Annurev Es 18 110187 001453

ANNUAL
REVIEWS Further
Quick links to online content
Ann. Rev. Ecol. Sl'st. 1987. 18:293-320

Copyright © 198 7 by Annual Reviews 1nc. All rights reserved
STABLE ISOTOPES IN ECOSYSTEM

STUDIES
Annu. Rev. Ecol. Syst. 1987.18:293-320. Downloaded from www.annualreviews.org
Bruce 1. Peterson and Brian Fry

Access provided by CAPES on 10/19/16. For personal use only.
The Ecosystems Center, Marine Bio logica l Laboratory, Woods Hole, Massachusetts
02543
INTRODUCTION
The use of sta ble isotopes to solve bio geochemical pro blems in ecosystem
ana lysis is increasing rapidly because sta ble isotope data can contri bute both
source-sink (tracer) and process information: The elements C , N, S, H, and 0
all have more than one isotope, and isotopic compositions of natural materials
can be measured with great precision with a mass spectrometer. Isotopic
compositions chan ge in predicta ble ways as elements cycle throu gh the
biosphere. These chan ges have been exploited by geochemists to understand
the glo ba l elementa l cycles. Eco lo gists have not until quite recently emp loyed
these techniques. The reasons for this are,first,that most ecologists do not
have the background in chemistry and geochemistry to be fully aware of the
possi bilities for exploiting the natural variations in sta ble isotopic composi
tions, and second, that sta ble isotope ratio measurements require equipment
not normally availa ble to ecolo gists. This is unfortunate because some of the
more intracta ble pro blems in ecology can be profita bly addressed usin g sta ble
isotope measurements. Sta ble isotopes are ideally suited to increase our
understanding of element cycles in ecosystems.
This review is written for ecolo gists who would like to learn more a bout
how sta ble isotope analyses have been and can be used in ecosystem studies.
We begin with an explanation of isotope terminology and fractionation, then
summarize isotopic distri butions in the C, N, and S biogeochemical cycles,
and conclude with five case studies that show how sta ble isotope measure
ments can provide crucial information for ecosystem analysis. We restrict this
review to studies of natural variations in C, N, and S isotopic a bundances,
exc ludin g from consideration 15N enrichment studies and hydro gen and oxy
gen isotope studies. Our focus on C, N, and S derives in part from our
293
0066-4162/87/1120-0293$02.00
294 PETERSON & FRY
experience that com binations of these measurements are often complementary

and in part from the need to limit the scope of the review.
TERMINOLOGY AND MEASUREMENT
Most ecolo gical studies express isotopic compositions in terms of a values,

which are parts per thousand differences from a standard:
1.
where X is l3 C, 15N, or 34S, and R is the correspondin g ratio l3 C/ 12C, 15N / 14N
2
or 34S;3 S. The {) values are measures of the amounts of heavy and li ght
isotopes ih a sample. Increases in these values denote increases in the amount

of the heavy isotope components (Fi gure I). Conversely, decreases in B
values denote decreases in the heavy isotope content, and a reciprocal in
crease in the li ght isotope component. Standard reference materials are car bon
in the PeeDee limestone, nitro gen gas in the atmosphere, and sulfur from the
Canyon Diablo meteorite. The precision of the measurements is typically
±O.2C>/C> 0 or better, and current analysis costs typically ran ge from $30--100
per sample throu gh commercial firms.
Many reactions alter the ratio of heavy to li ght isotopes, or "fractionate"
sta ble isotopes, but·the de gree of fractionation is typically quite small. Even
very lar ge chan ges of 1000/<> <> (10%) between rea ctants and products involve
only minute a bsolute chan ges of 0.04%, 0.11%, and 0.44% for the heavy
isotopes of nitro gen, car bon, and sulfur, respectively (Fi gure 1). A mass
spectrometer is required for accurate detection of these small differences and
gaseous samples are required for the isotopic determinations.
Sample preparation differs from many other ecolo gical measurements in
that quantitative yields (a complete conversion of sample to gas) are required.
When yields are not quantitative, isotopic fractionation between product and
residual materials may result in a false apparent isotopic composition of the
samples. Many com bustion schemes have been developed to quantitatively
break down diverse molecules into the simple gases most suitable for mass
spectrometry. Most la boratories currently employ a hi gh tempe rature sealed
tu be com bustion to convert car bon and nitro gen compounds to COz and Nz
( 70). N2 can also be prepared from Kjeldahl di gestions or ammonia ( 70).
Sulfur-containin g materials are typically converted to sulfates and sulfides,
which are in tum converted quantitatively to SOz (30, 41, 122). Pure COz,
N2, and S02 are separated from one another and from water usin g various
cold traps that allow differential volatilization and trappin g under hi gh
vacuum conditions . A pure gas is then introduced into a dual or triple
collector isotope ratio mass spectrometer, and its isotopic composition mea
sured relative to a known standard.
STABLE ISOTOPES IN ECOSYSTEMS 295
O.40 ��""""""T""---r---'r---or--,...-"""'---r...., 99.60
0.39
:z
+ 0.38
v
:z
!!2
* 0.37 +
0.36
0.1 "100 = 0.00004 "10
0.35 L...-...L--L..---I._-'----'--"_-'--1.---' 99.65
-W 0 W 40 60 00
I . 12 r--..,.-�--,....,-T""""...,.._--r-___r-r---I 98.88
1 . 10
• 1.08
U
N
':1U f_06
�
1.04
1.02
0.1 %0= 0.00011 %
1.00 E-....-1-..--i.
.. _.1.-....--I.----10
.. _�....I---I 99.00
-100 -80 -60 -40 -20 0
4.50 r--..,.-....,...--r-----,r---or--,.-.---r---, 94.69
4.40
• 4.30
(/)
...
ff')
*
4.20
+
4.10
0.1%0: 0.00044 %
4. 00 �...L-""""---'_.l..--'----'�.l..-�-> 95.24
-W -40 -W 0 20 40
J34S
Figure I Relationship of N, C, and S stable isotope content to .')15N, .')I3C and .')34S values.
Large variations of IOO�1 c> c> correspond to only slight variations in percent J3C, 15N or 34S. The
linear relations shown were derived from simultaneous solution of Equation I (text), and the
following isotope ratios for standards: J3CI12CPDB = 0.0112372, 15NI14NAIR = 0.0036765 and
34St'2SCI)T = 0.045004 (15,51,77). By definition (Equation 1) standards have 0°1 c> c> 6 values.
Isotopic Fractionation
Stable isotopes record two kinds of infonnation. Where physical and
chemical reactions fractionate stable isotopes, the resulting isotopic distri
butions reflect reaction conditions (process infonnation). Stable isotope dis
tributions also record infonnation about the origins of samples (source
296 PETERSON & FRY
information). The source sets an isotopic baseline that can subsequently

be shifted by isotopic fractionation. A well-studied example is carbon isotope
fractionation in photosynthesis. A 1974 study showed that terrestrial C3
0 0
plants average -27.8 100 (l15). This was a bout 20 /00 more negative
than the sou rce of ca rbon fo r p lants, CO2 in ai r (8I3Cco2 -7.4% 0 in
=
1974; 55). The overall p lant isotopic composition thus ref lected both sou rce
(-7.4% 0) and fractionation (-20.4% 0) information: -27.8PLANT ::::;
-7 .4souRCE-20.4FRACTIONATION
Isotopic f ractionation is a mass-dependent phenomenon. The addition of
neutral mass (neutrons) does not alter most aspects of chemical reactivity so
that different isotopes of the same e lement a re functiona l ly equiva lent in most
chemica l and biochemica l reactions. The s li ght differences that do occur are
measured as a partial isotopic separation or fractionation. In this introduction,

we focus on t wo kinds of isotope effects, equi li brium and kinetic, and on ho w
isotopic fractionation is expressed in ecosystems.
Where chemical exchange occurs between two molecules,small equilibri
um isotope effects a re common . One examp le is the exchange of ca rbon
bet ween CO2 in ai r and bicar bonate in the ocean (74). Bi ca rbona te equili
brated with CO2 in ai r is enriched in 13C by 10.8 to 7.4% 0 rela tive to the
CO2 at 0-30°C. Unde r conditions of f ree exchan ge, the gene ra l ru le is that
heavy isotopes concentrate in the mo lecu le whe re bond st ren gths a re greatest,
in this case,in bica rbonate (HC03 -) rathe r than CO2, Equi li brium isotopic
f ractionations va ry in ma gnitude with tempe ratu re and can be p redicted f rom
bond strength measurements for reactions involving simple molecules (23,
116).
Most biolo gica l reactions are more comp lex than simp le equi librations, and
such reactions involve kinetic isotope effects. Kinetic isotope effects a re most
simp ly i llust rated in physica l p rocesses such as diffusion. Fo r examp le,
diffusion of 34S02 (ma ss 66) is a bout 1.6% or 16% 0 slower in a vacuum
than diffusion of 32S02 (mass 64). This is because application of the same
force displaces the mass 66 sulfur dioxide more slo wly than its li ght-isotope
mass 64 counterpart. The % 0 isotope effect o r discrimination, D, ran ges
from 0 to 100% 0 for most kinetic reactions invo lvin g C , N, and S stab le
isotopes. The discrimination ( D ) va lues a re positive in si gn when li ght isotope
species react faste r than thei r heavy isotope counte rpa rts and can be closely
approximated as the % ° diffe rence bet ween a su bst rate and p roduct fo rmed
at an instant in tim e from that su bstrat e (83):
D == 8SUBSTRATE - 8PRODUCT
The maximum isotopic discrimination represented by a D va lue is an
i mpo rtant unit used in modeling isotopic dist ri butions. This maximum dis
crimination is often not rea lized, and the de gree of o bse rved f ractionation
depends strongly upon reaction conditions. The simplest case in which full
discrimination occurs is a one-step reaction starting with an essentially unlim

ited supply of substrate. Under these open system conditions, the substrate
and product isotopic compositions are related simply by 5PRODUCT =
5SUBSTRATE - D.
A somewhat more complex case occurs in closed systems where a limited
amount of substrate is initially available, and this substrate is completely
converted to product over time. Closed and partially closed systems include
laboratory bottle incubations and some sediments and soils. In closed sys
tems, the substrate gradually increases in heavy isotope content (Figure 2,
100%
SUBSTRATE CONSUMPTION
60 ,.,
/ .",.""
,/ "",. SO!-
0
7°f
'" _0
�V) 4
20
�••,,'"
0=57.5%0
.l�
o
-20 0-""'-
0% 100%
SULFATE DEPLETION
Figure 2 Top: Model of closed system isotopic changes where substrate is converted to two
kinds of products-a cumulative product and an instantaneously forming product. Bottom: Isotop
ic changes in marine sediment core 2092, a partially closed system (43). Sulfides produced from
sulfate are an average of 57.5°/<> <> depleted in 34S. Isotopic values of sulfate increase with depth
(sulfate depletion) but not as fast as expected for a 57.5°/<> c> fractionation (dashed line), possibly
because of increased diffusion 32S0l- vs. 34sol- from overlying seawater (50) or sulfide
oxidation (2).
298 PETERSON & FRY
top) due to isotopic fractionation during the formation of heavy-isotope

depleted (isotopically light) products. This change in substrate isotopic com
position contrasts with open systems where substrate is continually renewed
and hence does not change in isotopic composition. The cumulative product
in closed systems follows an isotopic trajectory that preserves mass balance as
substrate is consumed (Figure 2). As in open systems, however, the product
forming at any instant in time differs from the substrate isotopic composition
by D (Figure 2).
The decomposition pr ocess of sulfate reduction, for example, occurs in
a semi-closed system in marine sediments and results in marked sulfur iso

topic changes. As sulfate is consumed in sediments, the 34 S content of the
residual sulfate increases from a surface <534 S value near + 21 % 0 to values
>+60% 0 at depth (Figure 2,. bottom). A large isotope effect during sul
fate reduction (typical D 30 to 70% 0; 38) is responsible for this increase,
=
as production of 34 S-depleted sulfides leaves residual sulfate increasingly

enriched in 34S. Marine sediments are not truly closed systems because of
continual, albeit slow substrate inputs (50), but models of closed system
isotopic behavior are nonetheless useful for obtaining a qualitative under
standing of isotopic changes accompanying many diagenetic reactions (6 7).
This discussion of fractionation has thus far been limited to consideration of
single reactions. Multiple coupled reactions, perhaps the common reality in
ecosystems,have also been extensively modeled. As examples, we consider
th ree cases: a t ightly linked reaction sequence w it h several enzymatic steps, a
two-step reaction in which the first step is reversible, and a branched reaction
chain with two products (Figure 3).
In many biological reactions, chemical intermediates are nearly quantita
tively converted to a final product in a series of linked, essentially unidirec
tional enzymatic steps. If fractionation is observed in the final product, this
fractionation must have occurred in the first step of the reaction. It is the first
step that determines the isotopic input into the reaction chain; by mass
balance, the final product, or output, must match in isotopic composition with
this input. This finding is a more general formulation of the rule that when
reactions go to completion (all substrate is converted to product) there is no
oppor tunity for isotopic fractionation to occur.
A second example concerns a reaction sequence with an early reversible
step (Figure 3, middle). This occurs in photosynthetic carbon fixation by C'l
terrestrial plants (8 3). The diffusion of CO2 from the atmosphere into internal
leaf air spaces is reversible, since CO2 can diffuse bac k out to the atmosphere.
The observed isotopic fractionation depends in part on this back diffusion,
and in par t on the carboxylation of CO2 into simple plant sugars. Where back
diffusion is negligible, the overall fixation reaction is unidirectional into the
leaf and all CO2 entering the leaf is carboxylated. The only isotope effect
expressed in this circumstance is that associated with diffusion (D = 4.4<> /00;
A-::'B�C
Figure 3 The outlined reaction sequences contain starting substrate (A), intennediate (B), and
product(s) (C & D). Each reaction step could result in isotopic fractionation if measured in
isolation. but linking reactions modifies expression of the individual fractionations. In a sequence
of tightly linked reactions (top), overall isotopic fractionation is associated with the first step (A
� B). Where a reversible equilibration occurs before a unidirectional reaction (middle), isotopic
fractionation depends on the fraction of B converted to C versus the back reaction of B to A. In
branched reactions (bottom), the proportion of mass flow diverted from product C to product D
strongly influences isotopic compositions of both of these products.
25),. the first step in the overall fixation process. The other extreme occurs
when carboxylation is much slower than diffusion, and the intemal leaf CO2
concentration approaches that of the atmosphere. Diffusion no longer controls
reaction ·ratcs, and a larger carboxylation discrimination of about 29°10 (97)
°
will be expressed. Actual fixation occurs in an intermediate situation where
neither diffusion nor carboxyla tion 'Completely lim its the overall fixation rate,
and the observed fractionation is intermediate between 4.4 and 29°100, at
about 2 1 °1<> (25). The reversibility of the diffusional step accounts for this
°
intermediate value; if the flow of CO2 were unidirectional into the leaf, only
the 4.4°/0 0 di ffus iona L fractionation would be expressed. Revers ibi lity of
diffusional fluxes may be important for isotopic fractionation in other uptake
- -
reactions involving HCO 3 , SO/-, N03 NH + etc. To the extent that
4
,
nutrient uptake steps are not simply unidirectional, the magnitude of isotopic
fractionation will reflect the balance in the rates of nutrient fixation and
nutrient efflux from the sites of uptake. Very low substrate concentrations or
slow diffusion steps often result in small overall fractionations since isotope
effects for diffusion of inorganic nutrients in air and water are typically small,
<5°/00 (83, 84, 95, 120).
300 PETERSON & FRY
Our photosynthesis example is actually a special case of branched reac

tions, with back-branching occurring during CO2 efflux from the leaf. For
branched reactions with one or more side products (Figure 3, bottom), the
product isotopic compositions depend not only upon the isotopic discrimina
tion factors for individual steps, but also upon how the mass flow is parti
tioned between these steps (44). The isotopic compositions of many metabo
lites such as amino acids, proteins, and lipids are controlled by branched
reactions (I, 42, 62). Investigations of branched reaction networks show that
isotopic compositions of especially small pools with rapid turnover can vary
widely depending on the reactions leading away from these pools. Isotopic
compositions record source information most faithfully when there is no
fractionation in reactions leading away from or to the pool in question.
In summary, isotopic fractionation in most biochemical reactions arises

when similar molecules of slightly different mass react at different rates.
Chemical and biochemical studies typically divide reactions into a series of
individual steps that, when combined in kinetic models, yield the appropriate
fractionation for the overall reaction. These models can be expanded and
applied at an ecosystems level to understand fluxes of materials but have not
yet been intensively used by ecologists to do so.
OVERVIEW OF C, N, AND S DISTRIBUTIONS

IN NATURE
The natural abundance isotopic compositions of C, N, and S in ecosystems

are illustrated in Figures 4--6. Our objective with these figures is to give a
comparative overview of C, N, and S stable isotopic distributions at the
ecosystem level, rather than to give detailed values for all parts of each cycle.
Our values are representative but do not encompass the full spectrum of
observed values. Because space prevents us from a detailed treatment, we
suggest that interested readers consult the references cited in the figure
legends for further information.
The Carbon Cycle

The carbon cycle involves active exchanges of CO2 between the atmosphere
and both terrestrial ecosystems and the surface ocean (Figure 4). The 8l3C
value of atmospheric CO2 is decreasing in response to inputs of l3 C depleted
CO2 from fossil fuel plus biomass burning and decomposition (88). Over the
past 30 years the decrease may have been almost 1°/<::><::>. Carbon uptake by
the dominant C3 plants on land involves a net fractionation of about 21 % °
between the atmosphere (-7% 0) and plant biomass (-28% 0) (17).
Carbon uptake by C4 plants, mainly tropical and salt grasses, involves a small
fractionation of about 6% 0. Soil organic matter globally contains several-
ATMOSPHERE
CO� -7
0 6 0
7 eq.
-13
Tropical C-4 To101 Dissolved CO2 0

Soi I Organic MaUer - 26
Grasslands POM -22

DOM -23
LAKE OCEAN
Figure 4 The a"c distribution in ecosystems. Single arrows indicate CO2 fluxes. The double
arrow signifies an equilibrium isotope fractionation. Numbers for pools indicate ,s"e values
(""/ "" 0) and numbers for arrows indicate the fractionation (D) occurring during transfers . POM =
Particulate Organic Matter, DOM = Dissolved Organic Matter. Sources: 5, 16, 17,35, 83, 104,
121.
fold more car bon than either the atmosphere or living plant biomass and in
general is similar or slightly enr iched in 13 C in comparison with the dominant
vegetation_ Wh ile eithe r differential preservation or mineralization of soil
components with different Sl3 C values does lead to gradual shifts in soil 13 C
content (6, 22), on average there is little fractionation of resp ired CO2 (83)_
The exc han ge of CO2 between the atmosphere and the surface of the ocean
involves an equili br ium chemical fractionation between atmospheric CO2
(-7% 0) and the total COiIco2, mostly bicar bonate) in surface ocean
water (0% 0) (74)- The withdrawal of car bon to form car bonates involves
little isotopic fractiona tion whereas uptake of dissolved inorganic car bon in
planktonic photosynthesis involves larger kinetic fractionation that results in
algal values of a bo ut - 19 to - 24 % 0- Both the dissolved and the particulate
o rg an ic matter in the oceans reflect predominantly a mar ine plankton ic origin
(121).
The I3 C contents of components of the car bon cycle of fresh waters vary
widely depending on the source of d issolved CO2 in the waters-from
car bonate rock weathering, from m inera l springs, from the atmosphere or
from respired organic matter. Where respiration inputs are strong, Ol3C values
for dissolved inorganic car bon may approach - 20°I00, and algae that further
fractionate during car bon uptake can measure -45% 0 (93, 94, 99)_
302 PETERSON & FRY
ATMOSPHERE
Nz gas 0
PRECIPITATION I I eq.
(lypiC<JI)
NH l -18 to +8
N03 -t5 to +3
NOx - 2 10+4
NH3 -810 -4
Fertilizer
DissolvedNz +1.0
Soi I Organic Matter
NH4 -0 POM -2 to +11
N03 -+3
Deep Water N03 +4 to +6
LAKE
OCEAN
Figure 5 The al5N distributions in ecosystems. See Figure 4 legend for explanation of symbols.
Sources: 26, 27, 14, 48, 52, 60, 63, 71, 75, 76, 106, 108, 109.
The Nitrogen Cycle

Most nitrogen in the biosphere is present as N2 gas in the atmosphere. This
massive reservoir is well-mixed with an isotopic composition that is es
sentially constant at 0% 0 (63). Nitrogen in most other parts of the biosphere
also has an isotopic composition near this 0% 0 value, from -10 to
+ 10% 0 (Figure 5), primarily because the rate of nitrogen supply often
limits reactions such as plant growth and bacterial mineralization. Under these
conditions all available nitrogen can be consumed without isotopic fractiona
tion. The rates of supply and amounts of substrate N are thus important in
understanding nitrogen isotopic distributions.
Some cumulative and large fractionations do occur in the nitrogen cycle. A
cumulative faster loss of 14N than 15N during particulate N decomposition in
soils (66) and in the sea (100) results in 15N increases of 5-10% 0 with
increasing depth. Nitrification and denitrification in the sea both proceed with
substantial isotope effects (D = 10-40% 0; 14,65,85), and where nitrate is
abundant, assimilation by phytoplankton proceeds with a smaller effect (D =
4 to 6% 0; 3,119). With two exceptions (24,86),nitrogen isotopic values in

lakes have received little study, although large contrasts might be expected
between lakes in which primary production is limited by N (no fractionation
by phytoplankton) vs P (abundant N � large fractionations during N uptake
by phytoplankton). Where phytoplankton have different 615N values than
terrestrial vegetation, the nitrogen isotopes may function as source markers
ATMOSPHERE
�
Stratospheric SO - +2.6 Background
-4
CONTINENTAL MARINE
PRECIPITATION PRECIPITATION
sot +1 to+7 �
SO - -+13
similar
Salt Marsh POM
Soi I Organic Matter -
+17to+2t
to
vegetation Plants �
SO - +21
LAKE OCEAN
Figure 6 The 834S distributions in ecosystems. See Figure 4 legend for explanation of symbols.
Sources: 8, 9, 13, 46, 52, 53, 54, 58, 77, 79, 91, 101.
for autochthonous and allochthonous organic matter. This approach has been
successfully applied in marine environments (90).
There is a wide range reported for nitrogen isotopic values for ammonium
0
and nitrate in precipitation from about -20 to + 10 /00 (Figure 5) (48, 75,
76). Some of the more negative values are related to soil and anthropogenic
emissions in highly industrialized areas (26,27). Further study may show that
stable isotope studies are helpful in identifying the sources and fates of N that
human activities are currently adding to many forests and lakes.
The Sulfur Cycle

Sulfate in the ocean is a large well-mixed sulfur reservoir whose isotopic
composition is 21 C>/ 00 heavier than primordial sulfur in the meteorite stan
dard, Canyon Diablo Troilite (96). Fixation of sulfate by phytoplankton
occurs with a small isotope effect (D = 1-2% 0; 53), but dissimilatory
sulfate. reduction in marine sediment occurs w.ith a large effect of 30--70% °
( 10, 38). Over geological time, and partially in response to global-scale

fluctuations in sulfate reduction activities, the a34s values of oceanic sulfate
have varied from about + 10 to +33% (77). Uplift and preservation-of marine
sulfides and sulfate-containing evaporites on land have produced a patchwork
of terrestrial environments, each with different S34S values for bedrock sulfur
(e.g. 46). Thus, large 834S ranges must be assfgned in general sulfur cycle
diagrams (Figure 6). In spite of this, continental vegetation seems to average
304 PETERSON & FRY
ne ar +2 to +6°/ 0 ° over l arge are as (13) and is quite distinct from the +1 7 -
to +21 °/ 0 0 v alues of m arine pl an kton and se aweeds.

The st able isotopic composition of sulfur entering the atmosphere c an also
be quite v ari able. For inst ance, S02 emissions from a sour g as pl ant in
Albert a, C an ad a v ary between +8 and +25°/ 0 0(58), but in e astern C an ad a
and the northe astern United St ates initi al studies show aver age ambient 834 S
v alues of 0 to 2°/ 0 0 for S02 (79, 101). The oxid ation of S02 to sulf ate
occurs with an over all inverse effect (D -4°/ 0 0 ) th at f avors concentr ation
=
of the he avy 34 S isotope in the product sulf ate; this inverse effect arises from
an e quilibrium step between S02 and H S03 - prior to fin al oxid ation to sulf ate
(1 01). Oxid ation of other sulfur-cont aining molecules also occurs with sm all
isotope effects, D < 5°/ 0 0 (37).
R ainf all sulf ate over the open oce ans h as a signific antly lower 834 S v alue
th an se a-spr ay sulf ate (-+ 13 vs +21°/ 0 0; 1 3), possibly bec ause of slow
oxid ation of reduced sulfur g ases (45). The isotopic compositions of these
g ases-H2S, c arbonyl sulfide and dimethyl sulfide- are poorly known, but
further study m ay cl arify the rel ative contributions of human vs n atur al
sources of these atmospheric sulfur compounds.
Stable Isotopes in Animals
Anim als are not represented in our C, N, and S di agr ams (Figures 4-6), but
they are import ant components of ecosystems. Anim als are simil ar in isotopic
compositions to their diets for c arbon and sulfur, but aver age 3 to 5°/ 0 0
he avier th an diet ary nitrogen (Figure 7). Diet-switching and turnover ex
periments for c arbon cle arly show th at the diet is the prim ary determin ant of
CARBON
·1 0
I 2 3 4 5 6 7 8 9 10
N
I�r I
+
i
SULFUR
I I I I
-3 ·2 -I 0 3 4 7 8 9 10
NITROGEN
I�r .+ IZ\
-3 -2 ·1
I J""RI
0 I 2 3 4 5 6 7 8 9 10I i
6{6ANuIAl-oo'ETl
Fif?,ure 7 Relationships between animal and diet isotopic compositions for carbon, sulfur and
nitrogen stable isotopes. Animals are on average only slightly enriched in ..,c and J4S by
0 . 2=/00 (have positive .1 values) vs their diets (arrows denote averages). A larger 3 . 2=/0<:>
average enrichment occurs for nitrogen isotopes due to excretion of i5N depleted nitrogen.
Sources: 3 1 , 35, 6 1 ,68, 69, 92.
STABLE ISOTOPES IN ECOSYSTEMS 30 5
animal isotopic compositions (34, 59, 114). For example, gerbils that were
switched from a -12.2"'/"'0 corn diet to a -21.8"'/00 wheat-based diet
approached the wheat carbon isotopic composition with time (14). This
should be true for sulfur as well, and also for nitrogen, with the caveat that
animals should be somewhat enriched in 15 N vs the new diet.
The 15 N enrichments vs diet are mainly due to excretion of isotopically
light nitrogen in urine. Initial studies with cows, fish, and zooplankton show
that animals and feces are enriched in 15 N vs the diet, but urinary nitrogen
(both NH3 and urea) is depleted in 15N (II, 12,69, 73, 109). For example,
cow urine is -I to -4°/",,,, depleted in 15 N vs diet; cow feces are -+2% 0
0
enriched in 15N, and milk and blood are +4 /00 enriched in 15 N (109). As
they must be to preserve mass balance, the urinary losses of 14 N are thus
offset by 15 N enrichments in other nitrogen pools.

When whole food webs are examined, differences between animal process
ing of C, N, and S isotopes stand out even more clearly. Nitrogen isotopic
0
values increase by 10 to 1 5 /00 in many food webs; these increases are due
to the presence of 3 to 5 successive trophic transfers, each of which effective
ly boosts the 15 N content by 3 to 5"'/ 0 0 (69). The opposite effect-no change
with increasing trophic level-is observed for sulfur (68, 92), making the
sulfur measurements particularly good indicators of which plant or bacterial
food sources are most important for consumers. Carbon appears to be in
termediate between N and S, showing modest increases between 0.0 and
1.00/00 per trophic level (19, 3 5, 36). This small enrichment may be due to
carbon isotopic fractionation during assimilation or respiration. The distinct
behavior of each isotope allows a cross-referenced trophic structure analysis
through combined C, N, and S measurements (32, 91).
Although diets control the overall isotopic compositions of animals, con
siderable isotopic variation still exists among different tissues and metabolites
within individual animals. The bone protein collagen, for instance, is 2 to
6"'/00 enriched in 13 C vs the diet, while lipids in fat reserves are 2 to 80/00
depleted in J3 C (87, 117). These enrichments and depletions arise during the
many internal enzymatic steps that fractionate stable isotopes after dietary
uptake in animals (I, 102, 123). Use of stable isotopes to study diets is based
on use of animal tissues that bear a fixed isotopic enrichment or depletion vs
the diet. In some cases, whole animals are used, while in others, analyses of
muscle or protein fractions have proven adequate indicators of diet. These
analyses complement other methods of studying diets in that the stable
isotopic compositions of tissues are a measure of the assimilated (not just
ingested) diet, reflect both long-term and short-term diets in slow and fast
turnover tissues, and provide a unique way to study food webs of the past,
detrital food webs, and diets of animals that are hard to observe. Two of our
case studies illustrate how stable isotopes can be used to reconstruct diets
when other direct dietary information is lacking.
306 PETERSON & FRY
CASE STUDIES
Rather than attempting an exhaustive review o f a rapidly growing field, we

have chosen five case studies to illustrate how ecosystems scientists are
currently using stable isotopes as natural tracers. These studies show that
stable isotopes are being used to indicate sources ( N2 fixation, archaeology,
detrital food webs), to help estimate large-scale fluxes (global carbon), and to
discern how sul fate loading a ffects an important decomposition process in
lake sediments (acid deposition in lakes). This wide variety o f applications is
remarkable but represents only a small part o f the spectrum o f current uses of
stable isotopes.
8/5N Measures of N2 Fixation

Nitrogen stable isotope measurements can be used to estimate plant fixation o f

atmospheric Nz. Plants fixing N2 from the atmosphere have 8 15 N values o f
about -2 to +2% 0, close to the 0% 0 value o f atmospheric N2 (107).
Plants that cannot fix Nz from the atmosphcre have 815 N values that are
usually closer to those o f total nitrogen in soils and vary widely from 8 to -
+ 100/00, depending on location (66, 107; K. Nadelhoffer & B. Fry, un

published). For plants whose nitrogen source is unknown, values close to
0% ° may indicate strong reliance on Nz derived from the atmosphere
( Nd fa)., e�pecially i f soil organic nitrogen has a 815 N value very di fferent from
0% 0' An agricultural experiment with soybeans illustrates this approach
(Figure 8). Nodulating soybeans grown hydroponically in greenhouse trials
had values o f + 1 0/0 for total plant N, but in field planting experiments,
c>
nodulating soybeans had values close to those o f re ference plants that did not
fix Nz (in this case, the re ference plants were soybeans that lacked Nz- fixing
SOYBEAN O'5N
3 4 5 6
I i I I
N2 FIXING PLANTS
Hydroponic
Corn Cobs Added
No Corn Cobs
REFERENCE PLANTS
Corn Cobs Added
No Corn Cobs
100%
N2 FIXATION 0%
Figure 8 The nitrogen stable isotopic composition of nitrogen in soybeans depends on cultiva
tion conditions. Soybean S'5N varies according to the fraction derived from the atmosphere vs
soils (reference plants). Sources: 56. 57.
nodules). Presumably, the nodulating soybeans derived most of the nitrogen

from the soil, as did reference plants. Addition of com cobs changed these
results. Com cobs provide a rich carbon source for soil microorganisms that
deplete available nitrogen in the soil. Enhancement of microbial growth in
soils sets up a competition for soil nitrogen stocks so that plants capable of
fixing atmospheric N2 may increasingly do so. The lower S15N values of
soybeans grown in com-cob amended soils are consistent with a greater
dependence on atmospheric nitrogen (Figure 8).
This natural abundance method of measuring the fixation of atmospheric
nitrogen has been extensively tested against other methods and appears
accurate at the 5 to 15% level in many situations (107). Simply collecting

leaves of presumed N2-fixers and reference plants to estimate in situ patterns
of N fixation is a nonmanipulative procedure that has great simplicity and

intrinsic appeal for ecosystems studies. Interesting results have been found in
comparative field studies. For instance, recent findings show that presumed
N2 fixers can range widely in their reliance on Ndfa in different habitats
(108). The extent to which Ndfa enters and contributes to nutrition of neigh
boring reference plants, and also acts as a source of new nitrogen in ecosys
tems, has not been fully explored in spite of some initial' attempts (7, 64).
The Global Carbon Cycle and the CO2 Problem
Carbon isotope research is making substantial contributions to understanding

the factors controlling the CO2 balance in the atmosphere. While it is well
known that the CO2 content of the atmosphere has been increasing steadily in
r ecent decades, the relative importance .of CO2 from combustion of fossil
fuels and from oxidation of forest and soil organic matter in causing this rise
has been debated (47). While the fossil fuel CO2 emission history is known
fairly well, the timing and amount of carbon dioxide releases from burning
and decay of terrestrial organic matter is not. However, the addition of
terrestrial CO2 to the- atmosphere can be calculated through use of carbon
cycle models that incorporate measurements of the time-course and magni
tude- Qf the changes in I3C content of atmospheric CO2 from 1800 to the
present.
The approach uses the fact that the addition of large quantities of CO2 from
both fossil fuel combustion (o13C --27% 0) (110) and oxidation of terres
trial organic matter (S\3C --28% 0) has. lowered the a\3c values of
atmospheric CO2 (S13C �-7% 0). Since the time course and amount of
fossil fuel use are well known (98), it is possible to calculate by difference
both the time course and the magnitude of release of terrestrial biomass
carbon to the atmosphere. The calculations require both an accurate time
course of atmospheric SJ3C values and the use of models of the carbon cycle
308 PETERSON & FRY
since atmospheric CO2 exchanges continuously with oceanic CO2 and

biospheric carbon.
Carbon isotopes in tree rings have been analyzed as a surrogate to measure
trends in a13c values of atmospheric CO2, While different trees show a wide
variability in their isotopic records due to climatic and physiological factors,
the grand average of many tree-ring records indicates a 1.5°/<><> decrease in
tree ring 513C values from 175 0 to 198 0 (Figure 9) (88). The inference is that
atmospheric 513C values have also gradually declined from 180 0 to 195 0 and
declined more rapidly since 1950. Recent analyses of atmospheric CO2
trapped in Antarctic ice cores have supported the approximate timing and
magnitude of the atmospheric al3c changes deduced from tree ring analysis
(29). The interesting point is that the initial decline in atmospheric 513C
values was occurring during the 1800s well before the major upswing in fossil
fuel use. This has been attributed to a long-term and large-scale release of
l3C-depleted CO2 caused by the clearing and burning of forests and oxidation
of soil organic matter (a13C -28% 0)' The more rapid recent al3c decrease
correlates with the increase in fossil fuel use.
Through use of carbon cycle models, the time course and amount of
biospheric carbon release required to account for the observed tree ring a13c
decrease have been computed (88, 89, 110). The calculations are sensitive to
small changes in the 13C trends, but the general conclusions are (a) that
0.0 -------_--=:-ModeJ Fossil

-- .... Fuel
-0.4 ',Only
� ,
u
-0.8 ,
"<J \
-1.2
-
1 .6
1780 1820 1860 1900 1940 1980
5.0 ;"
,
'"
4.0
Fossil Fuel .
'!!g
-
'"
3.0
�:'
OJ 2.0
!:i
8
1.0
YEAR
Figure 9 Top. The changes in aI3c values (.1 from historical tree ring baseline) observed in tree
rings from 1870 to 1980 (solid line) and the calculated change expected due solely to increased
fossil fuel use (dashed line). Note the decline in I3C (declining .1 value) in tree rings prior to the
decline expected from fossil fuel use. The difference between the two lines may be due to carbon
release from terrestrial biomass and soils accompanying clearing of forests and prairie (88).
Bottom. The time course of fossil fuel CO2 emission (98) and, using /)I3C data, the calculated
biospheric CO2 emissions from terrestrial soils and forests (88).
carbon inpu t from the terres trial carbon s tocks to the a tmosphere was grea tes t
be tween 184 0 and 194 0 bu t (b) tha t af ter 1958 fossil fuel became the
predominan t cause of the a tmospheric CO2 increase (Figure 9; 88 ). The to tal
in tegra ted CO2 inpu t from each of the two sources un til 198 0 was abou t equal,
rou ghly 14 0 X \ 09 tons from the biosphere and 17 0 X \ 09 tons from fossil
fuels, according to recen t model calcula tions (88) . This model allows back
calcula tion of the preindus trial a tmospheric CO2 level tha t provides the bes t
fi t to bo th the isotopic trends and the recen tly measured a tmospheric CO2
values. The bes t es tima te of 266 ppm is consis ten t wi th ice core values of 258
to 289 ppm (28).
This example illus tra tes the usefulness of the iso topic tracer approach for
solving mass balance problems, especially where a well-mixed reservoir such
as the global a tmosphere can be sampled over time. Al terna tive me thods of
calcula ting the loss of biospher ic carbon through analysis of land-use pa tterns
and defores ta tion are uncertain due to the lack of accura te his torical land-use
records (49 ). The exis tence of two independen t me thods of compu ting
changes in biospheric carbon s tocks (8uC vs his torical land use records) is
impor tan t considering the urgency of gaining accura te unders tanding of the
con trols of a tmospheric CO2 levels.
Sulfur and Acid Deposition
Human per turbation of the na tural sulfur cycle is pronounced, as the majori ty
of sulfur curren tly emi tted in to the a tmosphere is probably an thropogenic in
origin (4; R. Howarth, personal communica tion). An thropogenic sulfur emis
sions ( SOz, S03, SO l - ) have increased drama tically wi th indus trializa tion,
and these changes have been recorded by changes in the sulfur con ten t of lake
sedimen ts. The studies of Canadian lakes by Jerome Nriagu and colleagues
illus tra te these changes ( 78, 79, 8 0, 8\ ).
A very large smel ter of copper-nickel sulfide ores loca ted in Sudbury,
On tario, has accoun ted for about 2 0% of to tal Canadian S emissions. Sudbury
smel ters began opera tion in abou t 1889, and sharp increases in the percen tage
of sulfur in the sediments of nearby lakes have been dated to the 1880-1890
horizons (8 0 ). The iso topic composi tion of the sulfur in lake sedimen ts has
also changed since the 1880s (Figure 1 0 ). The weigh ted average S34 S value of
sulfur in ores from seven mines in the Sudbury area is +2.1°/00 (range =
0.5 to 7.2°10 0; 1 05 ), and this is sligh tly deple ted in 34 S rela tive to sulfur
collec ted from chimney s tacks, precipi ta tion, lake wa ter, and older pre
indus trial lake sediments tha t all average abou t 4-5°100 in and near Sudbury
(78, 79, 8 0 ). Simple addi tion of o re-derived sulfur should only sligh tly
0
depress 834 S values in the Sudbury area towards the +2.1 1 00 average value
of ore sulfides,bu t in fac t much larger 34 S deple tions of -3 0°/0 0 have been
found in sulfur from recen t lake sedimen ts.
310 PETERSON & FRY
Analysis of the chemical forms of the sulfur in recent sediments provided a

key to understanding how additions of sulfur at +2 to + 5°/ 0 0 could lead to
-10 to - 30% 0 values in surface sediments of lakes. Reduced sulfur
species (HzS, So, and pyrite) characteristically formed during dissimilatory
sulfate reduction have been found in large quantities in two of the Sudbury
lakes (81). Bacterial sulfate reduction in these lake sediments appears to be
stimulated by atmospheric sulfate additions; low sulfate levels in lake water
normally limit sulfate reduction. Increased sulfate loading stimulates sulfate
reduction, increases the production of 34S depleted sulfides, and since sulfides
react with iron and organic matter in sediments, results in decreases in the
S34S value of total sulfur in lake sediments. The decrease in lake sediment
S34S is thus not primarily due to a change in the isotopic composition of
source sulfur but rather to changes at the process level as sulfate reduction is
stimulated.
As in the preceding example of S13C and global CO2 changes, this sulfur
case study shows that isotopic measurements can be used to identify fluxes of
anthropogenic pollutants. However, because sulfate concentrations limit an
important ecosystem process (sulfate reduction), the sulfur isotopic response
is not governed by simple mixing as was the case for anthropogenic CO2
additions. Models that relate sulfur isotopic distributions in lake sediments to
increased sulfate loading are rudimentary at this time ( 3 3), but further de
velopment and testing should improve our understanding of long-term
changes in both sulfate reduction activities and historical rates of an
thropogenic sulfate loading in lakes.
'loS .:; '·s

0.0 0.2 0.4 0.6 0.8 1.0 -to -5 0 5 to
0 � 0
'\- <---,::-'
to �) to )
] 20
\ 20
:I:
f--
Cl.
4.J 30 i Pristine
Lake 30
J
C>
40 I 40
i Sudbury
50 ! Lake 50
60
\ 60
Figure 10 Sedimentary sulfur profiles differ between a pristine lake in western Ontario and a
lake with high sulfate loading near Sudbury, Canada. Triangles denote lake water sulfate 834S
values. The increases in %S and decreases in 834S in the Sudbury lake contrast strongly with the
uniform vertical profiles from the pristine lake. Increased sulfate loading from smelter activities
at Sudbury has led to production and storage of 34S-depleted sulfides in lake sediments, causing
the recent increases in %S and decreases in 1)34S of sediments. Sources; 80, 81.
75
-10
-12 �. ...
I
50 a"
-14
I w
N
J
-16 Ci
:;:
� 25
-18
j;>
"<>
�,'I'
-20
0
-22 -T-----I--1 ---------
-24
-26
-28
3000 2000 1000 0 1000
• 8.C. A.D.-
YEAR
Figure 11 Change in diets of North American Indians are recorded in (iJ3C contents of the
collagen bone protein. Older collagen averages - 2 1 .5% 0 , about 5=/00 enriched in I3C
relative to common C, plants that average -26.5=/ (117). With the introduction of maize,
==
13C contents rise to -- 1 I =/ <:> 0' indicating a 60% reliance on this C4 species (a 100%
dependence would produce a -4=/00 813C value for collagen). Sources: 1 1 6, 1 1 7, 1 07.
StabLe Isotopes in ArchaeoLogy
The study of human diets in ancient settings is a key to understanding both

cultural evolution .and human modification of ancient ecosystems. For ex
ample, a civilization that relied heavily on com was probably organized
around farming practices and differed in social s tructure and land use from a
hunter-gatherer civilization. Archaeologists glean evidence about ancient
diets from charred remnants of foods and from s keletons. Stable isotopic
s tudies have been used to quantify prehistoric human diets and have proven
valuable supplements of the more qualitative visual estimates.
A case in point is the use of bone collagen ('j13C to document the transition
to maize cultivation by North American Indians (Figure II). Collagen ex
tracted from Indian bones averaged 21 to - 22% 0 from3 0 0 0 Be to 5 0 0AD,
-
but underwent a rapid increase in l3C to - II0/0 0 by 13 0 0 AD. This

-
increase s tems from the advent of widespread maize cultivation by the Upper
Mississippian Indians, and the 13C increase is such that -60% of the dietary
carbon was derived from maize. This finding is interesting because traces of
maize plants were found in earlier sites and might have been judged impor
tant. However, the isotopic analyses of collagen from those earlier peoples do
not show values expected for a dietary dependence on maize or maize-fed
animals. This supports the idea that for these earlier peoples maize was a
312 PETERSON & FRY
minor dietary item whose presence was probably due to an extensive trade
network ( 1 1 8) .
Subsequent archaeological investigations have been extended to coastal
areas where marine and terrestrial foods differ in both C and N stable isotopic
compositions, with marine foods being relatively enriched in both l 3C and
ISN. Counterintuitive results have sometimes emerged from those in
vestigations . For example, prehistoric humans living within I km or so of
coastal waters might be expected to depend heavily on marine foods , but this
has not always been the case. Analyses of collagen from skeletons of pre
historic Danish coastal dwellers showed that mesolithic Danes (before 4000
Be) had relatively heavy C and N isotopic compositions ( � - 1 2% 0 813C,

�+ 1 4% 0 8 1 5N ) , reflecting a consumption of predominantly marine foods .
0
Postmcsolithic Danes had substantially lightcr C and N values ( � - 20 /0 0

(j I 3C , � +9% o (j15N: 1 03 , 1 1 2 ) . The isotopic shifts near 4000 Be are
consistent with shifts from an early subsistence-level marine-based ecology to
that involving increased agriculture and trade. Farming and trade items
apparently came to constitute the bulk of the diet of even the coastal Danes
after about 4000 Be ( 1 1 2) .
The use o f stable isotopes i n anthropology has thus led to a more quantita
tive understanding of food webs and civilizations from the last 6000 years .
Stable isotope studies may be extended to decipher the dietary basis of human
subsistence for other areas and times where archaeological evidence is much
less extensive. Caution must be exercised in selection of samples and in
terpretation of results , however, as structural analyses show that collagen in
bones slowly degrades and undergoes replacement, sometimes resulting in
large C and N isotopic changes (20, 2 1 , 42) . Uses of stable isotopes In
archaeology have been the subject of two excellent reviews ( 1 8 , 1 1 7).
Detrital Organic Matter in Salt Marshes

The need for chemical tracers of organic matter now and trophic relationships
is greatest in ecosystems dominated by detritus because the origins of detritus
can not be determined visually. Tidal salt-marsh estuaries contain vast areas
of highly productive salt-marsh grasses, often predominantly Spartina alter
niflora. Large amounts of detrital Spartina become available to the de
composers and detrital food webs, and it has long been thought that export of
this detritus is l argely responsible for the high secondary productivity of
salt-marsh estuaries (82 , 1 1 3 ) .
One way t o test the hypothesis that Sparlina detritus is the dominant source
of organic matter in estuarine waters and for consumers is through stable
i sotope analysis . Sparlina is enriched in 1 3C ( li 1 3C - 1 3% 0) relative to
0 0
either plankton ( -22 /0 0) or upland C-3 plants ( - 28 /0 0) . Haines (39) was
ST ABLE ISOTOPES IN ECOSYSTEMS 313
the first to point out that seston in tidal creeks at Sapelo Island, Georgia was
not isotopically simi l ar to Spartina but was in the range expected for organic
matter derived from phytoplankton. Subsequent studies of consumers in
dicated that filter feeders such as the oyster (Crassostrea virginica) also had
8 1 3C values more similar to plankton than to Spartina . Other consumers such
as ribbed mussels had (5\3C values intermediate between plankton and Sparti
na (40, 72) .
The carbon isotope data provided strong evidence that Spartina was prob
ably not the primary source of detritus or of food for filter feeders in Sapelo
Island salt-marsh creeks. However, since other sources of organic matter,

such as benthi c algae ( - 1 7 % 0) or upland organic matter ( - 28% 0)
carried by rivers , might be present , the 813C values could not identify the
origin of the detritus unambiguously. This is a common problem of isotopic

tracer studies when more than two sources are present and the sample has an
intermediate isotopic value .
One way of i ncreasing the abi l ity to identify organic matter sources is to
employ simultaneously additional tracers such as sulfur and nitrogen isotopes .
In marshes and estuaries , sulfur is especially appropriate because upland
plants, marine phytoplankton, and Spartina have different 834S values reflect
ing their different sources of sulfur. Phytoplankton use seawater sulfate
( + 2 1 % 0), whereas Spartina also uses 34S-depleted sulfi des which are
produced via sulfate reduction in anoxic sediments (8). Upland plants obtain
sulfates from precipitation or weathering and often have 834S values in
termediate between Spartina and phytoplankton. A plot of a34s versus 8 13e
for organic matter producers in and near Sippewissett salt marsh on Cape Cod
illustrates the clear two-dimensional separation (analogous to a two
dimensional chromatograph) that can be achieved in favorable circumstances
with this dual isotope approach (Figure 12 ). Analyses of pooled samples of
ribbed mussels from nine locations along an ocean-to-i nner marsh transect
demonstrated that the isotopic composition of these filter-feeding mussels was
a function of location where the organisms grew. Mussels col lected near
the ocean were isotopically similar to plankton, whereas mussels from the
smallest creeks and the marsh surface were isotopically similar to Spar
tina. The food resources available to mussels at various sites in the marsh
appeared to be determined in l arge part by the geometry and physical char
acteristics of the ecosystem. Transect sampling of stable isotopes in sedi
ments, plants, and animals can be a powerful way to define gradients and
boundaries of biogeochemical processes and cycles that are not otherwise
apparent.
The multiple isotope approach might be carried further through addition of
more isotopes or other types of tracers. For example, if carbon and sulfur
314 PETERSON & FRY
20 Plank Ion
10
o
- 10 I...-----I____--l____---l
-30 - 20 - 10
O'3C
Figure 12 The I}l3e and 1}34S values for upland plants, plankton and Spartina alterniflora at
Sippewissett salt marsh. The numbers 1-9 indicate the isotopic composition of filter-feeding
ribbed mussels, Geukensia demissa, collected along a transect from the inner marsh ( 1-4) to the
ocean (9). Source: 9 1 .
isotopes can identify the ultimate sources of the or ganic matter, the BI5N
value could give an estimate of trophic level. At our present level of un
derstanding, there are problems in doing this. For example, there are potential
foods in estuaries such as benthic microal gae that have not been well charac
terized isotopicall y , and there are sometimes changes in B'5N values of
detritus as it ages ( 1 24). Nonetheless, the use of multiple tracers has si gni fi
cantly increased our ability to trace or ganic matter flo ws in the detrital food
webs of marshes and estuaries. Determining the importance of marsh grass
production for secondary production in estuaries is critical because of the
intense development pressures on coastal ecosystems, and stable isotopic
tracer studies can help evaluate these relationships.
CONCLUSIONS
Stable isotope tracers are already present and circulating in natural systems,
and their natural distribution reflects an inte grated history of physical and
metabolic processes withi n ecos ystems. As our case studies sho w, the ma jor
advantage of the stable isotope approach lies in field studies where measure
ments of existin g isotopic distributions sho w ho w components o f ecosystems
are co nne cted. Where clear-cu tti ng, fer tiliza tio n, bur ni ng, or o ther k inds of
ecosys tem -level pertur ba tio ns al ter flows of eleme nts , s ta ble iso to pes ca n be
used to follow these cha nges a nd show whi ch pro cesses or com po ne nts are
mos t se nsi tive to pe rturba tio n.
I t is o ften im possible to jud ge on theore ti cal grounds alone whe ther or no t
s table iso to pes will be useful i n solvi ng a pa rticula r field research problem.
However, by a nalyzi ng a few carefully sele cted sam ples, o ne ca n o fte n
de termi ne whe ther fur ther a nalyses wi ll co ntribu te si gnifi ca ntly to a solu tio n.
One ini tial obje ctive is to de termine the si gnal- to-noi se ra tio. If iso to pi c
differen ces be twee n pools are ver y l ar ge a nd the varia tio n wi thi n pools i s
small, iso to pes may provide a very powerful tool, a nd a few sam ples may
be very effe ctive. For exam ple, i t is easy to dis ti nguish be twee n C4
( ll 1 3C - 1 3% 0) a nd C 3 ( o 1 3C - 28% 0) pla nts usi ng s table C iso to pes. O n

the other hand , i t would be very diff icul t to es ti mate nitrogen fi xa tio n usi ng
the 8 1 5N tech nique where soil or ga ni c ma tter is a bou t +2°/ 0 0 si nce a tmo
s pheri c N 2 is 0% 0. It would be far b etter to choose a n e cosys tem where the
soil or ga nic ma tter had 815N values o f +6 to + 1 00/e e which co ntras t
s tro ngly with the atmos pher ic value.
Measureme nts of iso to pic com posi tio ns of s ta ndi ng s to cks need to be
bala nced by pro cess s tudies tha t de fine fra ctio na tio ns u nder na tural co ndi tio ns
in e cosys tems ; the iso to pi c com posi tio ns of pools are de termined no t only by
i npu ts bu t also by a ny iso to pic fra ctio na tio n occur ri ng duri ng efflux of
ma terials. Pre cise u nders ta ndi ng of iso to pic frac tio na tio n allows jud gme nt as
to whe n the s ta ble iso to pes reco rd so urce i nforma tio n a nd whe n they record
process i nforma tio n. It is this com bi na tio n of source a nd process i nforma tio n
e ncoded i n the na tural dis tributio ns of s ta ble iso to pes tha t make these
measureme nts valua ble i nde pe nde nt i ndi ca tors of C , N , a nd S cy cli ng i n
e cos ys tems.
The s pecial ized chem ical k nowled ge a nd the so phis tica ted a na ly tica l equip
me nt required for iso to pe de termi na tio ns has resul ted u ntil now i n a par tial bu t
real se gre ga tio n of iso to pe s tudies f rom o ther ecolo gica l i nves ti ga tio ns . A
produ ctive develo pme nt for the fu ture would be an in creasi ng in te gra tion of
s ta ble iso to pe informa tio n i nto a varie ty of e cosys tem s tudie s .
ACKNOWLEDGMENTS
The au thors tha nk Luis Cifue ntes, Jo n Cole, David De Ma ra is , Marily n Fo gel,
Anne Gi bli n, Ro ber t Howa rth , Da niel Kohl, and Geor gia Shearer for com
me nts o n i ni tial dra fts of this ma nus cri pt. We also tha nk the ma ny s cie ntis ts
too numer ous to lis t i ndividually who provided re pri nts, theses, commen ts,
a nd ideas for our co nsidera tio n. This effor t was su ppo rted by the Ecosys tems
C enter, Ma ri ne Biolo gical La bora tory, Woods Hole, MA.
31 6 PETERSON & FRY
Literature Cited
I . Abelson, P. H., Hoering, T. C. 1961. 14 . Cline, J. D . , Kaplan, I. R. 1975. Isotop
Carbon isotope fractionation in forma ic fractionation of dissolved nitrate dur
tion of amino acids by photosynthetic ing denitrification in the eastern tropical
organisms. Proc. Natl. Acad. Sci. USA north Pacific Ocean. Mar. Chern. 3 :
47 : 62 3-32 27 1-99
2. Aller, R. C. 1986. Anoxic oxidation of 15. Craig, H. 1957. Isotopic standards for
sulfides in marine sediments. Eos carbon and oxygen and correction fac
67:996 (Abstr.) tors for mass spectrometric analysis of
3. Altabet, M. A . , McCarthy, J. J . 1985. carbon dioxide. Geochim. Cosmochim .
Temporal and spatial variations in the Acta 12:133-49
natural abundance of 'SN in PaN from a 16. Degens, E. T. 1 969. Biogeochemistry of
warm-core ring. Deep-Sea Res. 32:755- stable carbon isotopes . In OrganiC
72 Geochemistry, ed. G. Eglington, M. T.

4. Anderson, J. W. 1 97 8 . Sulphur in biolo J. Murphy, pp. 304-29. Berlin:
gy. Inst. Bioi. Stud. Bioi. No. IOJ . 60 Springer-Verlag
pp. 17. Deines, P. 1980. The isotopic composi
5. Anderson, T. F . , Arthur, M. A. 1983. tion of reduced organic carbon. In Hand

S table isotopes of oxygen and carbon book of Environmental Isotope Geo
and their application to sedimentologic chemistry. Vol. I., ed. P. Fritz, J. Ch.
and paleoenvironmental problems. In Fontes, pp. 326-406. Netherlands: Else
Stable Isotopes in Sedimentary Geology. vier Sci. Pub!.
ed. M . A. Arthur, T. F. Anderson, I. R. 18. DeNiro, M. J. 1987. Stable isotopy and
Kaplan, J. Veizer, L. S. Land , 1 : 1-1 51. archaeology. Am. Sci. 75: 1 82-9 1
Dallas: Soc. Econ. Paleontol. Mineral. 1 9 . DeNiro, M. J . , Epstein, S. 1978 . In
6. Benner, R . , Fogel, M . • Hodson, R . , fluence of diet on the distribution of car
Sprague, K . 1986. Depletion of J3C in bon isotopes in animals. Geochim. Cos
the lignin fraction of plants: Implications mochim. Acta 42:495-506
for source identification of detritus. Eos 20. DeNiro, M. J . , Epstein, S. 198 1 . In
67 :990 (Abstr.) fluence of diet on the distribution of ni
7. B inkley, D., Sollins, P. , McGill, W . B . trogen isotopes in animals. Geochim .
1985. Natural abundance o f nitrogen-15 Cosmochim . Acta 45:34 1-5 1
as a tool for tracing alder-fixed nitrogen. 21. DeNiro, M. J . , Schoeninger, M. J . ,
Soil Soc. Am . J. 49:444-47 Hastorf, C . A . 1985 . Effect o f heating
8. Carlson, P. R. Jr. , Forrest, J. 1982. Up on the stable carbon and nitrogen isotope
take of dissolved sulfide by Spartina ratios of bone collagen. J. Archaeol.
alterniflora: Evidence from natural sul Sci. 12: 1-7
fur isotope abundance ratios. Science 22. Dzurec, R . S., Boutton, T. W . , Cald
2 1 6:633-35 well, M. M . , Smith, B. N. 1985 .
9. Castleman, A. W. Jr. , MUnkelwitz, H . Carbon isotope ratios of soil organic
R . , Manowitz, B . 1974. Isotopic studies matter and their use in assessing
of the sulfur component of the community composition changes in Cur
stratospheric aerosol layer. Tellus 26: lew Valley, Utah. Oecologia 66: 1 7-
222-34 24
10. Chambers, L. A., Trudinger, P. A. 23. Epstein, S . , Buchsbaum, R . , Lowen
1 979. Microbiological fractionation of starn, H. A . , Urey , H. C. 1953.
stable sulfur isotopes: A review and cri Carbonate-water isotopic temperature
tique. Geomicrobiol. J. 1 :249-93 scale. Bull. Geol. Soc. Amer. 64: 1 3 1 5-
I I . Checkley, D. M. Jr. , Entzeroth, L. C. 26
1985. Elemental and isotopic fractiona 24. Estep, M. L. F . , Vigg, S. 1985. Stable
tion of carbon and nitrogen by marine, carbon and nitrogen isotope tracers of
planktonic copepods and implications to trophic dynamics in natural populations
the marine nitrogen cycle. J. Plankton and fisheries of the Lahontan Lake Sys
R es . 7:553-68 tem, Nevada. Can . J. Fish. Aquat. Sci.
12. Checkley, D. M. Jr. , Miller, C. A . 42: 1 7 1 2-19
1 986. Nitrogen isotope fractionation by 25 . Farquhar, G . D., O'Leary, M . H.,
oceanic zooplankton. Eos 67:988 Berry, J . A. 1982. On the relationship
(Abstr.) between carbon isotope discrimination
13. Chukhrov, F. V . , Ermilova, L. P . , and the intercellular carbon dioxide con
Churikov, V . S . , Nosik, L. P. 1980. centration in leaves . Aust. J. Plant Phy
The isotopic composition of plant sulfur. siol. 9 : 1 2 1-37
Org. Geochem. 2:69-75 26. Freyer, H. D. 1978. Preliminary 15N
studies on atmospheric nitrogenous trace analyzed using DCI'2C ratios . t;cology

gases. Pageoph 1 1 6:393-404 60:48-56
27 . Freyer, H . D. 1 97 8 . Seasonal trends of 4 1 . Halas, S" Shakur, A . , Krouse, H . R .
NH4 + and NO, - nitrogen isotope com 1 982. A modified method o f S02 extrac
position in rain collected at Hilieh, Ger tion from sulphates for isotopic anal y sis
many. Tellus 30:83-92 using NaPO,. /sotopenpraxis 1 8 433-35 :
2 8 . Fricdli, H . , Moor, E . , Oeschger , H . , 42. Hare, P. E . , Estep, M . L F. 1983. Car
S iegenthaler, U . , Stauffer, B . 1 984. bon and nitrogen isotopic com position of
1 3C! 1 2C ratios in CO, extracted from amino acids in modern and fossil col
Antarctic ice. Geophy� . Res. Lett. I I : lagens. Carnegie Inst. Wash. Yrbk.
1 145-48 1 982-1 983 4 1 0- 1 4
29. Friedli , H . , Lotscher, H . , Oeschger, H . . 43 . Hartmann, V . M . , Nielsen. H . 1 969.
S i eg en tha l er , U . , Stauffer, B . 1 986. Ice il34S-werte in rezenten meeresse
core record of the 13C! 12C ratio of atmo diment en und ihre deutung am be ispiel
spheric CO2 in the past two centuries. einiger sedimentprofile aus der west
Nature 324:237-38 lichen ostsee. Geol. Rund. 58:62 1 -55
30. Fritz, P . , Drimmie, R. J . , Nowicki, V . 44. Hayes , 1. M. 1 98 3 . Practice and princi
K . 1 974. Preparation o f sulfur dioxide ples of isotopic measurements in organic
for mass spectrometer analyses by com geochemistry. In OrKanic Geochemistry

bustion of sulfides with copper oxide. of Contemporaneous and Ancient Sedi
Anal. Chern . 46: 1 64--66 ments. ed. W. G . Meinschein , 5 : 1 -3 1 .
3 1 . Fry, B. 1 98 1 . Tracing shrimp migra B loomington. [nd: Great Lakes Sect . ,
lions and diets using natural variations Soc. Econ. Paleontol . Mineral.
in stable isotopes. PhD thesis. Univ. 45. Hitchcock, D. R . , Black, M. S . 1 984.
Tex . , Austin. 225 pp. 34S/32S evidence of biogenic sulfur ox
32. Fry, B . 1 98 3 . Fish and shrimp migra ides in a s al t marsh at mos phere . A rmos.
tions in the northern Gulf of Mexico Environ. 1 8 : 1 - 1 7
analyzed using stable C , N and S i so 46. Hitchon , B . , Krouse, H . R . 1 972. Hy
tope ratios. Fish. Bull. U.S. 8 1 :789- drogeochemistry of the surface waters of
80 1 the Mackenzie River drainage basin,
3 3 . F ry , B . 1 986. Stable sulfur isotopic dis Canada-III . Stable isotopes of oxygen ,
tributions and sulfate reduction in lake carbon and sulphur. Geochim . Cos
sediments of the Adirondack Mountains, mochim. A cta 36: 1 337-57
New York . Biogeochemistrv 2 : 329-43 47. Hobbie, J . E" Cole, J . , Dungan, I . ,
34. Fry, B . , Arnold, C . 1 982. Rapid !.lCI Houghton , R . A . , Peterson , B . J . 1 98 4 .
1 2C turnover during growth of brown The controversy on the role of the biota
shrimp (Penaeus aZlccus). Oeeologia in the global CO2 balance. BioScience
54:200--04 34:492-498
35. Fry , B . , Sherr , E. B . 1984 . (l13C 48 . Haering , T. 1 957. The isotopic com
measurements as indicators of carbon position of the ammonia and the nitrate
tlow in marine and freshwater ecosys ion in rai n . Geochim . Cosmochim . Acta
tems. Collfrib. Mar. Sci. 27: 1 3-47 1 2:97- 1 02
36. Fry, B . , Macko, S . A . , Zieman, I. C . 49 . Houghton, R. A . , Hobbie, I . E . , Melil-
1 987. Review of stable isotopic in 10, 1 . M . , Moore, B . , Peterson , B. J . , et
vestigations of food webs in seagrass al. 1 98 3 . Changes i n the carbon content
meadows . In Froc. Subtropical-Tropical of terrestrial biota and soils between
Seagrasses of the Southeastern U.S. , ed. 1 860 and 1 980: A net release of CO, to
M. Durako, R. Lewis, R. C . Phillips. the atmosphere. Ecol. Monogr. 53 : i 3 5-
Fla. Mar. Res. Pub!. 42. In press 62
37. Fry, B . , Cox, 1 . , Gest, H" Hayes, J . M . SO. Jorgensen, B . B. 1 979. A theoretical
1 986. Discrimination between 34S and model of the stable sulfur isotope dis
32S during bacterial metabolism of in tribution in marine sediments. Geochirn .
organic sulfur compounds . 1. Bacteriol. Cosmochirn . Acta 43:363-74
1 65:328-30 51. 1unk, G . , Svec, H. 1 958. The absolute
3 8 . Goldhaber, M. B . , Kapl a n , I. R. 1 975. abundance of the nitrogen isotopes in the
Controls and consequences of su lfate atmosphere and compressed gas from
reduction rates in recent marine sedi various sources. Geochim. Cosmochim.
ments. Soil Sci. 1 1 9:42-55 A cta 1 4:234-43
39 . Haines, E. B . 1 977. The origins of de 52. Kaplan, I. R. 1 98 3 . Stable isotopes of
tritus in Georgia salt marsh estuaries. sulfur, n i troge n and deuterium in recent
Oikos 29:254-60 marine environments. In Stable Isotopes
40. Haines, E. B . , Montague, C . L 1 979. in Sedimentary Geology, ed. M. A.
Food sources of estuarine invertebrates Arthur, T . F . Anderson , I . R . K ap lan , J .
3 18 PETERSON & FRY
Veizer, L. S. Land, 2 : 1 - 1 08 . Dallas: ing Pasture Management, 6 1-77. Vien

Soc. Econ. Pa1eontol. Mineral. na: Int. Atomic Energy Agency
53. Kaplan, I. R . , Rittenberg, S . C. 1 964. 65 . Mariotti , A . • Lancelot, C . • B illen, G .
Microbiological fractionation of sulphur 1 984. Natural i sotopic composition of
isotopes. J. Gen. Microbial. 34: 1 95- nitrogen as a tracer of origin for sus
212 pended organic matter in the Scheidt es
54. Kaplan, I . R . , Emery, K . 0 . , Ritten tuary. Geochim. Cosmochim. Acta
berg , S. C. 1 963. The distribution and 48:549-55
isotopic abundance of sulphur in recent 66. M ariotti , A . . Pierre, D . , Vedy, J. c . ,
marine sediments off southern Califor Bruckert, S . , Guillemot , J . 1980. The
nia. Geochim. Cosmochim. Acta 27: abundance of natural nitrogen 15 in the
297-33 1 organic matter of soils along an altitu
55. Keeling, C . D . , Mook, W . G . , Tans, P. dinal gradient. Catena 7:293-300
P. 1 979. Recent trends in the 1 3C/ ' 2C Mariotti, A . , Germon, 1. c . , Hubert. P. ,
67.
ratio of atmospheric carbon dioxide. Na Kaiser, P. , Letolle, R . , et al. 1 98 1 . Ex
ture 277: 1 2 1-23 perimental determination of nitrogen
56. Kohl, D . H . , Shearer, G . 1 980. Isotopic kinetic isotopic fractionation: Some
fractionation associated with symbiotic principles; illustration for the denitrifica
N2 fixation and uptake of NO, - by tion and nitrification processes. Plant

plants. Plant Phvsiol. 66: 5 1 -56 Soil 62 : 4 1 3-30
57. Kohl, D. H . , Shearer, G . , Harper, J. E. 68. Mekhtiyeva, V . L. , Pankina, R. G . ,
1 980. Estimates of N2 fixation based on Gavrilov, Y . Y . 1 976. Distributions and
differences in the natural abundance of isotopic compositions of forms of sulfur
15N in nodulating and nonnodulating iso in water animals and plants. Geochem.
lines of soybeans . Plant Physiol. 66:61- Int. 1 3 :82-87
65 69. Minagawa, M . , Wada, E . 1 984. Step
58. Krouse, H . R . 1 980. Sulphur isotopes in wise enrichment of 15N along food
our environment. I n Handbook of En chains: Further evidence and the relation
vironmental Isotope Geochemistry. between 8" N and animal age. Geochim.
Volume I, ed. P . Fritz, J . Ch. Fontes, Cosmochim. Acta 48: 1 1 35-40
pp. 435-72. Netherlands: Elsevier Sci. 70. Minagawa, M . , Winter, D. A . , Kaplan,
Publ . J. R. 1 984. Comparison of Kjeldahl and
59. LaCroix, M . , Mosora, F. 1 97 5 . Varia combustion methods for measurement of
tions du rapport isotopique 1 3C1 ' 2C dans nitrogen isotope ratios in organic matter.
Ie metabolisme animal. In (Isotope Anal. Chem. 56: 1 859-61
Ratios as Pollutant Source and Be 71. Miyake, Y . , Wada, E. 1 967. The
haviour Indicators . ) Atomic Energy abundance ratio of ' 5N / ' 4N in marine
Agency, pp. 343-5 8 . Vienna environments. Rec. Oceanogr. Works,
60. Libes, S. M . 1 98 3 . Stable isotope Jpn 9:37-53
geochemistry of nitrogen in marine par 72. Montague, C. L. , Bunker, S. M . ,
ticulates. PhD thesis. Woods Hole Haines, E . B . , Pace, M . L . , Wetzel , R .
Oceanogr. Inst.lMIT. WHOI-83-9. 288 L. 1 98 1 . Aquatic macroc onsumers . I n
pp. The Ecologv of a Salt Marsh , ed . L. R .
61. Macko, S. A . , Lee , W. Y . , Parker. P. Pomeroy, R . G . Wiegert, p p . 69-85.
L. 1 982. Nitrogen and carbon isotope New York, Springer-Verlag. 271 pp.
fractionation by two species of marine 73. Montoya, J . P . , Horrigan, S . G . 1986.
amphipods: Laboratory and field stud Ra�id changes in the natural abundance
ies . J. Exp . Mar. Bioi. Eco!. 63: 1 45- of sN in plankton and dissolved nitro
49 gen in the Chesapeake Bay. Eos 67:988
62. Macko, S. A . . Estep, M . L. F. , Hare, P. (Abstr. )
E . , Hoering. T . C . 1 983. Stable nitrogen 74. Mook, W . G . • Bommerson, J . c . ,
and carbon isotopic ' composition of in Staverman, W . H . 1 974. Carbon isotope
dividual amino acids isolated from cul fractionation between dissolved bicar
tured microorganisms. Carnegie Insr. bonate and gaseous carbon dioxide.
Wash. Yrbk 1982-1983, 404 - 1 0 Earth Planet. Sci. Lett. 22 : 1 69-76
63. Mariotti , A , 1 98 3 . Atmospheric nitro 7 5 . Moore, H. 1974, Isotopic measurement
gen is a reliable standard for natural N
IS of atmospheric nitrogen compounds.
abundance measurements . Nature Tel/us 26: 1 69-74
303:685-87 76. Moore, H . 1 977. The isotopic composi
64. Mariotti , A. J . , Mari ott i , F. , Amarger, tion of ammonia, nitrogen dioxide and
N. 19 8 3 . Use of natural 1 5N abundance nitrate in the atmosphere. Almas. En
in the measurement of symbiotic fixa viron. 1 1 : 1 239-43
tion. In Nuclear Techniques in Improv- 77. Nielsen. H. 1 978 . Sulfur Isotopes in
nature. In Handbook of Geochemistry used to trace the flow of organic matter

II-2, ed. K. H . Wedepohl, 1 6 B : I-40. in estuarine food webs. Science 227:
Springer-Verlag, Berlin 1 36 1 -63
78 . Nriagu , J. 0 . , Harvey, H. H . 1 978 . 92 . Peterson, B . 1 . , Howarth. R. W . , Gar
Isotopic variation as an index o f sulphur ritt, R. H. 1 986. Sulfur and carbon iso
pollution in lakes around Sudbury, topes as tracers of salt-marsh organic
Ontario. Nature 273:223-24 matte r flow. Ecology 67:865-74
79. Nriagu, 1. 0 . , Coker, R. D. 1 978. 93 . Rau, G. H. 1 978. Carbon- 1 3 depletion
isotopic composition of sulphur in atmo in a subalpine lake: Carbon flow im
spheric precipitation around Sudbury, plications. Science 20 1 :901-02
Ontario. Nature 274:883-85 94. Rau, G. H. 1 980. Carbon- 1 3/carbon- 1 2
80. Nriagu, J. 0. , Coker, R. D. 1 983. Sul variations in sub alp ine lake aquatic in
phur in sediments chronicles past sects: Food source implications. Can. J.
changes in lake acidification. Nature Fish. Aquat. Sci. 37:742--46
303:692-94 9 5 . Rees, C . E. 1 97 3 . A steady-state model

81. Nriagu, J. 0 . , Soon, Y. K . 1 985. Dis for sulphur isotope fractionation in
tribution and isotopic composition of bacterial reduction processes. Geochim.
sulfur in lake sediments of northern Cosmochim. Acta 37: 1 14 1 -62
Ontario. Geochim. Cosmochim . Acta 96. Rees, C. E . , Jenkins, W. 1 . , M onster , J .

49:823-34 1 978. The sulphur isotopic composition
82. Odum, E. P . , de la Cruz, A . A. 1967. of ocean water sulphate . Geochim . Cos
Particulate organic detritus in a Georgia mochim. Acta 42:377-8 1
salt marsh-estuarine ecosystem. In Es 97 . Roeske, C. A . . O'Leary, M. H . 1984.
tuaries. ed. G. H. Lauff, 83:383-88. C arbon isotope effects on the enzyme
AAAS Publ . New York catalyzed carboxylation of ribulose
83. O' Leary, M. H . 1 98 1 . Carbon isotope bisphosphate. Biochemistry 23 :6275-
fractionation in plants. Phytochemistry 84
20:553-67 98 . Rotty, R. M . , Marland, G. 1 986. Fossil
84. O ' Leary , M. H. 1 984 . Measurement of fuel combustion: Recent amounts, pat
the isotope fractionation associated with terns, and trends of CO2• In The Chang
diffusion of carbon dioxide in aqueous ing Carbon Cvcle: A Global Analysis,
solution. J. Phvs. Chem . 88:823 ed. J. R. Trabalka, D. E. Reichle , pp.
85. Owens, N . J. P. 1 985. Variations in the 474--90. New York: Springer-Verlag
natural abundance of t5N in estuarine 99. Rounick, 1. S . , Winterbourn, M. J .
suspended particulate matter: A spec ific 1986. Stable carbon isotopes and carbon
indicator of biological processing. Es flow in ecosystems. BioScience 36: 1 7 1 -
tuarine, Coastal Shelf Sci. 20:505- 1 0 77
8 6 . Pang, P. C . , Nriagu, J . 0. 1 977. isotop 100. Saino, T . , Hattori, A. 1980. t5N natural
ic variations of the nitrogen in Lake Su abundance in oceanic suspended particu
perior. Geochim. Cosmochim. Acta late matter. Nature 283:752-54
4 1 : 8 1 1-14 l O t . Saltzman, E. S . , Brass, G. W . , Price,
8 7 . Parker, P. L. 1 964. The biogeochemis D. A. 1 983. The mechanism of sulfate
try of the stab le isotopes of carbon in a aerosol formation: Chemical and sulfur
marine bay. Geochim. Cosmochim . Acta isotopic evidence. Geophys. Res. Lett.
28: 1 1 55-64 1 0:5 1 3- 1 6
88. Peng, T. -H . , Freyer, H . D. 1986. Re 102. Schoeller, D . A . , Minagawa , M . , Sla
vised estimates of atmospheric CO2 vari ter, R . , Kaplan, I. R. 1 986. Stable iso
ations based on the tree-ring D C record . topes of carbon, nitrogen and hydrogen
In The Changing Carbon Cycle : A Glob in the contemporary North American hu
al Analysis. ed. J . R. Trabalka, D. E. man Food web. Ecol. food Nutr.
Reichle', pp. 1 5 1 -59 New York: 1 8 : 1 59-70
Springer-Verlag 103. Schoeninger, M. J . , DeNiro, M. J . ,
89. Peng, T.-H. , Broecker, W. S . , Freyer, Tauber, H. 1 983. Stable nitrogen iso
H. D . , Trumbore , S. 1983. A de tope ratios of bone collagen reflect
convolution of the tree ring based SUC marine and terrestrial components of
record . J. Geophys . Res. 88:3609-20 prehistoric human diet. Science 220:
90. Peters, K . E . , Sweeney , R. E . , Kaplan, 1 3 8 1-83
I. R. 1 978. Correlation of carbon and 1 04 . Schwarcz, H. P. 1 969. Isotopes in na
nitrogen stable isotope ratios in ture. I. The stable isotopes of carbon.
sedimentary organic matter. Limnol. In Ha ndbook of Geochemistry II- I ,
Oceanogr. 23:598--604 ed. K . H . Wedepohl , 6B: 1 - 1 6. Berlin:
9 1 . Peterson, B . J . , Howarth, R . W _ , Gar Springer-Verlag
ritt, R . H. 1 985. Multiple stable isotopes 1 05 . Schwarcz, H. P. 1 973. Sulfur
320 PETERSON & FRY
i sotope analyses of some Sudbury, plants . Carnegie Inst. Wash. Yrbk

Ontario, ores. Can. 1. Earth Sci. 7 3 :768-80
1 0: 1 444-59 1 1 6. Urey, H . C. 1 947. The thermodynami c
1 06 . Schwarcz, H. P. , Melbye, 1 . , Katzen properties of i sotopic substances. 1 .
berg, M. A . , Knyfe, M . 1 985. Stable Chern . Soc. 1 947:562-8 1
isotopes in human skeletons o f southern 1 17. van der Merwe, N. J. 1 982. Carbon iso
Ontario: Reconstructing Palaeodiet. 1. topes. photosynthesis, and archaeology.
Archaeol. Sci. 1 2 : 1 87-206 Am. Sci. 70:596--606
1 07 . Shearer , G . , Kohl, D. H. 1 986. N T 1 18. van der Merwe , N . J . , Vogel, J . C .
fixation in field settings: Estimations 1 97 8 . D e content o f human collagen as
based on natural 1 5 N abundance. Austr. a measure of prehistoric diet i n wood
1. Plant Phvs;o/. 1 3 :699-757 land North America . Natllre 276:8 1 5- 1 6
'
1 08 . Shearer. G . , Koh l . D. H . . Virginia. R . 1 1 9. Wada, E . 1 980. Nitrogen isotope
A . , Bryan , B . A . , Skeeters, J . L. , e t al. fractionation and its significance in
1 983. Estimates of No-fixation from biogeochemical processes occurring i n

variation in the natural abundance of 15N marine environments. In Isotope Marine
in Sonoran Desert ecosystems. Dec% Chemistrv, ed. E. D. Goldberg, Y .
gia 56:365-73 Horibe, K . Saruhashi, pp. 375�98.
1 09 . Steele, K. W . , Daniel , R. M . 1 97 8 . Tokyo: Uchida Rotakuho

Fractionation o f n itrogen isotopes by an 1 20. Wada, E . , Hattori , A. 1 97 8 . N itrogen
i m a ls : A further complication to the use isotope effects in the assimilation of in
of variations in the natural abundance of organic n itrogenous compounds by
1 5 N for tracer studies. 1. ARric. Sci . marine diatoms. Geornicrobiol. 1. 1 :85-
90:7-9 101
1 1 0 . Stuiver, M. 1 97 8 . Atmospheric carbon 121. Williams, P . M . , Gordon, L. I . 1 970.
dioxide and carbon reservoir ch anges . Carbon- 1 3 : carbon- 1 2 ratios i n dissul ved
Science 1 99:253-58 and particulate organic matter in the sea.
1 1 1 . Tans, P. 1 98 1 . 1 3C1 '2C of industrial Deep-Sea Res. \ 7 : 1 9-27
CO2 , In Carbon Cvcle Model/inR. 1 22 . Y anagi sawa , F . , Sakai , H. 1 983 . Ther
SCOPE 1 6 , ed. B. Bolin, pp. 1 27- 1 29 . mal decomposition of barium sulfate
New York: Wiley vanadium pentoxi de-s i lica glass mix
1 1 2 . Tauber , H. 1 98 1 . "c evidence for di ture s for preparation of sulfur dioxide in
etary habits of prehisto ri c mall in Den sulfur isotope ratio measurements. Anal.
mark . Nature 292:332-33 Chern. 55:985-87
1 1 3 . Teal, J. M. 1 962. Ene rgy now i n the salt 1 23 . Yoneyama, T . , Ohta, Y . , Ohtani, T.
marsh ecosystem of Georgia. Ec% gy 1 983. Vari ations of natural 1 3C and 15N
43:6 1 4-24 abundances in the rat tissues and their
1 1 4 . Tieszen , L. L . . Boutton, T. W . . Tes correlation . Radioisotopes 32:330--3 2
dahl, K . G . , Slade, N. A. 1 983. 1 24 . Zieman, J . C . , Macko, S . A . , M i l l s , A.
Fractionation and turnover of stable car L . 1 984. Role of seagrasses and man
bon isotopes in animal tissues: Im groves in estuarine food webs: Temporal
plications for Q"e analysis of d iet . and spatial changes in stable isotope
Oec% gia 57:32-37 composi tion and amino acid content dur
1 1 5 . Troughton, J . H . , Card, K. A . , Hendy, ing decompos i tion . Bull. Mar. Sci.
C . H. I lJ74. Photosynthetic pathways 35:380--92
and carbon isotope discrimination by

Annurev Es 18 110187 001453

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Annurev Es 18 110187 001453

Uploaded by

Copyright:

Available Formats

ANNUAL

Ann. Rev. Ecol. Sl'st. 1987. 18:293-320

STABLE ISOTOPES IN ECOSYSTEM

Bruce 1. Peterson and Brian Fry

experience that com binations of these measurements are often complementary

TERMINOLOGY AND MEASUREMENT

Most ecolo gical studies express isotopic compositions in terms of a values,

isotopes ih a sample. Increases in these values denote increases in the amount

O.40 ��""""""T""---r---'r---or--,...-"""'---r...., 99.60

4.50 r--..,.-....,...--r-----,r---or--,.-.---r---, 94.69

information). The source sets an isotopic baseline that can subsequently

measured as a partial isotopic separation or fractionation. In this introduction,

discrimination occurs is a one-step reaction starting with an essentially unlim­

top) due to isotopic fractionation during the formation of heavy-isotope

a semi-closed system in marine sediments and results in marked sulfur iso­

as production of 34 S-depleted sulfides leaves residual sulfate increasingly

Our photosynthesis example is actually a special case of branched reac­

In summary, isotopic fractionation in most biochemical reactions arises

OVERVIEW OF C, N, AND S DISTRIBUTIONS

The natural abundance isotopic compositions of C, N, and S in ecosystems

The Carbon Cycle

Tropical C-4 To101 Dissolved CO2 0

Grasslands POM -22

The Nitrogen Cycle

4 to 6% 0; 3,119). With two exceptions (24,86),nitrogen isotopic values in

The Sulfur Cycle

( 10, 38). Over geological time, and partially in response to global-scale

to +21 °/ 0 0 v alues of m arine pl an kton and se aweeds.

Stable Isotopes in Animals

offset by 15 N enrichments in other nitrogen pools.

Rather than attempting an exhaustive review o f a rapidly growing field, we

8/5N Measures of N2 Fixation

Nitrogen stable isotope measurements can be used to estimate plant fixation o f

+ 100/00, depending on location (66, 107; K. Nadelhoffer & B. Fry, un­

Corn Cobs Added

nodules). Presumably, the nodulating soybeans derived most of the nitrogen

accurate at the 5 to 15% level in many situations (107). Simply collecting

of N fixation is a nonmanipulative procedure that has great simplicity and

The Global Carbon Cycle and the CO2 Problem

Carbon isotope research is making substantial contributions to understanding

since atmospheric CO2 exchanges continuously with oceanic CO2 and

0.0 -------_--=:-ModeJ Fossil

Sulfur and Acid Deposition

Analysis of the chemical forms of the sulfur in recent sediments provided a

'loS .:; '·s

StabLe Isotopes in ArchaeoLogy

The study of human diets in ancient settings is a key to understanding both

but underwent a rapid increase in l3C to - II0/0 0 by 13 0 0 AD. This

Be) had relatively heavy C and N isotopic compositions ( � - 1 2% 0 813C,

Postmcsolithic Danes had substantially lightcr C and N values ( � - 20 /0 0

Detrital Organic Matter in Salt Marshes

Island salt-marsh creeks. However, since other sources of organic matter,

origin of the detritus unambiguously. This is a common problem of isotopic

( ll 1 3C - 1 3% 0) a nd C 3 ( o 1 3C - 28% 0) pla nts usi ng s table C iso to pes. O n

72 Geochemistry, ed. G. Eglington, M. T.

5. Anderson, T. F . , Arthur, M. A. 1983. tion of reduced organic carbon. In Hand­

studies on atmospheric nitrogenous trace analyzed using DCI'2C ratios . t;cology

for mass spectrometer analyses by com­ geochemistry. In OrKanic Geochemistry

Veizer, L. S. Land, 2 : 1 - 1 08 . Dallas: ing Pasture Management, 6 1-77. Vien­

N2 fixation and uptake of NO, - by tion and nitrification processes. Plant

nature. In Handbook of Geochemistry used to trace the flow of organic matter

303:692-94 9 5 . Rees, C . E. 1 97 3 . A steady-state model

discrimination occurs is a one-step reaction starting with an essentially unlim

a semi-closed system in marine sediments and results in marked sulfur iso

Our photosynthesis example is actually a special case of branched reac

+ 100/00, depending on location (66, 107; K. Nadelhoffer & B. Fry, un

5. Anderson, T. F . , Arthur, M. A. 1983. tion of reduced organic carbon. In Hand

for mass spectrometer analyses by com geochemistry. In OrKanic Geochemistry

Veizer, L. S. Land, 2 : 1 - 1 08 . Dallas: ing Pasture Management, 6 1-77. Vien