Tree Physiology 25, 1399–1408
© 2005 Heron Publishing—Victoria, Canada
Net carbon storage in a poplar plantation (POPFACE) after three
years of free-air CO2 enrichment
B. GIELEN,1,2 C. CALFAPIETRA,3 M. LUKAC,4 V. E. WITTIG,5 P. DE ANGELIS,3
I. A. JANSSENS,1 M. C. MOSCATELLI,6 S. GREGO,6 M. F. COTRUFO,7 D. L. GODBOLD,4
M. R. HOOSBEEK,8 S. P. LONG,5 F. MIGLIETTA,9 A. POLLE,10 C. J. BERNACCHI,5,11
P. A. DAVEY,12 R. CEULEMANS1 and G. E. SCARASCIA-MUGNOZZA3
1
University of Antwerpen, Campus Drie Eiken, Dept. of Biology, Research Group of Plant and Vegetation Ecology, Universiteitsplein 1, B-2610
Wilrijk, Belgium
2
Corresponding author ([email protected])
3
University of Tuscia, Dept. of Forest Environment and Resources (DISAFRI), Via S. Camillo De Lellis, I-01100 Viterbo, Italy
4
University of Wales, School of Agricultural and Forest Sciences, Bangor, Gwynedd LL57 2UW, U.K.
5
University of Illinois, Dept. of Plant Biology, 190 Edward R. Madigan Laboratory, 1201 West Gregory Drive, Urbana, IL 61801-3838, USA
6
University of Tuscia, Soil Biochemistry Laboratory, Dept. of Agrobiology and Agrochemistry, Via S. Camillo De Lellis, I-01100 Viterbo, Italy
7
Second University of Naples, Dept. of Environmental Sciences, Via Vivaldi 43, I- 81100 Caserta, Italy
8
Wageningen University, Laboratory of Soil Science and Geology, Dept. of Environmental Sciences, P.O. Box 37, 6700 AA Wageningen, The
Netherlands
9
IBIMET-CNR, Via Caproni 8, 50145 Firenze, Italy
10
Georg August Universität Göttingen, Institut für Forstbotanik, 37077 Göttingen, Germany
11
Illinois State Water Survey, 2204 Griffith Drive, Champaign, IL 61820, USA
12
University of Essex, Dept. of Biological Sciences, Wivenhoe Park, Colchester, CO4 3SQ, U.K.
Received February 8, 2005; accepted April 15, 2005; published online August 16, 2005
Summary A high-density plantation of three genotypes of
Populus was exposed to an elevated concentration of carbon dioxide ([CO2]; 550 µmol mol – 1) from planting through canopy
closure using a free-air CO2 enrichment (FACE) technique.
The FACE treatment stimulated gross primary productivity by
22 and 11% in the second and third years, respectively. Partitioning of extra carbon (C) among C pools of different turnover
rates is of critical interest; thus, we calculated net ecosystem
productivity (NEP) to determine whether elevated atmospheric
[CO2] will enhance net plantation C storage capacity. Free-air
CO2 enrichment increased net primary productivity (NPP) of
all genotypes by 21% in the second year and by 26% in the third
year, mainly because of an increase in the size of C pools with
relatively slow turnover rates (i.e., wood). In all genotypes in
the FACE treatment, more new soil C was added to the total soil
C pool compared with the control treatment. However, more
old soil C loss was observed in the FACE treatment compared
with the control treatment, possibly due to a priming effect
from newly incorporated root litter. FACE did not significantly
increase NEP, probably as a result of this priming effect.
Keywords: global change, NEP, NPP, Populus.
Introduction
The ongoing anthropogenic increase in atmospheric carbon
dioxide concentration ([CO2]) is a primary factor in climate
change (Houghton et al. 2001). Mitigation of the increase in
atmospheric [CO2] is an important goal for humanity. Terrestrial ecosystems, and in particular forest ecosystems, are the
focus of intensive research on the effects of elevated [CO2] because of their importance in the global carbon (C) cycle,
(DeLucia et al. 1999, Hendrey et al. 1999, Isebrands et al.
2001, Norby et al. 2001). Forest plantation fossil C storage capacity is of particular interest as a [CO2] reduction strategy, for
the fulfillment of Kyoto Protocol requirements (Article 3.3,
UNFCC 1997). Among various agricultural land-use and
management strategies, bioenergy crops have the largest potential for C storage (Smith et al. 2000). Fast-growing tree species such as poplar are important components of temperate and
boreal ecosystems and are especially well suited for plantation
culture. Short-rotation culture (SRC) of poplar is increasingly
used as a source of renewable energy; other applications include removal of excess fertilizers and phytoremediation
(Isebrands and Karnosky 2001).
Experiments using the free-air CO2 enrichment (FACE)
technique provide a powerful tool for the study of whole-eco-
1400
GIELEN ET AL.
system C budgets. To date, only two FACE-exposed forest
ecosystem C budgets have been published; however, both
studies used stepwise [CO2] increases in established stands.
The C budget may be fundamentally different in forest ecosystems established and grown in elevated [CO2]. Net primary
productivity (NPP) of an intact Pinus taeda L. forest increased
by 25% after 2 years of FACE, a stimulation that was sustained
over 4 years (DeLucia et al. 1999, Hamilton et al. 2002). This
increase was caused by increased tree growth rates (Hamilton
et al. 2002). Similarly, FACE increased NPP of a closed-canopy deciduous forest (Norby et al. 2002). However, although
most of the additional net C uptake in the first year was allocated to woody biomass, subsequent years saw a shift from
woody biomass to fine-root production (Norby et al. 2002).
Because wood has a much slower turnover rate than fine roots
(Gaudinski et al. 2001, Norby et al. 2002), this finding has important implications for net forest C storage capacity. Nevertheless, increased fine-root productivity may also serve an
important role in the long-term accumulation of C in terrestrial
ecosystems by adding C to the soil, thereby ultimately increasing C stores in long-lived soil organic matter (SOM)
pools (Lukac et al. 2003).
Much of the current knowledge about forest ecosystem C
source and sink strength is based on estimates of net ecosystem C fluxes, but our understanding of forest C budgets at the
process level is poor. In both chamber as well as FACE experiments, attempts to quantify soil C stores have found only small
changes in response to increased [CO2] (Leavitt et al. 1994,
Hungate et al. 1996, Schlesinger and Lichter 2001). However,
because of the magnitude and high spatial variation of soil C
stores, quantifying changes is difficult. Many CO2 enrichment
systems use petrochemically derived CO2, which is depleted in
13
C, thus functioning as a tracer of C fluxes between vegetation
and soils. Several studies have made use of this tracer to quantify C input from the vegetation to the soil (Leavitt et al. 1994,
Hungate et al. 1996), but it was impossible to assess control
treatments in these studies. To overcome this limitation, we
used the C 3 /C4 stable isotope method (Balesdent et al. 1988,
Ineson et al. 1996). The CO2 gas used for fumigation in our
study had a δ13C signal of –6‰, close to the ambient value of
–8‰. The method consists of growing C 3 plants (i.e., with a
mean δ13C of –27‰) in C4 soils (i.e., a soil developed under C4
vegetation with a mean δ13C of –18‰), thus creating a tracer
of plant-derived C input into the soil, independent of the elevated [CO2] treatment.
In this paper, we report on the C budget of a FACE research
site (POPFACE) where three Populus genotypes have been
grown from planting through canopy closure in a high density
plantation (Scarascia-Mugnozza et al. 2000, Miglietta et al.
2001). At the end of a 3-year growth period, the aboveground
woody biomass was 15 to 27% higher in FACE plots than in
control plots, depending on genotypes (Calfapietra et al.
2003). Belowground, FACE increased total root biomass by 47
to 76% (Lukac et al. 2003). The FACE treatment had a positive
effect (50 to 97%) on the amount of plant-derived C incorporated into SOM during the third year (Hoosbeek et al. 2004).
Based on these findings, we hypothesized that the net C storage capacity of these plantations may increase in a future
CO2-enriched atmosphere. To test this hypothesis, we integrated relevant data from the FACE site to calculate NPP and
net ecosystem productivity (NEP) for the second and third
years.
Materials and methods
Description of the POPFACE site
The POPFACE experimental facility is located in central Italy
(42°22′ N, 11°48′ E, 150 m a.s.l.) on a formerly agricultural,
9-ha field. The soil has a loam texture and a deep A horizon,
and is classified as a Xeric Alfisol (Hoosbeek et al. 2004). After soil preparation, Populus × euramericana (Dode) Guinier
(Clone I-214) hardwood cuttings were planted in late spring of
1999 at 2 × 1 m2 spacing. Six experimental plots were positioned within the plantation in a way that minimized enrichment pollution. Three control plots were left under natural
conditions, whereas the remaining three plots had an elevated
[CO2] (550 µmol mol – 1) provided by the FACE technique.
Measured FACE plot mean [CO2] were 544 ± 48, 532 ± 83 and
554 ± 95 µmol mol – 1 in the first, second and third years, respectively. A detailed description of the FACE installation and
of system performance is provided in Miglietta et al. (2001).
Each plot was 22 m in diameter and contained about 350
plants spaced at 1 × 1 m. Each plot was further divided into six
sectors, of which two were planted with trees of a single
Populus genotype. The genotypes used were: P. alba L. (Clone
2AS11), P. nigra L. (Clone Jean Pourtet) and P. × euramericana (P. deltoides Bart. ex Marsh. × P. nigra, Clone I-214).
Further information on genotypic properties is detailed in
Calfapietra et al. (2001). During the growing seasons, the
plantation was drip-irrigated at a rate of 6 to 10 mm of water
per day; weeds were removed manually or mechanically, and
insecticides were applied as necessary.
Carbon pools and increments
In accordance with Hamilton et al. (2002), a C pool was defined as a C reservoir lasting 1 year or longer, and a C increment was defined as the annual change in the size of each pool.
All data reported are for either the second (Year 2000) or third
year (Year 2001) of the experiment.
Aboveground woody biomass
Following the method of Calfapietra et al. (2003), at the end of
each year, the standing pool of aboveground woody biomass
was calculated from genotype-specific allometric relationships established at the end of the second and third years by destructive harvests. Second-year allometric relationships were
used to estimate biomass at the end of the first year. Biomass of
the stump was determined from aboveground biomass using a
mean genotype-specific ratio determined from harvested trees.
Annual increments for both aboveground biomass and stump
were determined from biomass at the end of each year minus
biomass at the end of the previous year. Biomass was con-
TREE PHYSIOLOGY VOLUME 25, 2005
CARBON BUDGET OF PLANTATION EXPOSED TO FACE
verted to C based on a mean C concentration of 48%. Further
details are in Calfapietra et al. (2003).
Leaf litter production and decomposition
In the second and third years, litter production (g m – 2 of
ground area) was monitored in control and FACE plots with
108 0.13-m2 leaf litter traps, as described by Cotrufo et al.
(2005). For the first year, leaf litter production was estimated
from the total amount of leaf area produced (Gielen et al.
2001) and from mean values of specific leaf area. Leaf litter
produced from July to December of the second and third year,
was ground to a fine powder and analyzed for C concentration
(Carlo Erba NA 1500, Carlo Erba Strumentazione, Milan,
Italy) by sampling date and sector. Additionally, all litter produced from October to December of the second year was
pooled by sector for chemical analyses and the decomposition
study. Litter decomposition was monitored in the field with litter bags, and genotype and treatment decay rates were obtained. A detailed description of the experiment is in Cotrufo
et al. (2005).
The annual increment in the standing leaf litter C pool was
the cumulative value of the periodical C increments measured
for that year, i.e., the weekly amount of litter fall multiplied by
the corresponding value of C concentration. Annual C loss was
calculated by multiplying the annual litter production by the
yearly percentage mass loss. For the third year, C loss from the
decomposition of the remaining first year litter was calculated
by extrapolating the mass loss curves over a 2-year period. The
leaf litter C pool was defined as the sum of C in the litter produced in that year and the C remaining on the forest floor after
decomposition of the litter from previous years.
Root production and root turnover
Standing root biomass up to 40 cm in depth was sampled three
to five times per season with a corer (inner diameter of 8 cm).
Roots were divided into two diameter classes: fine (< 2 mm)
and coarse (> 2 mm). Based on standard criteria, only negligible amounts of necromass were detected. A modification of
the ingrowth-coring method, as described by Lukac and Godbold (2001), measured fine root production. Root turnover was
determined according to Dahlman and Kuèera (1965), as the
ratio between annual production and maximum standing crop.
These results are presented in detail in Lukac et al. (2003).
Carbon allocated to root system biomass was calculated
based on coarse and fine root biomass data expressed per season, corrected for ash content and converted from dry biomass
to C, based on actual C concentrations. Coarse root C increment was calculated as mean seasonal coarse root biomass minus the mean from the previous season, because no coarse root
turnover was observed during the 3-year experimental period.
To determine C allocation to fine roots, mean seasonal fine
root biomass was multiplied by fine root turnover.
At the end of the third year, one tree in each sector was harvested and a subsample of the root system was analyzed for C
by size class: fine (< 2 mm diameter), intermediate (2–5 mm)
and coarse (> 5 mm).
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Soil carbon
Data on soil C were derived from Hoosbeek et al. (2004). In
November of all 3 years, soil samples were collected from
each sector in all plots. Bulk density samples were taken by
metal rings with a diameter and height of 10 cm, at 0–10,
10 – 20 and 20 – 30 cm soil depth. The samples were dried,
crushed by hand and live roots removed. Carbon was measured with an elemental analyzer (Van Lagen 1996). Soil C
pools were expressed per 0.1 m3 using bulk densities, and
summed over 0 – 30 cm soil depth to approximate soil C per
m2. Annual changes in soil C pools were calculated from the
difference between soil C pools at the end of two consecutive
years.
We used the C 3 / C4 stable isotope method outlined by Balesdent et al. (1988) to estimate annual influx of plant C (leaves
and roots) to the soil. Root ingrowth cores (diameter of 4 cm,
length of 40 cm, 2 mm mesh), filled with soil material with a
C4-soil-like signature, were placed in the C3 soil of the plantation in March and collected in November of the second and
third years. The fraction of C in the soil derived from leaves
and roots during the incubation period ( f ) was calculated with
a simple mixing model, as described by Balesdent et al.
(1988). The amount of soil C newly accumulated (Cnew) during
the incubation period was obtained by multiplying the C content of the incubated sample by f. From Cnew and from the
change of the soil C pool between 2 years, the soil C loss per
year was estimated. For further details see Hoosbeek et al.
(2004).
Microbial biomass
Six soil cores (10 cm diameter, 20 cm depth) were taken from
the 1 – 20-cm layer in each of the six plots, two per genotype,
for a total of 36 soil cores on four sampling dates (March, June,
August and October of the third year). Soil samples were immediately sieved (2 mm) and the water content adjusted to
60% of soil water holding capacity. Microbial biomass C was
estimated by the fumigation extraction method (Vance et al.
1987). The results obtained for each sampling date were averaged and converted to g C m – 2 according to the soil bulk density of the layer 0 – 20 cm measured as described previously.
Gross primary productivity
Gross primary productivity (GPP) over the 3-year growth cycle was derived as described by Wittig et al. (2005). In brief,
GPP was calculated with the equations of Long (1991) and the
temperature corrections of Bernacchi et al. (2001, 2003b). The
inputs were photon flux and temperature, measured at 30-min
intervals from a nearby weather station, and leaf area index
(Gielen et al. 2001, 2003), maximum rate of leaf carboxylation
(Vcmax ) and electron transport (Jmax ), determined previously
throughout the growth cycle (Bernacchi et al. 2003a). From
the meteorological conditions recorded at 30-min intervals
and the biweekly leaf area index measurements, the microclimate of leaves within the plots was estimated with a radiation
transfer and energy balance model. This information was in
turn used as an input in the steady-state biochemical model of
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
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GIELEN ET AL.
leaf photosynthesis (Farquhar et al. 1980) to compute leaf
photosynthetic rate. The photosynthetic rates for different leaf
classes were summed to obtain canopy photosynthesis, i.e.,
GPP. We estimated GPP for each species and each plot, and the
means and standard errors for the three replicate plots are presented.
Results
Gross primary productivity
Free-air CO2 enrichment stimulated GPP in all genotypes by
22 and 11% in the second and third years, respectively
(P = 0.0002 and 0.0019, respectively) (Table 1).
Carbon pools
Net primary productivity and net ecosystem productivity
Annual NPP (g C m – 2 year – 1) was calculated as the summation of the increment of woody biomass (stem + stump +
branches + coarse roots) + leaf litter production + fine root
production. No data were available for branch litter and herbivory, but these are usually assumed to be negligible (DeLucia et al. 1999, Norby et al. 2002). Because the presence of
insects and herbivores was insignificant (N. Anselmi and
A. Olmi, Department of Plant Protection, University of Tuscia,
Italy, personal communication), C losses due to herbivory
were presumed to be minor. Branch litter was considered to be
negligible during the first 3 years of the experiment.
Annual net C storage was calculated according to Curtis et
al. (2002) from the increment of wood (stem, branches, stump)
plus the increment of coarse roots plus changes in the soil C
pool. Although no data for heterotrophic respiration were
available to explicitly calculate NEP, annual net C storage is a
valid approximation of NEP.
Statistical analysis
The main effects of CO2 treatment, genotype and their interaction were determined by an analysis of variance (ANOVA). A
randomized-complete-block design with treatment, genotype,
and treatment × genotype interaction as fixed factors, and
block as a random factor was applied. Plot was the unit of replication (n = 3). All statistical analyses were performed with
the SAS statistical software package (SAS System 8.2, SAS
Institute, Cary, NC) using the mixed procedure (Littell et al.
1996). In the case of a significant CO2 treatment × genotype
interaction, a posteriori comparison of means was performed
with Bonferroni corrections for multiple comparisons. Differences between parameter means were considered significant
when the P value of the ANOVA F test was < 0.05. Data were
tested for normality using the Shapiro-Wilk statistic. If not
otherwise stated, genotypes were significantly different and no
CO2 treatment × genotype interaction was found; we therefore
focus on the effects of the FACE treatment.
Total plant C differed significantly between control and FACE
treatments in both the second (P = 0.0019) and third years (P =
0.0005). Relative differences were in the range of 17–38%
(second year) and 18 – 29% (third year) for the three genotypes
(Figures 1A and 1B). With the exception of P. alba in the second year, relative treatment effects on plant C pools were a factor of 2.6– 4 times larger for root than for stem and branch
standing biomass (Figures 1A and 1B). The positive effects of
FACE on fine root, coarse root, stump, stem and branch biomass were statistically significant (Calfapietra et al. 2003,
Lukac et al. 2003). The leaf litter pool did not differ between
treatments (second and third years) or between genotypes
(second year) (Figures 1A and 1B). Stems and branches typically accounted for 61 to 74% of total plant C pools. In the
third year, the ratio of stems + branches to total woody biomass was slightly lower in the FACE treatment than in the control treatment, i.e., 0.84 versus 0.88 for P. alba and P. nigra and
0.81 versus 0.84 for P. × euramericana (P < 0.0001; Figure 1B). Upon establishment of the plantation, the soil C pool
reflected the site’s land-use history (Hoosbeek et al. 2004).
There was considerable variation in the soil C pool among
plots. At the end of the second year, in both control and FACE
treatments, the soil C pool was nearly double that of the biomass C pool. After 3 years in FACE, the total plant biomass
pools for P. alba, P. nigra and P. × euramericana were 3373,
4076 and 3403 g C m – 2, respectively, and were similar to, or
exceeded, the soil C pools (down to 0.3 m; Figure 1B). At the
end of the third year, the control treatment soil C pools still exceeded the biomass pools. Soil microbial biomass accounted
for 1.7% (on average) of total soil C (Figure 1B). Although
FACE did not affect microbial biomass, the microbial quotient, i.e., the fraction of microbial biomass over the total soil
C, was 44% larger in the FACE plots than in the control plots
(P < 0.01).
Net primary productivity
The NPP for all genotypes was increased by FACE by 21 (SE =
7%, P = 0.0046) and 26% (SE = 5%, P = 0.0008) in the second
Table 1. Gross primary productivity (g C m – 2 year – 1) in high-density stands of three Populus genotypes in control and FACE treatments. Means
(SE) of three plots for the second and the third years are presented and were obtained by modeling (Wittig et al. 2005). Carbon dioxide treatment
effect was significant for both years.
P. alba
Second year
Third year
P. × euramericana
P. nigra
Control
FACE
Control
FACE
Control
FACE
1875 (35)
2585 (65)
2297 (154)
2829 (128)
2075 (66)
2773 (94)
2476 (46)
2921 (36)
1781 (36)
2150 (46)
2204 (132)
2550 (39)
TREE PHYSIOLOGY VOLUME 25, 2005
CARBON BUDGET OF PLANTATION EXPOSED TO FACE
1403
Figure 1. Carbon pools in high-density stands of P. alba, P. nigra and P. × euramericana (P. × eur) in the second (A) and third (B) years under control and FACE treatments. All values are means (SE) in g C m – 2 (n = 3). Coarse roots are defined as > 2 mm, whereas fine roots are defined as
< 2 mm. An explanatory legend is presented at the bottom of Figure 1A. Abbreviation: MB = microbial biomass.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1404
GIELEN ET AL.
and third years, respectively, compared with control conditions (Table 2). All components, except leaf litter, were significantly affected by FACE (Table 2). The coarse root increment
in the second year was significantly larger in the FACE treatment only for P. × euramericana (P = 0.0030, P value of CO2
treatment × genotype = 0.0229). The effect of FACE on coarse
root increment in the third year was marginally insignificant
(P = 0.0509) because the coarse root increment of P. × euramericana was unaffected by FACE (P value of CO2 treatment
× genotype = 0.1590). On a relative basis, FACE stimulated
fine root production more than the other components of NPP,
except for P. alba, in the third year. Fine root production of
P. alba was not significantly affected by FACE in the third
year. However, in the second year, stimulation of the aboveground woody component accounted for 65 (P. alba),
33 (P. nigra) and 54% (P. × euramericana) of the total
FACE-induced increase in NPP. In the third year, these proportions increased to 67, 53, and 60% for P. alba, P. nigra and
P. × euramericana, respectively.
Under control conditions, the NPP:GPP ratio in the second
year was 0.60 (P. alba), 0.69 (P. nigra) and 0.64 (P. × eur-
americana), and in the third year, it was 0.58 (P. alba), 0.72
(P. nigra) and 0.71 (P. × euramericana). The FACE treatment
had a positive effect (14%) on NPP:GPP in the third year (P =
0.0125).
Litter and soil C fluxes
Excess litter production in relation to decomposition resulted
in litter accumulation. For P. nigra in the second year, the
amount of C lost from the litter pool through decomposition
was larger in the FACE treatment than in the control treatment
(P = 0.0012, P value of CO2 treatment × genotype = 0.055; Table 2). Carbon loss from litter greatly increased in the third
year, but did not differ between CO2 treatments or genotypes.
In the third year, more Cnew was accumulated in the mineral topsoil of FACE plots compared with control plots
(P = 0.0062; Table 2), whereas there was no effect from FACE
in the second year. Except for the third year of FACE treatment
in P. nigra and P. × euramericana, the amount of mineral soil
C increased each year (Table 2). FACE did not significantly affect changes in soil C or amounts of old soil C lost by respiration (Table 2). Although treatment means suggest much larger
Table 2. Components of net primary productivity (NPP) and net yearly carbon (C) fluxes in high density stands of three Populus genotypes in control and FACE treatments. Means (SE) of three plots for the second and the third years are presented in g C m – 2 year – 1. The P values of the CO2
treatment effect are indicated. Abbreviations: NEP = net ecosystem productivity (= increment of wood (stem, branches, stump) + increment of
coarse roots + ∆ soil C); litter C loss = C lost from the litter layer C pool due to decomposition of leaf litter; new soil C = new C input into soil C
pool, from dead leaves, dead roots and mycorrhizal C; soil C loss = C loss from the soil C pool by respiration; and ∆ soil C = new soil C – soil C
loss.
CO2
P value
P. alba
P. × euramericana
P. nigra
Control
FACE
Control
FACE
Control
FACE
Second year
Above woody
Litter production
Woody stump
Coarse roots
Fine roots
Above/below NPP
NPP
Litter C loss
New soil C
Soil C loss
∆ Soil C
NEP
0.0296
0.8283
0.0130
0.0086
0.0001
0.0020
0.0046
0.0006
0.4949
0.2259
0.3211
0.5103
755 (52)
208 (7)
81 (6)
45 (13)
43 (3)
5.8 (0.6)
1132 (57)
3.15 (0.54)
469 (14)
352 (84)
117 (77)
998 (74)
891 (102)
216 (26)
95 (11)
47 (8)
92 (9)
4.7 (0.1)
1341 (151)
4.95 (1.19)
594 (64)
495 (153)
99 (89)
1133 (168)
1035 (41)
224 (10)
81 (3)
46 (7)
52 (8)
7.1 (0.7)
1437 (31)
5.47 (0.13)
572(73)
396 (229)
177 (157)
1338 (144)
1076 (62)
224 (8)
84 (5)
65 (20)
113 (25)
5.2 (0.9)
1562 (79)
10.61 (0.94)
603 (44)
601 (99)
3 (99)
1228 (69)
694 (29)
238 (9)
99 (4)
56 (23)
44 (7)
4.7 (0.5)
1130 (35)
3.20 (0.18)
666 (106)
408 (65)
258 (171)
1098 (135)
911 (51)
238 (19)
130 (7)
147 (16)
104 (10)
3.0 (0.1)
1530 (100)
4.85 (0.33)
628 (132)
505 (32)
122 (116)
1311 (189)
Third year
Above woody
Litter production
Woody stump
Coarse roots
Fine roots
Above/below NPP
NPP
Litter C loss
New soil C
Soil C loss
∆ Soil C
NEP
0.0120
0.2493
0.0001
0.0509
0.0001
0.0003
0.0008
0.4681
0.0062
0.0741
0.4546
0.1733
1102 (11)
234 (12)
40 (3)
22 (12)
96 (5)
8.6 (0.8)
1493 (4)
36.40 (1.15)
294 (67)
113 (153)
180 (95)
1344 (92)
1462 (228)
250 (14)
122 (20)
80 (24)
116 (9)
5.4 (0.8)
2029 (232)
37.30 (4.49)
525 (101)
365 (263)
160 (211)
1824 (113)
1438 (43)
300 (24)
43 (3)
110 (14)
92 (4)
7.2 (0.5)
1983 (13)
35.88 (1.51)
319 (122)
234 (303)
85 (184)
1676 (211)
1665 (41)
323 (25)
85 (3)
156 (31)
184 (24)
4.7 (0.1)
2413 (72)
37.01 (1.31)
617 (62)
690 (250)
–74 (188)
1833 (247)
1040 (69)
283 (5)
28 (7)
46 (14)
136 (9)
6.4 (0.6)
1532 (71)
44.05 (1.73)
412 (217)
471 (304)
–59 (164)
1055 (220)
1234 (67)
292 (3)
58 (8)
35 (6)
234 (22)
4.7 (0.3)
1853 (95)
37.44 (3.05)
605 (104)
819 (303)
–214 (220)
1113 (290)
TREE PHYSIOLOGY VOLUME 25, 2005
CARBON BUDGET OF PLANTATION EXPOSED TO FACE
soil C losses in the FACE plots compared with the control
plots, plot variation was too large to detect significant differences. New C input into the soil C pool, from dead leaves, dead
roots and mycorrhizal C (New soil C), C loss from the soil C
pool by respiration (soil C loss), and new soil C minus soil C
loss (∆ soil C) did not differ among genotypes (Table 2).
Net ecosystem productivity
Partly because of considerable plot variation, there was no significant effect of FACE on NEP. In the second year, the mean
stimulation of NEP by FACE for P. alba and P. × euramericana was very small, and was nonexistent for P. nigra (Table 2). The effect of FACE on NEP was slightly larger in the
third year, but not significant (Table 2). The effect of genotype
on NEP was not significant.
Discussion
Averaged across genotypes, the irrigated high density plantation of poplar in a Mediterranean climate reached NPP values
of 1233 and 1669 g C m – 2 in the second and third years, respectively. Wood production at our site was within the range
reported for other poplar plantations (Calfapietra et al. 2003),
and NPP was similar to that of a sweetgum stand (Norby et al.
2002).
As a result of the sustained increase in leaf-level photosynthesis in response to FACE (Bernacchi et al. 2003a), GPP was
22 and 11% higher in the FACE plots than in the control plots
in the second and third years, respectively (Wittig et al. 2005).
As discussed by Wittig et al. (2005), the decline in the FACEinduced stimulation of GPP with time was a function of canopy closure without systematic down-regulation of photosynthetic capacity. In the context of net forest plantation C storage
capacity, the partitioning of this extra C among pools of different turnover rates is of critical interest. Mean stimulation of
NPP by FACE for the three poplar genotypes was comparable
with the 21% stimulation of NPP in a sweetgum stand (Norby
et al. 2002) and with the 27% increase in NPP in a Pinus taeda
forest (Hamilton et al. 2002). In the first year, the FACE-induced increase in NPP in the sweetgum stand was attributed to
an increase in the size of slow turnover (wood) C pools, but in
the third year, it was attributed to an increase in the size of fast
turnover C pools (leaves and fine roots) (Norby et al. 2002). At
our site, in both the second and third years, more than 50% of
the FACE-induced increase in NPP resulted from increased
stem and branch increments. The contribution of fine root
stimulation to the total FACE-induced increase in NPP was
greater than the contribution of stems and branches only in
P. nigra in the second year. Increased fine root production accounted for 4 to 30% of the FACE-induced increase in NPP in
the other genotypes. Increased leaf litter accumulation accounted for less than 5% of the FACE-induced increase in
NPP.
At the POPFACE site, litter was accumulating on the forest
floor, as shown by Cotrufo et al. (2005). Leaf litter decay rates
at the site, examined over an 8-month period, were low but not
1405
unusually so for the Mediterranean region (Moro and Domingo 2000, Cotrufo et al. 2005). However, afforestation of
agricultural soil at the POPFACE site may have affected the
capacity of the soil biological community to degrade a “new”
substrate such as poplar litter, slowing down decomposition
and resulting in fast litter accumulation, forming a distinct litter layer on top of the soil (Hoosbeek et al. 2004, Cotrufo et al.
2005). The microbial biomass accounted for 1.7% of the total
soil C pool, which is low compared with the value of about 3%
reported in similar studies (Rice et al. 1994, Hungate et al.
1997). This discrepancy may be associated with strong competition from poplar trees for nutrients, especially nitrogen,
and the conversion of the site from agricultural use. Cotrufo et
al. (2005) found slightly higher litter decay rates in the FACE
plots, possibly because of increased rhizodeposition and soil
biological activity (Hoosbeek et al. 2004). However, in elevated [CO2], an increased amount of undecomposed litter is
predicted to remain on the forest floor because it contains
lower initial N concentrations (Cotrufo et al. 2005). It is presumed that this remaining litter slowly enters the SOM, and
possibly promotes C storage; however, this process has not
been verified in any FACE study. Although more litter accumulates in response to elevated [CO2], no significant increase
in long- lived SOM has been reported (Schlesinger and Lichter
2001). During our 3-year study, leaf litter contributed only a
small amount to new soil C. Cumulative input of C from leaf
litter, averaged across genotype and treatment, was 505 g C
m – 2. The mean input through leaf litter was larger than the
mean input through fine root turnover by a factor of more than
two. This ratio is similar to that calculated for Norway spruce
(Picea abies L.) stands (Godbold et al. 2003) and many other
forest ecosystems (Vogt et al. 1986). However, the largest new
soil C contributor over the full 3-year fumigation period was
mycorrhizal hyphae (Godbold et al., unpublished results).
Despite the positive effect of FACE on the accumulation of
Cnew into the soil in the third year, the increase in the total soil
C pool was smaller in the FACE plots than in the control plots.
Hoosbeek et al. (2004) suggested that these opposing effects
were caused by a priming effect of the newly incorporated root
litter. The priming effect was defined as the stimulation of
SOM decomposition caused by the addition of labile substrates (Dalenberg and Jager 1989, Cheng 1999). Through extrapolations from other experiments (e.g., Fox and Comerford
1990, DeLucia et al. 1997, Jones et al. 1998), Hoosbeek et al.
(2004) suggested that FACE induced an increase in the fraction of low molecular weight C components in the soil. In contrast to, for example, the Duke FACE site, the extra and more
easily degradable C may increase the growth of the microbial
populations in the fertile soil of the POPFACE site (Jenkinson
and Rayner 1977, Van Veen et al. 1984, Dalenberg and Jager
1989). The soil microbial biomass did not increase in response
to the FACE treatment, and much uncertainty exists about microbial biomass responses to elevated [CO2] (Larson et al.
2002, Pendall et al. 2004). The microbial quotient, however,
was significantly increased by the FACE treatment, which
means that more C was available for microbial growth (Ander-
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1406
GIELEN ET AL.
son 2003). Soil respiration rates may have been increased in
response to FACE because of the priming effect (Hoosbeek et
al. 2004). Large increases in soil CO2 effluxes were observed
in the FACE treatment, in both the second and third years
(King et al. 2004). Many factors appeared to contribute to
FACE stimulation of soil respiration. FACE increased both
root biomass (Lukac et al. 2003) and specific root respiration
(I.A. Janssens, unpublished results), as well as C input to the
soil (Hoosbeek et al. 2004). We estimated tree respiration by
subtracting NPP from GPP and obtained values from 638 to
743 g C m – 2 year – 1 (control) and 675 to 956 g C m – 2 year – 1
(FACE) in the second year, and from 618 to 1091 g C m – 2
year – 1 (control) and 508 to 800 g C m – 2 year – 1 (FACE) for the
three genotypes in the third year. This corresponds to a relative
FACE stimulation of 28% (SE = 10%, P = 0.0047) in the second year, and a nonsignificant mean reduction of 16% (SE =
11%, P = 0.0665) in the third year.
The positive effect of FACE on GPP decreased from the second to the third year, whereas the effect on NPP was similar in
both years, resulting in higher NPP:GPP ratios in the FACE
treatment. At our site, NEP was not significantly enhanced by
FACE. In contrast, FACE stimulated NEP of a pine forest by
41% (Hamilton et al. 2002). However, NEP calculated for the
pine forest also includes litter accumulation and fine root increments; only a fraction of this labile C is incorporated in the
soil (Hamilton et al. 2002). At the POPFACE site, FACE stimulated respiration of soil C more than the incorporation of new
C. Our estimate of NEP is derived from pool size estimates at
the end of each year. Although there are errors involved in the
upscaling of biomass determinations, this method is superior
to extrapolation of specific respiration rates (Hamilton et al.
2002). Although soil CO2 efflux was increased by FACE at our
site and our results suggest increased soil C losses in response
to FACE, a remaining challenge is to carefully quantify and
understand the effect of elevated [CO2] on soil C losses. Our
study plantation site was converted from agricultural use,
which may have influenced soil processes, cancelling out the
FACE stimulation of NPP. Although 3 years of research in a
fast-growing tree plantation captured the aboveground responses for a closed canopy, belowground processes may need
longer to stabilize. Therefore, further research should shed
light on the longer term C storage capacity, especially that
belowground. The lack of real NEP stimulation at our site is
critical in assessing the impact of new plantations established
to meet Kyoto Protocol climate change commitments. We
have shown that there is no evidence that the C storage capacity of these plantations will improve in a CO2-enriched atmosphere.
In conclusion, the stimulating effect of FACE on NPP was
mainly attributed to an increase in size of relatively slow turnover C pools (wood). In contrast, NEP was not significantly increased by FACE, largely because of increased soil C respiration, which Hoosbeek et al. (2004) attributed to the priming
effect of newly incorporated root litter.
Acknowledgments
This research was supported by the European Community through the
Fifth Framework Programme, research contract ENV4-CT97-0657
(POPFACE), as well as by the Centre of Excellence “Forest and Climate” (MIUR Italian Ministry of University and Research) and
MIUR-COFIN 2000 (coordinator Marco Borghetti). We acknowledge the following persons for help in the field and with data collection: M. Anniciello, B. Assissi, G. Avino, B. Bartoli, A. Claus,
I. Laureysens, H. Larbi, T. Oro, M. Tamantini, D. Van Dam and
K. Brinkmann. We thank S. Van Dongen for statistical advice.
B. Gielen is a post-doctoral research fellow of the Fund for Scientific
Research-Flanders (F.W.O.-Vlaanderen).
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