry weights for means of all trees per treatment. Diameters were measured approximately 5 cm above the ground. Means with different letters are significantly different at a = 0.05 using the Duncan’s option in ANOVA-SAS. Asterisks indicate differences significant at a = 0.01. Total weight aboveground may not equal leaf + stem due to missing leaf data.
were studied. Irrigation and pest control were provided as necessary, in order to maintain optimal growing conditions. Chamber fans were operated from 8:OO to 22:OO Eastern Standard Time (EST) beginning on June 6 through September 28,1984. Ozone and sulfur dioxide were sampled at 30-min intervals in each chamber at a point at the center of the chamber volume. Ambient air at the site was sampled 4 times per hour while the chamber fans were on and at 2.5-min intervals during the rest of the day. Ozone data were collected with a UV photometer (Dasibi Model 1003-PC analyzer). The monitor was calibrated weekly witla an identical photometer outfitted to correct for temperature and pressure variations. Sulfur dioxide concentrations were monitored with a Thermo Electron Model 43 analyzer. Sulfur dioxide levels were almost entirely below the detection limits (26.2 pg m4 or 0.01 ppm) of the instrument during the growing season. In September of 1984, saplings were cut at ground level, and height, diameter, number of leaves and shoots on the plant, leaf weight, and stem weight were recorded. Weights were recorded as oven dry (70 OC for approximately 1 week). Duncan’s multiple range comparisons were used for all tests of significance. Results and Discussion
Over the growing season, ozone dose was reduced by 67% in the filtered-chambered vs. ambient-chambered treatment (Figure 2). Thus, ozone concentrations in the
filtered-chambered treatments were generally well below those known to cause plant injury. Ambient air in the nonfiltered chambers was only slightly lower than in open Environ. Sci. Technoi., Vol. 20, No. 11, 1986
1123
Table 11. Number of Days during Which a 1-h Average of 157 pg m-3 (0.08 ppm) and 235 pg m-3 (0.12 ppm) Was Exceeded for 1982, 1983, and 1984 at Millbrook, NY 157 pg m-3
235 pg m-3
year
June
July
AW
Sept
June
July
AW
Sept
1982 1983 1984
4 19 '3
8 7 5
1 8 6
3 6 6
0 3 ' 0
1 1 0
0 1 1
0 1 0
"Partial month record (11 days recorded).
Unflltar*d
L. 1
1
I 6
12
18
24
Hour of the Day
Figure 2. Seasonal (June through September) mean Ozone concgntration for each hour of the day for ambient-chambered and filteredchambered treatments. Sixty-seven percent of the ozone was removed by filtration during this period. Daily maxlmum hourly averages of ozone were also reduced in filtered chambers with no hours during the growing season exceeding an hourly average of 153 pg m-3.
plots (79 vs. 84 pg m-3, seasonal average, 0900-2100 h). At the end of the growing season, aboveground production of hybrid poplars in the ambient-chambered treatment was 19% less (significant, a = 0.01) than that in the filtered-chambered treatment (Table I). A change in the allocation of carbon to plant parts also occurred. In the ambient-chambered treatment, while biomass decreased by 19%, the number of lateral shoots per tree was reduced by 53%. The ratio of lateral leaves to the total was reduced from 50 (52.0/103.5) to 42 (30.0/71.8),a 16% change in leaf distribution. In previous studies (19),statistically significant reductions in biomass production, 12-24%, were measured for P. tremuloides in 1982 and 1983 at the same site using similar techniques. These observations from field studies of growth reductions resulting from ambient ozone are consistent with the large body of laboratory and greenhouse research indicating the susceptibility of Populus to ozone concentrations below 235 pg m-3, including studies showing reduced growth (20-24) and lower photosynthetic rates (7, 25, 26). The ambient-chambered treatment lowered aboveground weight, tree height and number of leaves of both P. deltoides and R. pseudoacacia (Table I). Aboveground production was reduced 17% for cottonwood and 16% for black locust, a magnitude similar to that for hybrid poplar. However, none of the differences were significant ( a = 0.05). Cottonwood leaf production (dry weight) was lower in the ambient-chambered treatment ( a = 0.25). Of the parameters measured, only diameter of black locust was higher (12.0 vs. 11.9 cm) in ambient-chambered than in filtered-chambered treatments. The presence of a chamber (comparing ambient open with ambient chambered, Table I) resulted in a 10-20% increase in aboveground biomass for hybrid Populus (significant, a = 0.05), an increase for P. deltoides (not 1124
Environ. Sci. Technol., Vol. 20, No. 11, 1986
significant, a = 0.05), and a decline for R. pseudoacacia (not significant, a = 0.05). Thus, chamber effects were present but of a variable nature. Little additional experimental data are available on the quantitative effect of ambient ozone on the growth of trees under field conditions. Duchelle et al. (27) found only weak trends (significant, a = 0.10) in seedling height growth in two out of seven tree species exposed to ambient air in open-top chambers. Foliar injury has been used to document the widespread effect of ozone on forests (28,29). Characteristic symptoms of leaf injury (stippling) due to ambient air were not observed on any of the three species studied. This supports our earlier observations (19) that substantial reductions in growth can occur without accompanying visible symptoms. Thus, it is probably prudent to conclude that ozone effects on forest ecosystems are more widespread and intensive than indicated by visible symptomology alone. The ambient air quality at our rural study site was generally below ambient air quality standards. Only once during the 1984 growing season (June through September) did ozone exceed the 1-h average maximum daily concentration of 235 pg m-3 (30) (Table 11). These 1984 values were typical, if not low, in comparison with two previous years of monitoring (19). Although ozone data for nonurban areas is limited (31,32), existing data suggests that the ambient air quality at our site may be similar to large forested areas throughout the Eastern United States (33-38) and Europe (39, 40). While it is difficult to extrapolate to mature forests from controlled field experiments on saplings, our results suggest that there is a considerable potential for major growth suppression of Populus over much of the estimated 20 million ha where it is dominant in the United States (12). Because growth reductions at concentrations below 235 pg m-3 (30) were substantial and occurred without visible injury, the need for studies of additional tree species at all stages of their life history is essential to assessing the threat of air pollution to forest ecosystems. Acknowledgments
We thank W. H. Smith, R. Bowden, and G. Geballe for comments on drafts of the manuscript. Registry No. Ozone, 10028-15-6.
Literature Cited (1) Smith, W. H. Air Pollution and Forests; Springer-Verlag: New York, 1981. (2) Bormann, F. H.Bioscience 1985,35,434-441. (3) Materna, J. In Air Pollution and Plant Life;Treshow, M., Ed.; Wiley: New York, 1984;pp 397-416. (4) Johnson, A. H.; Siccama, T. G. Enuiron. Sci. Technol. 1983, 17, 294A-305A. (5) German Federal Ministry of Nutrition, Agriculture and Forests Forest Damage from Air Pollution; MunsterHiltrup, FRG,1982;Series A, Applied Science, Vol. 273.
(6) Abelson, P. H. Science (Washington, D.C.) 1986,230,617. (7) Reich, P. B.; Amundson,R. G. Science (Washington, D.C.) 1985,230, 566. (8) Lewis, E.; Brennan, E. J. Air Pollut. Control Assoc. 1977, 27,889-891. (9) Cameron, J. W.; Taylor, 0. C. J. Environ. Qual. 1973,2, 387-389. (10) Heck, W. W. Environ. Sci. Technol, 1983,l7,573A-581Aa (11) Heagle, A. S.; Body, W. E.; Heck, W. W. J. Environ. Qual. 1973,2, 365-368. (12) International Poplar Committee and Food and Agriculture Organization of the United States. “Poplars and Willows in Wood Production and Land Use”; Rome, Italy, 1979. (13) Cushman, J. H.; Wright, L. L.; Trimble, J. L.; Ranney, J. W. In International Bio-Energy Directory and Handbook; Bente, P. F., Jr., Ed.; Bio-Energy Council: Washington, DC, 1984; pp 5-13. (14) Mandl, R. H.; Weinstein, L. H.; McCune, D. C.; Keveny, M. J. Environ. Qual. 1973, 2, 371-376. (15) Heagle, A. S.; Philbeck, R. B.; Rogers, H. H.; Letchworth, M. B. Phytopathology 1979,69, 15-20. (16) Davis, J. M.; Rogers, H. H. J. Air Pollut. Control Assoc. 1980,30,905-908. (17) Unsworth, M. H.; Heagle, A. S.; Heck, W. W. Atmos. Enuiron. 1984, 18, 381-385. (18) Last, F. T. In Proceedings of the Karlsruhe Symposium on Acid Deposition: A Challenge for Europe; Ott, H., Stangl, H., Eds.; Commission of the European Communities: Brussels, Belgium, 1984; XII/ENV/45/83, pp 102-126. (19) Wang, D.; Karnosky, D. F.; Bormann, F. H. Can. J. For. Res. 1986, 16, 47-55. (20) Jensen, K. F.; Dochinger, L. S. Environ. Pollut. 1974, 6, 289-295. (21) Mooi, J. Plant Dis. 1980, 64, 772-773. (22) Noble, R. D.; Jensen, K. F. Am. J.Bot. 1980,67,1005-1009. (23) Jensen, K. F. Enuiron. Pollut. 1981,26, 243-250. (24) Harkov, R.; Brennan, E. Plant Dis. Rep. 1982,66,587-589. (25) Reich, P. B. Plant Physiol. 1983, 73, 291-296. (26) Jensen, K. F.; Nobel, R. D. Can. J. For. Res. 1984, 14, 385-388. (27) Duchelle, S. F.; Skelly, J. M.; Chevone, B. I. Water Air Soil Pollut. 1982, 12, 363-373.
(28) Naegele, J. A,; Feder, W. A,; Bryant, C. J. Assessment of Air Pollution Damage to Vegetation in New England July 1971-July 1972; U.S.Environmental Protection Agency: Waltham, MA, 1972. (29) Skelly, J. M.; Johnson, J. W. Oxidant Air Pollution Impact to the Forests of Eastern United States-A Literature Review; U.S. Environmental Protection Agency: Corvallis, OR, 1979; EPA-600/3-79-045. (30) U.S. National Ambient Air Quality Standard. (31) Stasiuk, W. N., Jr.; Coffey, P. E. J. Air Pollut. Control ASSOC.1974, 4, 564-568. (32) Ludwig, F. L.; Shelar, E. Assessing the Representativeness of Ozone Monitoring Data; U.S. Environmental Protection Agency: Menlo Park, CA, 1979; Final Report, Contract 68-02-2548, SRI Project 7863, SRI International. (33) Spicer, C. W.; Joseph, D. W.; Sticksel, P. R.; Ward, G. F. Environ. Sci. Technol. 1979, 13, 975-985. (34) Evans, G. P.; Finkelstein, P.; Martin, B.; Possiel, N. J. Air Pollut. Control Assoc. 1983, 33, 291-296. (35) Pratt, G. C.; Hendrickson, R. C.; Chevone, B. I.; Christopherson, D. A.; O’Brien, M. V.; Krupa, S. V. Atmos. Environ. 1983, 17, 2013-2023. (36) Division Air Resources New York State Air Quality Report; New York Department of Environmental Conservation: 1977; DAR-78-1. (37) Air Quality Data-1973 Annual Statistics; U.S. Environmental Protection Agency: Research Triangle Park, NC, 1974. (38) Air Quality Data-1978 Annual Statistics, Including Summaries with Reference to Standards; U.S. Environmental Protection Agency: Research Triangle Park, NC, 1979; EPA-450/4-79-037. (39) Becker, K. H.; Fricke, W.; Lobel, J.; Schurath, U. In Air Pollution by Photochemical Oxidants; Guderian, R., Ed.; Springer-Verlag: Berlin, 1985; pp 11-67. (40) Ashmore, M.; Bell, N.; Rutter, J. Ambio 1985,14(2), 81-87.
Received for review January 7, 1986. Accepted June 2, 1986. The research was supported by a grant from the Mary Flagler Cary Charitable Trust and a grant to F.H.B. from the Andrew W. Mellon Foundation.
Environ. Sci. Technol., Vol. 20, No. 11, 1986
1125
