Applied Soil Ecology 28 (2005) 247–257
www.elsevier.com/locate/apsoil
Short-term CO2 emissions from planted soil subject
to elevated CO2 and simulated precipitation
David R. Smarta,*, Josep Peñuelasb
a
Department of Viticulture and Enology, University of California, One Shields Avenue, Davis, CA 95616-8749, USA
b
Unitat Ecofisiologia CSIC-CREAF, Center for Ecological Research and Forestry (CREAF),
Edifici C, Universitat Autonoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
Received 13 November 2003; accepted 26 July 2004
Abstract
Carbon dioxide emissions from soils beneath canopies of two Mediterranean plants, Artemisia absinthium L. and Festuca
pratensis Huds. cv. Demeter, were monitored over a 7-day period that included an artificial precipitation event of 4 cm. The
experiments were conducted using 0.2 m3 soil microcosms inside greenhouses with CO2 concentrations of either 360 or
500 mmol mol1. Carbon dioxide flux from the soil surface, as calculated using a diffusive transport model agreed well with CO2
flux measurements made using a dynamic flow system. Soil CO2 emissions did not differ significantly between the 360 and
500 mmol mol1 CO2 treatments when soils were dry (volumetric soil moisture content 9%). A simulated precipitation event
caused an immediate exhalation of CO2 from soil, after which CO2 emissions declined slightly and remained constant for
approximately 36 h. CO2 emissions from soil microcosms with F. pratensis plants growing in 500 mmol mol1 CO2 then rose to
levels that were significantly greater than CO2 emissions from soils in the microcosms exposed to 360 mmol mol1 CO2. For A.
absinthium growing in 500 mmol mol1 CO2, the rise in soil CO2 emissions following the wetting event was not significantly
greater than emissions from soils with A. absinthium growing under 360 mmol mol1 CO2. A. absinthium above ground biomass
increased by 46.1 17.9% (mean S.E., n = 4, P 0.05). Above ground biomass did not significantly increase for F. pratensis
(14.4 6.5%, P 0.10). Root biomass, on the other hand, increased for both species; by 50.6 17.9% (P 0.05) for A.
absinthium and by 55.9 12.7% (P 0.05) for F. pratensis. Our results demonstrate two events following precipitation onto dry
soils, an immediate release of CO2 followed by a gradual increase from enhanced biological activity The gradual increase was
greater for the herbaceous ruderal perennial F. pratensis under elevated CO2.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Elevated atmospheric CO2; Soil respiration; Mediterranean plants; Precipitation; Soil moisture; Soil CO2
1. Introduction
* Corresponding author. Tel.: +1 530 754 7143;
fax.:+1 530 752 0382.
Carbon dioxide concentrations ([CO2]) of approximately 1.5–2 times greater than the current ambient
concentration of 370 mmol mol1 can increase below
0929-1393/$ – see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.apsoil.2004.07.011
248
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
ground carbon allocation (Norby et al., 1992; Zak et
al., 1993; Rogers et al., 1994; Prior et al., 1997; Vose
et al., 1997; Walker et al., 1998; Jones et al., 1998;
Edwards and Norby, 1999; Mikan et al., 2000;
Pregitzer et al., 2000). In a recent review, Zak et al.
(2000) noted that in 35 of 41 cases soil respiration
apparently increased under exposure to elevated CO2.
A high-degree of variability existed within these
responses, and the apparent increase was statistically
significant (P 0.05) in only 12 of the 41 reports. The
percent increase in soil respiration for statistically
significant observations ranged from 5 to 89%. More
recently Sowerby (Sowerby et al., 1999) and Lin (Lin
et al., 2001) reported significant enhancement of soil
CO2 emissions from grassland and montane forest
soils, respectively, during CO2 fertilization.
The quantitative uncertainty among reports may
reflect differences in C partitioning by plants of
diverse ecological strategies. For example, trees and
other woody perennial taxa may divert more C to
construction of woody tissues that have slow metabolic rates and low seasonal turnover rates, while
ruderal herbaceous taxa may partition more C into
short lived fine roots with high metabolic rates, or C
exudation that would enhance microbial respiration
(Zak et al., 2000). Differences among woody versus
herbaceous taxa were not apparent in the investigations reviewed by Zak et al. (2000), but no direct
comparisons have been reported to our knowledge
where a woody and herbaceous taxa were simultaneously compared while growing in the same soil and
under similar environmental conditions. In order to
better understand the role of plant communities in
buffering anthropogenic CO2 additions to the atmosphere, it is important, we understand the response of
various plant types growing in a variety of conditions.
Soil temperature and soil moisture content are the
principal driving variables for soil CO2 emissions at
the global scale (Kim and Verma, 1992; Raich and
Schlesinger, 1992). Soil moisture content can change
extremely rapidly during precipitation events, or when
evapotranspiration activity is high. The influence of
factors like precipitation on soil CO2 emissions are not
well documented. Water infiltration displaces soil pore
gases resulting in CO2 ‘exhalation’ (Norman et al.,
1992), and can stimulate both soil microbial activity
and root respiratory activity (Edwards, 1991). Luo et
al. (1996) argued that measurements within 5 days of
precipitation events would bias soil CO2 emissions
estimates because of these changes. On the other hand,
if significant quantities of CO2 were released from
soils following precipitation, either from gas displacement or because biological activity is strongly
stimulated, then neglecting such CO2 fluxes may result
in underestimates of soil respiration (Liu et al., 2002).
This would be particularly true for Mediterranean or
other arid ecosystems where there are relatively short
growing seasons (e.g., 100 days or less, Luo et al.,
1996).
To test the hypothesis that below ground respiration
of woody and herbaceous plants responds differently
to elevated [CO2] and precipitation, we monitored soil
CO2 emissions throughout the entire course of a
simulated precipitation event using soil microcosms
that were sustained under an ambient [CO2] of
360 mmol mol1 and an elevated ambient [CO2] of
500 mmol mol1. The soil microcosms were planted
to an herbaceous perennial (Festuca pratensis Huds.
cv. Demeter) commonly grown in upland pastures in
the Montseny region of Catalunya, and a woody
perennial sub-shrub (Artemisia absinthium L.) found
in the same region.
2. Material and methods
2.1. Physical environment
The experiments were conducted in two 6.5 m wide
by 12 m long by 4 m high tunnel greenhouses with
controlled [CO2]. The CO2 control system consisted of
a data acquisition and control module (Omron model
C20K, Straumsberg, PA, USA), an infrared gas
analyzer (Lira, model 3600) operating in the absolute
mode was used to monitor [CO2]. Pure filtered CO2
(Supelco Inc., model Supelpure, Bellefonte, PA, USA)
was injected into each greenhouse using a pressure
regulated drip irrigation system. The system was used
to sustain [CO2]s of 360 mmol mol1 CO2 in one, and
500 mmol mol1 CO2 in another.
2.2. Cultural practices
Eight well-drained polyvinylchloride (PVC) tubes,
each with 0.5 m diameter by 1.1 m hieght, were set
upright in each greenhouse on top of plastic drain
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
plates. These soil microcosms were filled with a local
dystric colluvial mineral soil (Xerochrept). The soil
was sieved at 1 cm, so it was free of any large pieces of
root or other organic material, and it had a very low
initial carbon content of 0.2%. Water was applied to
saturation levels three times prior to the initiation of
the experiment to insure that the soil was well-settled
when plants were transplanted into it.
Six, 3-week old F. pratensis plants were transplanted into the soil microcosms described above in a
uniform hexagonal pattern. A. absinthium plants were
grown outdoors in 1 gallon pots for approximately 1
year. Then, 12 plants of the same size were selected,
and each was divided into four ramets. Two same sized
leaves were left on the shoots of each ramet. The roots
were carefully pruned to remove all new and fine root
material. The same volume of woody root material
remained on each ramet. Sixteen such ramets were
randomly selected out of the lot for each [CO2]
treatment. Four of these ramets were transplanted into
each of four microcosms in the low- and high-[CO2]
greenhouses using a pattern that maximized interplant
spacing and distance from the sides of the PVC tubes.
For the next 7 weeks, the microcosms were watered
every 2–3 days with 2 cm water so that the surface soil
was always moist. Soil moisture was allowed to
decline to less than 10% volumetric content over a 5day period following a final water application, after
which the soil wetting experiment was initiated.
2.3. Soil moisture content and temperature
Soil moisture content was monitored using time
domain reflectometry. In brief, a P2M probe (TRIMEFM2, IMKO, Ettlingen, UK) was inserted into the soil
once daily over the course of the experiment in a
pattern that avoided soil moisture being measured at
the same locality at any time. The soil moisture
measurements were taken before the wet-up treatment, immediately following wet-up, and then after
each soil CO2 emission measurement. Soil temperature was monitored continuously at 5 cm depth using
copper constantin thermocouples shielded from
moisture contact using nonconductive plastic shrink
tubing and silicone sealant. Four thermocouples
were placed in each of the two greenhouses (eight
total), two in A. absinthium microcosms and two in
F. pratensis microcosms.
249
2.4. Soil [CO2]
Three stainless steel tubes with an internal diameter
of 1.5 mm were installed at three depths of 15, 30, and
45 cm in each microcosm. The inserted end of the gas
sampling tubes was fitted with a small 2.25 cm long
polypropylene veil to prevent small soil particles from
entering. The protruding end was capped with a brass
swagelock union and fitted with a latex septa so that
gas samples could be withdrawn using a nylon syringe.
Each time a tube was sampled for soil atmosphere, we
withdrew 6 ml of gas and discarded it. Then a 12-ml
sample was withdrawn and injected into a 10-ml
evacuated vacutainer tube (Becton Dickinson, Franklin Lakes, NJ), insuring that a positive pressure was
sustained and inward gas diffusion was minimized
during the time elapsed before the gas was analyzed
for [CO2]. The vacutainers were prepared by flushing
the internal air space twice with pure N2 gas, and then
drawing a vacuum to 40 mTorr (approximately
0.00005 atm).
The soil gas samples were analysed for [CO2]
within 24 h after sampling by injecting them into a gas
chromatograph (Hewlett Packard, model 5890, series
II, Palo Alto, CA, USA) equipped with a Poropaq QS
column and a thermal conductivity detector. Standards
of 2012, 4024, 8048, 12,062, and 16,096 mmol mol1
CO2 were prepared and used to calibrate the
instrument. Certified standards of 506 and
10,100 mmol mol1 CO2 were injected after each
12 samples analyzed to correct for zero drift.
Calibrations yielded R2 values that were greater than
or equal to 0.997.
2.5. Soil CO2 emissions
A small PVC ring (12 cm diameter by 6 cm height)
was permanently established in the central position of
each microcosm. The rings were buried 2 cm into the
soil surface and the soil around the outside of the rim
lightly compressed in order to hold them in place. A
PVC cap that had been machined to fit loosely over the
ring was placed on top of it at the time of measurement.
To measure soil CO2 emission, air was moved through
the soil cuvette at approximately 50 cm3 s1 using a
portable infrared gas analyzer (IRGA, model LCA-2,
ADC, Hoddesdon Herts, UK). Soil CO2 emission rates
were recorded beginning 10 min after the cuvette was
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placed over a ring and the [CO2] in the incoming and
outgoing air streams had reached a steady-state
condition (Piñol et al., 1995). The [CO2] in the
incoming and outgoing air streams were recorded and
used to calculate soil CO2 emissions (J in mmol CO2
m2 s1) using the relationship:
J¼
Q DCO2
A
(1)
where A is the surface area of the chamber, Q the air
flow rate through the chamber, and DCO2 is the
difference in molar CO2 concentration between the
outgoing and the incoming air streams and were corrected for temperature and pressure (Smart et al.,
1999). Each day soil CO2 measurements were taken,
the IRGA response to CO2 was calibrated against
prepared standards of 282 and 627 mmol mol1 CO2.
Soil CO2 emissions were monitored before, during
and for 7 days following a simulated precipitation
event of 4 cm of distilled water. On the fifth day, at
120 h following wetting, no soil CO2 emission’s
measurements were taken because of instrumentation
malfunction. All of the measurements following the
first day were initiated 1.5 h before mid-day to
minimize temperature variation during the measurement period. Once the measurements were initiated, it
took approximately 3 h to complete the cycle. During
this time the soil temperature changed by about 2.5 8C
(Fig. 1).
A static chamber method (Rolston, 1986) was used
to determine the amount of CO2 lost from the soil
profile immediately following the precipitation treatment. The 4 cm of water were rained over the surface
for a period of approximately 12–15 min. Precipitation events of this intensity are not uncommon to the
region where cool Atlantic air masses descend and
mix with warm, humid air over the Mediterranean Sea.
Immediately following water application, a 12-ml gas
sample was withdrawn from inside the gas exchange
ring at 2 cm above the soil surface. Then a PVC cap
with dimensions identical to the one used for the
dynamic CO2 emissions measurements was placed on
top of the ring. Each cap was equipped with a fitting
that had a 0.125-in. port and a latex septum to allow
gas sampling from within the chamber. Five minutes
after the cap was placed over the ring, a second 12-ml
sample was slowly withdrawn from the chamber
through a stainless steel port and stored in a vacutainer.
The gas within the vacutainers was then analyzed for
[CO2] using the gas chromatograph described above.
Soil surface CO2 flux was also calculated at a few
selected intervals using a diffusive transport model
(De Jong and Schappert, 1972; Rolston, 1986). The
model assumes a steady-state soil CO2 flux, q,
controlled by diffusion of CO2 through the soil
profile, so that
q ¼ D
ðd½CO2 Þ
dz
(2)
and q calculated was mmol CO2 m2 s1. D is the
effective diffusion coefficient (m2 s1) for the soil
used in this investigation (Piñol et al., 1995). D was
calculated according to:
10=3
D¼
Fig. 1. Soil temperature at 5 cm, measured using copper constantin
thermocouples shielded from moisture contact using nonconductive
plastic shrink tubing and silicone sealant. Shown for each point is the
average temperature of four individual observations in separate soil
microcosms, two of which were in a greenhouse where the CO2
concentration was controlled at 360 mmol mol1 CO2 air and two of
which were in a greenhouse controlled at 500 mmol mol1 CO2 air.
dDa ðPeff Þ
E2
(3)
where d is a coefficient that compensates for the
existence of non-ideal pore volume, Da the diffusion
coefficient of CO2 in air (m2 s1), E is the voids ratio
or total soil porosity, Peff the effective soil porosity,
which is equal to the total soil porosity minus the
volumetric water content, provided from the soil
moisture curves shown in Fig. 2.
2.6. Plant biomass and leaf area
Shoots were clipped to ground level and all roots
and soil material were removed to a depth of 45 cm at
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
251
3. Results
3.1. Soil temperature and moisture
Fig. 2. Soil volumetric moisture content (%) in the upper 25 cm of
soil before, and for 7 days following a simulated 4 cm precipitation
event. Shown are the means and standard errors for eight observations
for (A) F. pratensis and (B) A. absinthium growing in microcosms
under two CO2 concentration treatments as described in the upper
right corner of each panel. Time at 12 h represents the time at which a
simulated precipitation event of 4 cm was rained onto the soil.
the end of the experiment. Visible roots were collected
immediately and washed. The soil was wet sieved
(2 mm) and all root material that did not pass through
the sieve was also collected. Fine root material that
floated to the surface of water following wet sieving
was removed manually. Root biomass is reported on a
45-cm depth basis because visual inspection revealed
that root density fell quickly below about 45 cm.
Whole plant shoots were removed and leaf area
determined using a planimeter (Licor Inc., model LI3000, Lincoln, Nebraska, USA). The leaf and root
material were placed in a drying oven at 65 8C for 3
days after which weights were recorded.
The average daily minimum temperature at 5 cm
for microcosms in the 360 mmol mol1 CO2 greenhouse was 13.1 0.6 8C (mean S.E.) over the 7day experimentation, and 13.0 1.0 8C for containers
in the 500 mmol mol1 CO2 greenhouse. The corresponding average maximum temperatures were 22.2
3.7 and 21.7 2.7 8C. On the third and seventh
days following the wetting treatment, there was some
cloud cover. On those days maximum soil temperatures at 5 cm depth during the period when soil CO2
emissions measurements were being taken were about
6–8 8C lower than on sunny days (Fig. 1). There was
no evidence suggesting this variation in mid-day
temperature strongly influenced soil CO2 emissions,
or the relative differences between ambient [CO2]
treatments or plant taxa.
Before water was applied, soil moisture was
approximately 4% lower in soils under F. pratensis,
(Fig. 2A) but soil moisture increased to the same level
in all microcosms following the wetting treatment
(Fig. 2A and B). Soil moisture content thereafter
declined rapidly and at nearly the same rate regardless
of [CO2] treatment. There was some evidence that soil
moisture was depleted more rapidly over the first 36 h
in the soil microcosms with F. pratensis plants (Fig. 2),
(pairwise t-test, t < 0.05). After 36 h, soil moisture
changed in a similar manner for both species and both
CO2 treatments (Fig. 2A and B). Under all treatment
conditions it took more than 120 h for soil moisture to
decline to approximately the same levels observed
prior to wetting.
2.7. Statistical analyses
3.2. Plant biomass and leaf area
Root and shoot biomass were analyzed using
analysis of variance (ANOVA) with a randomized
block design (General Linear Models Procedure, SAS
Inc., 1986), where [CO2] and plant taxa represented
the independent variables. Carbon dioxide emissions
were analyzed according to a repeated measures
ANOVA where daily CO2 emission was the repeated
measure. Unless otherwise indicated, any mean
comparison designated significantly different refers
to the probability of commiting a type I error of
P 0.05.
Both A. absinthium and F. pratensis showed
positive growth responses to exposure to elevated
[CO2] (Fig. 3), but biomass allocation patterns
between shoots and roots differed between the two
taxa. Elevated [CO2] significantly increased shoot
biomass production by A. absinthium (46.1 17.9%,
mean S.E., n = 4), but did not significantly increase
shoot biomass production by F. pratensis (14.4 6.5%). The increase in new shoot biomass for A.
absinthium corresponded to an increase in leaf area
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D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
F. pratensis were 38.5 3.3% under 360 mmol mol1
CO2 increasing significantly to 51.5 2.8% under
500 mmol mol1 CO2 (Fig. 3).
3.3. Soil CO2 emissions
Fig. 3. Root and shoot biomass for A. absinthium and F. pratensis
grown in a greenhouse environment under controlled CO2 concentrations of 500 and 360 mmol mol1 CO2 air.
and leaf area index (LAI, m2 leaf area m2 ground
area); whereas, F. pratensis did not show a statistically
significant increase in either leaf area or LAI (Figs. 3
and 4). The root biomass of A. absinthium also
responded positively to elevated [CO2], where it
increased, on average, by 104.6 21.9%. Root
biomass for F. pratensis (Fig. 3) increased significantly by 55.9 12.7% in elevated [CO2]. The A.
absinthium root biomass represented 23.6 1.0% of
the total biomass under 360 mmol mol1 CO2, and
28.6 3.3% under 500 mmol mol1 CO2 (P 0.05,
Fig. 3). The corresponding values for root biomass of
Fig. 4. Leaf area index for A. absinthium and F. pratensis grown in a
greenhouse environment under controlled CO2 concentrations of
500 and 360 mmol mol1 CO2 air.
Our estimates of soil CO2 flux based on the
diffusion model agreed well with rates of soil CO2
emissions measured using the dynamic flow system
(compare Table 1 with Figs. 5 and 6). The absolute
flux rates predicted by the model were slightly lower
immediately following wet-up, than those measured
using the dynamic flow system. The differences were
not large, being less than about 20%, and did not alter
interpretation of the results, because the same general
patterns emerged whether using dynamic flow
measures or estimates generated by the model
exercises.
Carbon dioxide emissions from soils were similar
for both F. pratensis and A. absinthium prior to the
wet-up treatment (Fig. 5A and B), although the
modeled values were slightly higher for F. pratensis
under ambient [CO2] (Table 1). The CO2 emissions
from soils of A. absinthium and F. pratensis growing in
elevated versus ambient [CO2] were also similar
before water addition (Fig. 5A and B). Soil CO2
‘exhalation’ caused by soil gas displacement immediately after wetting was considerable. For both A.
absinthium and F. pratensis, the rates CO2 was
released immediately following wetting were more
than 10 times higher than the steady-state CO2
emission rates (Fig. 5A and B). None of the exhalation
rates, we measured, were statistically significantly
different among CO2 treatments or between A.
absinthium and F. pratensis (Fig. 5A and B).
At 4 h following the precipitation treatment, CO2
emissions from soils of each plant species had not
significantly changed from those measured prior to the
wet-up treatment (Fig. 5A and B). In the case of F.
pratensis, the model predicted CO2 emissions actually
declined slightly at 4 h (Table 1, pairwise t-test, t <
0.05). Soil CO2 emissions from F. pratensis cultures
began to rise between 24 and 48 h following wet-up
(Fig. 5B) and 48 h following water addition for A.
absinthium (Fig. 5A). Seventy two to one hundred
forty four hours following precipitation, the increase
in CO2 emissions from soil microcosms of both plant
species and at both external [CO2] concentrations
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
253
Table 1
Carbon dioxide emission from soils beneath canopies of Artemisia absinthium and Festuca pratensis grown in soil microcosms under two CO2
concentrations as indicated
Time (h)
Artemisia absinthium
360 (mmol mol1)
0
4
72
144
3.4
2.4
8.3
5.6
0.3
0.9
1.6
1.2
Festuca pratensis
500 (mmol mol1)
6.3
3.0
12.5
7.6
0.8
0.7
0.8
1.4
360 (mmol mol1)
8.2
1.7
14.0
9.7
1.6
0.3
0.6
1.2
500 (mmol mol1)
7.6
3.0
17.8
11.9
1.3
0.7
1.9
1.0
Shown are the means one standard error of the mean (n = 4) reported as mmol m2 s1.
reached an apparent maximum and started to decline.
Carbon dioxide emissions at the maximum rate we
measured increased two to three times above the prewet-up rates for A. absinthium and three to five times
higher for F. pratensis. The relative magnitude of these
changes differed because soil CO2 emissions from
F. pratensis microcosms were initially slightly greater
than A. absinthium under all measurement conditions.
When analyzed according to a repeated measures
ANOVA, soils of F. pratensis microcosms exposed to
elevated [CO2] had significantly higher CO2 emissions
over the entire course of the soil wetting treatment (P
= 0.011), but soils of A. absinthium did not (P = 0.23).
When soil water content declined below 10% (144–
168 h), the difference between ambient and elevated
CO2 treatments did not persist, and CO2 emissions
returned to rates observed before water was applied.
3.4. Soil [CO2]
Soil [CO2] increased immediately (4 h) and
substantially following wet-up. Carbon dioxide concentration in soil was 3106 213 mmol mol1 at
15 cm (n = 8 for ambient and elevated CO2 treatments
combined), 7366 386 mmol mol1 at 30 cm and
8622 1327 mmol mol1 at 45 cm for A. absinthium
before water addition. Soil [CO2] increased to 5731 417, 12,314 627 mmol mol1 at 30 cm and 14,761
954 mmol mol1 at 45 cm after 4 h. The magnitude of these changes were similar in soils of the
Fig. 5. Soil CO2 emissions during a 7-day period following a simulated precipitation event for soils under (A) Artemisia absinthium and (B)
Festuca pratensis grown in a greenhouse environment under controlled CO2 concentrations of 500 and 360 mmol mol1 CO2 air as indicated.
The arrow indicates the point at which a 4 cm precipitation treatment was applied.
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Fig. 6. Soil CO2 concentration with depth for (A) Artemisia
absinthium and (B) Festuca pratensis grown in soil micocosms
and exposed to either 360 or 500 mmol mol1 CO2. Shown are the
means and standard errors of the means (n = 8) for combined
observations of the two CO2 concentration treatments.
F. pratensis microcosm (Fig. 6B). The concentration
of CO2 further increased (72 h), particularly at the
shallower depths, and then relaxed back to levels
approaching those measured prior to the wet-up
treatment (data not shown). At that time (144 h), the
[CO2] with depth was not statistically significantly
different from that measured prior to the precipitation
treatment.
4. Discussion
The primary objective of this study was to
determine how soil CO2 fluxes respond to short-term
episodes of water addition. Information on such
responses may assist in ecosystem level efforts to
model seasonally dry Mediterranean and other
ecosystems that experience seasonal wetting and
drying cycles. Our results supported a general
hypothesis of soil CO2 emissions being driven largely
by rapid changes in soil moisture content in soils of
warm arid or semi-arid environments (Liu et al., 2002;
Maestre and Cortina, 2003) that can be divided into
two components. There was an immediate release of
CO2 from soils, probably as a result of water
displacement of pore space gas and its release as a
consequence of pressure variation (Norman et al.,
1992). Our investigation contributes to understanding
the quantitative importance of such CO2 emissions:
the immediate release of CO2 from the soil occurred at
about 10 times the average rate of CO2 emission
observed over the entire course of the 7-day period
following wet-up (Figs. 5 and 6) but of very short
duration. Four hours following wet-up, the rates of
CO2 emission had returned to values equal to or lower
than the rates observed before wet-up (Figs. 5 and 6).
The total amount of CO2–C released during the 12 min
we measured CO2 exhalation was approximately 6%
of the integrated total CO2–C released during the 7day monitoring period. Thus, given that exhalation
phenomena in natural ecosystems are of short
duration, they may contribute to a relatively small
fraction of the total CO2 released, depending on
frequency. Previous investigations conducted under
field conditions have not accounted for CO2 exhalation. For example, Liu et al. (2002) provide
comprehensive information concerning the overall
duration of enhanced CO2 emissions following wet-up
of prairie soils. However, their first measurements of
soil CO2 emissions were taken at approximately 24 h
following the precipitation event.
Water addition quickly stimulated CO2 production,
as evidenced by a rapid increase (4 h) of CO2
concentration in the soil profile (Fig. 6A and B).
Nonetheless, this did not lead to an immediate
increase (24 h) in CO2 emissions (Fig. 5A and B).
Soil water content and thus water filled pore space was
higher during the first 24–36 h following wet-up. This
would slow diffusion of CO2 out of the soil and this
idea was supported by the modeling exercises that
use water filled pore space as a variable (Eq. (3) and
Table 1). It is unlikely that pressure caused by the
precipitation event resulted in CO2 moving down in
the soil profile (Fig. 6A and B), because large amounts
of CO2 were released and the relaxation of such
pressure (<4 h) did not result in [CO2] returning to
levels similar to those measured immediately before
the precipitation event.
Soil moisture did not differ between the two CO2
treatments. Soil moisture following wet-up declined
slightly faster in the F. pratensis microcosms during
the first 24 h following the wet-up treatment (Fig. 2A),
but subsequently declined at the same rate for both
CO2 treatments and for both plant taxa (Fig. 2A and
B). We anticipated that soil moisture might change
more slowly in the elevated CO2 treatments because
CO2 lowers stomatal conductance and thus evapo-
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
transpiration from soils may decline (Field et al., 1995).
The increase in leaf surface area of approximately 30%
forA.absinthium(Fig.5A),alongwithanincreaseinroot
density, apparently compensated for any effects of
lowered stomatal conductance by elevated [CO2]. This
may not have played as strong a role for F. pratensis,
where the apparent 14.4% increase in leaf area (Fig. 4)
was not statistically significant.
Elevated [CO2] significantly increased soil CO2
emissions for F. pratensis (Fig. 5B), but for A.
absinthium (Fig. 5A) the increase in CO2 emission was
not statistically significant (P < 0.05). Furthermore,
elevated [CO2] significantly increased root biomass
and root:shoot ratio for F. pratensis, and these changes
in below ground carbon allocation were also evident in
A. absinthium (Fig. 3). Thus, both species responded
to elevated [CO2] in a manner consistent with that
observed for other plants (Zak et al., 2000). It has been
estimated, even for soils with high litter contents like
forest soils, that 30–50% of the total soil respiration
activity can be attributed to root respiration (Bowden
et al., 1993; Andrews et al., 1999), and much less
attributed to non-rhizosphere soil heterotrophic
microbial activity (Johnson et al., 1994). Estimates
of the contribution of rhizosphere respiration to total
soil respiration are uncertain, but it may contribute
substantially (Killham and Yeomans, 2001). New
evidence showing that recently fixed photosynthate is
the primary driver of soil respiration in boreal pine
forests (Hogberg et al., 2001) supports this contention.
It was likely that root plus rhizosphere respiration was
the major component of soil respiration reported here.
Soils used in this investigation were disturbed, with no
surface litter and very little organic carbon content
(0.2%). Root biomass and soil respiration increased
proportionally for F. pratensis, and this trend was
apparent for A. absinthium as well (Fig. 5A).
The two species differed in their response to
elevated CO2 and may reflect different strategies for
acquiring below ground resources. F. pratensis is an
herbaceous taxa that may allocate larger amounts of
carbon into fine root production and rhizodeposition in
order to stimulate mineralization and release of soil
nutrients (Hobbie, 1992). A. absinthium, on the other
hand, is a drought tolerant woody perennial that may
allocate a larger amount of below ground carbon to
sustaining long lived roots that can access water. Thus,
F. pratensis may produce greater numbers of fine or
255
very fine roots of shorter lifespan than those of A.
absinthium. Turnover and decomposition of such roots
may contribute to higher microbial respiratory
activity. When we harvested roots, we noted that F.
pratensis had many very fine roots (<1 mm) and a
number of these were turning brown. In contrast A.
absinthium had no new roots of <2 mm diameter.
We did not attempt to separate microbial from root
respiration, a difficult if not impossible exercise
(Killham and Yeomans, 2001). Zak et al. (2000), have
pointed out that the changes reported for such pools
were neither consistent or statistically significantly
different, and variability within the measurements so
large that little could be concluded about them. Lin et
al. (1999, 2001) found evidence from isotopic
signatures on soil respired CO2 supporting that
rhizosphere respiration (root respiration plus that of
rhizosphere microbes) was strongly stimulated by
elevated CO2. Whether soil CO2 production in the
microcosms used in this investigation was derived
from root respiration or microbial respiration, our
results support that below ground C allocation,
including soil respiration activity, increases in
response to CO2 fertilization.
5. Summary
Our investigation shows that using a few discrete
sampling dates over long time periods may not fully
quantify soil CO2 loss in arid or semi-arid ecosystems
with frequent rainfall events during the wet season.
For both grass species and woody perennial shrub, a
4 cm precipitation event caused soil CO2 emissions to
increase by more than 10 times immediately following
soil wetting. Water filled pore space then appeared to
limit CO2 efflux for several hours. Our data further
indicate that a woody perennial shrub responded in a
manner different from that of a ruderal herbaceous
taxa when both species were grown and measured
under the same conditions and exposed to elevated
CO2. We found that soil microcosms were reasonable
proxies for conducting investigations concerning the
influence of elevated CO2 on mechanisms governing
soil respiration responses to elevated CO2. This is an
important consideration when taking into consideration the substantial expense involved in conducting
CO2 fertilization treatments under field conditions.
256
D.R. Smart, J. Peñuelas / Applied Soil Ecology 28 (2005) 247–257
Acknowledgements
We acknowledge support from CICYT CLI 990479 and CICYT REN-2000-0278/CLI and Carburos
Metalicos S.A. We thank Angela Ribas and Nuria
Querol for general assistance in many phases of the
project and to Jose Montero for technical assistance
with the greenhouse system. Robert Save, Carme Biel,
Juan Ignacio Montero, and Oriol Marfa of the Institut
de Recerca i Tecnologia Agroalimentaries (IRTA)
helped providing facilities for the project.
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