Abstract

Forest soils account for a large part of the stable carbon pool held in terrestrial ecosystems. Future levels of atmospheric CO2 are likely to increase C input into the soils through increased above- and below-ground production of forests. This increased input will result in greater sequestration of C only if the additional C enters stable pools. In this review, we compare current observations from four large-scale Free Air FACE Enrichment (FACE) experiments on forest ecosystems (EuroFACE, Aspen-FACE, Duke FACE and ORNL-FACE) and consider their predictive power for long-term C sequestration. At all sites, FACE increased fine root biomass, and in most cases higher fine root turnover resulted in higher C input into soil via root necromass. However, at all sites, soil CO2 efflux also increased in excess of the increased root necromass inputs. A mass balance calculation suggests that a large part of the stimulation of soil CO2 efflux may be due to increased root respiration. Given the duration of these experiments compared with the life cycle of a forest and the complexity of processes involved, it is not yet possible to predict whether elevated CO2 will result in increased C storage in forest soil.

Introduction

Increasing concentrations of atmospheric carbon dioxide could have significant implications for long-term storage of carbon in forest soils. Since forests account for more than 75 per cent of carbon stored in terrestrial ecosystems (Schlesinger, 1997) and most of this carbon is stored below ground (Dixon et al., 1994), the effect of future levels of atmospheric CO2 on soil C pools is of global significance. Initial experiments using greenhouses and closed- and open-top chambers have indicated that elevated CO2 increases tree productivity (Ceulemans and Mousseau, 1994; Curtis and XianZhong, 1998; Ceulemans et al., 1999). However, it is not possible to extend the response of single plants to that of a forest ecosystem. In fact, a wide range of physiological and environmental factors mediate the response of such ecosystems to elevated CO2 and its capacity to sequester carbon, especially in the long term. To this end, a series of large-scale Free Air Carbon Dioxide Enrichment (FACE) experiments on tree dominated ecosystems has been initiated worldwide. These FACE systems use a number of different tree species such as poplar (Populus alba L., Populus nigra L. and Populus x euramericana Dode Gunier) in EuroFACE, aspen (Populus tremuloides Michx.), maple (Acer saccharum Marsh.) and birch (Betula papyrifera Marsh.) in Aspen FACE, loblolly pine (Pinus taeda L.) in Duke FACE and finally sweetgum (Liquidambar styraciflua L.) in ORNL FACE.

A common response to elevated CO2 is increased allocation of assimilated C below ground (Rogers et al., 1994). This phenomenon can result in increased below-ground C inputs by a shift in C allocation between foliage and roots (Finzi et al., 2001), increased production and turnover of fine roots (Zak et al., 2000), by greater proliferation of mycorrhizal symbionts (Staddon and Fitter, 1998) or by increased root exudation (Fitter et al., 1997; Thomas et al., 1999). All these processes have been observed in FACE experiments with the exception of an increase in root exudation, which is notoriously difficult to measure in field conditions. Assessment of the relative contribution of these processes to the soil C pool is ridden with technical and methodological difficulties. However, it seems that the turnover of ephemeral tissues constitutes the greatest source of C entering the soil C pool (Vogt et al., 1986; Kubiske et al., 1998). In a spruce forest, biomass inputs to soils via root necromass were 32 per cent of total biomass (above and below ground) inputs (Godbold et al., 2003) and overall about one-third of a forest ecosystem Net Primary Production(NPP) is assigned to roots (Jackson et al., 1997). The fate of this C entering the soil is, however, less clear (Canadell et al., 1996). In new plantation of eucalyptus established on former sugar cane fields, Binkley et al. (2004) showed that the new C entering the system from the C3 eucalyptus was balanced by loss of the older C4 soil carbon originating from sugar cane and already present in the soil at the time of eucalyptus introduction. Similarly, (Schlesinger and Lichter, 2001) report that increased C accumulation in the litter layer under elevated CO2 did not translate into an increase in soil C content. Other published studies indicate that varying responses of soil C pools and fluxes to elevated CO2 are likely to be dependent on soil characteristics and nutrient status (Zak et al., 2000). Six et al. (2002) suggested that organic matter in soils is protected from degradation by both physical protection, due to microaggregation and association with silt and clay particles, and by chemical protection. Chemical protection by strong molecular bonds is an inherent property of the plant input material or can be attained through chemical transformations during decomposition. Any potential effect of elevated CO2 on this chemical protection is unknown at present.

In this paper, we present our observations of root production and turnover and soil CO2 efflux from 3-year measurements in a fast growing poplar plantation under a FACE treatment (EuroFACE). We compare our results with those obtained at a similar FACE experiment with an early-stage forest ecosystem (Aspen FACE) and with observations from other two FACE experiments on established forest stands (Duke FACE and ORNL FACE). We assess the feasibility and reliability of predictions of long-term C storage in temperate forest soils based on currently available datasets.

Methods

EuroFACE

The EuroFACE experimental facility was established in 1999, in central Italy (42° 22′ N 11° 48′ E) on a former agricultural field. The soils are Pachic Xerumbrepts (Hoosbeek et al., 2004). Populus. x euramericana was planted during the spring of 1999 over 9 ha of former agricultural field at 2 × 1 m spacing. Within this plantation, six experimental plots were established: three control plots were left under natural conditions, while in the remaining three plots elevated CO2 treatment (550 p.p.m.) was provided by the FACE technique. The site and soil characteristics are detailed in Table 1, while an in-depth description of the FACE installation and the performance of the system is given by Miglietta et al. (2001).

Table 1:

Site description and soil characteristics of forest FACE experiments

Experiment Species Year planted Year FACE started Soil type Soil texture Total soil C (g kg−1Total soil N (g kg−1
Aspen FACE Populus tremuloides 1997 1997 Alfic Haplorthod Sandy loam 16.1 1.2 
P. tremuloides and Betula papyrifera 
Duke FACE Pinus taeda 1983 1996 Ultic Hapludalf Clay loam 13.2 0.8 
ORNL FACE Liquidambar styraciflua 1988 1998 Aquic Hapludult Silty clay loam 7.4 1.1 
EuroFACE Populus alba 1999 1999 Pachic Xerumbrept Loam and silt loam 11.9 1.1 
Populus nigra 
Populus x euramericana 
Experiment Species Year planted Year FACE started Soil type Soil texture Total soil C (g kg−1Total soil N (g kg−1
Aspen FACE Populus tremuloides 1997 1997 Alfic Haplorthod Sandy loam 16.1 1.2 
P. tremuloides and Betula papyrifera 
Duke FACE Pinus taeda 1983 1996 Ultic Hapludalf Clay loam 13.2 0.8 
ORNL FACE Liquidambar styraciflua 1988 1998 Aquic Hapludult Silty clay loam 7.4 1.1 
EuroFACE Populus alba 1999 1999 Pachic Xerumbrept Loam and silt loam 11.9 1.1 
Populus nigra 
Populus x euramericana 

Each of the plots is 22 m in diameter, containing ∼350 plants spaced at 1 × 1 m. Each plot was further divided into six sections, and two each planted out with trees of a single species of P. alba, P. nigra or P. x euramericana. Further information on the genotypes is given in Calfapietra et al. (2001). Trees are drip irrigated throughout the growing season to avoid drought stress. There was no fertilizer application during the first rotation from 1999 to 2001 as the soil did provide sufficient nutrients for these fast-growing trees. Methods used for measuring fine root biomass, soil respiration and microbial biomass and respiration are briefly outlined in Table 2.

Table 2:

Methods applied to measure fine root biomass, soil CO2 efflux and microbial biomass and respiration

Experiment Fine root biomass (roots <2 mm thick) Soil CO2 efflux Microbial biomass and respiration 
Aspen FACE Coring on one occasion in August 1999, 5.5 cm corer, 10 cm core depth Bi-weekly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, calibrated on-site daily, 10 measurements One sampling in September 2000, respiration measurement started 1 h after addition 
Duke FACE Bi-monthly between November 1997 and November 1999, 5 cm corer, 20 cm core depth Monthly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, 12 measurements Not available 
ORNL FACE Coring in July 2002 and October 2003, 10 cm corer, 15 cm core depth Bi-weekly, Li-Cor 6200 closed-mode IRGA, cuvette placed directly on soil, 6 measurements Samples collected in May, July and September in 1999 and 2000, microbial activity determined colourimetrically by BIOLOG GN and ECO plates 
EuroFACE Sequential coring three (1999) or five (2000 and 2001) times per season, 8 cm corer, 40 cm core depth Bi-weekly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, 5 measurements Five samplings (October 2000 to October 2001), chloroform fumigation–extraction method 
Experiment Fine root biomass (roots <2 mm thick) Soil CO2 efflux Microbial biomass and respiration 
Aspen FACE Coring on one occasion in August 1999, 5.5 cm corer, 10 cm core depth Bi-weekly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, calibrated on-site daily, 10 measurements One sampling in September 2000, respiration measurement started 1 h after addition 
Duke FACE Bi-monthly between November 1997 and November 1999, 5 cm corer, 20 cm core depth Monthly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, 12 measurements Not available 
ORNL FACE Coring in July 2002 and October 2003, 10 cm corer, 15 cm core depth Bi-weekly, Li-Cor 6200 closed-mode IRGA, cuvette placed directly on soil, 6 measurements Samples collected in May, July and September in 1999 and 2000, microbial activity determined colourimetrically by BIOLOG GN and ECO plates 
EuroFACE Sequential coring three (1999) or five (2000 and 2001) times per season, 8 cm corer, 40 cm core depth Bi-weekly, PP Systems EGM-2 closed-mode IRGA, cuvette placed on fixed PVC collars, 5 measurements Five samplings (October 2000 to October 2001), chloroform fumigation–extraction method 

Aspen FACE

The Aspen FACE research project is located at the USDA Forest Service, North Central Research Station, near Rhinelander, Wisconsin (45° 40′ N 89° 37′ E). The 32-ha facility is a randomized complete block design, with three replicates (blocks) of four treatments: control, elevated CO2, elevated O3 and elevated CO2 plus elevated O3 (Karnosky et al., 1999; Dickson et al., 2000). The ozone treatment is not relevant for the purposes of this paper and is not further described. The experiment was established in 1997 when three community types were planted within the experimental plots: five separately planted clones of aspen, pairs of a single aspen clone and sugar maple and finally pairs of mixed-stock birch and a single aspen clone. The soils are classified as mixed, frigid, coarse loamy Alfic Haplorthods (King et al., 2001). Design and performance of the experimental system is published in Dickson et al. (2000).

Duke FACE

The Duke Forest FACE experiment is located near Chapel Hill, North Carolina (35° 58′ N 79° 05′ W). The forest was established in 1983 and is dominated by P. taeda with L. styraciflua and Liriodendron tulipifera as subdominants (DeLucia et al., 1999). The soil has been classified as a clay-rich Alfisol with low nitrogen and phosphorus availability (Schlesinger and Lichter, 2001).

Three circular FACE experimental plots were established alongside three control plots and fumigation started in 1996. The plots are 30 m in diameter with the CO2 concentration in FACE plots maintained at ambient +200 p.p.m. (Hendrey et al., 1999).

ORNL FACE

The site of this experiment is a sweetgum (L. styraciflua) plantation near Oak Ridge, Tennessee (35° 54′ N 84° 20′ W), established in 1988 on a floodplain terrace. The soil is an alluvial aquic hapludult with an organic carbon content of ∼1 per cent and a silty clay loam texture (Miegroet et al., 1994). The experiment consists of five 25-m diameter rings, three of which receive ambient air (controls) and two (FACE) receive ambient air amended with CO2 to create a target concentration of 565 p.p.m. Fumigation began in April 1998, the details of design and operation of the FACE apparatus for forest systems is described in Hendrey et al. (1999) and Norby et al. (2001).

Results and discussion

Since these four experiments are investigating the effects of elevated CO2 on forest ecosystems, valuable information can be attained by comparison of the observations and measurements of below-ground C allocation and cycling. In general, fine root biomass consisting of live roots <2 mm thick did increase under elevated CO2 in all the ecosystems studied (Table 3). Lukac et al. (2003) found that the total root biomass increased in the range of 54–82 per cent under elevated CO2 in EuroFACE. However, due to the longevity of coarse roots, coarse root biomass did not appear to play a major role in C input into the soil during the period of observation, but may contribute to total soil respiration. Live fine root biomass and necromass, on the other hand, is actively involved in exchange of compounds, water and gases with the surrounding soil. The fine root system represents a biomass pool with relatively fast turnover contributing to soil C cycling through root respiration, root exudation and the input of dead organic matter. Elevated CO2 increased live fine root biomass in all four ecosystems studied to differing degrees (Table 3). The largest increases in fine root biomass were found in tree species ecosystems still in their initial expanding state (Aspen FACE and EuroFACE). These two systems have also exposed the trees to elevated CO2 since the establishment of the stands. The other two FACE systems, ORNL and Duke, contain older trees and have used a step increase in CO2 since the original planting. The magnitude of the fine root biomass increase under FACE is probably also related to the successional status of particular tree. Early successional fast growing species, at least in the initial stages of stand development, seem to have greater response to CO2 enrichment than late successional and slower growing tree species.

Table 3:

Effect of FACE on standing fine root biomass

Experiment Species Control FACE Response to CO2 enrichment, % 
Aspen FACE* Populus tremuloides 260 555 +113 
 P. tremuloides and Betula papyrifera 173 317 +83 
Duke FACE† Pinus taeda 238 (31) 325 (26) +36 
ORNL FACE‡ Liquidambar styraciflua 113 (40) 195 (97) +73 
EuroFACE§ Populus alba 103 (14) 160 (44) +54 
 Populus nigra 111 (32) 202 (55) +81 
 Populus x euramericana 140 (34) 256 (34) +82 
Experiment Species Control FACE Response to CO2 enrichment, % 
Aspen FACE* Populus tremuloides 260 555 +113 
 P. tremuloides and Betula papyrifera 173 317 +83 
Duke FACE† Pinus taeda 238 (31) 325 (26) +36 
ORNL FACE‡ Liquidambar styraciflua 113 (40) 195 (97) +73 
EuroFACE§ Populus alba 103 (14) 160 (44) +54 
 Populus nigra 111 (32) 202 (55) +81 
 Populus x euramericana 140 (34) 256 (34) +82 

Data shown are dry root biomass in g m−2 (±SD).

Allen et al. (2000), fine root production.

Continuous growth and dieback of ephemeral fine roots constitutes significant soil C input as well as an important nutrient return source (Rasse, 2002). The size of C input from fine root turnover is strongly related fine root biomass (Berntson and Bazzaz, 1996). Thus, an increase in fine root biomass will eventually lead to an increase in C input from fine root necromass, even if the rate of turnover remains constant. Lukac et al. (2003) report a significant increase of fine root turnover under the FACE treatment (27–55 per cent) for some of the Populus species grown in plantation, while (Allen et al., 2000) observed a 25 per cent non-significant increase of root turnover in loblolly pine. At the Duke FACE site in loblolly pine, live fine root biomass increased under elevated CO2 soon after the initiation of fumigation (Matamala and Schlesinger, 2000), but no increase of fine root longevity was observed (Matamala et al., 2003). Although they did not estimate turnover, King et al. (2001) measured a 140 per cent increase of fine root necromass alongside an increase of live fine root biomass in Aspen FACE, indicating a greater amount of C being cycled through fine roots. Thus again, all sites show an increase in C input to the soil from fine root necromass. This may be either simply from the increase in fine root biomass which ultimately ends up as dead root tissue or due to a higher turnover of the fine root biomass.

In addition to C input from necromass, considerable C inputs are thought to occur from exudation of low molecular weight organic acids or root mucilage. In one of the few studies of this process in trees, rates of rhizodeposition increased under elevated atmospheric CO2 in pot-grown Betula pendula (Ineson et al., 1996). In Pinus ponderosa mycorrhizal with Pisolithus tinctorius (DeLucia et al., 1997) could show an increase in oxalate in the soil under elevated CO2. It has, however, not been conclusively established how elevated CO2 affects root exudation, with some studies reporting no effect (Norby et al., 1987; Uselman et al., 2000) and others showing an increase in exudation (Rouhier et al., 1994; Jones, 1998). Sinsabaugh et al. (2003) investigated fine root density, microbial biomass nitrogen and substrate utilization by soil bacteria in ORNL FACE in order to confirm increased labile C input into the soil, but observed no changes due to elevated CO2. However, given the instability/volatility of organic compounds released by roots as exudates (Uselman et al., 2000), it is unlikely that any increase of root exudation will result in an increase of long-term C storage in the soil. In soils, the turnover of low molecular weight organic acids is rapid, and the measured soil solution concentration reflects the equilibrium concentration between production and removal processes, which includes microbial degradation and adsorption to mineral surfaces (van Hees et al., 2002). In order to separate the contribution of various processes to measured soil CO2 efflux, Luo et al. (2001) carried out a deconvolution analysis at Duke forest and concluded that elevated CO2 does not affect root exudation and that this kind of fast C transfer process is of minor importance in C cycling in this type of ecosystem. At the EuroFACE experimental site, Lagomarsino et al. (2006) reported a significant increase of water-soluble carbon and extractable C in FACE soils. Since these forms of C represent the most labile C fractions in the soil, it is possible that a substantial proportion of this pool originates from root exudates. An analogous increase in plant derived labile organic matter in the soil was observed in response to the CO2 enrichment in the Duke forest experiment (DeLucia et al., 1997; Schlesinger and Lichter, 2001). However, to complicate things further, an increase of C inputs from roots to soil has been shown to induce contrasting effects on soil C balance (Hamilton et al., 2002; Gielen et al., 2005) depending on its allocation and/or storage (Allen et al., 2000).

Soil microbial biomass is another labile pool of soil carbon characterized by a very rapid turnover. At EuroFACE, Gielen et al. (2005) reported a significant increase of the microbial quotient (microbial C as a fraction of total organic C) in FACE soils compared to control. This suggests that some of the extra carbon made available under elevated CO2 was used to build up more microbial biomass. Heath et al. (2005) have shown that even though elevated CO2 increases soil C input, at the same time it stimulates microbial respiration, thus potentially negating any sequestration of root-derived C in the soil. In addition, elevated CO2 has been shown to alter the composition of microbial community resulting in a loss of soil C (Carney et al., 2007).

When assessing whether elevated CO2 increases soil C storage, alongside measuring inputs, equal importance must be given to the estimates of the amount of C leaving the soil. Forest soil respiration has been indicated as a main pathway for C leaving temperate forest ecosystems and therefore plays a major role in determining sequestration potential (Valentini et al., 2000). Soil CO2 emanating from the soil is a product of both autotrophic (plant roots) and heterotrophic (soil biota, fungi and microbial biomass) respiration. A likely effect of greater root systems found under elevated CO2 is an increase of autotrophic respiration (Janssens et al., 1998). Since soil CO2 efflux is controlled by a diffusion gradient, an increase in CO2 concentration in soil atmosphere resulting from increased respiration will cause increased soil CO2 efflux. The other pathway for C to leave soil – leaching of dissolved inorganic carbon (DOC) to ground water – appears to be only of minor significance in studied ecosystems. Andrews and Schlesinger (2001) report that in the Duke forest, this downward flux represents only ∼1 per cent of annual NPP. In contrast, soil CO2 efflux in the same ecosystem represents 56 per cent of Gross Primary Production. Similarly, King et al. (2001) have found in Aspen FACE that the leaching losses of C through DOC flux were not affected by FACE and amounted only to 0.9 g C m−2 per growing season compared with the soil respiration C flux of 760 g C m−2 in control and 1028 g C m−2 in FACE. Therefore, when considering the effect of elevated CO2 on soil C storage, it is important to take into account the response of C inputs and that of soil CO2 efflux. Table 4 lists the changes in soil CO2 efflux resulting from FACE treatment in forest experiments.

Table 4:

Effect of FACE on soil CO2 efflux

Experiment Period of measurement Species Control FACE Response to CO2 enrichment, % 
Aspen FACE* 1998–2001 Populus tremuloides 862 1053 +22 
Populus tremuloides and Betula papyrifera 762 1035 +38 
Duke FACE† 1997–2003 Pinus taeda 1504 1747 +16 
ORNL FACE* 1998–2001 Liquidambar styraciflua 844 947 +12 
EuroFACE* 2000–2001 Populus alba 730 986 +35 
Populus nigra 749 1093 +46 
Populus x euramericana 766 1079 +41 
Experiment Period of measurement Species Control FACE Response to CO2 enrichment, % 
Aspen FACE* 1998–2001 Populus tremuloides 862 1053 +22 
Populus tremuloides and Betula papyrifera 762 1035 +38 
Duke FACE† 1997–2003 Pinus taeda 1504 1747 +16 
ORNL FACE* 1998–2001 Liquidambar styraciflua 844 947 +12 
EuroFACE* 2000–2001 Populus alba 730 986 +35 
Populus nigra 749 1093 +46 
Populus x euramericana 766 1079 +41 

Data shown are in g m−2 year−1 (±SD).

At all sites, FACE conditions increased soil respiration. The increase was of a similar order at all sites, ranging from +12 to +16 per cent in the older forests from +22 to +46 per cent in the newly established forests. George et al. (2003) in their breakdown of sources of autotrophic respiration in Duke and ORNL experiments conclude that maintenance respiration accounts for the greatest part of CO2 lost from living roots. Hence, if the autotrophic element of soil respiration under elevated CO2 increases in line with increased C allocation below ground (Vose et al., 1995; Pregitzer et al., 2000), the response of microbial respiration to greater C inputs might tip the balance between soil C loss or sequestration. Given the commonly observed C limitation of decomposition (Zak and Pregitzer, 1998) and a simultaneous limitation of microbial activity in forest soils by the lack of labile C and N (Allen and Schlesinger, 2004; Vance and Chapin, 2001), additional C originating from decomposing root biomass is likely to have an effect on soil microbial communities (Zak et al., 1993). There are considerable difficulties with assessing the impact of elevated CO2 on soil microbes from step-increase CO2 enrichment experiments. Greater rates of microbial respiration under elevated CO2 generally indicate that increased litter inputs and/or root exudation are being metabolized by a soil microbial population that is larger, more active or both (Karnosky et al., 2003). Microbial communities are utilizing C stored in soil C pools and, especially in soil with high organic matter content, are probably not immediately reacting to increased C input (Zak et al., 2000). Larson et al. (2002) did not find any effect of elevated CO2 on microbial respiration in soil from Aspen FACE. Similarly, no change in the microbial activity in ORNL FACE Liquidambar plantation 3–4 years after the start of CO2 fumigation was found (Sinsabaugh et al., 2003). At the EuroFACE experiment, elevated CO2 stimulated microbial respiration in all species of Populus by a non-significant 5 per cent on average (Gielen et al., 2005b). Zak et al. (2000) have reported in their review that the degree to which microbial respiration was stimulated under elevated CO2 is highly variable and ranged from a 4 per cent decline to a 72 per cent increase beneath woody plants. This review is followed up by an analysis of observations from three forest FACE experiments which shows that elevated CO2 did not affect microbial N, mineralization or microbial immobilization and hence probably did not increase heterotrophic respiration which would result from increased microbial activity (Zak et al., 2003; Table 5).

Table 5:

Effect of elevated CO2 on soil microbial respiration

Plant species Experimental site and fumigation technique Response to CO2 enrichment 
Nutrient poor grassland SACC* +10% NS 
Tallgrass prairie OTC† +11.3% Sign 
Aspen–Maple Aspen FACE‡ +1% NS 
Aspen Aspen FACE‡ +33% Sign 
Aspen–Birch Aspen FACE‡ +55% Sign 
Populus spp EuroFACE§ +5% NS 
Populus grandidentata SC¶ – Rhizosphere soil +28% Sign 
P. grandidentata SC¶ – Bulk soil +15% NS 
Weedy field Ecotron NERC# +16% NS 
Alpine grassland OTC** +11% NS 
Plant species Experimental site and fumigation technique Response to CO2 enrichment 
Nutrient poor grassland SACC* +10% NS 
Tallgrass prairie OTC† +11.3% Sign 
Aspen–Maple Aspen FACE‡ +1% NS 
Aspen Aspen FACE‡ +33% Sign 
Aspen–Birch Aspen FACE‡ +55% Sign 
Populus spp EuroFACE§ +5% NS 
Populus grandidentata SC¶ – Rhizosphere soil +28% Sign 
P. grandidentata SC¶ – Bulk soil +15% NS 
Weedy field Ecotron NERC# +16% NS 
Alpine grassland OTC** +11% NS 

SACC = screen aided CO2 control; OTC = open-top chambers; SC = small open-top chambers; NS not significant; Sign = significance.

In an experiment on young Picea abies (L.) H.Karst. and Fagus sylvatica (L.) trees grown under elevated CO2, Spinnler et al. (2002) found that soil respiration rate was not increased in acidic soil. In contrast, elevated CO2 stimulated both fine root density and soil CO2 efflux on calcareous soil, suggesting that initial soil properties may play a greater role in determining the magnitude of soil C cycle than C input. Butnor et al. (2003) concluded from their unreplicated observations at Duke FACE prototype plots that the amount of C cycled through the soil of a temperate forest is greatly dependent on soil fertility. Similarly, George et al. (2003) observed different responses of soil CO2 efflux and root maintenance respiration to FACE treatment in Duke and ORNL experiments and suggest that the varied response might be due to different length of CO2 fumigation or to unequal nitrogen availability in the soil. Zak et al. (2003) in their synthesis of nitrogen cycling in three US-based FACE sites report that microbial biomass and specific rates of microbial respiration do not appear highly responsive to elevated CO2 and that any results obtained so far can not be used to characterize long-term interactions between CO2 and soil fertility.

At the EuroFACE site in all three poplar species in the third year of fumigation soil, CO2 efflux increased by ca. 250–300 g C m−2 a−1 (Table 4). This value is approximately five times the C inputs from fine root turnover (Lukac et al., 2003). For both the Duke and ORNL FACE sites, similar increases of between 250 and 300 g C m−2 a−1 were also found. Andrews et al. (1999) using 13C labelling at Duke FACE established that the upper limit of the root respiration contribution to soil CO2 efflux is ∼55 per cent in elevated CO2. This value for loblolly pine is considerably higher than those estimated by Matamala and Schlesinger (2000) using a different technique in the same forest. On the basis of their measurements, they have concluded that root respiration accounts for only 20 per cent of the increased soil CO2 efflux and suggested that the remainder may be due to a number of sources such as increased fine root turnover, increased above-ground litter inputs, increased root exudation and increased mycorrhizal colonization.

At the EuroFACE site, inputs from above-ground litterfall increased on average by only 20 g C m−2 a−1 in the growing season 2001 (M.F. Cotrufo, personal communication), considerably less than the increase in soil CO2 efflux. As an example, in a mass balance calculation for P. x euramericana in 2001 under FACE conditions compared with ambient, soil CO2 efflux increased by 268 g C m−2 a−1, above-ground litter by 9 g C m−2 a−1, standing fine root biomass by 46 g C m−2 a−1 and soil C input due to root turnover by 75 g C m−2 a−1. If it is assumed that the root respiration per unit of root biomass is the same under ambient and FACE conditions and if we take the maximal value of 55 per cent measured by Andrews et al. (1999) – bearing in mind this has been measured in different soil and under different tree species – as the proportion of root respiration in soil CO2 efflux, the following calculation can be made. In ambient CO2 conditions, the CO2 efflux in P. x euramericana is 724 g C m−2 a−1 and the fine root biomass 140 g m−2, then CO2 efflux per gram root is 2.84 g C a−1. In elevated CO2 conditions, the fine root biomass is increased by 116 g m−2, which would add 330 g C m−2 a−1 to the soil CO2 efflux. This value corresponds with measured increase of 338 g C m−2 a−1 under FACE for P. x euramericana. Calculations with similar results can be obtained for P. alba and P. nigra. These results suggest that a large part of the increase in soil CO2 efflux must be from live root respiration, the remainder is probably from root and hyphal exudation and/or mycorrhizal hyphal respiration. Our results are further supported by the findings of King et al. (2004), who found that the dominant tree species is a major factor controlling of the soil CO2 efflux and those of Taneva et al. (2006) who found that 71 per cent of CO2 soil efflux in FACE plots originated from a C pool <35 days old.

In addition, old C already present in the soil may also be lost due to the priming effect. This occurs when additional C entering the soil under FACE conditions induces faster breakdown of old soil C by stimulating microbial decomposition (Hoosbeek et al., 2004). We have observed the priming effect in EuroFACE during the initial 3 years after planting, but after this period a faster accumulation of soil C under FACE has been shown (Hoosbeek et al., 2006), suggesting that the priming effect might have run its course.

Conclusions

Elevated levels of atmospheric CO2 result in increased C allocation below ground. In all forest FACE experiments, increased below-ground C allocation has been accompanied by greater soil CO2 efflux making predictions of enhanced C sequestration in elevated CO2 difficult from the data currently available. Present FACE experiments would need to be run for much longer to account for the breakdown of C already present in the soil at the onset of fumigation and for coarse root decomposition to manifest itself. The results from the EuroFACE site suggest that much of the increase in below-ground C allocation is rapidly lost through autotrophic respiration. Whether increased input of C will result in increased soil C sequestration by temperate forests depends on the combination of various factors such as soil fertility, temperature and moisture, which influence the rate and magnitude of root and microbial respiration and ultimately the fate of extra C allocated to the soil.

Conflict of Interest Statement

None declared.

This research was conducted within the framework of the following programmes: EU-EuroFACE (ENV4-CT97-0657), Centre of Excellence ‘Forest and Climate’ (MIUR Italian Ministry of University and Research), MIUR-COFIN 2000 (coord. Marco Borghetti). The authors acknowledge G. Scarascia Mugnozza (University of Tuscia) for the coordination of the EuroFACE project, M. Sabatti and C. Calfapietra for running the experimental site. We also thank T. Oro, H. Larbi and M. Tamantini for technical assistance.

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