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Carbon dynamics in a temperate grassland soil after 9 years
exposure to elevated CO2 (Swiss FACE)
Zubin Xiea,b,*, Georg Cadischb,1, Grant Edwardsb,e, Elizabeth M. Baggsc, Herbert Blumd
aState Key Laboratory of Soils and Sustainable Agriculture (Institute of Soil Science, Chinese Academy of Science), Nanjing 210008, ChinabImperial College London, Wye Campus, Department of Agricultural Sciences, Wye, Ashford, Kent TN25 5AH, UK
cSchool of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UKdInstitute of Plant Science, Swiss Federal Institute of Technology (ETH), 8092 Zurich, Switzerland
eAgriculture and Life Sciences Division, P.O. Box 84, Lincoln University, Canterbury, New Zealand
Received 29 April 2004; received in revised form 13 December 2004; accepted 16 December 2004
Abstract
Elevated pCO2 increases the net primary production, C/N ratio, and C input to the soil and hence provides opportunities to sequester
CO2–C in soils to mitigate anthropogenic CO2. The Swiss 9 y grassland FACE (free air carbon-dioxide enrichment) experiment enabled us
to explore the potential of elevated pCO2 (60 Pa), plant species (Lolium perenne L. and Trifolium repens L.) and nitrogen fertilization (140
and 540 kg haK1 yK1) on carbon sequestration and mineralization by a temperate grassland soil. Use of 13C in combination with respired
CO2 enabled the identification of the origins of active fractions of soil organic carbon. Elevated pCO2 had no significant effect on total soil
carbon, and total soil carbon was also independent of plant species and nitrogen fertilization. However, new (FACE-derived depleted 13C)
input of carbon into the soil in the elevated pCO2 treatments was dependent on nitrogen fertilization and plant species. New carbon input
into the top 15 cm of soil from L. perennne high nitrogen (LPH), L. perenne low nitrogen (LPL) and T. repens low nitrogen (TRL)
treatments during the 9 y elevated pCO2 experiment was 9.3G2.0, 12.1G1.8 and 6.8G2.7 Mg C haK1, respectively. Fractions of FACE-
derived carbon in less protected soil particles O53 mm in size were higher than in !53 mm particles. In addition, elevated pCO2 increased
CO2 emission over the 118 d incubation by 55, 61 and 13% from undisturbed soil from LPH, LPL and TRL treatments, respectively; but
only by 13, 36, and 18%, respectively, from disturbed soil (without roots). Higher input of new carbon led to increased decomposition of
older soil organic matter (priming effect), which was driven by the quantity (mainly roots) of newly input carbon (L. perenne) as well as
the quality of old soil carbon (e.g. higher recalcitrance in T. repens). Based on these results, the potential of well managed and established
temperate grassland soils to sequester carbon under continued increasing concentrations of atmospheric CO2 appears to be rather limited.
q 2005 Elsevier Ltd. All rights reserved.
Keywords: Elevated CO2; Swiss FACE; carbon sequestration; 13C; Soil fractionation; Priming effect; CO2 emission
1. Introduction
Carbon sequestration in soil organic matter has been
identified by the IPCC (Intergovernmental Panel on Climate
Change) as one of the options for moderating increasing
atmospheric CO2 concentrations (IPCC, 2001). There are
0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.soilbio.2004.12.010
* Corresponding author. Address: State Key Laboratory of Soils and
Sustainable Agriculture (Institute of Soil Science, Chinese Academy of
Science), Nanjing 210008, China.1 Present address: Institute of Plant Production and Agroecology in the
Tropics and Subtropics, University of Hohenheim, 70593 Stuttgart,
Germany.
two general ways to increase soil carbon stocks in
agricultural soils: (1) reducing carbon losses from the soil
through fewer disturbances or sequestering of carbon in
more stable soil pools; and (2) increasing carbon input to the
soil by using improved crop varieties, fertilization, and
irrigation (Kauppi et al., 2001). Elevated atmospheric pCO2
increases plant photosynthesis, production and allocation of
photosynthate to below ground components (Hebeisen et al.,
1997; Warwick et al., 1998; Daepp et al., 2000), hence
soil C sequestration is expected to be enhanced under
elevated pCO2.
New carbon input into the soil is higher under
elevated pCO2 than under current ambient air
Soil Biology & Biochemistry 37 (2005) 1387–1395
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Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–13951388
concentrations (Hungate et al., 1997; Van Kessel et al.,
2000a; Gill et al., 2002). Enhanced soil carbon sequestration
requires either an increase in new carbon input without an
equivalent increase in mineralization of new input carbon or
older soil organic matter, or requires a decrease in carbon
mineralization without a commensurate decrease in net
primary production (Van Kessel et al., 2000b).
Decomposability of newly input litter mediates nutrient
cycling in the soil and turnover of soil organic matter.
Studies of the decomposability of litter produced under
elevated pCO2 have not shown consistent effects: with
increases (Ross et al., 2002), decreases (Lutze et al., 2000;
Ross et al., 2002) and no effects (Gorissen and Cotrufo,
2000) being reported. Litter decomposability induced by
elevated pCO2 has sometimes been found to be related to
plant species and nitrogen fertilization (Lutze et al., 2000;
Gorissen and Cotrufo, 2000; Van Ginkel et al., 2000; Ross
et al., 2002). Other studies have found that under elevated
pCO2 a higher percentage of newly input carbon exists in
soil sand and silt particles O53 mm (Van Kessel et al.,
2000b; Cardon et al., 2001). Cardon et al. (2001) observed
that exposure of California grassland communities to
elevated pCO2 retarded decomposition of older soil organic
carbon. In contrast, Van Kessel et al. (2000a) reported that
higher carbon input under elevated pCO2 stimulated the
decomposition of older soil organic carbon—in other words,
the higher carbon input induced a priming effect. Clearly,
additional information is needed to understand the influence
of newly input carbon under elevated pCO2 on dynamics of
carbon in soil, particularly on decomposition of older soil
carbon or carbon in different sized soil particles and to
quantify potential priming effects.
2. Materials and methods
2.1. Experimental design
The free air carbon-dioxide enrichment (FACE)
experiment, Eschikon, near Zurich, Switzerland was
established in 1993 and consisted of six 18 m diameter
plot rings separated from each other by at least 100 m.
During the daylight hours, three of the rings received
ambient air with 36 Pa pCO2, and the other three received
60 Pa pCO2. The experiment was set up as a split-plot
design with CO2 as the main plot treatment, and sward type
and fertilizer application rate as sub-plot treatments.
Further details of the experimental site can be found in
Hebeisen et al. (1997), Van Kessel et al. (2000b). The CO2
used for fumigation was from a petrochemical source
highly depleted in 13C (d13C signals were approximately
K48‰ in the first two years and K45‰ in subsequent
years). Mixing of the supplemental CO2 with ambient air in
the CO2-enriched rings resulted in a lower d13C value than
that of ambient air (K8‰). This enabled us to use d13C
analysis to trace the source of the CO2-C emitted from
fresh plant input.
Soil cores (8 cm outer diameter!15 cm length) were
taken from sub-plots containing Lolium perenne
L. (perennial ryegrass) at high nitrogen fertilization
(560 kg haK1 yK1; LPH), L. perenne L. at low nitrogen
fertilization (140 kg haK1 yK1; LPL), and Trifolium
repens L. (white clover) at low nitrogen fertilization
(140 kg haK1 yK1; TRL) in September 2002 using an
electrical auger, and transported to Imperial College
London, Wye campus, United Kingdom for the incubation
experiment reported here. These cores were treated as
undisturbed and disturbed.
2.2. Undisturbed soil cores
Two undisturbed soil cores (bulk densityZapproxi-
mately 1.2 g cmK3) were taken from each sub-plot treat-
ment replicate, and above-ground biomass was cut at the
soil surface. The cores were weighed and inserted into
plastic tubes (8 cm internal diameter!25 cm length) to
facilitate leaching. A cap with a drainage tube was placed
over the bottom of each plastic tube and was sealed with
silicone. A glass fiber filter was placed at the inner bottom of
the cap with 1.5 cm of acid-washed silica sand above it. The
tubes were loosely covered with tin foil to reduce water
evaporation and placed in a dark incubation room main-
tained at 28 8C.
Chambers (20 cm internal diameter!35 cm height) were
used for CO2 sampling and were comprised of two parts: an
upper chamber and a bottom base. The bottom base
consisted of a PVC (polyvinyl chloride) board (30!30!0.4 cm) with two rings (internal diameters 18 and
25 cm!height 5 and 5 cm) which were sealed onto the
board with heated PVC thread. A lid was sealed at one end
of the upper chamber, and the other end was left open. For
efficient mixing of the gas in the chamber, a battery-driven
fan was put on the inner side of the lid. A suba-seal (Fisher
Scientific, UK) was inserted into a hole on the lid for gas
sampling and sealed with silicone. Before each sampling
occasion, two undisturbed soil cores were placed within the
inner ring on the bottom board. Water was added to the
space between the inner and outer rings, and the upper
chamber was put in the water between the rings to form a
gas-tight seal.
2.3. Disturbed soil cores
Two undisturbed soil cores were taken from each sub-
plot treatment replicate and above-ground biomass was cut
at the soil surface. The soil was passed through a 4 mm sieve
and mixed well. Visible roots and stubble were removed,
washed, and dried for analysis of dry weight, carbon,
nitrogen, and 13C. Stones were removed and weighed.
Aliquots of disturbed soil were put into tubes (3.9 cm
internal diameter!20 cm length), packed to a height of
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–1395 1389
10 cm with a bulk density of approximately 1.2 g cmK3 and
maintained in a dark incubation room at 28 8C. Cores were
placed in storage jars (2085 ml) with gas-tight lids contain-
ing a gas-sampling port for sampling of CO2.
2.4. Analysis of CO2 concentration and 13C-CO2
Gas samples were taken after incubation for 2 or 6 h,
depending on the respiration rate. Sampling was divided
into four stages: stage 1, days 1–14 (samples taken on days
1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 12, and 14); stage 2, days 17–28
(samples taken on days 17, 20, 23, and 28); stage 3, days 31
to 59 (samples taken on days 31, 34, 38, 45, and 59); and
stage 4, days 62 to 118 (samples taken on days 62, 69, 76,
90, and 118). Samples were analyzed for CO2 on an Agilent
6890 gas chromatograph fitted with a FID and methaniser.
Enrichment of 13C–CO2 was determined on a 20–20 Europa
mass spectrometer coupled to an ANCA-TGII trace gas
analyzer (PDZ, Crewe, UK).
2.5. Soil and plant analyses
Soil samples were air-dried, and all visible plant material
was removed. To remove inorganic carbon, excess HCl was
added to the soil (in the form of a 10% HCl v/v and 9.2%
FeSO4 w/v solution) until effervescence stopped. The soil
samples were washed with deionized water and oven dried
(Nelson, 1982).
Particle size fractionation was conducted by wet sieving
based on a procedure modified from Cardon et al. (2001). A
10 g sample of air-dried soil (inorganic carbon removed)
was dispersed in 50 ml of 5 g LK1 sodium hexametha-
phosphate and shaken for 2 h at 300 rpm. Dispersed soil
samples were passed through a 53 mm sieve and rinsed with
deionized water. Soil particles in the solution (!53 mm, silt
and clay fraction) were centrifuged at 1100 g (equivalent to
3000 rpm) for 30 min and washed with deionized water.
Materials remaining on the 53 mm sieve (O53 mm, sand
fraction) and material in centrifuge tubes (!53 mm) were
transferred to beakers and oven dried at 105 8C.
Plant root and soil samples were fine ground in a ball
mill. Total carbon, nitrogen, and 13C in the samples were
determined using a 20–20 Europa isotope ratio mass
spectrometer coupled to an automated elemental analyzer
(Roboprep carbon and nitrogen biological sample converter;
PDZ, Crewe).
2.6. Calculations
2.6.1. CO2 flux
For each sampling day, CO2 fluxes from soil respiration
were calculated from the difference between the chambers
or jars with and without soil after closing them for 2 or 6 h
The cumulative CO2 emission over 118 d was calculated by
linear and non-linear interpolation according to the flux
dynamics at different stages.
2.6.2. 13C isotopic compositions
The 13C isotopic compositions of CO2, plant, and soil
samples were expressed in d units (‰) (van Kessel et al ,
2000b):
d13C ZRsample
Rstandard
K1
� �!1000
where RZ13C/12C. The d13C values were calculated with
reference to Vienna Pee Dee Belemnite (Rstandard-
Z13C/12CZ0.0112372).
2.6.3. Fraction of CO2 and soil carbon derived from plant
input under FACE
The fraction (f) of CO2 and soil carbon derived from
plant input in elevated pCO2 (FACE) treatments was
calculated as follows (Balesdent et al., 1988):
f Zde Kd0
d1 Kd0
where de and d0 are the d13C values (‰) for CO2 carbon or
soil carbon from elevated pCO2 (FACE) (de) and ambient
pCO2 plots (d0), respectively; and d1 is the average d13C
value of the roots of T. repens and L. perenne in the FACE
plots (meanGSEZ-37.0G0.2‰).
2.6.4. d13C of CO2 emitted from soil
The d13C of CO2 emitted from soil (d13CO2 soil) was
calculated from the isotopic mass balance by subtracting13C in the blank (Schweizer et al., 1999):
d13CO2 soil ZdT !cT Kdb !cb
cT Kcb
where dT and cT are the d13C values (‰) and the
concentrations (in ppmv), respectively, of the gas samples
from chambers or jars with soil; and db and cb are the d13C
value and the concentration (in ppmv), respectively, of the
gas samples from chambers or jars without soil.
2.6.5. Evaluation of FACE-derived carbon
The emitted CO2 from FACE-derived carbon was
calculated as:
FACE CO2 KC Z SAi½ðfi C fjÞ=2�
where Ai is the total emitted CO2 (g CO2–C kgK1 dry soil)
during each stage; and fi and fj are the contributions of
FACE-derived carbon to the emitted CO2 at the beginning
and at the end of each stage of incubation, respectively.
The decomposition of old (pre-FACE) soil organic
carbon (CO2–Cold C) during the incubation was determined
as follows:
CO2 KCold C Z CO2 KCtotal KFACE CO2 KC
The fraction of old or FACE-derived soil carbon pools
(g C kgK1 dry soil) decomposed (fR) during the incubation
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–13951390
(respiration loss) was calculated by:
fR Z CO2 KCold;FACEKC=Cold;FACEKC
where CO2–Cold, FACE-C are emitted CO2–C from old soil
organic C and FACE-derived C, respectively; Cold, FACE-C
are old soil C and FACE-derived C pools, respectively.
The proportional increases in carbon contents (fDC)
induced by elevated pCO2 were calculated as:
fDC ZCe KC0
C0
!100
where Ce and C0 are carbon contents at elevated and
ambient pCO2, respectively.
2.7. Statistical analysis
A split-plot statistical design was used with pCO2 as the
main plot factor (nZ2) and the nitrogen level (nZ2) and
plant species (nZ2) as sub-plot factors. The effects of the
main and sub-factors and their interactions were analyzed
using the Univariate-Full factorial of SPSS (SPSS Inc.,
1999). Univariate-Custom of SPSS was used when the effect
of a single factor was tested. Differences were considered
significant only when P!0.05.
3. Results
3.1. Carbon dynamics and particle size fractions
After nine years exposure to elevated pCO2 the average
total soil organic carbon under elevated pCO2 increased by
7.8, 16.0 and 7.2% in LPH, LPL, and TRL treatments,
respectively (Table 1); however, the difference was not
statistically significant (PZ0.23) Total soil organic carbon
was also found to be independent of plant species (PZ0.94)
and nitrogen fertilization (PZ0.99). In contrast, soil d13C
decreased significantly in all treatments (P!0.001) after the
nine years of CO2 fumigation and was significantly
dependent on plant species (P!0.05) but independent of
nitrogen fertilization (PZ0.37). The most FACE-derived
carbon was found in the soil of the LPL treatment, and there
was a higher amount of FACE-derived carbon in soil from
L. perenne compared to T. repens. The average inputs of
FACE-derived carbon to the soil in LPL, LPH, and TRL
Table 1
Total soil C, d 13C and FACE-derived C input in soil under ambient (A) and elev
Species N level Total SOM-C (g kgK1 soil)
A E A
L. perenne High 21.2G3.0 22.9G5.2 K22
Low 20.2G3.1 23.4G3.8 K22
T. repens Low 21.1G2.6 22.6G4.7 K22
a Soil bulk density 1.2 g cm3 was used to calculate FACE-derived C input in tob MeanG1SE.
treatments were 12.1, 9.3, and 6.8 Mg haK1, respectively
(Table 1), and the differences between LPL and LPH
(PZ0.02) and between LPL and TRL (PZ0.03) were
significant.
After nine years exposure to elevated pCO2 there was a
higher carbon content in O53 mm particles than in !53 mm
particles (Table 2). The carbon content in soil particles
O53 mm prior to incubation increased by 15, 21 and 16% in
LPH, LPL, and TRL treatments, respectively (P!0.05), in
response to elevated pCO2, but in soil particles !53 mm the
increases were lower (5, 11 and 8%, respectively) and not
significant (PO0.05). After the 118 d incubation the carbon
content in soil particles O53 mm was lower compared to
soil prior to incubation, but had increased in soil particles
!53 mm.
The d13C values were significantly lower (P!0.001) in
particles O53 mm than in particles !53 mm in response to
elevated pCO2. This effect was dependent on plant species
(PZ0.02) but not on nitrogen fertilization (PZ0.20).
Additionally, the fraction of FACE-derived carbon
(f value) was higher in particles O53 mm than in particles
!53 mm, and, after the 118 d incubation, the f values
increased in particles O53 mm from LPH, LPL, and TRL
treatments by 36, 28, and 37%, respectively (PZ0.01).
However, in particles !53 mm there were no significant
increases in f values. After incubation, the FACE-derived
carbon in the particles O53 mm had decreased, compared to
prior to incubation, but had increased in particles !53 mm
(Table 2).
3.2. CO2 emission
Total CO2 emitted over the 118 d experimental period
was significantly higher from both disturbed and undis-
turbed soils subjected to elevated pCO2 than from those
receiving ambient pCO2 (P!0.05; Table 3) In undisturbed
soil cores the increase in CO2 emissions in response to
elevated pCO2 was significantly greater in L. perenne
(55–61%) than in T. repens treatments. In disturbed soils the
greatest increase of 36% (P!0.05) was in the LPL cores.
There was little effect of nitrogen fertilizer history (high vs.
low nitrogen) on total CO2 emissions. In addition,
undisturbed soil cores emitted in excess of two-fold greater
CO2 than disturbed soil cores, and soil samples from
ated pCO2 (E) after 9 years of fumigation
d 13C‰ Fraction of FACE
derived C (f)
FACE-derived C
input (Mg haK1)a
E E E
.8G0.4 K25.9G0.2 0.22G0.01 9.3G2.0b
.6G0.4 K26.8G0.1 0.29G0.02 12.1G1.8
.7G0.3 K24.9G0.6 0.16G0.05 6.8G2.7
p 15 cm soil.
Table 2
Particle C content, d13C and fraction of FACE-derived C in soil particles prior to and after incubation under ambient (A) and elevated CO2 (E) after 9 years of
fumigationa
Species N level Particle size Prior to or after
incubation
Particle C content (g kgK1 soil particle) d13C‰ Fraction of
FACE C (f)
A E fDCb A E E
L. perenne High O53 mm Before 22.0 25.4 15.5 K23.4 K27.3 0.28
After 18.3 20.1 9.8 K23.4 K28.6 0.38
!53 mm Before 20.2 21.2 5.0 K23.4 K25.8 0.18
After 25.6 29.0 13.3 K22.8 K25.4 0.18
Low O53 mm Before 21.0 25.4 21.0 K23.6 K28.0 0.32
After 14.7 19.8 34.7 K23.7 K29.3 0.41
!53 mm Before 19.5 21.7 11.3 K23.4 K25.9 0.18
After 26.9 29.5 9.7 K23.0 K26.0 0.21
T.repens Low O53 mm Before 21.6 25.0 15.7 K23.5 K26.7 0.24
After 13.3 18.3 37.6 K23.1 K27.6 0.33
!53 mm Before 19.6 21.1 7.7 K23.0 K25.5 0.18
After 26.1 28.4 8.8 K22.7 K24.9 0.16
SED O53 mm Before 1.59 2.69 1.71 0.2 0.3 0.02
After 2.09 2.62 9.00 0.2 0.1 0.01
!53 mm Before 1.78 1.61 1.86 0.2 0.3 0.03
After 2.27 2.71 1.41 0.3 0.2 0.01
a SED is one standard error.b Proportional increase of carbon content in particles.
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–1395 1391
L. perenne emitted more CO2 (P!0.05) than soil samples
from T. repens.
Compared with samples of soil receiving ambient pCO2,
the CO2 emitted from incubated FACE soil samples were
significantly depleted in 13C (Fig. 1). The d13C–CO2 emitted
from undisturbed elevated pCO2 T. repens cores was
significantly (P!0.05) less negative than that from
L. perenne cores. The 13C signatures of CO2 emitted from
undisturbed soil samples became more depleted over the
first 28 days of the incubation, and then increased until the
end of the experiment. In disturbed soil samples, the 13C
signatures of emitted CO2 generally decreased throughout
the experiment, except at day 14. Furthermore, 13C–CO2
from disturbed soil were less depleted than from the
undisturbed soil at the beginning of incubation, but more
depleted at the end of incubation (Fig. 1).
The contribution of FACE-derived carbon to CO2
emissions increased during the first 28 d in undisturbed
soil samples (PZ0.01, 0.03, and 0.14 for LPH, LPL,
Table 3
Total CO2 emission and FACE-derived CO2–C after 118 d incubation (g CO2–C
Treatment N level Total CO2 emission
(g CO2–C kgK1 dry soil)
FA
(g
dr
Undisturbed Disturbed Un
Aa E A E
L. perenne High 3.3 5.1 1.6 1.8 3.3
Low 3.3 5.3 1.4 1.9 3.3
T. repens Low 2.4 2.7 1.1 1.3 1.3
SED 0.2 0.6 0.1 0.1 0.4
a A and E are with the same meaning as in Table 1. SED is one standard error
and TRL, respectively) and decreased thereafter (Fig. 2).
However, in disturbed soil there was no significant increase
in contribution during almost the whole incubation period.
The FACE-derived carbon from the T. repens treatment
contributed less to the emitted CO2 than that from the
L. perenne treatment. In undisturbed soil samples the
contribution of emitted CO2 from the LPH treatment was
similar to that of the LPL treatment, but, in disturbed soil
samples, the FACE-derived carbon from the LPL treatment
often contributed more than that from the LPH treatment. At
the beginning of the incubation, the FACE-derived carbon
in undisturbed soil samples contributed about 20% more
than that in disturbed soil samples, but at the end of the
incubation, FACE-derived carbon in undisturbed soil
samples contributed about 20% less than in disturbed soil
samples.
In the L. perenne treatment the FACE-derived carbon
contributed about 3-fold more carbon to the emitted CO2
in undisturbed soils than in disturbed soils, while
kgK1 dry soil)
CE-derived CO2–C
CO2–C kgK1
y soil)
Decomposition of old soil
organic C (g CO2–C kgK1
dry soil)
Proportional
decomposition in
disturbed cores (fR)
disturbed Disturbed Undisturbed Disturbed FACE-C Old C
1.0 1.8 0.8 0.20 0.05
1.2 2.0 0.7 0.18 0.04
1.1 1.4 0.2 0.30 0.01
0.1 0.2 0.1 0.04 0.01
.
Em
itte
d d
13C
-CO
2
–38
–36
–34
–32
–30
–28
–26
–24
–22
–20
Days
0 20 40 60 80 100 120 0 20 40 60 80 100 120
Fig. 1. 13C–CO2 emission during 118 d incubation. Symbols: Solid, ambient; open, elevated; circle, L. perenne-high N; triangle, L. perenne-low N; square,
T. repens-low N. Error bars indicate one standard error of the means.
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–13951392
the difference in the T. repens treatment was not significant
(PO0.05) (Table 3). Furthermore, FACE-derived CO2–C
was more than double in the undisturbed L. perenne
treatments compared to the T. repens treatment, but no
significant plant/fertilizer effects occurred in the disturbed
samples.
Soil carbon loss from old (pre-FACE) organic matter
during the 118 d incubation was higher in undisturbed than
in disturbed soils (Table 3). Respiration losses (fR)
accounted for only 1–5% of old soil carbon stocks in
disturbed soils but accounted for 18–30% of FACE-derived
C. Significantly more (P!0.05) carbon from old SOC was
respired in undisturbed than in disturbed soils, and more old
soil organic matter was lost from L. perenne than from
T. repens soils.
Undisturbed
D
0 20 40 60 80 100 120
Per
cen
tag
e o
f em
itte
d C
O2
fro
m F
AC
E-d
eriv
ed C
(%
)
0
20
40
60
80
100
LPHLPLTRL
Fig. 2. Contributions of emitted CO2 from FACE-derived C. LPH, LPL and TR
respectively. Error bars indicate one standard error of the means.
4. Discussion
4.1. Effect of elevated CO2 on C stocks
One of the options to increase carbon sequestration in
soils is to increase C input into the soil, and given that
elevated atmospheric pCO2 increases plant production and
allocation of photosynthate to below ground components
(Hebeisen et al., 1997; Warwick et al., 1998; Daepp et al.,
2000), soil carbon sequestration would be expected to be
increased under elevated pCO2. However, in the present
investigation the apparent small increases in carbon stocks
under elevated atmospheric pCO2 were not statistically
significant (PO0.05). Large soil carbon pools and
complexities of soil organic carbon turnover make it
ays
Disturbed
0 20 40 60 80 100 120
L repensent L. perenne-high N, L. perenne-low N, and T. repens-low N,
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–1395 1393
difficult to detect changes in total soil carbon in short
duration experiments even if they extend over several years,
such as the Swiss FACE experiment. On the other hand, the
absence of significant changes in topsoil total soil organic
carbon after 9 years of exposure to elevated pCO2 confirms
short-term observations by Van Kessel et al. (2000a) and
Van Groeningen et al. (2002) at the same site. These
observations suggest that the systems were already in, or
close to, equilibrium (Jenkinson, 1981), or ‘saturated’
(Hassink, 1997), i.e. the soil’s organic matter protection
capacity was already exceeded before the start of the
experiment. This is in contrast to disturbed arable soils
which are often depleted in soil organic matter and where,
based on 7- to 35-year arable land experiments performed in
the European Union, the annual increase of soil organic
carbon is reported to be linearly related to straw input
(Smith et al., 1997). Soil fractionation results suggested that
most of the new soil C was in the larger sand sized fraction
where it would have been less protected from decompo-
sition. This observation agrees with those of Van Kessel
et al. (2000a) and adds to our understanding of the low
protection of newly added carbon.
Based on our results it appears that soil carbon
sequestration in well-maintained older temperate grasslands
is limited. Even if the apparent maximum increases in C
over 9 y of elevated pCO2 were used to estimate soil carbon
sequestration under predicted elevated pCO2 levels, the
annual additional grassland soil C sequestration in the
15 nations of the European Union could only account for
3–7% of anthropogenic CO2–C produced in Western
Europe, or 0.5–1% of the global production.
4.2. C dynamics under elevated pCO2
Despite the absence of major chances in total soil
carbon stocks, the 13C methodology revealed significant
changes in the composition of organic matter Fractions of
new input carbon in the soil reached 22, 29 and 16% in
L. perenne-high N, L. perenne-low N and T. repens-low N
treatments, respectively, after 9 years exposure to elevated
atmospheric pCO2 (Table 1). This suggests a substantial
turnover of the old (pre-FACE) soil organic carbon, as also
observed to a similar degree by Van Kessel et al. (2000a).
Consistent with these previous observations the proportion
of FACE-derived C input was lowest under the legume
(T. repens) sward. This is in agreement with lower plant
productivity and particularly lower below-ground recycling
in the legume sward, e.g. elevated CO2 increased
aboveground and root biomass of L. perenne at high N,
on 3 years’ average, by 2.6 t haK2 and 1.3 t haK2,
respectively, whereas for T. repens at low N corresponding
values were 1.9 and 0.02 t haK2 (derived from Figs. 1 and
4 from Hebeisen et al. (1997)). The similar total soil
organic carbon stocks, but lower fraction of FACE derived
soil C in T. repens compared to the grassland soils,
suggests a larger size of remaining ‘old’ (pre-FACE)
carbon under the legume sward compared with the
grassland swards. Van Kessel et al. (2000a) observed a
similar effect and suggested a priming effect occurred
under L. perenne swards which resulted in higher losses of
old soil carbon.
A large increase in respiration was observed under
elevated pCO2 in undisturbed cores from L. perenne
swards (1.8–2.0 g CO2–C kgK1 soil) while in the T. repens
soil the elevated pCO2 response was only small (0.3 g
CO2–C kgK1 soil). Increases in respiration in disturbed
samples without roots were even smaller. This suggests that
the large FACE-induced increase in respiration was due to
root input since they were removed in the disturbed cores. In
fact new carbon inputs by roots from L. perenne-HN,
L. perenne-LN and T. repens under elevated pCO2 were 2.4,
2.2, and 0.7 g kgK1 dry soil (data from disturbed soil cores)
which are consistent with the contrasting respiration
responses in L. perenne and T. repens treatments,
respectively. These results suggest very different carbon
dynamics in the two swards despite their similarities in total
soil C content. Alternatively, the slightly greater respiration
rates under elevated pCO2 in disturbed soils may indicate
the presence of more small root debris or root exudates in
these treatments.
4.3. Use of 13C–CO2 methodology to investigate C dynamics
Use of the 13C technique in combination with respired
CO2 data enabled us to distinguish the origins of active
fractions of soil organic carbon and thus provided a better
insight into current carbon dynamics than would have been
possible by isotopic analysis of solid soil samples alone. At
the beginning of the incubations 13C signatures of CO2
emitted from undisturbed soil samples were more depleted
than those from disturbed soil samples. This was most likely
due to a root effect since 13C signatures of roots grown
in ambient and elevated pCO2 treatments were K28.8 and
K37.0‰, respectively. Additionally, at the beginning of
incubation in undisturbed soil samples, the roots were
probably still alive, so the emitted CO2 would have included
that from both root and heterotrophic microbial respiration,
whereas in disturbed soil samples all the visible roots were
removed and hence CO2 would have mainly been derived
from heterotrophic respiration.
At later stages of the incubation CO2 emitted from
undisturbed soil became less depleted in 13C than CO2 from
disturbed soil suggesting increased contribution of CO2–C
from pre-FACE (old) carbon. In order to decompose the
more recalcitrant root components in undisturbed soil
samples, enzymes such as ligninases and cellulases would
have been required, which can also attack older soil organic
matter (Wu et al., 1993), and this may have led to the
observed priming of older soil organic matter. In contrast, in
disturbed soil samples, there was no (or little) root material
available hence less priming occurred. These effects also
explain the higher percentage of FACE-derived CO2-C
Z. Xie et al. / Soil Biology & Biochemistry 37 (2005) 1387–13951394
(Fig. 2) in disturbed than in undisturbed soils at the end of
the incubation.
The proportion of FACE-derived CO2–C (25–85%;
Fig. 2) was much higher than the proportion of FACE-
derived carbon in total soil organic carbon (16–29%;
Table 1). This suggests that the new soil carbon was much
more active than the remaining old carbon. The difference
between evolution of FACE-derived CO2–C and that of
total CO2 yields provides an insight into the activity of old
soil organic carbon. Decomposition of older soil organic
carbon in undisturbed soil cores was thus estimated at 2.0
and 1.4 g C kgK1 for grass and legume low N treatments
respectively, while they were estimated at 0.7, and
0.2 g C kgK1, respectively, in disturbed soil cores. These
results reinforce the observations above that the two swards
types exerted a different priming effect on decomposition of
old organic matter.
4.4. Turnover of old and new soil C
Significant apparent priming of old soil organic carbon
has been observed in this experiment, with L perenne having
a stronger effect on decomposition of old soil organic
carbon than T. repens. The fact that the L. perenne
treatments had significantly higher root biomass than
T. repens leads us to suspect that this was a direct root
induced response, as discussed above. Additionally, the
decomposition of old carbon was substantially higher (by
1–1.3 g C kgK1) in the presence of roots (undisturbed soil
cores) compared to samples without roots (disturbed
samples), which points to a direct root-induced priming
effect.
Alternatively, a closer evaluation of data from the
disturbed samples revealed that the decomposition of old
soil carbon in T. repens samples was much lower
(0.2 g C kgK1) than that of L. perenne treatments (0.7–
0.8 g C kgK1) even in the absence of roots. This effect
suggests differences in the decomposability of old carbon of
different plant origin or indirect impacts of root/above
ground fine debris and root exudates, which were not
directly quantified in this experiment. An evaluation of the
sand and clay-silt sized particle carbon contents revealed no
significant difference between L. perenne or T. repens soils.
Thus the results suggest the occurrence of differences in
quality of old carbon between the two species investigated.
Indeed, more old carbon remained after nine years of CO2
fumigation (calculated from Table 1). Additional evidence
for differences in quality of stabilized organic matter
between species was obtained from a comparison of their
decomposition coefficients (Table 3) which revealed that
only 1% of old carbon in the T. repens treatment
decomposed during the 118 d incubation compared to
4–5% in the L. perenne treatments. Conversely, decompo-
sition coefficients of new (FACE-drived) carbon of
L. perenne treatments were lower (!20%) than that of
new carbon of T. repens (30%). The results thus suggest that
higher respiration under L. perenne swards was caused by i)
decomposition of a higher root biomass and ii) a direct root
priming of old carbon. In contrast, under T. repens FACE-
derived carbon was turned over faster but older soil organic
matter was more resistant to microbial attack.
5. Conclusions
The carbon sequestration potential of the Swiss grassland
was rather limited under the future elevated atmospheric
60 Pa pCO2 scenario. Increased C inputs under elevated
pCO2 led to larger FACE-derived carbon stocks, particu-
larly in L. perenne treatments compared to T. repens swards,
as well as higher respiration activities. Evidence of the
stimulation of decomposition of older soil organic carbon
under elevated CO2 came from analyzing stable
isotopic signatures of carbon stocks as well as from respired13C–CO2. The resulting priming effects were only partly
controlled by presence of roots and new C input. The data
revealed that stability of old and new (FACE derived)
carbon differs between sward species while N treatment did
not significantly affect turnover of the different organic
matter pools.
Acknowledgements
We wish to express our gratitude to the Key Project on
Basic Sciences and Technologies from the Ministry of
Science and Technology of China, the Natural Science
Foundation of China, and the Innovation Program of the
Chinese Academy of Sciences for financial support. We also
gratefully acknowledge the valuable technical assistance of
John Fear and Trudi Krol at Wye, and the team at ETH,
Eschikon.
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