Organic Carbon Isotope Systematics of Coastal Marshes

imedea.uib.csic.es

Organic Carbon Isotope Systematics of Coastal Marshes

Estuarine, Coastal and Shelf Science (1997) 45, 681–687

Organic Carbon Isotope Systematics of Coastal

Marshes

J. J. Middelburg a , J. Nieuwenhuize a , R. K. Lubberts b and O. van de Plassche b

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 13 C are presented for Spartina-dominated marsh sediments from a

mineral marsh in SW Netherlands and from a peaty marsh in Massachusetts, U.S.A. 13 C 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 13 C of organic matter in marsh sediments is due to trapping of allochthonous organic matter which

is depleted in 13 C. 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 (2–100 gCm 2 year 1 ) is a small fraction (1–5%) of plant production

(2000gCm 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

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 13 C value

(about 12‰) that is distinct from that of most other

organic carbon sources (e.g. Haines, 1976). Accordingly,

the 13 C 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

0272–7714/97/050681+07 $25.00/0/ec970247 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 5050 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 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

13 C characteristics. During senescence and degradation,

Spartina material becomes enriched in nitrogen

but 13 C values remain rather invariant. Sedimentary

organic matter has a lower C/N ratio and is depleted in

13 C 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 13 C 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 13 C value of low and high marsh

sediments are related to elevation, i.e. tidal flooding

frequency. The depleted 13 C values of upper

marsh sediments are due to the presence of brackish

macrophytes such as Phragmites, Typha and Scirpus.

Discussion

13 C-Corg relationship

These results indicate that the 13 C of sedimentary

organic carbon in peaty marshes (e.g. Great Marshes)

is close to that of Spartina material, whereas the 13 C

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

13 C 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 13 C 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


Table 1. Organic carbon and nitrogen contents and 13 C of plant and sediments at marsh near

Waarde Marsh

Material

Carbon

(wt%)

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 13 C of bulk litter will consequently become more

negative. This mechanism may potentially result in

13 C 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 13 C-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 13 C 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 13 C values of marsh sediments dominated by

Spartina vegetations. Sediments from Waarde and

Great Marshes represent the end-members of the

organic carbon versus 13 C plot. Marsh sediments

Nitrogen

(wt%)

C/N

(mol mol)

13 C

(‰)

Spartina above-ground 39·2 0·62 74·2 12·2

Spartina below-ground 31·5 0·53 69·8 12·5

Spartina senescent stems 38·3 0·81 55·3 12·8

Spartina litter 37·2 1·16 37·3 13·1

Sediments

0–5 cm 1·19 0·08 17·0 22·0

5–10 cm 1·69 0·11 18·3 23·7

10–15 cm 1·56 0·11 17·3 24·6

15–20 cm 2·07 0·12 19·4 23·9

20–25 cm 2·33 0·15 17·9 22·4

25–30 cm 2·57 0·17 17·7 23·6

30–35 cm 2·50 0·18 16·6 23·8

35–40 cm 2·00 0·13 17·7 23·5

40–45 cm 1·30 0·08 17·7 22·6

Allochthonous matter

Intertidal sediments 1·4 0·09 18·3 25·5

Sedimentary organic carbon (wt%)

40

30

20

10

0 –26

Organic carbon isotope systematics 683

δ 13 –24 –22 –20 –18 –16 –14

C of bulk organic carbon

–12

Figure 1. Bulk sedimentary organic carbon concentrations

(wt%) versus 13 C 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%, 13 C plant = 12·5‰)

and allochthonous (C all =1·4 wt%; 13 C all = 25·5‰) endmembers;

––––,Spartina end-member depleted by 2‰ due

to diagenesis; — —, allochthonous end-member heavier

(C all =1·4 wt%; 13 C all = 21‰).


684 J. J. Middelburg et al.

Table 2. Organic carbon and nitrogen contents and 13 C of sediments from Great Marshes near

Barnstable

Material

Carbon

(wt%)

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:

13 C sed =(C all * 13 C all +C plant * 13 C plant )/C sed (1)

with a Spartina end-member (C plant =40 wt%;

13 C plant = 12·5‰) and an allochthonous endmember

(being nearby tidal flat or creek sediments:

C all =1·4 wt%; 13 C=25·5‰) can be used to

describe the isotopic composition of marsh sediments

( 13 C sed ) as a function of sedimentary organic carbon

(C sed ). 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 13 C 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

Nitrogen

(wt%)

C/N

(mol mol)

13 C

(‰)

High marsh sediments

0–5 cm 26·2 1·44 21·2 14·1

5–10 cm 28·1 1·27 25·8 13·8

10–15 cm 30·2 1·36 25·9 13·9

15–20 cm 26·8 1·24 25·2 14·2

Surface sediments

Creek bottom 1·1 0·07 18·3 21·0

Low marsh, creek bank 5·6 0·41 15·9 19·5

High marsh, creek bank 21·4 1·03 24·2 14·5

High marsh 36·7 1·26 34·0 13·4

Upland border 11·9 0·82 16·9 24·5

low marsh surface samples have 13 C values (21–

19·5‰) and organic carbon contents (1·1–5·6%)

that are significantly different from those of high

marsh samples ( 13 C=13·4–14·5‰; C org=21–

36 wt%; Table 2). Similarly, Ember et al. (1987)

reported more positive 13 C 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

13 C 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 13 C values

between (grain-) size fractions in a single sample, with

fine fractions being depleted in 13 C with respect to

coarse fractions (Ember et al., 1987; Creach, 1995).

Accordingly, sedimentary 13 C 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 13 C 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


Table 3. Carbon balance

mass-balance approach is to balance carbon inputs

of allochthonous (C all ) and plant (C plant )

materials against the burial of marsh carbon (C sed ).

Mathematically:

(1-) all all C all + plant F NEP=

(1- ) sed sed C sed

(2)

where is the porosity of marsh sediment; all and

sed (cm year 1 ) are the accumulation rate of mineral

and associated allochthonous organic matter, and

total matter, respectively; all , plant , sed (g cm 3 ) are

the dry densities of mineral matter, plant organic

matter and bulk sediments, respectively; C all , C sed

(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 ( sed ) and bulk dry density of

marsh sediments ( sed ) are estimated from the plant

and allochthonous contributions. Table 3 presents the

carbon mass balances for Waarde Marsh and Great

Waarde Marsh Great Marshes

Observations

C sed (wt%) 1·2–2·6 21–37

13 C sed (‰) 22–24·6 13·4–14·5

sed (cm year 1 ) 0·88 a

Organic carbon isotope systematics 685

0·15–0·2 b

Model parameters

13 C (‰) 25·5 c

21 c

C all (wt%) 1·4 c

1·1 c

13 C plant (‰) 12·5 12·5

0·72 0·85

all (cm year 1 )

Model estimates


0·87 0·08

13 C sed -based

NEP (g C m 2 year 1 ) 2–10 5–20

sed (cm year 1 )

C

0·87–0·88 0·093–0·13

sed -based

NEP (g C m 2 year 1 ) 100

sed (cm year 1 )

Carbon flows

0·33

Primary prod. (g C m 2 year 1 ) 2300 e

1918 d

Respiration (g C m 2 year 1 ) 1924 f

1678 d

Burial (g C m 2 year 1 ) 105 96

Difference (g C m 2 year 1 ) 269 144

C plant =40 wt%; all =2·5gcm 3 ; plant =1·5gcm 3 ; F=2·5.

a Zwolsman et al. (1993), b de Rijk (1995), c tidal flat sediments (Waarde Marsh) or creek bottom sediments (Great

Marshes), d Hopkinson (1988), e above-ground production=2*maximum standing stock biomass and aboveground/below-ground

production=1, f based on measured CO 2 fluxes (Klaver, unpubl. data) and complete

decomposition of above-ground biomass.

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 13 C and C, because

Equations 1 and 2 are coupled through C sed . Estimates

based on 13 C 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, 13 C-based NEP estimates for peaty marshes

are very sensitive to the 13 C 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

20gCm 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

100gCm 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 .

Implications for the use of sedimentary 13 C 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 13 C 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 13 C record of

mineral marshes primarily reflects alternations in relative

importance of local plant versus allochthonous

carbon sources.

Finally, the sedimentary 13 C 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

13 C values of Ceriops tagal (22·7‰) and Rhizophora

mucronata (25·3‰) sediments are enriched

with respect to 13 C 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

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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