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OCR for page 143
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
OCR for page 144
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
OCR for page 145
-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
OCR for page 146
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.
OCR for page 147
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~.
OCR for page 148
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
OCR for page 149
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.
OCR for page 152
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.
OCR for page 153
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.
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OCR for page 155
Representative terms from entire chapter:
carbon isotope
155
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