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Rising atmospheric carbon dioxide (CO2) could alter the carbon (C) and nitrogen (N) content of ecosystems, yet the magnitude of these effects are not well known. We examined C and N budgets of a subtropical woodland after 11 yr of exposure to elevated CO2. We used open-top chambers to manipulate CO2 during regrowth after fire, and measured C, N and tracer 15N in ecosystem components throughout the experiment. Elevated CO2 increased plant C and tended to increase plant N but did not significantly increase whole-system C or N. Elevated CO2 increased soil microbial activity and labile soil C, but more slowly cycling soil C pools tended to decline. Recovery of a long-term 15N tracer indicated that CO2 exposure increased N losses and altered N distribution, with no effect on N inputs. Increased plant C accrual was accompanied by higher soil microbial activity and increased C losses from soil, yielding no statistically detectable effect of elevated CO2 on net ecosystem C uptake. These findings challenge the treatment of terrestrial ecosystems responses to elevated CO2 in current biogeochemical models, where the effect of elevated CO2 on ecosystem C balance is described as enhanced photosynthesis and plant growth with decomposition as a first-order response.
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Cumulative response of ecosystem carbon and nitrogen stocks to
chronic CO
2
exposure in a subtropical oak woodland
Bruce A. Hungate
1
, Paul Dijkstra
1
, Zhuoting Wu
1,2
, Benjamin D. Duval
1,3
, Frank P. Day
4
, Dale W. Johnson
5
,
J. Patrick Megonigal
6
, Alisha L. P. Brown
4
and Jay L. Garland
7
1
Department of Biological Sciences and The Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ 86011, USA;
2
US Geological Survey, Flagstaff, AZ 86001,
USA;
3
US Dairy Forage Research Center, USDA-ARS, Madison, WI 53706, USA;
4
Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529, USA;
5
Department of
Natural Resources and Environmental Science, University of Nevada, Reno, NV 89557, USA;
6
Smithsonian Environmental Research Center, Edgewater, MD 21037, USA;
7
Environmental
Protection Agency, Microbiological and Chemical Exposure Assessment Research Division, Cincinnati, OH 45268, USA
Author for correspondence:
Bruce A. Hungate
Tel: +1 928 523 0925
Email: bruce.hungate@nau.edu
Received: 24 January 2013
Accepted: 10 April 2013
New Phytologist (2013)
doi: 10.1111/nph.12333
Key words: carbon cycling, elevated CO
2
,
global change, long-term experiment,
nitrogen cycling, scrub oak, soil carbon,
subtropical woodland.
Summary
Rising atmospheric carbon dioxide (CO
2
) could alter the carbon (C) and nitrogen (N) con-
tent of ecosystems, yet the magnitude of these effects are not well known. We examined C
and N budgets of a subtropical woodland after 11 yr of exposure to elevated CO
2
.
We used open-top chambers to manipulate CO
2
during regrowth after fire, and measured
C, N and tracer
15
N in ecosystem components throughout the experiment.
Elevated CO
2
increased plant C and tended to increase plant N but did not significantly
increase whole-system C or N. Elevated CO
2
increased soil microbial activity and labile soil C,
but more slowly cycling soil C pools tended to decline. Recovery of a long-term
15
N tracer
indicated that CO
2
exposure increased N losses and altered N distribution, with no effect on N
inputs.
Increased plant C accrual was accompanied by higher soil microbial activity and increased C
losses from soil, yielding no statistically detectable effect of elevated CO
2
on net ecosystem C
uptake. These findings challenge the treatment of terrestrial ecosystems responses to elevated
CO
2
in current biogeochemical models, where the effect of elevated CO
2
on ecosystem C
balance is described as enhanced photosynthesis and plant growth with decomposition as a
first-order response.
Introduction
Many experiments have examined the responses of plant produc-
tion and ecosystem carbon (C) balance to rising atmospheric
CO
2
(Reich et al., 2006a; Norby & Zak, 2011). Results from
these feature prominently in assessments of potential feedbacks
between the biosphere and the changing atmosphere (Dolman
et al., 2010). Compared to responses of photosynthesis and plant
growth to elevated CO
2
, the response of soil C is less well under-
stood, because changes in soil C content are difficult to detect
(Smith, 2004). Increased C in soil in response to elevated CO
2
is
sometimes found (Jastrow et al., 2005; Iversen et al., 2008,
2012), although more frequently there is no effect, whether
because of low statistical power or the absence of an important
effect is unclear (Hungate et al., 2009). Ecosystem-scale invento-
ries assessing C balance responses to elevated CO
2
also often
show no effect (Hungate et al., 1997b; Gielen et al., 2005; Gill
et al., 2006; Niklaus & Falloon, 2006; Adair et al., 2009),
although in aggregate some analyses suggest an effect is apparent
(Luo et al., 2006). Thus, global models projecting future C
dynamics of the biosphere have strong support for the effects of
CO
2
on plant growth (Denman et al., 2007), but less empirical
support for assumed effects on total ecosystem C storage. Our
first goal in this work was to construct a complete C inventory
for a subtropical oak woodland after 11 yr of exposure to elevated
CO
2
, to test whether the CO
2
treatment altered total system C
accumulation, and determine how any changes in C accumula-
tion were distributed among plant and soil pools.
Total ecosystem C content is a function of plant growth and
accumulation of plant biomass and detritus and also of C losses
through microbial decomposition. Microbial decomposition is
typically assumed to be a first-order process (Parton et al., 1987),
responding predictably and constantly to changes in substrate
supply, and thus is not expected to respond to elevated CO
2
independently of changes in substrate accumulation (Denman
et al., 2007). Challenging this idea, inputs of C to soil can stimu-
late mineralization of native soil organic matter (Lohnis, 1926;
Broadbent & Norman, 1947; Broadbent & Bartholomew, 1949;
Van Veen et al., 1991), and increased atmospheric CO
2
has been
shown to promote microbial activity (Dieleman et al., 2010) and
even soil C loss (Hoosbeek, 2004; Trueman & Gonzalez-Meler,
2005; Carney et al., 2007; Hagedorn et al., 2008; Paterson et al.,
2008; Taneva & Gonzalez-Meler, 2008; Langley et al., 2009;
Trueman et al., 2009; Drake et al., 2011; Reid et al., 2012).
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Research
Thus, soil processes influence potential C accumulation in
response to increasing atmospheric CO
2
, yet how and to what
extent are not well understood. Our second goal in this work was
to examine changes in soil microbial activity during the 11 yr of
CO
2
enrichment, and to test whether patterns of CO
2
effects on
soil microbial activity might help explain any effects (or lack of
effects) of elevated CO
2
on soil C stocks.
Carbon cycling in ecosystems is linked to cycles of other ele-
ments (Finzi et al., 2011), such as nitrogen (N). Simulations of
land carbon uptake using models with coupled N and C dynam-
ics usually differ, and in many cases differ strongly, from those
ignoring N (e.g. compare Cramer et al., 2001 and Thornton
et al., 2007), because N limits plant growth and C storage
(LeBauer & Treseder, 2008), and because N cycling is sensitive
to environmental change (Galloway et al., 2008). With N cycling
included, simulations project smaller increases in terrestrial C
storage in response to rising CO
2
, because N availability limits
plant growth and its response to elevated CO
2
(Thornton et al.,
2007; McMurtrie et al., 2008; Sokolov et al., 2008; Jain et al.,
2009; Wang & Houlton, 2009; Friedlingstein & Prentice, 2010;
Zaehle et al., 2010).
While model simulations bear out the importance of including
N, these models do not necessarily demonstrate a consistent
pattern of effect. Results differ in magnitude, direction and
mechanism, suggesting that additional data and analyses are
needed to evaluate conditions under which CN coupling is
important. For example, some simulations project only a modest
limitation of terrestrial C uptake with coupled CN interactions
in the long term (at equilibrium), but strong effects of CN
interactions on the dynamics of C cycling and storage after dis-
turbance (Gerber et al., 2010). Although the models generally
agree that including N limitation of plant production reduces the
terrestrial C sink, the magnitude of this effect is highly variable
(Arneth et al., 2010). Experiments also indicate that CN inter-
actions are critical modulators of the long-term CO
2
fertilization
response, but different experiments provide support for different
mechanisms underlying that modulation. In some cases, CN
interactions appear to constrain strongly the CO
2
response
(Reich et al., 2006a,b; Norby et al., 2010; Garten et al., 2011),
but in others, plants appear able to access the extra N needed to
support the growth response (Johnson et al., 2006; Drake et al.,
2011). Effects of CO
2
concentration on microbial N transforma-
tions that influence the plantsoil distribution of N are extremely
variable, with negative, positive and neutral effects observed for
the same processes (Dıaz et al., 1993; Zak et al., 1993; Morgan
et al., 1994; Zanetti et al., 1996; Hungate et al., 1997a,c; Johnson
et al., 1997; Hofmockel & Schlesinger, 2007; van Groenigen
et al., 2011, 2012). Furthermore, other concomitant global envi-
ronmental changes will modulate N constraints on C balance
responses to elevated CO
2,
including changes that alter N cycling
directly, such as warming, altered precipitation and atmospheric
N deposition, as well as indirect effects, such as changes in plant
species composition. There is considerable debate as to the mag-
nitude of the impact of such effects on ecosystem C sequestra-
tion, however (Jenkinson et al., 1999; Nadelhoffer et al., 1999;
Arneth et al., 2010). Thus, both model simulations and data can
be invoked to support N cycling constraining, increasing, or hav-
ing little effect on the terrestrial C sink. Our third goal in this
research was to compare C and N inventories in response to 11 yr
of CO
2
exposure in a subtropical woodland, in order to test how
rising CO
2
affects these elements in concert.
One of the challenges in investigating CN interactions in eco-
system experiments is that the timescale of measurements of N
cycling rates is typically far shorter than the timescale of N
cycling processes that influence ecosystem responses. Elevated
CO
2
can alter multiple processes within the soil N cycle simulta-
neously, with strong temporal dynamics, and with opposing
impacts on plant N availability, making it very difficult to extrap-
olate short-term measurements to long-term effects. Following
an isotope tracer over multiple years can help overcome this chal-
lenge.
15
N tracers reflect short-term effects on N cycling processes
and integrate these into long-term effects on
15
N distribution
among plant and soil components within the system. Because the
15
N is added in labile form, losses of added
15
N will be relatively
larger than losses of total ecosystem N, so can be detected with
greater sensitivity. Our fourth goal in this research was to use a
long-term
15
N tracer to characterize changes in N distribution
and N losses in response to elevated CO
2
.
Here, we report a whole system inventory of the C and N con-
tent of a scrub-oak ecosystem after 11 yr of experimental CO
2
exposure. We also show how soil microbial activity responded to
chronic CO
2
exposure. We also report recovery and distribution
of a
15
N tracer applied early in the experiment, in order to assess
how elevated CO
2
alters the system-level distribution of labile N
over the timescale of a decade.
Materials and Methods
The scrub-oak experiment occurred at the Merritt Island
National Wildlife refuge on the east coast of Florida, USA
(28°38N, 80°42W). After controlled burning, 16 open-top
chambers were established over the regrowing vegetation, each
covering 9.42 m
2
ground area, with 8 chambers receiving ambi-
ent air and 8 receiving ambient air +350 ppm V CO
2
(referred
to as the ‘elevated CO
2
’ treatment). A large blower circulated air
through each chamber at a rate of 2430 m
3
min
1
, replacing
the chamber air volume 1.31.6 times min
1
(Dijkstra et al.,
2002). The chambers increased air temperature and vapor
pressure deficit while decreasing light (Dore et al., 2003), micro-
environmental effects that did not significantly alter growth or
species composition (Seiler et al., 2009). The experiment began
in May 1996 and was maintained until June 2007.
In JuneJuly 2007, all aboveground material was harvested
from the chambers (see Seiler et al., 2009), and roots and soils
were collected using multiple cores in each chamber (see Day
et al., 2013). For aboveground biomass, all shoots were cut at the
base of the stem, weighed immediately, and subsampled for the
determination of water content and elemental analysis of leaves
and stems. Ten surface cores (010 cm) and five deep cores were
collected from each plot at 10 cm increments; all cores were 7 cm
diameter. Core depth varied among plots from 2 to 3 m due to
differences in the depth to the water table and the spodic (B
h
)
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horizon. For purposes of the element inventory conducted here,
depth increments were combined into 010, 1030, 3060 and
60100 cm. Samples were hand-picked to remove large roots,
and subsamples separated into coarse particulate organic matter,
roots and mineral soil. Belowground biomass was also sampled
indirectly using ground-penetrating radar (Stover et al., 2007,
Day et al., 2013). Material on the forest floor was gathered from
1/8th of each plot by hand, collecting until no visibly identifiable
plant fragments remained. Material was dried, sifted to remove
adhering sand, and weighed.
We used a combination of density and biological fractiona-
tions to estimate soil carbon (C) pools of varying turnover
rates. We used incubations to estimate labile and active soil C
pools (and, by difference residual C), using the technique of
Nadelhoffer (1990). We measured CO
2
production from
laboratory incubations, combining short-term incubations of
soils immediately after collection (McKinley et al., 2009) with
541-d incubations conducted in the lab at Northern Arizona
University. We used density fractionations as described previ-
ously (Hungate et al., 2006; Carney et al., 2007), separating light
(<1.5 g cm
3
), medium (1.51.8 g cm
3
), heavy (1.8
2.2 g cm
3
) and residual (>2.2 g cm
3
) organic matter fractions.
Total soil C, N,
15
Nand
13
C were also measured on bulk sam-
ples collected from the cores. Our fractionation analysis focused
on soils from the 060 cm depths. For bulk soil analyses where
we measure total C, N and
15
N, we present the data to 1 m to
correspond with the depth of the root biomass inventory.
We measured microbial biomass using the chloroform-fumi-
gation extraction method (Vance et al., 1987) in mineral soil
(015 cm) sampled in July 1997; June, July, September and
December 1998; September 1999; and May 2004. Soil subs-
amples (2025 g at field moisture content) were extracted in
75 ml 0.5 M K
2
SO
4
before and after 24-h fumigation with eth-
anol-free chloroform. The K
2
SO
4
extracts were dehydrated in a
forced-air drying oven at 60°C, the salts ground in a mortar
and pestle, and the resulting powder analyzed for C, N, d
15
N
and d
13
C on a CE 2100 elemental analyzer coupled to a
Thermo DeltaPLUS-XL isotope-ratio mass spectrometer
(http://www.isotope.nau.edu). Microbial biomass was calculated
as the difference in mass (of C, N,
13
Cor
15
N) between fumi-
gated and nonfumigated samples, divided by 0.54 to correct
for extraction efficiency (Vance et al., 1987). For samples col-
lected after the
15
N tracer application (June 1998), we also
measured the
15
N content of mineral soil (015 cm depth).
After milling, soil N and
15
N contents were determined as
described above.
The CO
2
added to the elevated-CO
2
treated plots was
depleted in
13
C. We used a two-member mixing model to
determine mineral soil C derived from new photosynthate
(Leavitt et al., 1994; Hungate et al., 1996). Stem tissue pro-
duced in the elevated CO
2
treatment (d
13
C
S,E
) provided an
integrative measure of the d
13
C value of new photosynthate
(average across five sampling dates, -42.6 0.3 &). However,
because mineral soil (d
13
C
M,A
) and stem d
13
C(d
13
C
S,A
)
differed in the ambient C
a
treatment, we calculated the d
13
C
signature of new carbon (d
13
C
new
) as:
d13Cnew ¼d13 CS;Eðd13 CS;Ad13CM;AÞ:Eqn 1
The d
13
C of the mineral soil in the ambient CO
2
treat-
ment was used as the end member for organic matter fixed
before the experiment began. Carbon, N,
15
N, and
13
Cwere
determined for all plant and soil components using coupled
Dumas combustion isotope-ratio mass spectrometry (Carlo-
Erba elemental analyzer and Finnigan Delta-V mass spectrom-
eter) at the Colorado Plateau Stable Isotope Laboratory
(www.isotope.nau.edu).
For testing soil microbial activity, we collected soil and litter
samples in May through July of 2004, after 8 yr of CO
2
treat-
ment. Soil sampling, preparation of microbial inocula, carbon
and nutrient amendments, and incubation conditions are
described in Brown et al. (2009). Carbon substrates included glu-
cose and hot-water extracts of roots and leaf litter collected from
the ambient and elevated CO
2
treatments. Microbial inocula
from litter, rhizosphere and bulk soil communities were also
prepared from the two CO
2
treatments. We used the BD-oxy sys-
tem (BD Oxygen Biosensor System, BD Biosciences, Bedford,
MA, USA (Garland et al., 2003; Vaisanen et al., 2005; Zabaloy
et al., 2008) to evaluate microbial respiration. The system uses a
fluorophore that fluoresces as O
2
is consumed during the 48 h
incubation. Normalized relative fluorescence was calculated as
relative fluorescence after 48 h normalized by dividing by relative
fluorescence after 1 h. The response to substrate addition was cal-
culated as:
Relative response ¼ðRrRcÞ=Rc100%Eqn 2
(R
c
, normalized relative fluorescence in the absence of resource
addition; R
r
, normalized relative fluorescence with the added
resource. Brown et al. (2009) present data from the ambient CO
2
treatment; here, we expand on this past analysis to evaluate
responses of microbial respiration to elevated CO
2
. We used
ANOVA to test for effects of habitat (rhizosphere, litter or bulk
soil), inoculum source (ambient or elevated CO
2
), substrate
source (ambient or elevated CO
2
), substrate type (litter or root),
N, and P. We used a separate ANOVA to test compare responses
to the addition of glucose vs natural substrates extracted from
roots and litter. Where appropriate, ANOVAs were designed as
split-plots, to account for the nonindependence of inocula col-
lected from individual experimental plots subject to multiple
combinations of resource treatments in the BD-Oxy assay.
We used resampling to infer the effects and estimate the mag-
nitude of the elevated CO
2
treatment on ecosystem C and N
pools and recovery of tracer
15
N. We estimated 5% and 95%
confidence limits for the difference in means between elevated
and ambient CO
2
treatments, using 1000 samples with replace-
ment (n=8 for each treatment).
Results
Elevated CO
2
increased plant biomass, including the mass of C
(g C m
2
) in leaves, stems and coarse roots, and the total mass of
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C in plants (Table 1). The mass of C in fine roots was not signifi-
cantly affected by the elevated CO
2
treatment at the final harvest
(Table 1), although fine roots did exhibit significant increases at
other times during the experiment (Day et al., 2013). On average,
plant C accumulation by the end of the experiment was
71.5 g C m
2
yr
1
higher in elevated compared to ambient CO
2
,
roughly equally distributed aboveground (37.5 g m
2
yr
1
) and
belowground (33.5 g m
2
yr
1
). The C content of the litter layer,
coarse particulate organic matter, total mineral soil C, and the
light and medium density fractions did not significantly respond
to the CO
2
treatment, whereas the heavy density soil C pool sig-
nificantly declined. Elevated CO
2
had no effect on soil C in the
spodic horizon, with no significant effect on total mineral soil C,
or on the light, medium and heavy density fractions (Table 2);
thus, C in the deep soil was also insensitive to the CO
2
treatment.
In general, increased mass of plant C caused by elevated CO
2
did
not translate to increased C storage in other ecosystem reservoirs
(Table 1).
Elevated CO
2
increased the N content of plants above-
ground (Table 3), but the N contents of coarse and fine roots
did not respond to elevated CO
2
, yielding no effect on total
plant N. The N content of most soil fractions was not signifi-
cantly altered by elevated CO
2
, except the medium density
fraction at 3060 cm, which increased, and the light fraction at
1030 cm, which declined. Increased C in plant pools with only
small changes in N means higher C to N ratios. Higher C to N
ratios under elevated CO
2
were observed for leaves, coarse roots
and the sum of all plant parts; elevated CO
2
also increased the C
to N ratio of the litter layer (Table 4). Elevated CO
2
did not
increase the C to N ratio of any soil pool; the only soil pool to
respond the heavy density fraction actually declined in C to
N ratio. Changes in plant and soil C to N ratios were compensa-
tory, such that elevated CO
2
had no effect on the C to N ratio of
the plantsoil system to 1 m depth.
Elevated CO
2
increased recovery of tracer
15
N in above-
ground plant tissues, but reduced recovery in coarse roots, in the
soil light fraction at 1030 cm depth, and in the soil residual
fraction at 060 cm (Table 5). Together, these changes resulted
in a significant decline in whole-system
15
N recovery under ele-
vated CO
2
. Elevated CO
2
reduced the d
15
N of plant tissue
(weighted average of all plant parts), a dilution of the added
15
N
tracer with unlabeled
15
N. This pattern indicates that elevated
CO
2
increased plant access to N, either through new N inputs
or redistribution from existing ecosystem N reservoirs. But,
because total plant N did not respond to elevated CO
2
, the
increase in inputs of new N to plants were matched by N losses
from plants, such that CO
2
enhanced N turnover through the
plant system. In contrast to plant d
15
N, the d
15
N of soils did
Table 1 Inventory of carbon after 11 yr exposure to increased atmospheric CO
2
in a subtropical oak woodland
a
Carbon (g C m
2
) Ambient Elevated Effect 5% & 95% CLs
Aboveground 624.5 54.6 1043.0 77.5 418.5 (274.8 to 556.9)
Oak leaves 212.2 22.3 318.4 29.6 106.2 (47.6 to 157)
Oak stems 347.1 34.2 621.6 60.8 274.5 (164.8 to 374.2)
Other species 38.3 10.7 63.1 10.2 24.7 (1.7 to 47.4)
Standing dead 26.9 8.4 39.8 13.8 13.0 (9.7 to 39.5)
Litter layer 332 41.2 368.1 42.4 36.1 (57.9 to 127.7)
Roots 2886.7 90.2 3261.3 174.6 374.6 (73.6 to 674.5)
Fine roots 909.4 62.8 803.9 43.3 105.5 (226.8 to 9.7)
Coarse roots 1977.3 102.8 2457.4 177.7 480.1 (168.9 to 790.0)
Plant 3511.2 102.0 4304.3 221.3 793.1 (437.4 to 1172.7)
CPOM (0100 cm) 1406.5 386.4 1168.5 272.1 238.0 (957 to 354.4)
Soil (0100 cm) 5513.1 411.5 5025.6 647.4 487.5 (1456.5 to 636.8)
Light, 060 cm 2534.7 260.2 2394.4 333.3 140.4 (746.8 to 473.2)
010 cm 1530.9 284.8 1415.8 316.8 115.0 (760.1 to 565.5)
1030 cm 480.2 94.5 331.2 36.5 149.1 (297.9 to 6.7)
3060 cm 523.7 149.9 647.3 169.2 123.7 (214.9 to 474.5)
Medium, 060 cm 1306.3 302 1208.4 177.3 97.9 (633.8 to 380.3)
010 cm 660.3 115.3 560.7 108.2 99.6 (346.4 to 158.9)
1030 cm 370.9 109.2 341.5 55.2 29.4 (222.4 to 147.1)
3060 cm 275 157.8 306.2 88.6 31.1 (267.6 to 289.2)
Heavy, 060 cm 706.3 120.5 396 92.1 310.4 (553.2 to 86.0)
010 cm 110.9 27 81.2 19.9 29.7 (81.7 to 22.0)
1030 cm 148 23.7 83.5 30.6 64.6 (122.9 to 2.0)
3060 cm 447.4 107.6 231.3 87.2 216.1 (402.7 to 3.3)
Residual, 060 cm 965.8 1026.9 1026.9 330.9 61.1 (782.3 to 925.2)
Soil (60100 cm) 1547.0 129.3 1877.6 359.8 330.7 (274.4 to 925.4)
Total ecosystem 12309.8 582.1 12744.1 444.3 434.4 (723 to 1529.9)
a
Values are means SE of the mean for the Ambient and Elevated CO
2
treatments, the Effect of the CO
2
treatment (EA), and the bootstrapped 5% and
95% CLs (confidence limits) for the treatment effect. CPOM, coarse particulate organic matter. Soil fractions are density fractions, including light
(<1.5 g cm
3
), medium (1.51.8 g cm
3
), heavy (1.82.2 g cm
3
) and residual (calculated as total soil total minus the sum of measured density fractions).
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not change with elevated CO
2
, nor was whole-system d
15
N
affected (Table 6).
While elevated CO
2
did not alter total ecosystem C, and
effects on soil C were either nil or negative, several results indicate
that elevated CO
2
increased soil microbial activity. Elevated CO
2
increased C mineralization in laboratory incubations, particularly
for the first 24 h after collection in the field (Fig. 1, and see
McKinley et al., 2009), indicating a larger and more rapidly
cycling labile soil C pool. Elevated CO
2
also increased the pro-
portion of soil organic matter that occurred in the soil microbial
biomass: averaged across seven sample dates from 1997 to 2004,
more soil C, N and
15
N was contained in the soil microbial bio-
mass in the elevated CO
2
treatment (P=0.012 for C, P=0.096
for N, and P=0.049 for
15
N; Fig. 2). When common inocula
were presented with the labile substrates produced by leaves and
roots, substrates produced in the elevated CO
2
treatment were
respired more completely than substrates from the same sources
in the ambient CO
2
treatment (Fig. 3a), indicating that the sub-
strates produced in the high-CO
2
environment were more sus-
ceptible to microbial decay. For the litter and rhizosphere
microbial communities, microbial inocula from the elevated
CO
2
treatment consumed more O
2
than inocula collected from
the ambient CO
2
treatment when presented with a common C
substrate (Fig. 3b). Glucose induced a greater response in bulk
soil inoculum from the ambient treatment (Fig. 3b), which may
reflect CO
2
-depletion of available soil C susceptible to priming
(Brown et al., 2009).
The incorporation of the depleted d
13
C signature into organic
matter pools revealed rates and patterns of flow of ‘new’ C into
the system, where new C is that fixed since CO
2
fumigation
Table 2 Soil carbon (C) in the spodic horizon of the subtropical oak woodland
Ambient Elevated
P-value
Ambient Elevated
P-value%C d
13
C
Total C 0.77 0.10 0.60 0.15 0.383 25.6 0.1 25.1 0.3 0.157
Light 18.3 2.8 11.9 1.2 0.151 25.3 0.1 25.3 0.1 0.943
Medium 14.2 3.8 9.4 2.0 0.288 25.6 0.2 25.3 0.1 0.178
Heavy 13.2 2.3 12.2 1.0 0.710 25.6 0.1 25.2 0.2 0.116
Table 3 Inventory of ecosystem nitrogen
(g N m
2
) after 11 yr exposure to increased
atmospheric CO
2
in a subtropical oak
woodland
a
Ambient Elevated Effect 5% & 95% CLs
Aboveground 8.4 0.8 13.1 0.9 4.7 (3.0 to 6.3)
Oak leaves 4.7 0.6 6.6 0.6 1.9 (0.5 to 3)
Oak stems 3.0 0.3 5.1 0.5 2.2 (1.2 to 3.1)
Other species 0.5 0.1 1.1 0.2 0.5 (0.2 to 0.9)
Standing dead 0.2 0.1 0.3 0.1 0.1 (0.1 to 0.3)
Litter layer 5.7 0.7 6.0 0.9 0.3 (1.4 to 2.2)
Roots 29.3 1.8 27.8 2.5 1.4 (6.4 to 3.1)
Fine roots 8.3 0.8 7.3 0.9 1.0 (2.8 to 0.9)
Coarse roots 21.0 1.2 20.5 2.5 0.4 (4.6 to 4.2)
Plant 37.7 1.8 41.0 2.9 3.3 (1.8 to 8.3)
CPOM (0100 cm) 20.7 5.7 15.2 3.5 5.4 (15 to 3.0)
Soil (0100 cm) 159.5 15.0 145.4 17.5 14.2 (44.2 to 15.9)
Light, 060 cm 55.9 7.0 54.9 8.9 1.0 (19 to 16.6)
010 cm 37.2 7.6 37.6 8.9 0.4 (17.9 to 18.5)
1030 cm 9.6 1.8 6.5 0.7 3.1 (5.8 to 0.1)
3060 cm 9.1 2.8 10.8 2.1 1.7 (4.2 to 6.4)
Medium, 060 cm 30.7 5.5 30.9 4.1 0.2 (10.9 to 11)
010 cm 18.8 3.4 15.4 3.0 3.4 (10.4 to 3.5)
1030 cm 7.9 2.0 7.0 1.0 0.9 (4.3 to 2.3)
3060 cm 4.0 1.5 8.5 2.6 4.6 (0.4 to 9.3)
Heavy, 060 cm 17.3 2.1 15.6 4.9 1.7 (9.2 to 6.8)
010 cm 3.4 0.8 2.4 0.6 1.0 (2.7 to 0.5)
1030 cm 4.1 0.8 2.5 1.1 1.6 (3.3 to 0.5)
3060 cm 9.8 1.5 10.7 4.4 0.9 (6 to 8.9)
Residual, 060 cm 55.6 44.0 12.3 13.5 43.3 (40 to 17.3)
Soil (60100 cm) 51.3 3.2 55.3 8.8 4.1 (10.8 to 18.2)
Total ecosystem 274.8 10.9 262.9 13.9 12.0 (38.1 to 18.9)
a
Values are means SE of the mean for the Ambient and Elevated CO
2
treatments, the Effect of the CO
2
treatment (EA), and the bootstrapped 5% and 95% CLs (confidence limits) for the treatment effect.
CPOM, coarse particulate organic matter. Soil fractions are density fractions, including light (<1.5 g
cm
3
), medium (1.51.8 g cm
3
), heavy (1.82.2 g cm
3
) and residual (calculated as total soil total minus
the sum of measured density fractions).
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began in May 1996. By 2007, coarse roots contained
740 g C m
2
of new C, 31% of the total C contained in coarse
roots (Fig. 4), yielding a mean C residence time in coarse roots of
35.5 4.2 yr. The total difference in coarse root biomass
between E and A was 480 g C m
2
. This could have been caused
entirely by a stimulation of new root C (probably the most parsi-
monious interpretation), but it is possible that treatments dif-
fered in patterns of use of ‘old’, stored C an idea which should
not be immediately dismissed, given that these plants use old C
to build new roots (Langley et al., 2002). In the surface soil min-
eral fraction, the percent new C increased linearly (Fig. 5), with
an overall mean residence time of C of 33.6 2.1 yr. In the
spodic horizon, there was no evidence of new C accumulation in
the total mineral soil or in the light, medium, or heavy density
fractions (Table 2). Overall, elevated CO
2
did not significantly
alter the total C content of the system (Table 1), because
increased C in plant reservoirs were compensated by reduced C
from the soil (Fig. 6).
Discussion
In this subtropical oak woodland, 11 yr of exposure to elevated
CO
2
increased plant C by 22%, with a smaller (and not signifi-
cant) effect on plant N of 9%, well within the range of responses
typically observed in plants growing under a wide variety of
experimental conditions (Norby et al., 2005; de Graaff et al.,
2006; Luo et al., 2006). Absolute responses in the mass of C
above- and belowground were similar, consistent with elevated
CO
2
having little impact on the partitioning of biomass above-
and belowground (Tingey et al., 2000), in contrast to the expec-
tation that root growth would increase disproportionately (Stulen
& den Hertog 1993). In our experiment, the relative response
aboveground was actually larger than that belowground, because
most of the biomass in this system is belowground. The mean
residence time of C in coarse roots (revealed by incorporation of
the d
13
C tracer) was sufficiently long that, at the final harvest,
only about one third of the C in coarse roots represented new
growth over the course of this experiment. By contrast, all of the
standing aboveground biomass at the final harvest had accumu-
lated after fire. Thus, repeated cycles of fire disturbance and
recovery might yield a larger cumulative response of new C in
coarse roots.
The increased C content of plants suggests the potential for
elevated CO
2
to enhance ecosystem C uptake. Yet, increased C
contained in plants was not reflected in the C content of soil, nei-
ther in the top meter nor in the deeper spodic horizon. Possibly,
the experiment lacked sufficient power to detect soil C accumula-
tion (Smith, 2004). Alternatively, other mechanisms may have
operated to prevent soil C accumulation in this ecosystem. We
can place boundary conditions on the power problem: integrated
Table 4 Carbon to nitrogen ratios (g : g) in ecosystem components after 11 yr of experimental exposure of a subtropical woodland to increased
atmospheric CO
2a
Ambient Elevated Effect CI
Aboveground 74.7 2.2 79.3 2.1 4.6 (0.3 to 9.1)
Oak leaves 45.8 1.0 48.3 1.0 2.5 (0.2 to 4.9)
Oak stems 120.6 7.9 121.2 7.2 0.6 (13 to 14.5)
Other species 71.9 6.6 60.1 7.4 11.8 (23.7 to 1.3)
Standing dead 108.5 3.8 113.4 4.8 4.9 (4.5 to 13.8)
Litter layer 58.6 1.5 64.2 1.9 5.6 (0.7 to 10.6)
Roots 101.3 7.4 122.0 7.5 20.7 (2.3 to 39.7)
Fine roots 114.0 9.6 116.3 9.8 2.2 (16.8 to 23.6)
Coarse roots 97.0 8.1 128.9 8.1 32.0 (7.1 to 59.3)
Plants 94.6 5.3 106.9 5.6 12.4 (0.8 to 23.4)
CPOM (0100 cm) 71.1 9.1 76.2 8.7 5.1 (10.6 to 17.9)
Soil (0100 cm) 36.8 2.2 37.8 2.0 0.9 (3 to 4.6)
Light, 060 cm 46.8 3.9 45.0 1.4 1.8 (9.1 to 5.1)
010 cm 43.7 6.9 38.8 0.8 4.9 (17.9 to 3.7)
1030 cm 50.4 2.5 51.9 2.3 1.5 (4.5 to 7.4)
3060 cm 64.5 9.7 60.8 9.5 3.7 (21.8 to 11.2)
Medium, 060 cm 41.2 3.0 39.5 3.0 1.7 (8.2 to 4.1)
010 cm 35.4 0.6 37.2 0.7 1.8 (0.3 to 4.4)
1030 cm 45.6 2.9 48.2 2.9 2.7 (3.4 to 8.8)
3060 cm 53.2 8.3 44.9 8.6 8.3 (26.8 to 7.7)
Heavy, 060 cm 40.2 4.2 29.4 5.1 10.7 (18.5 to 3.5)
010 cm 32.8 1.4 33.7 1.4 0.9 (1.6 to 3.6)
1030 cm 41.2 5.1 38.4 5.1 2.9 (10.8 to 5.3)
3060 cm 45.5 10.0 27.7 10.6 17.8 (36.6 to 3.4)
Residual, 060 cm 30.1 1.4 33.2 1.5 3.1 (0.4 to 6.8)
Soil (60100 cm) 31.6 9.3 26.0 9.4 5.5 (24.1 to 10.4)
Total ecosystem 45.0 2.1 48.9 1.9 3.9 (0.1 to 8.1)
a
Values are means SE of the mean for the Ambient and Elevated CO
2
treatments, the Effect of the CO
2
treatment (EA), and the bootstrapped 5% and
95% CLs (confidence limits) for the treatment effect. CPOM, coarse particulate organic matter. Soil fractions are density fractions, including light(<1.5 g
cm
3
), medium (1.51.8 g cm
3
), heavy (1.82.2 g cm
3
) and residual (calculated as total soil total minus the sum of measured density fractions).
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over the top meter of soil, the mean effect of CO
2
on total soil C
was a decline of 44.3 g C m
2
yr
1
, with the 90% confidence
interval spanning a range of CO
2
effects from more rapid losses
of soil C (132.4 g C m
2
yr
1
) to gain (+57.9 g C m
2
yr
1
).
This range exhibits the power limitations typical when assessing
responses of total soil C to elevated CO
2
(Hungate et al., 2009).
Isolating components of the total soil C reservoir can help over-
come the problem of limited power (e.g. Iversen et al., 2012). In
our case, we found that by year 6 of the experiment, elevated
CO
2
had reduced the C contained in the light density (Carney
et al., 2007) and in the acid-hydrolysable (Langley et al., 2009)
fractions of soil C. These findings are consistent with the
response we observed at the final harvest reported here where ele-
vated CO
2
reduced the heavy density fraction of soil C (Table 1)
and decreased soluble C susceptible to glucose-induced priming
(Fig. 3). The pattern of declining soil C in soil fractions is diffi-
cult to reconcile with the concept of soil C accumulation as a
first-order response to enhanced plant growth.
The second explanation for not finding soil C accumulation in
response to elevated CO
2
is that it does not occur, because
increased C input to soil is compensated by increased C loss.
Elevated CO
2
could enhance export of C through leaching of
dissolved organic matter. But, if elevated CO
2
increased leaching
of C in this experiment, this response had no influence on the C
content or d
13
C composition of the spodic horizon; the absence
of any effect on d
13
C is especially unlikely if leaching was an
important pathway for C loss. These findings indicate that
elevated CO
2
did not substantially alter leaching losses of C from
the system.
In contrast to the absence of any apparent effect on leaching,
there was compelling evidence that elevated CO
2
increased the
rate of C cycling through the soil: elevated CO
2
significantly
increased the size and rate of C flow through the labile soil C
pool (Fig. 1), it enhanced the proportion of soil C (and N, and
15
N) that were cycling through the soil microbial biomass
(Fig. 2), and it increased the decomposability of labile plant sub-
strates and promoted a physiologically more responsive microbial
community (Fig. 3). Elevated CO
2
also increased fungal biomass,
Table 5 Inventory of tracer
15
N (mg excess
15
Nm
2
) after 11 yr exposure to increased
atmospheric CO
2
and 9 yr of integration of
the added
15
N tracer in a subtropical oak
woodland
a
Ambient Elevated Effect 5% & 95% CLs
Aboveground 2.8 0.4 3.7 0.4 0.9 (0.1 to 1.8)
Oak leaves 1.6 0.2 1.8 0.3 0.2 (0.3 to 0.7)
Oak stems 1 0.2 1.6 0.2 0.6 (0.2 to 0.9)
Other species 0.1 0 0.2 0 0.1 (0 to 0.2)
Standing dead 0.1 0 0.1 0 0.0 (0 to 0.1)
Litter layer 2 0.3 2 0.3 0.0 (0.8 to 0.8)
Roots 7.7 1.2 4.5 0.6 3.3 (5.2 to 1.4)
Fine roots 2.1 0.4 1.4 0.2 0.7 (1.5 to 0)
Coarse roots 5.6 1.1 3.1 0.6 2.6 (4.5 to 0.7)
Plant 10.5 1.0 8.2 0.8 2.4 (4.2 to 0.4)
CPOM (0100 cm) 0.6 0.1 0.7 0.1 0.1 (0.2 to 0.3)
Soil (0100 cm) 83.7 16.4 59.2 11.4 24.5 (53 to 3.7)
Light, 060 cm 28.5 4 29.2 4.8 0.7 (8.9 to 10)
010 cm 21.6 4.4 24 5 2.4 (8 to 12.8)
1030 cm 4 0.7 2.2 0.2 1.8 (2.9 to 0.7)
3060 cm 2.9 0.9 3.1 0.7 0.1 (1.8 to 1.8)
Medium, 060 cm 15.2 2.9 14.9 2.4 0.3 (5.6 to 5.6)
010 cm 11.2 2.1 10.1 2.2 1.2 (6 to 3.7)
1030 cm 2.8 0.7 2.5 0.4 0.3 (1.5 to 0.8)
3060 cm 1.1 0.4 2.3 0.8 1.2 (0.1 to 2.6)
Heavy, 060 cm 5.1 0.8 4.3 1.1 0.8 (2.7 to 1.3)
010 cm 1.9 0.5 1.5 0.4 0.3 (1.3 to 0.7)
1030 cm 1.2 0.2 0.8 0.4 0.4 (1 to 0.3)
3060 cm 2.1 0.3 2 0.8 0.1 (1.5 to 1.3)
Residual, 060 cm 34.8 10.8 14.2 9.5 20.7 (51.7 to 0.8)
Soil (60100 cm) 5.8 1.1 6.4 1.7 0.6 (2.5 to 4)
Total ecosystem 102.6 15.7 76.4 9.0 26.2 (55.1 to 0.8)
a
Values are means SE of the mean for the Ambient and Elevated CO
2
treatments, the Effect of the CO
2
treatment (EA), and the bootstrapped 5% and 95% CLs (confidence limits) for the treatment effect.
CPOM, coarse particulate organic matter. Soil fractions are density fractions, including light (<1.5 g
cm
3
), medium (1.51.8 g cm
3
), heavy (1.82.2 g cm
3
) and residual (calculated as total soil total minus
the sum of measured density fractions).
Table 6 d
15
N signatures (mean SEM) of plant, soil and whole system N
at the final harvest in July 2007
Ambient CO
2
Elevated CO
2
P-value*
Plant 76.3 5.4 55.0 4.2 0.008
Soil 103.7 13.9 85.4 11.6 0.422
System 100.4 11.6 80.8 10.0 0.317
*P-values are for one-way ANOVAs testing the effect of elevated CO
2
.
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as measured by ergosterol (Klamer et al., 2002), by direct mea-
surements of mycorrhizal fungal biomass (Langley et al., 2003),
and by the ratio of fungi to bacteria in the soil microbial biomass,
as indicated by the analysis of phospholipid fatty acid profiles
(Carney et al., 2007). These results indicate that higher microbial
activity was associated with a shift in the composition of the
microbial community.
Increased soil microbial activity may also explain why the
effect of elevated CO
2
on the C : N of plant tissues and the litter
layer was not apparent, and indeed in some cases may even have
been reversed, in soil organic matter. Specifically, elevated CO
2
increased the C : N ratio of individual plant tissues (Table 3) as
commonly observed (Cotrufo et al., 1998; Norby et al., 2001), of
the entire plant biomass, above- and belowground, and of the
litter layer. Yet, this shift was not observed in soil organic matter
after 11 yr of continuous inputs of plant material to the soil
organic matter pool. There are two possibilities for this discrep-
ancy: (1) either the inputs of plant material were too low com-
pared to background soil organic matter to drive a change in soil
organic C : N; or (2) by increasing soil microbial activity and the
processing of C in the soil system, elevated CO
2
caused a com-
pensatory response, tending to reduce soil C : N. Our finding
that elevated CO
2
reduced the total mass of soil N in the medium
density fraction, but increased it in the heavy fraction, is consis-
tent with this second explanation. The medium fraction has a
higher C : N ratio than the heavy fraction, and the medium frac-
tion is thought to cycle into the heavy fraction as the soil organic
matter is processed by microbial activity and interactions with
minerals (Camberdella & Elliott 1992). Thus, the pattern we
observe may indicate increased processing and turnover of soil N,
promoting transfer to pools with lower C : N ratios, and a ten-
dency for CO
2
to decrease soil C : N.
Some previous measurements at this site indicated that ele-
vated CO
2
reduced or had no effect on microbial activity during
the first 18 months of the experiment, with reduced gross N min-
eralization (Hungate et al., 1999) and either reduced or no
impact on microbial biomass N (measured as ninhydrin-reactive
N) and microbial activity (measured as fluorescein diacetate
hydrolysis) in the rhizosphere (Schortemeyer et al., 2000),
although the mechanism(s) for these changes were not apparent.
These early responses were apparently transient, and did not indi-
cate the decadal-scale response of soil microorganisms to elevated
CO
2
. The measurements reported here of microbial biomass, the
size of the labile soil C pool, and the distribution and retention
of
15
N cycling through the system are more representative of the
entire duration of the experiment (e.g. Fig. 2). Results from this
experiment are consistent with the general finding that elevated
CO
2
stimulates soil microbial activity (de Graaff et al., 2006;
Dieleman et al., 2012), and the turnover of soil organic matter
(Marhan et al., 2010; Phillips et al., 2012; Dawes et al., 2013).
Elevated CO
2
can stimulate microbial activity by increasing
soil water content, especially in grasslands (Hungate et al., 1997a;
Morgan et al., 2004), and this response can counterbalance the
increased C inputs from enhanced plant growth at elevated CO
2
,
causing no change in soil C accumulation (Marhan et al., 2010).
In the scrub-oak experiment reported here, elevated CO
2
slightly
0.00
5.00
10.00
15.00
20.00
25.00
30.00 0–10 cm
0.00
2.00
4.00
6.00
8.00
10.00
12.00
10–30 cm
0.00
0.50
1.00
1.50
2.00
2.50
3.00
3.50
4.00
1 5 50 500
30–60 cm
0.00
1.00
2.00
3.00
4.00
5.00
6.00
7.00
1 5 50 500
60–100 cm
Soil CO
2
production (µg CO
2
–C g
–1
d
–1
)
Days of soil incubation
(a) (b)
(c) (d)
Fig. 1 CO
2
production during soil incuba-
tions for four soil depths (a, 010 cm; b,
1030 cm; c, 3060 cm; d, 6100 cm) in a
subtropical oak woodland exposed to 11 yr
of increased CO
2
. Ambient CO
2
, open
circles; elevated CO
2
, closed circles. Bars
show 2 SEM.
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increased surface soil water content during the first several years
(Hungate et al., 2002), but this effect disappeared with leaf area
development (Li et al., 2007), and elevated CO
2
had no effect on
soil temperature (Hymus et al., 2003). Thus, the changes in
microbial activity and organic matter turnover that we observed
are unlikely to have been driven by differences in temperature,
although increased soil moisture may have played a role early on.
Elevated CO
2
can also increase microbial activity by enhanc-
ing the supply of C substrates to soil microorganisms, a
response consistent with past reports that, in this experiment,
elevated CO
2
stimulated the ‘priming effect’ (Carney et al.,
2007; Langley et al., 2009), the phenomenon where there occurs
‘extra decomposition of native soil organic matter in a soil
receiving an organic amendment’ (Bingeman et al., 1953). In
the experiment described here, the O
2
consumption assay indi-
cates that C derived from the litter and roots is more labile in
the elevated CO
2
treatment (Fig. 3), leading to a larger quantity
of labile organic matter (Fig. 1). The higher rates of microbial
activity observed are consistent with the notion that these new
inputs of labile C to soil increased mineralization of native soil
organic matter (Van Veen et al., 1991; Carney et al., 2007).
This phenomenon has been observed for some time (Lohnis,
1926; Broadbent & Norman, 1947; Broadbent, 1948) and evi-
dence for it has grown: isotope tracer experiments in soil incu-
bations show that substrate additions can more than treble the
decomposition rate of native soil organic matter in the short
term (Cheng & Johnson, 1998; Cheng et al., 2000). Substrate
additions can influence the oxidation of old soil C reservoirs,
for example, in deep soil (Fontaine et al., 2007), and can shape
the response of soil C to elevated CO
2
(Hoosbeek, 2004; Tru-
eman & Gonzalez-Meler, 2005; Carney et al., 2007; Hagedorn
et al., 2008; Paterson et al., 2008; Taneva & Gonzalez-Meler,
2008; Langley et al., 2009; Trueman et al., 2009; Drake et al.,
2011; Reid et al., 2012). Increased oxidation of old soil organic
matter is likely a transient response to a change in the rate of
labile C inputs. In the experiment described here, the reduction
in soil C observed by year 6 (Carney et al., 2007) was
0
500
1000
1500
2000
2500
3000
3500
4000
Litter
extract
Root
extract
Litter
extract
Root
extract
Litter
extract
Root
extract
Bulk soil
inocula
Litter
inocula
Rhizosphere
inocula
*
*
O2 consumption (normalized
relative fluorescence)
0%
40%
80%
120%
160%
200%
Glucose P N
**
Glucose P N
***
Glucose P N
400%
800%
1200%
Relative response of microbial
respiration to resource addition
(a)
(b)
Fig. 3 (a) Total respiration (O
2
consumption, expressed as normalized
relative fluorescence) of microbial inocula from three soil habitats (bulk
soil, litter, rhizosphere) on extracts of litter and roots. Circles, inocula from
ambient CO
2
; squares, from elevated CO
2
. Open symbols, substrates
produced in the ambient CO
2
treatment; closed symbols, substrates
produced in the elevated CO
2
treatment. Significant differences between
substrates produced under ambient and elevated CO
2
conditions (two-
way ANOVAs, effect of substrate origin); *,P<0.050. (b) The relative
responses of microbial respiration to single resource additions (glucose, N,
or P) for microbial inocula from the bulk soil, litter and rhizosphere
communities in the ambient (open circles) and elevated (closed circles)
CO
2
treatments. *Significant differences in resource limitation for
individual comparisons (t-tests) of inocula from the ambient and elevated
CO
2
treatments. For full statistical results, see Supporting Information
Tables S1 and S2. Bars show 2 SEM.
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
0.00 0.01 0.10 1.00 10.00
Microbial 15N (% of total soil 15N)
0.00%
0.50%
1.00%
1.50%
2.00%
2.50%
3.00%
Microbial N
Microbial N (g N g soil N–1 x 100%)
0.00%
0.10%
0.20%
0.30%
0.40%
0.50%
0.60%
0.70%
Microbial C
Microbial C (g C g soil C–1 x 100%)
Time (years after 15N tracer addition)
(a)
(b)
Fig. 2 (a) Soil microbial biomass nitrogen (N) and carbon (C) from the
ambient (open bars) and elevated (closed bars) CO
2
treated plots.
Microbial C and N (as a proportion of total soil C and N) are shown as
means across seven sample dates spanning 1997 to 2004, years 29of
CO
2
exposure. (b) Tracer
15
N in the microbial biomass (as a proportion of
tracer
15
N in total soil) over time after label addition (log scale). Bars
show 2 SEM.
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comparable to that found after 11 yr, suggesting that the sub-
strates susceptible to priming-induced loss had mostly been
degraded during the first 6 yr.
The implications of this response are not limited to C:
increased C input to soil, enhancing microbial activity and turn-
over, can also increasing nutrient availability to plants (Zak et al.,
1993). Observations elsewhere that elevated CO
2
increases
microbial activity in concert with greater plant N acquisition
from soil are also consistent with this interpretation (Drake et al.,
2011), although without direct evidence of increased soil organic
matter turnover, increased root exploration is a simpler explana-
tion. Results presented here call into question the notion that
feedbacks stimulating soil microbial turnover and N availability
necessarily lead to plant N accumulation and increased plant
growth. On the one hand, we did find that elevated CO
2
stimu-
lated plant N uptake and
15
N dilution in plant tissues, likely
driven by increased turnover of soil organic matter mediated by
microorganisms (Figs 1, 3; Johnson et al., 1998, 2001; Finzi
et al., 2007). On the other hand, increased microbial activity
0
200
400
600
800
1000
1200
1400
1600
1800
2000
1994 1996 1998 2000 2002
Year
2004 2006 2008
Coarse root C (g C m–2)
Fig. 4 Coarse root carbon (C) over time in the scrub-oak experiment,
showing ‘old’ (open circles) and ‘new’ (closed squares) carbon for the
elevated CO
2
plots, where new is defined as carrying a
13
C isotopic
signature of the CO
2
added to the elevated CO
2
plots. Modeling % old C
as exponential decay over time yielded a decomposition constant of
0.0325 yr
1
, considerably lower than decomposition assessed by litterbags
(0.22 yr
1
for ambient, 0.29 yr
1
for elevated). Bars show 2 SEM.
–10%
–5%
0%
5%
10%
15%
20%
25%
30%
35%
40%
Oct-95 Jul-98 Apr-01
Month, year
Jan-04 Oct-06 Jul-09
New soil carbon (% of total)
Fig. 5 New carbon in surface mineral soils over time. Bars show 2 SEM.
Fig. 6 Summary of ecosystem carbon (C) and nitrogen (N) inventories in a subtropical woodland after 11 yr of exposure to elevated CO
2
.
New Phytologist (2013) Ó2013 The Authors
New Phytologist Ó2013 New Phytologist Trust
www.newphytologist.com
Research
New
Phytologist
10
likely promoted N losses, accounting for our finding that elevated
CO
2
reduced recovery of added tracer
15
N (Table 4).
In this experiment, spanning more than a decade in a naturally
occurring ecosystem, photosynthesis and aboveground plant
growth exhibited strong responses to chronic exposure to elevated
atmospheric CO
2
(Dijkstra et al., 2002; Seiler et al., 2009), lead-
ing to the increased aboveground C content reported here, as well
as increased C in coarse roots (Day et al., 2013; Fig. 6). The ele-
vated CO
2
treatment did not affect C in fine roots at the final
harvest, although fine roots responded sporadically in this experi-
ment, with particularly strong responses following the initial fire
disturbance and after a hurricane in year 8 (Day et al., 2013). Ele-
vated CO
2
did not increase soil C, and in fact tended to decrease
it, likely a consequence of increased microbial activity. Elevated
CO
2
also increased plant N uptake, possibly driven by higher
microbial activity and increased soil N availability, but these
responses were also associated with reduced recovery of a long-
term
15
N tracer, likely indicating enhanced ecosystem N losses.
Thus, CO
2
altered the C and N cycles in this ecosystem, but not
in ways that promoted large or even detectable increments in
total ecosystem C mass. The effect of elevated CO
2
on soil C
turnover via the ‘priming effect’ was large enough to modulate
net carbon balance. This finding is not unique, and treatment of
this phenomenon in models of soil C cycling is likely warranted
(Heimann & Reichstein, 2008; Chapin et al., 2009). While the
importance of priming is becoming evident, the challenge to
include the phenomenon in models is not trivial: priming is still
poorly quantified and the mechanisms remain inscrutable. Meet-
ing this challenge could improve substantially our understanding
of terrestrial C cycling, replacing, or at least modifying, the stabi-
lizing first-order kinetics of decomposition used in virtually all
current models of the soil C cycle (Luo & Weng, 2011). The
response of soil C to labile substrate inputs suggests a previously
unrecognized sensitivity of what was thought to be a long-term,
stable C sink in the biosphere.
Acknowledgements
This research was supported by the US Department of Energy
(DE-FG-02-95ER61993, and subcontract 95-59, MPOOO02),
and by the National Science Foundation (DEB 9873715,
0092642, and 0445324). The National Aeronautics and Space
Administration at the Kennedy Space Center, the US Fish and
Wildlife Service at Merritt Island National Wildlife Refuge pro-
vided generous support throughout the CO
2
project. Thanks to
Bert Drake for visionary leadership and opportunity. Victoria
Albarracin, Mike Roberts, Mary Hummerick, Jan Bauer and
Lanfang Levine assisted in the laboratory.
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Supporting Information
Additional supporting information may be found in the online
version of this article.
Tables S1 & S2 Results from ANOVAs testing responses of soil
microbial respiration to CO
2
treatment, habitat, and substrate
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... Results from some studies suggest that even if rising CO 2 does not lead to increased carbon storage in forest biomass, it may increase carbon storage in soils (e.g., Iversen et al., 2012). However, increased soil carbon input also may accelerate microbial decomposition of carbon and thus soil carbon turnover, leading to less overall soil carbon storage (Hungate et al., 2013;van Groenigen et al., 2014). The strength and magnitude of soil carbon losses, therefore, remains highly uncertain (Georgiou et al., 2015;Walker et al., 2015). ...
... Results from some studies suggest that soil carbon storage may increase with rising atmospheric CO 2 (e.g., Iversen et al., 2012), even if the latter does not lead to increased carbon storage in forest biomass. However, soil carbon input may change microbial decomposition rates and the rate of soil carbon turnover, leading to less overall soil carbon storage (Hungate et al., 2013;van Groenigen et al., 2014). ...
... Total ecosystem N content may also increase under high CO 2 through alterations in the balance between N inputs and N outputs (Finzi et al., 2006;Sun et al., 2018). In addition, eCO 2 is generally associated with increases in N uptake (Finzi et al., 2007;Hungate et al., 2013;Hungate et al., 2006;Norby and Iversen, 2006) redistributing N from mineral soil to vegetation (Hungate et al., 2013;Hungate et al., 2006;Luo et al., 2006). Published results from other meta-analysis and synthesis work have also indicated significant modifications in the C:N ratios of vegetation and soil, ecosystem N capital, and the redistribution of N between vegetation and soils under eCO 2 (Liang et al., 2016;Luo et al., 2006;Shi et al., 2016;Terrer et al., 2018). ...
... Total ecosystem N content may also increase under high CO 2 through alterations in the balance between N inputs and N outputs (Finzi et al., 2006;Sun et al., 2018). In addition, eCO 2 is generally associated with increases in N uptake (Finzi et al., 2007;Hungate et al., 2013;Hungate et al., 2006;Norby and Iversen, 2006) redistributing N from mineral soil to vegetation (Hungate et al., 2013;Hungate et al., 2006;Luo et al., 2006). Published results from other meta-analysis and synthesis work have also indicated significant modifications in the C:N ratios of vegetation and soil, ecosystem N capital, and the redistribution of N between vegetation and soils under eCO 2 (Liang et al., 2016;Luo et al., 2006;Shi et al., 2016;Terrer et al., 2018). ...
Article
Interactions between the carbon (C) and nitrogen (N) cycles can impact on the sensitivity of terrestrial C storage to elevated atmospheric carbon dioxide (CO2) concentrations (eCO2). However, the underlying mechanisms associated with CN interactions that influence terrestrial ecosystem C sequestration (Cseq) remains unclear. Here, we quantitatively analyzed published C and N responses to experimentally eCO2 using a meta-analysis approach. We determined the relative importance of three principal mechanisms (changes in the total ecosystem N amount, redistribution of N between plant and soil pools, and flexibility of the C:N ratio) that contribute to increases in ecosystem C storage in response to eCO2. Our results showed that eCO2 increased C and N accumulation, resulted in higher C:N ratios in plant, litter, and soil pools and induced a net shift of N from soils to vegetation. These three mechanisms largely explained the increment of ecosystem Cseq under eCO2, although the relative contributions differed across ecosystem types, with changes in the C:N ratio contributing 50% of the increment in forests Cseq, while the total N change contributed 60% of the increment in grassland Cseq. In terms of temporal variation in the relative importance of each of these three mechanisms to ecosystem Cseq: changes in the C:N ratio was the most important mechanism during the early years (~5 years) of eCO2 treatment, whilst the contribution to ecosystem Cseq by N redistribution remained rather small, and the contribution by total N change did not show a clear temporal pattern. This study highlights the differential contributions of the three mechanisms to Cseq, which may offer important implications for future predictions of the C cycle in terrestrial ecosystems subjected to global change.
... Additional C acquisition under eCO 2 can enhance plant and soil C pools, the latter by increasing plant-derived C inputs to soils, reducing litter quality and thereby slowing litter decomposition rates, and/or by stimulating physical protection of soil organic matter (SOM) from microbial decomposition (13)(14)(15). However, some studies have observed no C accumulation under eCO 2 (16)(17)(18)(19)(20)(21). ...
Article
Full-text available
Whether the terrestrial biosphere will continue to act as a net carbon (C) sink in the face of multiple global changes is questionable. A key uncertainty is whether increases in plant C fixation under elevated carbon dioxide (CO 2 ) will translate into decades-long C storage and whether this depends on other concurrently changing factors. We investigated how manipulations of CO 2 , soil nitrogen (N) supply, and plant species richness influenced total ecosystem (plant + soil to 60 cm) C storage over 19 y in a free-air CO 2 enrichment grassland experiment (BioCON) in Minnesota. On average, after 19 y of treatments, increasing species richness from 1 to 4, 9, or 16 enhanced total ecosystem C storage by 22 to 32%, whereas N addition of 4 g N m ⁻² ⋅ y ⁻¹ and elevated CO 2 of +180 ppm had only modest effects (increasing C stores by less than 5%). While all treatments increased net primary productivity, only increasing species richness enhanced net primary productivity sufficiently to more than offset enhanced C losses and substantially increase ecosystem C pools. Effects of the three global change treatments were generally additive, and we did not observe any interactions between CO 2 and N. Overall, our results call into question whether elevated CO 2 will increase the soil C sink in grassland ecosystems, helping to slow climate change, and suggest that losses of biodiversity may influence C storage as much as or more than increasing CO 2 or high rates of N deposition in perennial grassland systems.
... These other mineral nutrients are derived from weathering, and their plant-available fraction in soils is heavily competed for by plants and microorganism ever since. Could a CO 2 -rich atmosphere affect soil nutrient acquisition and release more nutrients from the soil matrix (Körner and Arnone 1992;Schleppi et al. 2012;Hungate et al. 2013)? And if so, how long could that be sustained? ...
Chapter
The direction of science is often driven by contemporary theory, and theory emerges from consolidated empirical knowledge. What we know emerges from what we explore, and we explore what we have technical tools for. I feel that technical opportunities contributed strongly towards what is held as a contemporary, widely accepted theory. However, the presumed causality may become reverted, if one accounts for those less explored questions, for which tools are missing. Here, I will reflect on decades of research experience in empirical plant sciences, mainly plant water relations, plant carbon relations and biogeography, during which some mainstream paradigms became challenged. Scientific theory passes through waves and cycles and is even linked to fashion. Insight that seemed established at one time may become outdated by novel concepts facilitated by novel methods, and as time progresses, old concepts may find a revival. In the following chapter, I will illustrate such shifts in awareness and misleading paradigms that were driven by the contemporary availability of methods rather than stringent logics. Examples include plant responses to drought stress; the drivers of plant growth in general, as well as in the context of rising atmospheric CO2 concentrations; and how physiological plant ecology can contribute to resolving biogeographical questions such as range limits of plant species and plant life forms. My résumé is that explanations of plant responses to the environment are predominantly below ground and require an understanding of developmental and meristematic processes, whereas available tools often lead to attempts at above-ground answers based on primary metabolism (e.g. photosynthesis). Further, well-understood processes at the organ (leaf) level are losing relevance at the community or ecosystem level, where much less understood mechanisms come into action (e.g. stand density control). While the availability of certain convenient methods can open new research arenas, it may also narrow the scope and may direct theory development towards easily measurable parameters and processes.
... Early studies using pots and growth chambers hardly reflected the real forest ecosystem conditions (Curtis & Wang 1998, Norby et al. 2010, therefore experiments with Open-Top chamber (OTC) and Free Air CO2 Enrichment (FACE) techniques have been widely employed (Norby et al. 2010). Many OTC and FACE experiments reported an increased growth and photosynthesis under elevated CO2 (Hungate et al. 2013, Talhelm et al. 2014. However, whether these effects would last for a long time is questioned. ...
... For example, a decade of eCO 2 increased C soil at ORNL FACE (β dir,fut = 0.51 AE 0.6, 0-90 cm) (Iversen et al., 2012) and in a desert ecosystem (β dir,fut = 0.59 AE 0.62) (Evans et al., 2014), but not in a scrub oak ecosystem (β dir,fut = −0.15 AE 0.5) (Hungate et al., 2013). In the desert ecosystem, inorganic carbonate pools may have contributed to increases in C soil through nocturnal CO 2 uptake (Hamerlynck et al., 2013) although net effects are probably small (Soper et al., 2017). ...
Article
Atmospheric carbon dioxide concentration ([CO2]) is increasing, which increases leaf‐scale photosynthesis and intrinsic water‐use efficiency. These direct responses have the potential to increase plant growth, vegetation biomass, and soil organic matter; transferring carbon from the atmosphere into terrestrial ecosystems (a carbon sink). A substantial global terrestrial carbon sink would slow the rate of [CO2] increase and thus climate change. However, ecosystem CO2‐responses are complex or confounded by concurrent changes in multiple agents of global change and evidence for a [CO2]‐driven terrestrial carbon sink can appear contradictory. Here we synthesise theory and broad, multi‐disciplinary evidence for the effects of increasing [CO2] (iCO2) on the global terrestrial carbon sink. Evidence suggests a substantial increase in global photosynthesis since pre‐industry. Established theory, supported by experiments, indicates that iCO2 is likely responsible for about half of the increase. Global carbon budgeting, atmospheric data, and forest inventories indicate a historical carbon sink, and these apparent iCO2‐responses are high in comparison with experiments and theory. Plant mortality and soil carbon iCO2‐responses are highly uncertain. In conclusion, a range of evidence supports a positive terrestrial carbon sink in response to iCO2, albeit with uncertain magnitude and strong suggestion of a role for additional agents of global change.
Article
Full-text available
Terrestrial ecosystems remove about 30 per cent of the carbon dioxide (CO2) emitted by human activities each year¹, yet the persistence of this carbon sink depends partly on how plant biomass and soil organic carbon (SOC) stocks respond to future increases in atmospheric CO2 (refs. 2,3). Although plant biomass often increases in elevated CO2 (eCO2) experiments4,5,6, SOC has been observed to increase, remain unchanged or even decline⁷. The mechanisms that drive this variation across experiments remain poorly understood, creating uncertainty in climate projections8,9. Here we synthesized data from 108 eCO2 experiments and found that the effect of eCO2 on SOC stocks is best explained by a negative relationship with plant biomass: when plant biomass is strongly stimulated by eCO2, SOC storage declines; conversely, when biomass is weakly stimulated, SOC storage increases. This trade-off appears to be related to plant nutrient acquisition, in which plants increase their biomass by mining the soil for nutrients, which decreases SOC storage. We found that, overall, SOC stocks increase with eCO2 in grasslands (8 ± 2 per cent) but not in forests (0 ± 2 per cent), even though plant biomass in grasslands increase less (9 ± 3 per cent) than in forests (23 ± 2 per cent). Ecosystem models do not reproduce this trade-off, which implies that projections of SOC may need to be revised.
Article
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Forest ecosystems play an important role in regulating global temperatures through their capability to take up and store CO2 from the atmosphere, but the magnitude and sustainability of this carbon (C) sink is critically dependent on the availability of nutrients, particularly nitrogen (N). However, the extent to which the absolute amount of N or modifications in plant and soil C:N ratios controls long-term forest C sequestration (Cseq) remains uncertain. To assess this, we analyzed the results of 135 global field studies that investigated the dynamics of C and N availability during forest succession. The results showed that the accumulation of C and N in plant (including above- and below-ground vegetation) and litter pools decreased with forest age and approached an equilibrium value in the latter stages of stand development. Plant and litter C:N ratios increased during the first 10 - 20 years and remained relatively stable thereafter. The analysis further showed that the relative importance of a change in the total amount of N or modifications in the C:N ratio, to increases in Cseq, varied with forest age. Whilst the relative importance of a change in the total amount of N increased with forest age, the relative importance of a varied C:N stoichiometry decreased with forest age. Overall, a change in the total amount of N was the more important factor contributing to C storage during forest stand development and the C stored in vegetation dominated the total ecosystem C pool. These results show that ecosystem N availability is a key factor supporting long-term forest Cseq during forest succession. As most of the C is found in above-ground vegetation, this pool is particularly susceptible to abiotic or biotic factors and anthropogenically-related disturbances.
Chapter
Photosynthesis provides the energy that powers the biochemical reactions of life. That energy is captured form sunlight and stored in the carbon bonds of organic materials. Globally, plant production captures about 60 × 10¹⁵ g C yr⁻¹, which is available to the terrestrial biosphere. In regions with adequate soil moisture, plant growth is determined by the length of the growing season and mean annual temperature. Soil nutrients appear to be of secondary importance to NPP on land, perhaps because plants have various adaptations for obtaining and recycling decomposed. The decomposition process is remarkably efficient so only small amounts of NPP are added to the long-term storage of soil organic matter or humus. Soil organic matter consists of a dynamic pool near the surface and a large refractory pool of humic substance that are dispersed throughout the lower soil profile. Humans have altered the processes of NPP and decomposition on land, resulting in the transfer of carbon to the atmosphere, and perhaps a permanent reduction in the global rage of NPP.
Article
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This paper summarizes the data on nutrient uptake and soil responses in opentop chambers planted with ponderosa pine (Pinus ponderosa Laws.) treated with both N and CO2. Based upon the literature, we hypothesized that 1) elevated CO2 would cause increased growth and yield of biomass per unit uptake of N even if N is limiting, and 2) elevated CO2 would cause increased biomass yield per unit uptake of other nutrients only by growth dilution and only if they are non-limiting. Hypothesis 1 was supported only in part: there were greater yields of biomass per unit N uptake in the first two years of growth but not in the third year. Hypothesis 2 was supported in many cases: elevated CO2 caused growth dilution (decreased concentrations but not decreased uptake) of P, S, and Mg. Effects of elevated CO2 on K, Ca, and B concentrations were smaller and mostly non-significant. There was no evidence that N responded in a unique manner to elevated CO2, despite its unique role in rubisco. Simple growth dilution seemed to explain nutrient responses in almost all cases. There were significant declines in soil exchangeable K+, Ca2+, Mg2+ and extractable P over time which were attributed to disturbance effects associated with plowing. The only statistically significant treatment effects on soils were negative effects of elevated CO2 on mineralizeable N and extractable P, and positive effects of both N fertilization and CO2 on exchangeable Al3+. Soil exchangeable K+, Ca2+, and Mg2+ pools remained much higher than vegetation pools, but extractable P pools were lower than vegetation pools in the third year of growth. There were also large losses of both native soil N and fertilizer N over time. These soil N losses could account for the observed losses in exchangeable K+, Ca2+, Mg2+ if N was nitrified and leached as NO 3−.
Article
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The results of published and unpublished experiments investigating the impacts of elevated [CO2] on the chemistry of leaf litter and decomposition of plant tissues are summarized. The data do not support the hypothesis that changes in leaf litter chemistry often associated with growing plants under elevated [CO2] have an impact on decomposition processes. A meta-analysis of data from naturally senesced leaves in field experiments showed that the nitrogen (N) concentration in leaf litter was 7.1% lower in elevated [CO2] compared to that in ambient [CO2]. This statistically significant difference was: (1) usually not significant in individual experiments, (2) much less than that often observed in green leaves, and (3) less in leaves with an N concentration indicative of complete N resorption. Under ideal conditions, the efficiency with which N is resorbed during leaf senescence was found not to be altered by CO2 enrichment, but other environmental influences on resorption inevitably increase the variability in litter N concentration. Nevertheless, the small but consistent decline in leaf litter N concentration in many experiments, coupled with a 6.5% increase in lignin concentration, would be predicted to result in a slower decomposition rate in CO2-enriched litter. However, across the assembled data base, neither mass loss nor respiration rates from litter produced in elevated [CO2] showed any consistent pattern or differences from litter grown in ambient [CO2]. The effects of [CO2] on litter chemistry or decomposition were usually smallest under experimental conditions similar to natural field conditions, including open-field exposure, plants free-rooted in the ground, and complete senescence. It is concluded that any changes in decomposition rates resulting from exposure of plants to elevated [CO2] are small when compared to other potential impacts of elevated [CO2] on carbon and N cycling. Reasons for experimental differences are considered, and recommendations for the design and execution of decomposition experiments using materials from CO2-enrichment experiments are outlined.
Article
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Grasslands are globally widespread and capable of storing large amounts of carbon (C) in soils, and are generally experiencing increasing atmospheric CO2, nitrogen (N) deposition, and biodiversity losses. To better understand whether grasslands will act as C sources or sinks in the future we measured microbial respiration in long-term laboratory incubations of soils collected from a grassland field experiment after 9 years of factorial treatment of atmospheric CO2, N deposition, and plant species richness on a deep and uniformly sandy soil. We fit microbial soil respiration rates to three-pool models of soil C cycling to separate treatment effects on decomposition and pool sizes of fast, slow, and resistant C pools. Elevated CO2 decreased the mean residence time (MRT) of slow C pools without affecting their pool size. Decreasing diversity reduced the size and MRT of fast C pools (comparing monocultures to plots planted with 16 species), but increased the slow pool MRT. N additions increased the size of the resistant pool. These effects of CO2, N, and species-richness treatments were largely due to plant biomass differences between the treatments. We found no significant interactions among treatments. These results suggest that C sequestration in sandy grassland soils may not be strongly influenced by elevated CO2 or species losses. However, high N deposition may increase the amount of resistant C in these grasslands, which could contribute to increased C sequestration.
Article
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Free-air CO enrichment (FACE) experiments have provided novel insights into the ecological mechanisms controlling the cycling and storage of carbon in terrestrial ecosystems and contribute to our ability to project how ecosystems respond to increasing CO in the Earth's atmosphere. Important lessons emerge by evaluating a set of hypotheses that initially guided the design and longevity of forested FACE experiments. Net primary productivity is increased by elevated CO, but the response can diminish over time. Carbon accumulation is driven by the distribution of carbon among plant and soil components with differing turnover rates and by interactions between the carbon and nitrogen cycles. Plant community structure may change, but elevated CO has only minor effects on microbial community structure. FACE results provide a strong foundation for next-generation experiments in unexplored ecosystems and inform coupled climate-biogeochemical models of the ecological mechanisms controlling ecosystem response to the rising atmospheric CO concentration.
Article
The flow of carbon from photosynthesizing tissues of higher plants, through the roots and into the soil is one of the key processes in terrestrial ecosystems. An increased level of CO"2 in the atmosphere will likely result in an increased input of organic carbon into the soil due to the expected increase in primary production. Whether this will lead to accumulation of greater amounts of organic carbon in soil depends on the flow of carbon through the plant into the soil and its subsequent transformation in the soil by microorganisms. In this paper the major controls of carbon translocation via roots into the soil as well as the subsequent microbial turnover of root-derived carbon are reviewed. We discuss possible consequences of an increased CO"2 level in the atmosphere on these processes.
Article
Increased partitioning of carbon (C) to fine roots under elevated [CO2], especially deep in the soil profile, could alter soil C and nitrogen (N) cycling in forests. After more than 11 years of free‐air CO2 enrichment in a Liquidambar styraciflua L. (sweetgum) plantation in Oak Ridge, TN, USA, greater inputs of fine roots resulted in the incorporation of new C (i.e., C with a depleted δ13C) into root‐derived particulate organic matter (POM) pools to 90‐cm depth. Even though production in the sweetgum stand was limited by soil N availability, soil C and N contents were greater throughout the soil profile under elevated [CO2] at the conclusion of the experiment. Greater C inputs from fine‐root detritus under elevated [CO2] did not result in increased net N immobilization or C mineralization rates in long‐term laboratory incubations, possibly because microbial biomass was lower in the CO2‐enriched plots. Furthermore, the δ13CO2 of the C mineralized from the incubated soil closely tracked the δ13C of the labile POM pool in the elevated [CO2] treatment, especially in shallower soil, and did not indicate significant priming of the decomposition of pre‐experiment soil organic matter (SOM). Although potential C mineralization rates were positively and linearly related to total SOM C content in the top 30 cm of soil, this relationship did not hold in deeper soil. Taken together with an increased mean residence time of C in deeper soil pools, these findings indicate that C inputs from relatively deep roots under elevated [CO2] may increase the potential for long‐term soil C storage. However, C in deeper soil is likely to take many years to accrue to a significant fraction of total soil C given relatively smaller root inputs at depth. Expanded representation of biogeochemical cycling throughout the soil profile may improve model projections of future forest responses to rising atmospheric [CO2].
Article
After four growing seasons, elevated CO_2 did not significantly alter surface soil C pools in two intact annual grasslands. However, soil C pools in these systems are large compared to the likely changes caused by elevated CO_2. We calculated statistical power to detect changes in soil C, using an approach applicable to all elevated CO_2 experiments. The distinctive isotopic signature of the fossil-fuel-derived CO_2 added to the elevated CO_2 treatment provides a C tracer to determine the rate of incorporation of newly-fixed C into soil. This rate constrains the size of the possible effect of elevated CO_2 on soil C. Even after four years of treatment, statistical power to detect plausible changes in soil C under elevated CO_2 is quite low. Analysis of other elevated CO_2 experiments in the literature indicates that either CO_2does not affect soil C content, or that reported CO_2effects on soil C are too large to be a simple consequence of increased plant carbon inputs, suggesting that other mechanisms are involved, or that the differences are due to chance. Determining the effects of elevated CO_2 on total soil C and long-term C storage requires more powerful experimental techniques or experiments of longer duration.
Article
Nadelhoffer et al. use 15N-tracer studies in nine northern forests to argue that increasing inputs of combined nitrogen from the atmosphere are unlikely to cause the increase in forest growth that has been postulated as the `missing sink' for atmospheric CO2. Only about 20% of the tracer ended up in the trees and about 70% remained in the organic and mineral layers of the soil. If only 20% of the nitrogen input from the atmosphere were available for tree growth, then not enough combined nitrogen would be coming into the northern forests each year to explain the missing carbon sink.
Article
In recent years, increased awareness of the potential interactions between rising atmospheric CO2 concentrations ([ CO2 ]) and temperature has illustrated the importance of multifactorial ecosystem manipulation experiments for validating Earth System models. To address the urgent need for increased understanding of responses in multifactorial experiments, this article synthesizes how ecosystem productivity and soil processes respond to combined warming and [ CO2 ] manipulation, and compares it with those obtained in single factor [ CO2 ] and temperature manipulation experiments. Across all combined elevated [ CO2 ] and warming experiments, biomass production and soil respiration were typically enhanced. Responses to the combined treatment were more similar to those in the [ CO2 ]-only treatment than to those in the warming-only treatment. In contrast to warming-only experiments, both the combined and the [ CO2 ]-only treatments elicited larger stimulation of fine root biomass than of aboveground biomass, consistently stimulated soil respiration, and decreased foliar nitrogen (N) concentration. Nonetheless, mineral N availability declined less in the combined treatment than in the [ CO2 ]-only treatment, possibly due to the warming-induced acceleration of decomposition, implying that progressive nitrogen limitation (PNL) may not occur as commonly as anticipated from single factor [ CO2 ] treatment studies. Responses of total plant biomass, especially of aboveground biomass, revealed antagonistic interactions between elevated [ CO2 ] and warming, i.e. the response to the combined treatment was usually less-than-additive. This implies that productivity projections might be overestimated when models are parameterized based on single factor responses. Our results highlight the need for more (and especially more long-term) multifactor manipulation experiments. Because single factor CO2 responses often dominated over warming responses in the combined treatments, our results also suggest that projected responses to future global warming in Earth System models should not be parameterized using single factor warming experiments.