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HUMAN PERTURBATION OF C, N. AND S BIOGEOCHEMICAL CYCLES: HISTORICAL STUDIES WITH STABLE ISOTOPES B· _4 rlan cry The Ecosystems Center Marine Biological Laboratory Woods Hole, Massachusetts 02543 ABSTRACT Stable isotopes can serve as historical tracers of anthropogenic pollutants. For example, recent anthropogenic inputs of C, N. and S have altered! isotopic compositions of tree rings, lake sediments, and components of the atmosphere. Some of these effects are small in magnitude, 1 °/oo or less, and difficult to detect without extensive sampling. Examples include carbon isotope changes in tree rings due to local pollution effects or as a result of global changes in atmospheric CO: concentrations. Initial sulfur and nitrogen isotope studies suggest larger, more easily detectable changes of 2-7O/oo in precipitation and lake cores. Sulfur isotope changes have been used to establish chronologies of anthropogenic sulfur inputs in some lake sediments. Nitrogen isotope studies of precipitation, lake cores, and tree rings are at a very early stage, but show promise for tracing human nitrogen additions from atmospheric deposition. Use of carbon, nitrogen, and sulfur isotopes as historical pollution markers is appealing because they are natural tracers of, and cycle with, anthropogenic C, N. and S. INTRODUCTION The light elements H. C, N. O. and S all are important constituents of organic materials in the environment. These elements have two or more stable isotopes whose variation can be used to trace cycling of water and organic materials in the environment. Here I consider past and potential future uses of these natural tracers in historical studies of anthropogenic pollution. My focus is on carbon, nitrogen, and sulfur isotopes because human activities are causing significant alteration in the cycling of these elements. Studies of hydrogen and oxygen isotopes, in many ways complementary to the studies summarized here, are treated elsewhere (Burk and Stuiver 1981; Brenninkmeijer 1983; White et al. 1985; White 1988; Sternberg 1988~. Because studies of carbon isotope distributions in plants and especially tree rings have been pursued most vigorously to date, I use examples from these investigations to illustrate three different types of isotopic changes that can accompany anthropogenic alteration of element cycles. These three effects are related to changes in sources, in stress-induced metabolism and changes in the concentration of nutrients. Following this short review, I show examples of potential uses of nitrogen and sulfur isotopes to follow anthropogenic changes in the nitrogen and sulfur cycles. 143
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144 Because of the original and somewhat arbitrary choice of standards, 613C values for biological materials are almost always negative (-3 to -100°/~p) while the blSN and 634S values can be either positive or negative (-20 to +60 for ~ N and -60 to +40°/Oo for 834S). One may note that the absolute ~ values are usually unimportant; they most often serve as reference points from which to calculate isotopic differences (my. THEORY Isotopes of an element differ by the number of neutrons in the nucleus. The mass difference caused by extra neutrons slightly alters chemical equilibria and reaction kinetics for different isotopes of the same element. These differences are typically quite small, much less than 1% (e.g., Fig. 1 ). Using a highly sensitive mass spectrometer, it is possible to measure accurately these small differences, and an extensive theoretical and empirical knowledge of isotopic fractionation now exists (Peterson and Fry 1987~. In kinetic reactions, species containing the light isotope react somewhat faster because of lower activation energy. In equilibrium reactions, the light isotope will concentrate in those chemical species where it is less tightly bound. To cite well-known examples of these processes, kinetically-controlled reactions such as photosynthesis favor concentration of light carbon in plants, while CO2 in the atmosphere is depleted in the heavy carbon isotope during equilibrium exchange with bicarbonate dissolved in the ocean. These kinds of fractionations introduce signals into the natural environment that are present as background isotopic distributions. Human activities often lead to isotopic changes detectable against this natural background. EXAMPLES FROM 613C STUDIES 1. Source changes. Emission of CO2 into the atmosphere from burning of fossil fuels and biomass has influenced the isotopic composition of CO2 in the atmosphere. The preindustrial background isotopic composition of CO2, recently measured in gas bubbles from Antarctic ice cores, averaged about -6.~°/oo (Fig. 2~. In recent decades, anthropogenic activities have added CO2 with 61 3C = -25 to -30°/Oo to the atmosphere, resulting in a 613C decline of 1.3 °/OO to the current -7.8°/oo value for atmospheric CO2. In this case, simple mixing of carbon from natural and anthropogenic sources accounts for the observed isotopic changes. Prior to the ice core studies, many investigations addressed the possible decline in atmospheric CO2 61 3C by analysis of tree rings. Carbon in trees typically averages -20 to -35°/Oo, and is depleted in 13C relative to atmospheric CO2 due to kinetic isotope effects during carbon fixation in photosynthesis. Ideally, trees should maintain a constant offset to the isotopic composition of atmospheric COP if tree rings are to serve as accurate biorecorders of CO2 isotopic compositions. — ~, Figure 2 shows two examples of the scatter and variability often observed in tree ring studies. The record in one tree from southern Chile (Fig. 2b) is much more variable than the ice core measurements (Fig. 2a), although the same general decline of about 1°/oo is evident in recent years. The second Chilean tree has more consistent 613C values, but does not show evidence for a recent decline in 613C values (Fig. 2c). This disagreement between tree records is not atypical, and rather elaborate sampling methodology and large sample sizes (many tree ring records) have been used in attempts to obtain accurate representations of net isotopic changes (Tans and Mook 1980; Leavitt and Long 1983; Freyer and Belacy 1983; Stuiver et al. 1984; Leavitt and Long 1986; Leavitt 1987~. The averaging process carries implicit assumptions concerning the cause
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-6 _ ~ . _7 _ < - -8 _ -20 cot - 2 ~ _ con -22 _ -23 _ -20 _ - 2 1 _ 145 1740 t760 1780 1800 1820 1840 1860 1880 1900 1920 1940 1960 1980 ~ , -, , , , -, . . . . .. . ICE CORE, ANTARCTICA _ -6 —T _ -7 + + _ - 8 VALDIVIA TREE, CHILE -at, ARaUCARIA TREE, CHILE -20 -21 -22 _ -23 · e. ~ _ _19 -i I- .~ -a ·-~- - - ~ -it ·- - - 20 - 2 1 1 1 1 1 1 . I 1 . I I I I I 1740 1760 1780 1800 1820 1840 1860 1880 1900 1920 1940 1960 1980 YEAR Figure 2. 613C values in three historical records. Upper panel: The isotopic composition of atmospheric CO2 trapped in Antarctic ice has declined in recent decades (dots = CO2 extracted from ice, crosses = CO2 collected directly from the atmosphere at Hawaii). Lower panels: Tree rings record atmospheric CO2 61 3C, displaced by fractionations during photosynthetic metabolism. Tree ring records from two trees in Chile show typical scatter in 613C, and in only one of the trees is a recent decline in average 613C evident (middle panel). Dashed lines show pre-l900 average 613C values for reference. Sources: Friedli et al. 1986, Stuiver et al. 1984. and randomness of influences on 813C which, in light of recent studies, have not always been justified (Francey l98S). 2. Physiology and stress. Recent physiological work has emphasized that carbon isotopic compositions of plants respond not only to changes in ~ 1 3C of atmospheric CO2, but also to other factors such as water supply and, in some cases, light (Fig. 3; Francey 1983~. A general physiological model of carbon isotope change in plants has been formulated and extensively tested (O'Leary 1981; Farquhar et al. 1982; Francey and Farquhar 1982) and it is now recognized that environmental variables other than the isotopic composition of CO2 can significantly influence tree ring isotopic compositions
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146 TERMINOLOGY Isotopic distributions are measured relative to standard reference materials, and as such are difference ~ measurements where ~ = (RSTANDARD/RSAMPLE - 1) 1 000 and R = 13c/12C ISN/l4N or 34S/32S for carbon (613C), nitrogen (61SN) and sulfur (834S) ~ values, respectively. By this definition, standards have values of 0, and units are parts per thousand (difference), or °/OO. International standards are carbon from the PDB limestone, N ~ gas in air, and sulfur from the Canyon Diablo meteorite. The ~ terminology is in some ways awkward because of the several ratios involved In the ~ definition. However, ~ values turn out to be related to the percent heavy (or light) isotope content of a sample in a simple, linear manner (Fig. 1~. Increases in heavy isotope content cause increases in ~ values and samples with high ~ values are consequently "heavy" vs. samples with lower values. Conversely, samples with low ~ are depleted in the heavy isotope, but enriched in the light isotope, and therefore "light" (Fig. 1~. . u."u 1 0.39 ~ 0.38 ; - o 0. 3 0.36 0.35 , . . . -20 0 20 40 60 b f5N .10 "= rail - 0.1 %o~ 0.00004% 1 80 99.65 1 12 1 ~ ~ ~ ~ ~ ~ ~ ~ ~ 1 98-88 1.02 / , 0.1 Boom 0.00011 % 1.00 - 100 -80 - 60 -40 -20 b'3C 4 50 4.40 4.30 4.20 4.10 it/ 0.1%o~0.00044% 4.00 -60 ~40 -20 0 20 b34S 99.00 o ~ 94.69 cat 95.24 40 Figure 1. Relationship of ~ values to amounts of heavy and light stble isotopes for carbon, nitrogen and sulfur isotopes. Source: Reproduced, with permission, from the Annual Review of Ecology Systematics Vol. 18 c 1987 by Annual Reviews Inc.
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147 (Stuiver and Braziunas 1987~. In simplest form, the model states that isotopic compositions follow the ratio of internal CO2 concentration to external CO2 concentration (ci/ca). When ci/ca decreases due to stomata! closure accompanying water stress, or due to increased assimilation of CO2 upon strong illumination in water sufficient plants, then Sl3C values increase (or, more generally, when ci/ca decreases, Sl3C increases). Physiological variations related to CO2 fixation processes can therefore lead to larger 613C changes than the 0.5-1.5°/oo fossil fuel signal (compare Figs. 2 and 3). - 27 - 28 -29 WHEAT -30 ~ ~' / / .~ Abundant Mod. Dry Dry WATER SUPPLY 1 Very Dry Figure 3. Increases in 613C in response to water supply in wheat. Source: Reprinted with permission of Springer-Verlag N.Y. Inc. from Carbon isotope measurements in baseline air, forest canopy air, and plants 1982. Copyright 1982 by Springer-Verlag N.Y., Inc. The need for a physiological perspective in tree ring work has been emphasized (Francey 1983, 1985; Francey et al. 1984, 1985), and it is evident that the physiological component of tree rings variation needs to be recognized and "deconvoluted~ when using tree rings as substitutes for direct atmospheric CO2 measurements (Leavitt and Long, in prep.~. Several studies have- also specifically investigated the effects of air pollutants on tree rings. Generally, fumigation with SO2 or ozone causes increases in 613C values (Freyer 1979; Leavitt and Long 1987), presumably by affecting the ci/ca ratio (Greitner and Winner 1988~. These small + 1 to +2°/oo isotopic changes are in the opposite direction of the -0.5 to -1.5°/oo anthropogenic fossil fue! signal, and difficult to detect without intensive sampling (Fig. 4~.
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14R ~~13c +2 o _1L -2 D , , 90 1900 10 20 30 40 50 60 70 Year AD Figure 4. Isotopic variations in trees 50-100 m from a coal-fired foundry (o) vs. control trees at 2-3 km. distance (~3. The foundry was closed from 1929-1949 when tree isotopic compositions are similar. When the foundry was operating from 1890- 1929 and 1950- 1975, however, heavier values were evident in the polluted trees (higher ~ 1 3C), possibly because of long-term SO2 fumigation. Data were normalized first bay tree by subtracting average 1930- 1950 values from individual measurements to yield ~ 1 C values; means and 90% confidence intervals were obtained by averaging five trees per site. Source: Freyer 1979. 3. CO2 concentration. Isotopic changes can also result from changing concentrations of nutrients. The effects of increased CO: concentrations have not, to my knowledge, been specifically tested in trees, but concentration-related changes have been observed in studies with tomatoes, soybeans, and aquatic algae (Vogel 1980; Smith and Boutton 1981; Degens et al. 1968; Calder and Parker 1973; Mizutani and Wada 1985; Sharkey and Berry 1985~. In general, larger carbon isotopic discrimination occurs at higher CO2 concentrations (Fig. 5~. Conversely, as carbon supply becomes more and more limiting, smaller fractionations result, and in the extreme case, no fractionation results when all available carbon diffusing to a plant is taken up without regard for isotopic content. Present models of isotopic fractionation in trees and other C3 plants predict that
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1%o ) - 20 - 10 o 149 /ALGAE TOMATO arc 1 o/oo ) , I ~ I I I 0.03 0.33 0.5 1.0 1.5 Pco ~ vol .-°/0) 7 substrate ~ (atm. CO2 ) Figure 5. Isotopic fractionation in mixed algal cultures and for tomato grown with different levels of CO2. Slow diffusion of CO2 in water limits the degree of fractionation by algae grown under normal conditions (0.03% CO2 in air); the roughly 104 faster diffusion of CO2 in air than in water may account for the larger fractionations in tomato. Fractionation (~39) = ~ 13CpLANT - 613CFEED C02 Source: Vogel 1980. changing atmospheric CO2 levels will affect isotopic compositions only if the CO2 concentration gradient from external air to leaf-internal spaces changes significantly (Farquhar et al. 1982). For trees, drought and water relations may often be more important in affecting this concentration gradient than the amount of CO2 available in the atmosphere. SIGNAL-TO-NOISE The very extensive carbon isotope studies with tree rings have tackled a difficult problem in that the total atmospheric Ab signal is small at about 1°/oo and there is significant physiological noise that is often of this same magnitude or larger. The signal-to-noise ratio may be more promising for nitrogen and sulfur isotopes, where studies related to tree age and atmospheric pollution are just beginning. The promise of N and S isotope studies comes at the moment from investigations of lake cores (Fig. 6). The background variability (noise) seems similar for the C,N and S records, but the recent isotopic changes for N and S are larger at 2 and 7°/0O' respectively, than the
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150 approximate 1 Moo carbon change. Sulfur and nitrogen isotope studies may, therefore, deserve more attention in the future. E- 6 ro _7 me 3 _ z 2 _ - c~ 1 _ O _ ~ 1800 1850 1900 1950 1990 Or 8t 7t 5 Cal ATMOSPHERIC CO2 . .~., . -—· .—~ I.... -8 AL I ~ '`O~ 1800 1850 1900 1950 1990 LAKE CORE, BIG MOOSE LAKE LAKE CORE, LITTLE LONG POND · - ~ ·'! '' --. 6t 4t 3t 2 --eve . \~e,- 1 . ' 1800 1850 1900 1950 1990 YEAR Figure 6. Comparison of C,N and S isotope historical records. Top: 613C of CO2 from an Antarctic ice core. (Dots = CO2 from ice core, open circles = CO: measured from air at Hawaii). Middle: 61SN of Big Moose Lake sediments, Adirondack Mountains, New York. Bottom: 634S of sediments from Little Long Pond, Maine. Source: Friedli et al. 1986; Fry, unpublished.
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151 NITROGEN ISOTOPES The initial lake core results of Figure 6 suggest that known recent increases in anthropogenic N loading may be accompanied by a net decline in ~ 1 5N. A summary of atmospheric nitrate and ammonium isotopic compositions (Fig. 7) shows a great deal of variation from sample to sample that precludes definitive statements about possible recent 615N declines. However, it is suggestive that the earliest study (Hoering 1957) from rural and presumably unpolluted Arkansas showed the highest 61 5N values for ammonium anti nitrate; average values measured in industrial areas are much lower (Freyer 1978~. Because tree rings and lake cores can be expected to integrate isotopic compositions of input N. direct study of recent records may be the best way to evaluate whether anthropogenic N differs significantly in 815N from natural background N. Previous study shows that nitrogen present in tree ring wood is sufficiently abundant for 61 SN analysis, and is apparently not translocated after initial fixation in wood (Cotrufo 1983~. -20 -10 0 +10 +20 NO3 r ~ I ~ .e ~ Aerosol, Colorado Particulate ~ 0 0 cmo Co Dry Deposition, Pretoria ~ ~~ Pretoria NO3 J Rain ' ~ · ~ _~ M ~ Julich . ~ ~ ~ Arkansas -- Colorado NO3 NH4 I · ~ 0 - ~ · Aerosol, Colorado Particulate ~ 0 cD cmooo Dry Deposition1 Pretoria Pretoria N H 4 NH4 ~ Rain ~ :~_ JuliCh —~~ ~~ -~ Colorado -20 -10 0 +~0 +20 b IN Figure 7. b15N values of nitrogen in dry deposition and rainfall. Source: Heaton 1986.
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152 SULFUR ISOTOPES Several studies of lake cores have shown that large sulfur isotopic changes accompany increased sulfur loading in recently acidified lakes (Nriagu and Coker 1983; Nriagu and Soon 1985~. The isotopic record often reflects addition of anthropogenic S with different 634S, a change, therefore, in source 634S. For example, in lakes and ponds near the ocean, background values are influenced by +21 °/oo sulfate deposited from sea spray, but values decline in more recent sediments towards near zero values (e.g., Little Long Pond in Fig. 7~. The decline presumably occurs because of increased anthropogenic sulfur deposition from the atmosphere; 634S values of atmospheric sulfate currently average +3 to +5°/OO over much of North America (Nriagu and Coker 1978; Saltzman et al. 1983; B. Cook, pers. comma.. In more inland locations, however, background values often average near +3°/OO, and the new anthropogenic input is small and relatively difficult to detect with 634S measurements. Isotopic changes also occur in lake cores because of changing sulfate levels, and separating the source vs. concentration components of isotopic change can be complex (Fry 1986; Peterson and Fry 1987; Fry 1988~. As with studies of ~ 3C in plants, basic physiological investigations need to accompany studies of sulfur isotope change. Sulfur isotopic changes in stressed vegetation have also been documented (Winner et al. 1 97S, 1981). No tree ring work with sulfur isotopes has been published, in part because of the difficulty of making the 634S measurements, and in part because of the very low trace concentrations of sulfur in wood (~0.05%~. The strong isotopic signals seen in lake cores, however, suggest that development of new methods of analyzing trace amounts of tree sulfur for 83 S may prove very worthwhile. CONCLUSIONS Stable isotope changes in trees that are caused by specific air pollutants have been investigated in only a handful of studies. Initial results from these studies indicate that these changes are generally small and difficult to detect without intensive sampling. Careful comparisons of impacted vs. control trees are necessary to distinguish natural variations from effects associated with anthropogenic pollutants. Although assessing effects of specific pollutants may thus be labor-intensive, stable isotope studies may function in a wider pollution context as indicators of historical changes in C, N. and S loading to natural systems. Carbon isotope studies of tree rings show relatively small changes because the total increase in CO2 has been relatively small (<25%) to date and because equilibrium exchange of CO with bicarbonate in the ocean tends to dampen the isotopic signal associated with anthropogenic CO2 emissions. For sulfur, large isotopic changes occur in recent lake sediments in response to relatively large changes in sulfate loading. This historical record is being compared to records of sulfur emissions on a regional and national scale. Nitrogen isotope studies of tree rings have not yet been performed, but should also provide a record of anthropogenic N additions to forests. This record may be especially interesting since nitrogen often limits growth of forests.
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153 ACKNOWLEDGMENTS I thank Re Jo Francey, S. A. Leavitt, Re H. Waring, and W. E. Winner for helpful discussions during preparation of this paper. REFERENCES Brenninkmeijer, C. A. M. 1983. 2H, 180 and 13C variations in tree rings. Ph.D. thesis, University of Groningen. Burk, R.L., and M. Stuiver. l9Sl. Oxygen isotope ratios in trees reflect mean annual temperature and humidity. Science 211:1417-1419. Calder, I.A., and P.~. Parker. 1973. Geochemical implications of induced changes in 13C fractionation by blue-green algae. Geochim. Cosmochim. Acta 37:133-140. Cotrufo, C. 1983. Xylem nitrogen as a possible diagnostic nitrogen test for loblolly pine. Can. I. For. Res. 13:355-357. Degens, E. T., R. R. L. Guillard, W. M. Sackett, and J. A. Hellebust. 1968. Metabolic fractionation of carbon isotopes in marine plankton. I. Temperature and respiration experiments. Deep-Sea Res. 15:1-9. Farquhar, G.D., M.H. O'Leary, and I.A. Berry. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. I. Plant Physiol. 9:121-137. Francey, R. I. 1983. Carbon isotope measurements in baseline air, forest canopy air, and plants. Pp. 160-174 in I. R. Trabalka and D. E. Reichie (eds.), The Changing Carbon Cycle: A Global Analysis. Springer-Verlag, New York. Francey, R. I. 1985. Tree ring 13C/12C records - an alternate view. Post-conference report on "Carbon Transfer in the Atmosphere, Ocean and Terrestrial Systemn, Lake Arrowhead, May 5-10, 1985. Francey, R. J., and G. D. Farquhar. 1982. An explanation of 13C/12C variations in tree rings. Nature 297:27-31. Francey, R. I., M. Barbetti, T. Bird' D. Beardsmore, W. Coupland, I. E. Dolezal, G. D. Farquhar, R. G. Flynn, P. I. Fraser, R. M. Gifford, H. S. Goodman, B. Kunda, S. McPhail, G. Nanson, G. I. Pearman, N. G. Richards, T. D. Sharkey, R. B. Temple, and B. Weir. 1984. Isotopes in Tree Rings. Division of Atmospheric Research Technical Paper No. 4. CSIRO, Australia. 86 pp. Francey, R. I., R. M. Gifford, T. D. Sharkey, and B. Weir. 1985. Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii). Oecologia 66:211-218. Freyer, H. D. 1978. Preliminary 15N studies on atmospheric nitrogenous trace gases. Pageoph 116:393-404.
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154 Freyer, H. D. 1979. On the 13C record in tree rings. Part II. Registration of microenvironmental CO2 and anomalous pollution effect. Tellus 31:308-312. Freyer, H.D. and N. Belacy. 1983. 1 3C/ 1 2c records in Northern Hemisphere trees during the past 500 years - anthropogenic impact and climatic superpositions. J. Geophys. Res. 88: 6844-6852. Friedli, H., H. Lotscher, H. Oeschger, U. Siegenthaler, and B. Stauffer. 1986. Ice core record of the 1 3C/ 1 2c ratio of atmospheric CO2 in the past two centuries. Nature 324:237-239. Fry, B. 1986. Stable sulfur isotopic distributions and sulfate reduction in lake sediments of the Adirondack Mountains, New York. Biogeochem. 2:329-343. Fry, B. 1 9SX. Sulfate fertilization and changes in sulfur stable isotopic compositions of lake sediments. In P. W. Rundel, J. R. Ehlringer and K. A. Nagy (ads.), Stable Isotopes in Ecological Research. Springer Verlag, New York. Greitner, C. S., and W. E. Winner. 1988. Increases in 61 3C values of radish and soybean plants caused by ozone. New Phytol., in press. Heaton, T. H. E. 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: A review. Chem. Geol. 59:87-102. Hoering, T. 1957. The isotopic composition of the ammonia and the nitrate in rain. Geochim. Cosmochim. Acta 12:97-102. Leavitt, S. W. 1987. Stable-carbon isotopes in tree rings as environmental indicators. Pp. 61-74 in R. W. Hurst, T. E. Davis, and S. S. Augustithis (eds.), The Practical Applications of Trace Elements and Isotopes to Environmental Biogeochemistry and Mineral Resources Evaluation. Theophrastus Publications, Athens, Greece. Leavitt, S. W., and A. Long. 1983. An atmospheric 1 3C/ 1 2c reconstruction generated through removal of climate effects from tree-ring 13C/12C measurements. Tellus 35B:92-102. Leavitt, S. W., and A. Long. 1986. Stable-carbon isotope variability in tree foliage and wood. Ecology 67:1002-1010. Leavitt, S. W., and A. Long. 1987. Stable-carbon isotopic composition of plants near an Arizona smelter. Pp. 47-57 in R. W. Hurst, T. E. Davis, and S. S. Augustithis (eds.), The Practical Applications of Trace Elements and Isotopes to Environmental Biogeochemistry and Mineral Resources Evaluation. Theophrastus Publications, Athens, Greece. Mizutani, H., and E. Wada. 1982. Effect of high atmospheric CO2 concentration of 613C of algae. Origins of Life 12:377-390. Mizutani, H., and E. Wada. 1985. Carbon dioxide and the biosphere. Their historical relationship as inferred from carbon isotope records. Viva Origino 1 3:25-49.
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156 White, I. W. C., E. R. Cook, ]. R. Lawrence, and W. S. Broecher. 1985. The D/H ratios of sap in trees: implications for water sources and tree ring D/H ratios. Geochim. Cosmochim. Acta 49:237-246. Winner, W. E., J. D. Bewley, H. R. Krouse, and H. M. Brown. 1978. Stable sulfur isotope analysis of SO2 pollution impact on vegetation. Oecologia 36:351-361. Winner, W. E., C. L. Smith, G. W. Koch, H. A. Mooney, J. D. Bewley, and H. R. Krouse. 1981. Rates of emission of H2S from plants and patterns of stable sulphur isotope fractionation. Nature 289:672-673.
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