Directory UMM :Data Elmu:jurnal:S:Soil Biology And Chemistry:Vol32.Issue5.2000:
Soil Biology & Biochemistry 32 (2000) 699±706
www.elsevier.com/locate/soilbio
Temperature eects on the diversity of soil heterotrophs and the
d13C of soil-respired CO2
Jerey A. Andrews a,*, Roser Matamala a, Kristi M. Westover a, William H. Schlesinger a, b
a
Department of Botany, Duke University, Durham, NC 27708, USA
Division of Earth and Ocean Sciences, Nicholas School of the Environment, Duke University, Durham, NC 27708, USA
b
Received 5 May 1999; received in revised form 15 September 1999; accepted 28 October 1999
Abstract
We measured the respiration rates, d13C of respired CO2, and microbial community composition in root-free bulk soils
incubated at 4, 22 and 408C. The soils were obtained from the Duke Forest Free-Air CO2 Enrichment (FACE) experiment
where organic carbon in soils sampled from the elevated CO2 plots contained a unique 13C label that was derived from FACE
fumigation. The CO2 produced by soil heterotrophs at 48C was 2.2 to 3.5- enriched in 13C relative to CO2 respired at 22 and
408C and was similarly enriched relative to bulk soil carbon. There was no isotopic dierence between CO2 produced at 22 and
408C. Respiration rates increased exponentially with temperature from 0.25 mg CO2 g soilÿ1 dÿ1 at 48C to 0.73 mg CO2 g soilÿ1
dÿ1 at 408C. Microbial community composition, as measured by the dierences in populations of morphology types, diered
across the temperature range. Only eight of 67 microbial morphology types were common to all three incubation temperatures,
while six types were unique to 48C soil, 17 to 228C soil and 18 to 408C soil. Species richness, approximated from morphology
type, was signi®cantly lower at 48C than at 22 and 408C. This change in microbial community structure from 4 to 22 and 408C
caused a shift in mineralizable carbon pools, resulting in a shift in the isotopic composition of CO2 respired at the low
temperature. 7 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Isotope fractionation; Soil respiration; Soil carbon; Soil microbes
1. Introduction
Studies of carbon isotopes provide a powerful tool
to elucidate carbon dynamics in soils and are widely
used to understand ecosystem carbon budgets, gas ¯ux
from the soil and decomposition dynamics. The isotopic composition of soil CO2 is determined by the interplay of a variety of biological and physical processes,
as well as chemical reactions, in the soil environment
(Amundson et al., 1997). The carbon isotope ratios in
* Corresponding author. Present address: Department of Ecology
and Evolutionary Biology, MS 170, Rice University, P.O. Box 1892,
Houston, TX 77251-1892, USA. Tel.: +1-713-527-8750; fax: +1713-285-5232.
E-mail address: jandrews@rice.edu (J.A. Andrews).
soil CO2 are determined by the mixture of CO2 derived
from three sources: inward diusion from the overlying atmosphere, respiration of live roots and the oxidation of soil organic matter (SOM) by soil
heterotrophs.
Carbon isotope ratios in soil organic matter change
during decomposition. This change is mediated by
both the isotopic composition of the chemical constituents of SOM as well as discrimination during decomposition by soil heterotrophs (AÊgren et al., 1996).
The metabolic fractionation of carbon in plants during
photosynthesis and during the synthesis of various biochemical compounds (O'Leary, 1981) results in low
contents of 13C in slowly decomposing substances,
such as lignin (Benner et al., 1987). However, 12C may
be used preferentially by decomposers (Blair et al.,
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 2 0 6 - 0
700
J.A. Andrews et al. / Soil Biology & Biochemistry 32 (2000) 699±706
1985), resulting in a tendency for 13C enrichment in
the remaining SOM (Nadelhoer and Fry, 1988).
Therefore, variation in the composition of SOM and
the activity of soil heterotrophs will result in changes
in the carbon isotope composition of soil CO2.
It is widely known that temperature has an eect on
microbial activity (MacDonald et al., 1995) and that
certain groups of microbes are adapted to particular
temperature regimes (Allen and Brock, 1968; Zogg et
al., 1997). Zogg et al. (1997) have postulated that temperature-induced changes in the soil microbial community could result in a shift in the use of available
substrates in the soil. Because of the dierences in the
carbon isotopic ratios found among components of
SOM, it is likely that such a microbial community
shift would impact the isotopic composition of microbe-produced soil CO2 and soil respired CO2. Recognizing this eect on the isotopic composition of soilderived CO2 is an important factor for the interpretation of an increasing number of biogeochemical studies of soil carbon dynamics. In addition, an
understanding of how soil microbes aect the isotopic
composition of soil CO2 will increase our understanding of SOM formation.
Although there have been many studies on the isotopic composition of SOM, relatively few have examined
the factors controlling the carbon isotope ratios of
soil-derived CO2 (Amundson et al., 1997). In this
study, we examined the eect of temperature on the
isotopic composition of CO2 produced by soil heterotrophs and the concurrent relationship between temperature and soil microbial community composition.
Soils for our experiments were sampled from the Duke
Forest Free Air CO2 Enrichment (FACE) site. FACE
technology was developed to study the eects of high
CO2 on intact ecosystems without the use of enclosures
(Hendrey et al., 1999). The CO2 used to fumigate this
experiment is derived from natural gas and, because it
is strongly depleted in 13C, it serves as an isotopic
label of new plant tissues and soil organic matter. We
utilized this unique isotopic label to better characterize
soil heterotroph activity at various temperatures.
2. Material and methods
2.1. Study site
The study site was the Duke Forest Free-Air CO2
Enrichment (FACE) experiment, located in the central
Piedmont region of North Carolina, USA (35897'N
79809 'W). The site was cleared of a mixed forest in
1981, drum chopped and burned in 1982 and established as a loblolly pine (Pinus taeda L.) plantation in
1983. Soils are of the Enon series, a low-fertility Ultic
Al®sol that is typical of many upland areas in the
southeastern US. The soil is derived from igneous
rock, yielding a well-developed, acidic pH 5:75 pro®le with mixed clay mineralogy.
The site contains six 30-m dia circular plots in a
16-y-old loblolly pine forest. Each of the plots are surrounded by an array of vertical vent pipes that extend
to the top of the forest canopy. Three `elevated' plots
are fumigated with CO2 through the vent pipes to
maintain an atmospheric CO2 concentration inside the
plots that is 200 ml lÿ1 above ambient (575 ml lÿ1 average, May±October 1997). The remaining three `control' plots are fumigated with ambient air only. To
account for site variability each elevated plot is paired
with a control plot of similar topography and vegetation density. Continuous fumigation began 27
August 1996.
The CO2 used for fumigation is derived from natural
gas and is, therefore, strongly depleted in 13C d13 C
ÿ43:120:6- (2S.E.) versus PDB). The standard expression of stable carbon isotope ratios is in dierential notation (Craig, 1953), where
!
13
C=12 Csample ÿ 13 C=12 Cstandard
13
1000
1
d C
13
C=12 Cstandard
and is expressed in parts per thousand (-). The
accepted standard is the PDB carbonate (Craig, 1957).
Using this CO2 to elevate the atmospheric concentration by 200 ml lÿ1 changes the d13C of CO2 in the
FACE plot from ÿ8 to ÿ20-. The photosynthetic
fractionation (Farquhar et al., 1989) by the loblolly
pine
results
in
new
photosynthate
with
d13 C ÿ39:321:4-, as measured in young needles
sampled from September 1997 (Ellsworth, 1999). Fine
roots (
www.elsevier.com/locate/soilbio
Temperature eects on the diversity of soil heterotrophs and the
d13C of soil-respired CO2
Jerey A. Andrews a,*, Roser Matamala a, Kristi M. Westover a, William H. Schlesinger a, b
a
Department of Botany, Duke University, Durham, NC 27708, USA
Division of Earth and Ocean Sciences, Nicholas School of the Environment, Duke University, Durham, NC 27708, USA
b
Received 5 May 1999; received in revised form 15 September 1999; accepted 28 October 1999
Abstract
We measured the respiration rates, d13C of respired CO2, and microbial community composition in root-free bulk soils
incubated at 4, 22 and 408C. The soils were obtained from the Duke Forest Free-Air CO2 Enrichment (FACE) experiment
where organic carbon in soils sampled from the elevated CO2 plots contained a unique 13C label that was derived from FACE
fumigation. The CO2 produced by soil heterotrophs at 48C was 2.2 to 3.5- enriched in 13C relative to CO2 respired at 22 and
408C and was similarly enriched relative to bulk soil carbon. There was no isotopic dierence between CO2 produced at 22 and
408C. Respiration rates increased exponentially with temperature from 0.25 mg CO2 g soilÿ1 dÿ1 at 48C to 0.73 mg CO2 g soilÿ1
dÿ1 at 408C. Microbial community composition, as measured by the dierences in populations of morphology types, diered
across the temperature range. Only eight of 67 microbial morphology types were common to all three incubation temperatures,
while six types were unique to 48C soil, 17 to 228C soil and 18 to 408C soil. Species richness, approximated from morphology
type, was signi®cantly lower at 48C than at 22 and 408C. This change in microbial community structure from 4 to 22 and 408C
caused a shift in mineralizable carbon pools, resulting in a shift in the isotopic composition of CO2 respired at the low
temperature. 7 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Isotope fractionation; Soil respiration; Soil carbon; Soil microbes
1. Introduction
Studies of carbon isotopes provide a powerful tool
to elucidate carbon dynamics in soils and are widely
used to understand ecosystem carbon budgets, gas ¯ux
from the soil and decomposition dynamics. The isotopic composition of soil CO2 is determined by the interplay of a variety of biological and physical processes,
as well as chemical reactions, in the soil environment
(Amundson et al., 1997). The carbon isotope ratios in
* Corresponding author. Present address: Department of Ecology
and Evolutionary Biology, MS 170, Rice University, P.O. Box 1892,
Houston, TX 77251-1892, USA. Tel.: +1-713-527-8750; fax: +1713-285-5232.
E-mail address: jandrews@rice.edu (J.A. Andrews).
soil CO2 are determined by the mixture of CO2 derived
from three sources: inward diusion from the overlying atmosphere, respiration of live roots and the oxidation of soil organic matter (SOM) by soil
heterotrophs.
Carbon isotope ratios in soil organic matter change
during decomposition. This change is mediated by
both the isotopic composition of the chemical constituents of SOM as well as discrimination during decomposition by soil heterotrophs (AÊgren et al., 1996).
The metabolic fractionation of carbon in plants during
photosynthesis and during the synthesis of various biochemical compounds (O'Leary, 1981) results in low
contents of 13C in slowly decomposing substances,
such as lignin (Benner et al., 1987). However, 12C may
be used preferentially by decomposers (Blair et al.,
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 2 0 6 - 0
700
J.A. Andrews et al. / Soil Biology & Biochemistry 32 (2000) 699±706
1985), resulting in a tendency for 13C enrichment in
the remaining SOM (Nadelhoer and Fry, 1988).
Therefore, variation in the composition of SOM and
the activity of soil heterotrophs will result in changes
in the carbon isotope composition of soil CO2.
It is widely known that temperature has an eect on
microbial activity (MacDonald et al., 1995) and that
certain groups of microbes are adapted to particular
temperature regimes (Allen and Brock, 1968; Zogg et
al., 1997). Zogg et al. (1997) have postulated that temperature-induced changes in the soil microbial community could result in a shift in the use of available
substrates in the soil. Because of the dierences in the
carbon isotopic ratios found among components of
SOM, it is likely that such a microbial community
shift would impact the isotopic composition of microbe-produced soil CO2 and soil respired CO2. Recognizing this eect on the isotopic composition of soilderived CO2 is an important factor for the interpretation of an increasing number of biogeochemical studies of soil carbon dynamics. In addition, an
understanding of how soil microbes aect the isotopic
composition of soil CO2 will increase our understanding of SOM formation.
Although there have been many studies on the isotopic composition of SOM, relatively few have examined
the factors controlling the carbon isotope ratios of
soil-derived CO2 (Amundson et al., 1997). In this
study, we examined the eect of temperature on the
isotopic composition of CO2 produced by soil heterotrophs and the concurrent relationship between temperature and soil microbial community composition.
Soils for our experiments were sampled from the Duke
Forest Free Air CO2 Enrichment (FACE) site. FACE
technology was developed to study the eects of high
CO2 on intact ecosystems without the use of enclosures
(Hendrey et al., 1999). The CO2 used to fumigate this
experiment is derived from natural gas and, because it
is strongly depleted in 13C, it serves as an isotopic
label of new plant tissues and soil organic matter. We
utilized this unique isotopic label to better characterize
soil heterotroph activity at various temperatures.
2. Material and methods
2.1. Study site
The study site was the Duke Forest Free-Air CO2
Enrichment (FACE) experiment, located in the central
Piedmont region of North Carolina, USA (35897'N
79809 'W). The site was cleared of a mixed forest in
1981, drum chopped and burned in 1982 and established as a loblolly pine (Pinus taeda L.) plantation in
1983. Soils are of the Enon series, a low-fertility Ultic
Al®sol that is typical of many upland areas in the
southeastern US. The soil is derived from igneous
rock, yielding a well-developed, acidic pH 5:75 pro®le with mixed clay mineralogy.
The site contains six 30-m dia circular plots in a
16-y-old loblolly pine forest. Each of the plots are surrounded by an array of vertical vent pipes that extend
to the top of the forest canopy. Three `elevated' plots
are fumigated with CO2 through the vent pipes to
maintain an atmospheric CO2 concentration inside the
plots that is 200 ml lÿ1 above ambient (575 ml lÿ1 average, May±October 1997). The remaining three `control' plots are fumigated with ambient air only. To
account for site variability each elevated plot is paired
with a control plot of similar topography and vegetation density. Continuous fumigation began 27
August 1996.
The CO2 used for fumigation is derived from natural
gas and is, therefore, strongly depleted in 13C d13 C
ÿ43:120:6- (2S.E.) versus PDB). The standard expression of stable carbon isotope ratios is in dierential notation (Craig, 1953), where
!
13
C=12 Csample ÿ 13 C=12 Cstandard
13
1000
1
d C
13
C=12 Cstandard
and is expressed in parts per thousand (-). The
accepted standard is the PDB carbonate (Craig, 1957).
Using this CO2 to elevate the atmospheric concentration by 200 ml lÿ1 changes the d13C of CO2 in the
FACE plot from ÿ8 to ÿ20-. The photosynthetic
fractionation (Farquhar et al., 1989) by the loblolly
pine
results
in
new
photosynthate
with
d13 C ÿ39:321:4-, as measured in young needles
sampled from September 1997 (Ellsworth, 1999). Fine
roots (