Estuarine, Coastal and Shelf Science (1997) 45, 681–687
Organic Carbon Isotope Systematics of Coastal
Marshes
J. J. Middelburga, J. Nieuwenhuizea, R. K. Lubbertsb and O. van de Plasscheb
a
Netherlands Institute of Ecology, Centre for Estuarine and Coastal Ecology, Korringaweg 7, 4401 NT Yerseke,
The Netherlands
b
Faculty of Earth Sciences, Vrije Universiteit, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands
Received 14 October 1996 and accepted in revised form 13 December 1996
Measurements of nitrogen, organic carbon and ä13C are presented for Spartina-dominated marsh sediments from a
mineral marsh in SW Netherlands and from a peaty marsh in Massachusetts, U.S.A. ä13C of organic carbon in the peaty
marsh sediments is similar to that of Spartina material, whereas that in mineral marshes is depleted by 9–12‰. It is argued
that this depletion in ä13C of organic matter in marsh sediments is due to trapping of allochthonous organic matter which
is depleted in 13C. The isotopic composition and concentration of organic carbon are used in a simple mass balance to
constrain the amount of plant material accumulating in marsh sediments, i.e. in terms of the so-called net ecosystem
production. Net ecosystem production (22–100 g C m "2 year "1) is a small fraction (1–5%) of plant production
(22000 g C m "2 year "1). This small amount of plant material being preserved is nevertheless sufficient to support
marsh-accretion rates similar to the rate of sea-level rise.
? 1997 Academic Press Limited
Keywords: Isotope ratios; marshes; salt marshes; carbon; organic matter; biogeochemistry; marsh plants;
sedimentation rates
Introduction
Marsh plants are well known to play an important role
in determining the rate of vertical accretion of intertidal marshes (Redfield, 1972). The presence of
shoots induces lower water-current velocities which
results in enhanced trapping of suspended matter and
lower bottom shear stresses, hence lower erosion rates
(Leonard & Luther, 1995). Moreover, roots and
rhizomes of marsh plants stabilize the sediments.
As a result, marsh sediments represent a sink of
allochthonous particulate matter with associated
organic matter.
In addition to this indirect effect of marsh plants,
there is also a direct effect on vertical accretion
through input of autochthonous organic matter resulting from carbon dioxide fixation. Tidal salt marshes
are amongst the most productive ecosystems, with
part of the fixed carbon being invested in aboveground organic matter and part being allocated belowground for roots and rhizome growth. The majority
of biomass produced during the growing season is
degraded or exported, and only a small amount
remains available for accumulation in the marsh
sediments (Howarth, 1993).
The direct and indirect effects of plants on vertical
accretion rates of marshes relate directly to relative
0272–7714/97/050681+07 $25.00/0/ec970247
importance of mineral matter and organic matter
components (McCaffrey & Thomson, 1980), and
have led to the recognition of two end-member
depositional facies: the organogenic and minerogenic
modes (Allen, 1995). Organic matter accumulation
determines vertical accretion in sediment-starved
peaty marshes of New England (McCaffrey &
Thomson, 1980), whereas mineral matter accumulation controls accretion in marshes in SE United States
and NW Europe (Bouma, 1963; Allen, 1995). There
is also some interaction between these two modes
of accumulation, since mineral sedimentation may
stimulate plant growth (King et al., 1982). It will be
clear that the characteristics and isotopic composition
of the organic matter accumulating in salt marshes
depend on the relative importance of the two modes of
vertical accretion. In Spartina-dominated marshes, the
plant-derived organic matter input has a ä13C value
(about "12‰) that is distinct from that of most other
organic carbon sources (e.g. Haines, 1976). Accordingly, the ä13C value of bulk sedimentary organic
matter can be partitioned into that due to local higher
plant inputs and that due to mineral, algal and
non-local macrophyte inputs.
This paper reports data on organic carbon concentrations and carbon stable isotope ratios for a mineral
marsh (Waarde Marsh, SW Netherlands) and a peaty
? 1997 Academic Press Limited
682 J. J. Middelburg et al.
marsh (Great Marshes, Barnstable, Massachusetts,
U.S.A.). These data are combined with data reported
in the literature, and the combined data set is interpreted using a simple isotope-mixing model. This
mixing model is combined with a simple mass-balance
model to examine the factors controlling organic
matter accumulation in marsh sediments, and to
estimate the direct plant contribution to vertical
accretion rates of salt marshes.
Materials and methods
Waarde Marsh
In August 1994, three replicate cores were taken from
the salt marsh near Waarde, Westerschelde Estuary,
SW Netherlands. The vegetation of the lower zone of
the Waarde salt marsh is formed almost exclusively by
monospecific stands of Spartina anglica. The biomass of above-ground S. anglica was determined by
harvesting the shoots from three plots of 50#50 cm.
The above-ground material was washed in tap water
to remove adhering silt, separated into living, brown
and detrital material, and dried at 70 )C. Roots and
rhizomes were separated from soil particles by rinsing
the material over a 1 mm sieve. Bulk sediments,
without large rhizomes but with roots, were dried and
homogenized for analyses.
Great Marshes
Surface sediments of the marsh near Barnstable (MA,
U.S.A.) were sampled in the summer of 1992 using a
3·5 cm diameter PVC tube. Short, 15 cm cores were
taken from different saltmarsh (sub)-environments
along an elevation gradient. These include: (1)
organic-rich muds from the bottom of the tidal creeks;
(2) clayey lower creek bank sediments covered by
mono stands of Spartina alterniflora tall form; (3)
higher creek bank sediments dominated by Spartina
patens and Distichlis spicata; (4) high marsh sediment
covered by a mix of S. alterniflora stunted, S. patens
and D. spicata; (5) the highest high marsh areas close
to the uplands; and (6) upper marsh sediments
covered by brackish species like Phragmites australis,
Typha sp. and Scirpus sp.
Analysis
Plant and sediment carbon and nitrogen contents
were determined using a Carlo-Erba NA 1500 CN
analyser following a recently developed in situ HCl
acidification procedure (Nieuwenhuize et al., 1994).
Carbon isotopes have been determined using a Fisons
elemental analyser coupled on-line (via a continuous
flow interface) with a Finnigan Delta S mass spectrometer. Results of the carbon isotope analyses are
reported in the ä notation relative to Vienna-PDB.
Reproducibility based on replicate measurements was
better than 0·1‰.
Results
Above-ground biomass at Waarde Marsh averages
1435 g dry weight m "2. The carbon and nitrogen
content and carbon isotopic composition of S. anglica
and marsh sediments near Waarde Marsh are given in
Table 1. Above- and below-ground living material of
S. anglica are similar in terms of their C/N ratio and
ä13C characteristics. During senescence and degradation, Spartina material becomes enriched in nitrogen
but ä13C values remain rather invariant. Sedimentary
organic matter has a lower C/N ratio and is depleted in
ä13C by 9–12‰ relative to Spartina material.
At Great Marshes, organic matter in sediments
from high-marsh environments dominated by S.
alterniflora and S. patens, has ä13C values varying from
"13·4 to "14·5‰. These high marsh sediments are
organic-carbon rich and have molar C/N ratios that
vary from 21 to 34 (Table 2). The surface transect
samples show that organic carbon and nitrogen
concentration and ä13C value of low and high marsh
sediments are related to elevation, i.e. tidal flooding
frequency. The depleted ä13C values of upper
marsh sediments are due to the presence of brackish
macrophytes such as Phragmites, Typha and Scirpus.
Discussion
ä13C-Corg relationship
These results indicate that the ä13C of sedimentary
organic carbon in peaty marshes (e.g. Great Marshes)
is close to that of Spartina material, whereas the ä13C
of sedimentary organic carbon in mineral marshes
(e.g. Waarde Marsh) is depleted by 9–12‰ relative to
Spartina material. A similar negative shift in sedimentary ä13C from that of Spartina carbon has been
reported for marsh sediments from Georgia (Haines,
1976), South Carolina (Ember et al., 1987),
Louisiana (DeLaune, 1986; Chmura et al., 1987) and
Mont Saint Michel, France (Creach, 1995). Three
processes may explain these shifts in ä13C values.
The first process involves the preferential decomposition of labile, relatively heavy, components and the
selective preservation of refractory, relatively light,
components. Benner et al. (1991) reported that relatively labile polysaccharide and relatively refractory
Organic carbon isotope systematics 683
T 1. Organic carbon and nitrogen contents and ä13C of plant and sediments at marsh near
Waarde Marsh
Spartina above-ground
Spartina below-ground
Spartina senescent stems
Spartina litter
Sediments
0–5 cm
5–10 cm
10–15 cm
15–20 cm
20–25 cm
25–30 cm
30–35 cm
35–40 cm
40–45 cm
Allochthonous matter
Intertidal sediments
Carbon
(wt%)
Nitrogen
(wt%)
C/N
(mol mol)
ä13C
(‰)
39·2
31·5
38·3
37·2
0·62
0·53
0·81
1·16
74·2
69·8
55·3
37·3
"12·2
"12·5
"12·8
"13·1
1·19
1·69
1·56
2·07
2·33
2·57
2·50
2·00
1·30
0·08
0·11
0·11
0·12
0·15
0·17
0·18
0·13
0·08
17·0
18·3
17·3
19·4
17·9
17·7
16·6
17·7
17·7
"22·0
"23·7
"24·6
"23·9
"22·4
"23·6
"23·8
"23·5
"22·6
1·4
0·09
18·3
"25·5
lignins components are enriched ("12·5‰) and
depleted ("18·5‰), respectively, with respect to
whole Spartina tissue ("13·5‰). Upon decomposition, plant debris becomes enriched in lignins and
the ä13C of bulk litter will consequently become more
negative. This mechanism may potentially result in
ä13C values that are depleted by 5‰ relative to
Spartina material, but this depletion is usually limited
to 1–2‰ (Table 1; 1‰, Benner et al., 1991; 2‰,
Ember et al., 1987). This selective preservation
mechanism can therefore account only partly for the
isotopic shift observed.
Peterson et al. (1980) have proposed an alternative
mechanism to explain this isotopic shift. Their
mechanism is based on sulphur-oxidizing chemoautotrophic bacteria that fix 13C-depleted carbon
from the porewater total inorganic carbon pool. This
mechanism can probably be discounted because it
would require that bacterial organic carbon would
account for about 50% of the sedimentary organic
carbon in the Waarde Marsh.
The third, and most important, mechanism affecting sedimentary ä13C values involves the input of
allochthonous organic matter, which includes organic
matter sorbed on mineral matter, as well as estuarine
and marine phytoplankton, microphytobenthos and
non-local macrophytes. Figure 1 shows the relationship between sedimentary organic carbon contents
and ä13C values of marsh sediments dominated by
Spartina vegetations. Sediments from Waarde and
Great Marshes represent the end-members of the
organic carbon versus ä13C plot. Marsh sediments
40
Sedimentary organic carbon (wt%)
Material
30
20
10
0
–26
–24
–22
–20
–18
–16
δ13C of bulk organic carbon
–14
–12
F 1. Bulk sedimentary organic carbon concentrations
(wt%) versus ä13C values for various saltmarsh systems:
Waarde ( ) and Great Marshes ( ) (this study), South
Carolina ( , Ember et al., 1987); Georgia ( , Haines,
1976), Louisiana (*, DeLaune, 1986; Chmura et al., 1987)
and Mont Saint Michel (x, Creach, 1995). ——, isotope
mixing curve with Spartina (40 wt%, ä13Cplant = "12·5‰)
and allochthonous (Call =1·4 wt%; ä13Call = "25·5‰) endmembers; – – – –, Spartina end-member depleted by 2‰ due
to diagenesis; — —, allochthonous end-member heavier
(Call =1·4 wt%; ä13Call = "21‰).
684 J. J. Middelburg et al.
T 2. Organic carbon and nitrogen contents and ä13C of sediments from Great Marshes near
Barnstable
Material
High marsh sediments
0–5 cm
5–10 cm
10–15 cm
15–20 cm
Surface sediments
Creek bottom
Low marsh, creek bank
High marsh, creek bank
High marsh
Upland border
Carbon
(wt%)
Nitrogen
(wt%)
C/N
(mol mol)
ä13C
(‰)
26·2
28·1
30·2
26·8
1·44
1·27
1·36
1·24
21·2
25·8
25·9
25·2
"14·1
"13·8
"13·9
"14·2
1·1
5·6
21·4
36·7
11·9
0·07
0·41
1·03
1·26
0·82
18·3
15·9
24·2
34·0
16·9
"21·0
"19·5
"14·5
"13·4
"24·5
from Georgia (Haines, 1976), South Carolina (Ember
et al., 1987), and Louisiana (DeLaune, 1986; Chmura
et al., 1987) are intermediate. A standard twocomponent isotope mixing curve:
ä13Csed =(Call *ä13Call +Cplant *ä13Cplant)/Csed (1)
with a Spartina end-member (Cplant =40 wt%;
ä13Cplant = "12·5‰) and an allochthonous endmember (being nearby tidal flat or creek sediments:
Call =1·4 wt%; ä13C= "25·5‰) can be used to
describe the isotopic composition of marsh sediments
(ä13Csed) as a function of sedimentary organic carbon
(Csed). The short-dashed line in Figure 1 represents
an isotope mixing curve that includes a 2‰ isotopic
shift due to Spartina litter decomposition. These two
mixing curves adequately reproduce the observed
data. Changing the allochthonous end-member values
would affect the curves, but not their general appearance (long-dashed line in Figure 1). Clearly, this two
component model is highly simplistic given the
number of potential organic carbon sources (organic
matter sorbed on mineral matter, phytoplankton,
microphytobenthos and non-local higher plants) and
their range in isotopic values (e.g. Peterson &
Howarth, 1987), but sufficient to explain the majority
of variance. At the cross-system level (when minerogenic and organogenic marshes are compared), the
major factor governing the ä13C of sedimentary
organic matter in salt marshes is therefore the relative contribution of local plant and other carbon
inputs.
The relative proportions of allochthonous and
Spartina matter may also change with location in a
single marsh system or with depth at a single location.
At Great Marshes, creek bottom and creek-bank
low marsh surface samples have ä13C values ("21–
"19·5‰) and organic carbon contents (1·1–5·6%)
that are significantly different from those of high
marsh samples (ä13C= "13·4–14·5‰; Corg =21–
36 wt%; Table 2). Similarly, Ember et al. (1987)
reported more positive ä13C values with increasing
distance from the marsh creek; their values increase
from "21‰ at the creek bank to "18·4‰ at the
short S. alterniflora zone. These data indicate that
creek sediments and marshes near creeks receive
relatively more allochthonous matter than back marsh
sediments. Ember et al. (1987) also reported a significant positive correlation between organic carbon and
ä13C values at a single high marsh site in South
Carolina. This might reflect varying proportions of
allochthonous and Spartina matter with depth in
sediment. Also consistent with this two-component
mixing approach are differences in ä13C values
between (grain-) size fractions in a single sample, with
fine fractions being depleted in ä13C with respect to
coarse fractions (Ember et al., 1987; Creach, 1995).
Accordingly, sedimentary ä13C values of marshes
depend mainly on the relative proportion of local
marsh plant and other carbon sources. Isotope effects
due to selective preservation of isotopically light
refractory carbon are of secondary importance at the
ecosystem level.
Carbon balance
The observed large range of sedimentary ä13C values
(Figure 1) and the inferred variable proportions of
allochthonous and plant-derived organic matter put
some constraints on the carbon balance of saltmarsh
sediments, in particular the amount of plant carbon
that becomes buried. For organic carbon, the simplest
Organic carbon isotope systematics 685
T 3. Carbon balance
Observations
Csed (wt%)
ä13Csed (‰)
ùsed (cm year "1)
Model parameters
ä13C (‰)
Call (wt%)
ä13Cplant (‰)
Ö
ùall (cm year "1)
Model estimates
ä13Csed-based
NEP (g C m "2 year "1)
ùsed (cm year "1)
Csed-based
NEP (g C m "2 year "1)
ùsed (cm year "1)
Carbon flows
Primary prod. (g C m "2 year "1)
Respiration (g C m "2 year "1)
Burial (g C m "2 year "1)
Difference (g C m "2 year "1)
Waarde Marsh
Great Marshes
1·2–2·6
"22–24·6
0·88a
21–37
"13·4–"14·5
0·15–0·2b
"25·5c
1·4c
"12·5
0·72
0·87
"21c
1·1c
"12·5
0·85
0·08
2–10
0·87–0·88
5–20
0·093–0·13
<20
<0·89
>100
>0·33
2300e
1924f
105
269
1918d
1678d
96
144
Cplant =40 wt%; ñall =2·5 g cm "3; ñplant =1·5 g cm "3; F=2·5.
a
Zwolsman et al. (1993), bde Rijk (1995), ctidal flat sediments (Waarde Marsh) or creek bottom sediments (Great
Marshes), dHopkinson (1988), eabove-ground production=2*maximum standing stock biomass and aboveground/below-ground production=1, fbased on measured CO2 fluxes (Klaver, unpubl. data) and complete
decomposition of above-ground biomass.
mass-balance approach is to balance carbon inputs of allochthonous (Call) and plant (Cplant)
materials against the burial of marsh carbon (Csed).
Mathematically:
(1-Ö)ùallñallCall +ñplantF NEP=
(1- Ö)ùsedñsedCsed
(2)
where Ö is the porosity of marsh sediment; ùall and
ùsed (cm year "1) are the accumulation rate of mineral
and associated allochthonous organic matter, and
total matter, respectively; ñall, ñplant, ñsed (g cm "3) are
the dry densities of mineral matter, plant organic
matter and bulk sediments, respectively; Call, Csed
(g C g sed "1) are the organic carbon contents of
allochthonous matter and bulk marsh sediment,
respectively; F is the conversion factor from organic
carbon to organic matter; and NEP is the net ecosystem production of the salt marsh (g C m "2 year "1),
being the amount of locally produced plant carbon
that becomes buried in marsh sediments. The marsh
accumulation rate (ùsed) and bulk dry density of
marsh sediments (ñsed) are estimated from the plant
and allochthonous contributions. Table 3 presents the
carbon mass balances for Waarde Marsh and Great
Marshes. The model results should be considered as
first-order estimates because there are no studies
where plant production (including below-ground),
decomposition, sediment-accumulation rates and
sediment flux rates have been reported simultaneously
(Dame, 1989). Model estimates of NEP are therefore
based on information drawn together from various
sources. NEP estimates have been constrained
through the use of both ä13C and C, because
Equations 1 and 2 are coupled through Csed. Estimates based on ä13C are most accurate for mineral
marshes, whereas those based on organic carbon are
most appropriate for peaty marshes, because of their
sensitivity towards correct values of end members. For
instance, ä13C-based NEP estimates for peaty marshes
are very sensitive to the ä13C value of the plant
end-member. Moreover, any estimate should also
be consistent with measured rates of salt marsh
accretion.
At Waarde Marsh, the NEP varies from 2 to
20 g C m "2 year "1, which is less than 1% of annual
plant production and less than 20% of the carbon
burial. At Great Marshes, NEP is on the order of
100 g C m "2 year "1, similar to the carbon burial
rates, but only 5% of plant production. Although
686 J. J. Middelburg et al.
these estimates have large uncertainties, they clearly
indicate that a very small amount (1–5%) of the
carbon fixed by plants eventually enters the sediment, the majority being decomposed above- and
below-ground or being exported (Hopkinson, 1988;
Howarth, 1993). NEP is often taken to be identical to
the rate of burial (Hopkinson, 1988), which is a valid
approach in peaty marshes, but not in mineral
marshes (Table 3). It also appears that NEP is relatively more important in peaty marshes with relatively
high below-ground production rates (Dame, 1989;
Hopkinson, 1988) compared to mineral marshes
with relatively low below-ground production rates
(above-ground/below-ground > =1; Hemminga et al.,
1996). Nevertheless, these very small quantities of
NEP are sufficient to result in the net marshaccretion rates due to Spartina-derived organic matter
of 0·2–2·5 mm year "1.
Finally, the sedimentary ä13C values of other vegetated systems (such as mangroves and seagrass beds)
may be interpreted in a similar manner (Middelburg
et al., 1996). Carbon isotope signatures reported for
mangrove and seagrass sediments from Gazi Bay,
Kenya (Hemminga et al., 1994) illustrate this. The
ä13C values of Ceriops tagal ("22·7‰) and Rhizophora mucronata ("25·3‰) sediments are enriched
with respect to ä13C values of leaves ("24·1 and
"28·3‰, respectively), indicating import and burial
of heavy allochthonous carbon derived from seagrasses ("10·7–"19·7‰) or algae ("18–"21‰).
Similarly, seagrass sediments were depleted on average by 3·2‰ relative to seagrass tissue, indicating
trapping and burial of light allochthonous carbon
(algal or mangrove derived).
Acknowledgements
Implications for the use of sedimentary ä13C values
During the last decade, the sedimentary record of salt
marshes has received considerable attention (Allen,
1990; van de Plassche, 1991; Fletcher et al., 1992;
Nelson, 1993), since it may provide detailed information on fluctuations in the rate of relative sea-level
rise (RSLR). Disequilibrium between saltmarsh accretion and relative sea-level rise may result in alternating
sequences of mudflat, low-, high- and upper-marsh
facies according to conditions. These facies can be
recognized using floral (Niering et al., 1977), microfaunal (Scott & Medioli, 1978; Thomas & Varekamp,
1991), geochemical (Varekamp et al., 1992; Daoust
et al., 1996) and isotopic (e.g. Emery et al., 1967;
DeLaune, 1986; Chmura & Aharon, 1995) approaches. Chmura et al. (1987) and Chmura and
Aharon (1995) have advocated the use of a mixing
model for prediction of the ä13C of sedimentary
carbon. Their model is based on the assumption that
sources of sedimentary carbon are primarily autochthonous and contributed in direct proportion to the
above-ground biomass (or production) of each species
present. It will be clear from the results of this study
that their method can only be used if NEP equals the
burial rate, in other words if allochthonous sources
can be neglected. The carbon isotope record of peaty
salt marsh deposits may therefore be interpreted in
terms of alternating sequences of Spartina-dominated
low and high marsh with heavy carbon versus
Phragmites- Typha- Juncus-dominated upper marsh
with light carbon. However, the ä13C record of
mineral marshes primarily reflects alternations in relative importance of local plant versus allochthonous
carbon sources.
Drs Marten Hemminga, Ad Huiskes, Eric Boschker
and anonymous reviewers are thanked for constructive
comments on the manuscript, and Yvonne Maas for
analytical assistance. This is publication nr.2201 of
the Netherlands Institute of Ecology, Yerseke.
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