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Keywords:

  • C sequestration;
  • CO2;
  • free-air CO2 enrichment;
  • meta-analysis;
  • open top chamber;
  • plant root

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Aim

Plant root traits regulate belowground C inputs, soil nutrient and water uptake, and play critical roles in determining sustainable plant production and consequences for ecosystem C storage. However, the effects of elevated CO2 on root morphology and function have not been well quantified. We reveal general patterns of root trait responses to elevated CO2 from field manipulative experiments.

Location

North America, Europe, Oceania, Asia.

Methods

The meta-analysis approach was used to examine the effects of CO2 elevation on 17 variables associated with root morphology, biomass size and distribution, C and N concentrations and pools, turnover and fungal colonization from 110 published studies.

Results

Elevated CO2 increased root length (+26.0%) and diameter (+8.4%). Elevated CO2 also stimulated total root (+28.8%), fine root (+27.7%) and coarse root biomass (+25.3%), demonstrating strong responses of root morphology and biomass. Elevated CO2 increased the root:shoot ratio (+8.5%) and decreased the proportion of roots in the topsoil (–8.4%), suggesting that plants expand rooting systems. In addition, elevated CO2 decreased N concentration (–7.1%), but did not affect C concentration, and thus increased the C:N ratio (+7.8%). Root C (+29.3%) increased disproportionately relative to root N pools (+9.4%) under elevated CO2. Functional traits were also strongly affected by elevated CO2, which increased respiration (+58.9%), rhizodeposition (+37.9%) and fungal colonization (+3.3%).

Main conclusions

These results suggest that elevated CO2 promoted root morphological development, root system expansion and C input to soils, implying that the sensitive responses of root morphology and function to elevated CO2 would increase long-term belowground C sequestration.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Many studies suggest that increasing atmospheric CO2 will increase C sequestration in plant biomass, which could help to mitigate rising atmospheric CO2 concentration (Beedlow et al., 2004; Luo et al., 2006). Plant root systems play a crucial role in terrestrial C cycling because they not only take up soil nutrients and water for sustainable plant production (Luo et al., 2004) but also pump photosynthetically fixed C to soil organic matter (SOM) pools (Ainsworth & Long, 2005; Bonan, 2008). Elevated CO2 exerts a strong impact on plant root systems by influencing both morphology (e.g. root length and distribution) and function of C cycling (e.g. root respiration and rhizodeposition) (George et al., 2003; Iversen et al., 2008; Pritchard et al., 2008). However, experimental data show variability due to differences in species and the environments in which they grow (de Graaff et al., 2006; Luo et al., 2006). Uncertainties in projecting future terrestrial C cycling will be reduced by defining general patterns of the effects of atmospheric CO2 concentrations on root morphology and function.

Increasing research efforts using free-air CO2 enrichment (FACE) and open-top chamber (OTC) techniques around the world have been simulating the potential impacts of elevated CO2 on terrestrial plants, soil processes and ecosystems (Long et al., 2004; Norby & Zak, 2011). Studies of root traits provided early indications of the effects of elevated CO2 on root morphology and biomass (Milchunas et al., 2005; Pritchard et al., 2008) and the consequences for root turnover and C input to soils (George et al., 2003; Lukac et al., 2003). In many ways, root systems can sensitively respond to external CO2-induced stimulation. For example, root length and diameter continuously respond to elevated CO2 and dynamically explain the responses of biogeochemical cycles of ecosystems to elevated CO2 in long-term manipulation experiments (Norby et al., 2004; Iversen et al., 2008). In addition, root systems are integrators of elevated CO2 in that they store a mass of C and participate in SOM formation and turnover (Trumbore, 2000; Gielen et al., 2005). Globally, one-third of annual net primary production (NPP) is solely used for the growth of fine roots (Jackson et al., 1997). However, highly variable responses of plant root systems to experimental elevated CO2 have been observed in numerous individual studies. For example, root length has been observed to be related positively (Norby et al., 2004), negatively (Wan et al., 2004) or neutrally (Higgins et al., 2002) to elevated CO2. Similarly, the responses of root production and mortality to elevated CO2 are also highly uncertain (Norby & Jackson, 2000).

Several factors contribute to the highly variable responses of root systems to elevated CO2. First, experimental facilities, such as FACE and OTC, have different elevation efficiencies and growth constraints for plant root development. For example, a meta-analysis showed that FACE facilities had a larger stimulation in the root C pool of plants than OTC facilities (Luo et al., 2006). Second, experiments performed in various ecosystems inevitably involve different plant species, which vary in their responses to elevated CO2 (de Graaff et al., 2006; Luo et al., 2006). Third, response to long-term duration of elevated CO2 could differ markedly from short-term responses. For example, 5 years of elevated CO2 led to a gradual increase of root C:N ratios by 26% in a semi-arid grassland (Pendall et al., 2004a). It is therefore necessary to quantitatively analyse overall responses of plant root systems to elevated CO2.

Luo et al. (2006) extracted data from 104 papers that studied how elevated CO2 affects ecosystem C and N dynamics, and brought forward a concept that ecosystems may have intrinsic abilities to accumulate N in biomass. de Graaff et al. (2006) summarized the results of 117 papers on plant biomass, SOM dynamics and biological N2 fixation, suggesting that nutrient availability can strongly regulate the accumulation of plant biomass at elevated CO2. However, many uncertainties remain about the responses of plant root traits to elevated CO2. For example, to what extent will root turnover be altered by elevated CO2? Key uncertainties in model predictions of terrestrial C sequestration and soil nutrient and water uptake include root morphology (including root length and diameter) and biomass distribution (i.e. rooting depth) (Feddes et al., 2001; Bonan et al., 2002). In addition, more recent data from new manipulation experiments, such as the Prairie Heating and CO2 Enrichment (PHACE) experiment located in Wyoming, USA (Carrillo et al., 2011) allow us to more broadly quantify the responses of root traits to elevated CO2 than before.

This study synthesized 110 experimental studies from field-based experiments and provides a comprehensive analysis to quantify the general response patterns of 17 terrestrial plant root traits to elevated CO2. Root traits from different terrestrial ecosystems were grouped into four categories: morphology and biomass, C and N concentrations and pools, turnover and fungal colonization. This study provides a comprehensive analysis to identify the direction and magnitude of changes in root morphology and function under rising atmospheric CO2 concentration. The objectives of the analysis are to examine how and to what extent elevated CO2 affects plant root traits, and to elucidate the implications for potential feedbacks to elevated atmospheric CO2 and future functioning of terrestrial ecosystems.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Data collection

Data were collected by searching ISI Web of Knowledge from 110 peer-reviewed journal articles between 1990 and 2012 (Appendices S1 & S2 in Supporting Information). In total, 17 variables associated with plant root traits were examined from experiments in ambient and elevated CO2 treatments. Our analysis focused solely on outdoor facilities, FACE and OTC, because these field-based experiments allowed for long-term CO2 elevation with no root restrictions associated with pot culture. Ecosystem types included agriculture, desert, grassland and forest. Ambient CO2 concentrations ranged from 340 to 380 p.p.m. (one study at 400 p.p.m. did not yield an outlier), and those of elevated CO2 from 540 to 750 p.p.m. We did not find relationships between CO2 concentrations and response ratios, and thus data were not corrected for the degree of CO2 enrichment (data not shown). The following five criteria were applied to select appropriate studies: (1) the control and elevated CO2 plots were established to have the same ecosystem types, climatic conditions, dominant plant species, soil types and other conditions; (2) the experimental duration was clearly recorded and the measurements of treatment and control groups were performed at the same temporal and spatial scales; (3) the experimental durations were determined by the time from the start of experiments to data collection with any durations less than 1 year were considered as 1 year; (4) where a root variable was estimated at multiple time points, we chose reported value of the final measurement; (5) the means, standard deviations (SD) or standard errors (SE) and replicates (n) were directly extracted or could be calculated from the chosen data.

The compiled database included root morphology and biomass (i.e. root length, diameter, total root biomass, fine root biomass, coarse root biomass, root:shoot ratio and rooting depth distribution), root C and N concentrations and pools (i.e. root C and N concentrations, C:N ratio, and C and N pools), root turnover (i.e. root production, mortality, respiration and rhizodeposition) and fungal colonization. We selected these plant traits because they regulate belowground C inputs, soil nutrient and water uptake, and play critical roles in determining plant sustainable production and consequences for ecosystem C storage (Cotrufo & Gorissen, 1997; Norby et al., 1999; de Graaff et al., 2006; Luo et al., 2006; Brunner & Godbold, 2007; Bader et al., 2009; Iversen, 2010). Root length and diameter were quantified by a mini-rhizotron system or length measurement with a ruler. Biomass of total roots, fine roots (< 1 or 2 mm diameter) and coarse roots (> 2 mm diameter) were obtained from manually separated biomass or estimated from the mini-rhizotron system. Root distribution in the topsoil was determined by root biomass in the top 0–10 cm to 0–20 cm as a percentage of the total measured root profile. Root C and N concentrations, C:N ratio and pools were determined by plant biomass or combustion analysis for elemental concentration. Root production and mortality were quantified by production and decay rates of root biomass or length, respectively. Root respiration was determined by the in situ partitioning chamber and in vitro incubation method. Rhizodeposition, which is loss of C from roots to soil, was determined by a mass balance method or δ13C estimates. Fungal colonization was described by percentage root colonization.

Meta-analysis

The natural log-transformed response ratio (loge RR) of each plant trait at elevated CO2 (inline image) to that at ambient CO2 (inline image) was used to calculate the effect size of elevated CO2 treatments. More specifically, the mean, SD or SE (SD = SE√n), and n for each treatment were extracted to calculate the loge RR (equation (1)) (Hedges et al., 1999; Luo et al., 2006). To combine the results of multiple independent studies, the loge RR, variance (v) (equation (2)) and weighting factor (wij) (i = 1, 2, 3 … , m; j = 1, 2, 3 … , ki) (equation (3)) were used to calculate the weighted response ratio (RR++) (Eqn 4) and its 95% confidence interval (CI) (equations (5) & (6)) (Hedges et al., 1999; Luo et al., 2006). Here m is the group number (e.g. different experimental durations) and ki is the number of comparisons in the ith group:

  • display math(1)
  • display math(2)
  • display math(3)
  • display math(4)
  • display math(5)
  • display math(6)

If the 95% CI value of RR++ for a root trait overlapped with zero, elevated CO2 had no significant impact on the variable. Otherwise, they were statistically different (Luo et al., 2006). The percentage change of a variable was calculated by [exp(RR++) – 1] × 100%. To assess potential effects of experimental conditions on the response magnitudes of root traits to elevated CO2, observed data were grouped into the following categories: experimental facility, ecosystem type and duration of the entire experiment. RR++ for each group was calculated.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Root morphology and biomass

Considering the entire dataset, elevated CO2 significantly increased root length by an average of 26.0% (Fig. 1a). Elevated CO2 also significantly increased root diameter by an average of 8.4% (Fig. 1b). Within biome types, elevated CO2 decreased root length from desert (–20.8%; Fig. 1a), whereas root diameter in the agriculture ecosystem type showed insignificant responses to elevated CO2 (Fig. 1b). The small number of studies from desert and agricultural ecosystems limited the power of meta-analysis.

figure

Figure 1. The weighted response ratios for the responses to elevated CO2 of root length (a), root diameter (b), total root biomass (c), fine root biomass (d), and coarse root biomass (e). Bars represent the weighted response ratio ± 95% confidence interval. Values near each variable indicate the numbers of cases synthesized. FACE, free-air CO2 enrichment; OTC, open top chamber.

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Elevated CO2 significantly increased total root biomass (+28.8%; Fig. 1c), fine root biomass (+27.7%; Fig. 1d) and coarse root biomass (+25.3%; Fig. 1e) across all studies. Fine root biomass significantly increased in grassland by 16.3% and in forest by 33.4%, but was not significantly affected in agricultural systems.

Elevated CO2 had significant positive effects on root:shoot ratio of all ecosystems (+8.5%, Fig. 2a). This positive effect was significant for agriculture (+12.2%), grassland (+17.1%), and forest (+3.5%). Root:shoot ratio of the 6–10-year experimental duration showed a negative response to elevated CO2 (−10.2%; Fig. 2a).

figure

Figure 2. The weighted response ratios for the responses to elevated CO2 of root:shoot ratio (a) and the proportion of roots near the soil surface (b). Bars represent the weighted response ratio ± 95% confidence interval. Values near each variable indicate the numbers of cases synthesized. FACE, free-air CO2 enrichment; OTC, open top chamber.

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In addition, a significantly lower proportion of roots was distributed in topsoil (−8.4%; Fig. 2b) under elevated CO2 compared with ambient CO2, suggesting that elevated CO2 led to deeper rooting distribution. This observation held across ecosystem types except for agriculture (Fig. 2b).

Root C and N concentrations and pools

Root C concentration maintained a stable level because elevated CO2 did not significantly affect C concentration across facilities, ecosystems and experimental durations (Fig. 3a). However, elevated CO2 decreased root N concentration by an average of 7.1 % across studies (Fig. 3b). Although N concentration was significantly increased by 7.5% after 10-year elevated CO2 (Fig. 3b), the small number of cases from selected studies limited the power of this meta-analysis. In addition, C:N ratio significantly increased by 7.8% in response to elevated CO2 for all studies (Fig. 3c).

figure

Figure 3. The weighted response ratios for the responses to elevated CO2 of C concentration (a), N concentration (b), C:N ratio (c), C pool (d), and N pool (e). Bars represent the weighted response ratio ± 95% confidence interval. Values near each variable indicate the numbers of cases synthesized. FACE, free-air CO2 enrichment; OTC, open top chamber.

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Across all ecosystems elevated CO2 disproportionately increased the root C pool by 29.6% (Fig. 3d) compared with the root N pool by 9.4% (Fig. 3e). By contrast, the N pool significantly decreased (–12.0%) at elevated CO2 in the 6–10-year experimental duration in comparison with ambient CO2.

Root turnover

Elevated CO2 significantly enhanced average root production (+38.8%; Fig. 4a) and mortality (+56.7%; Fig. 4b). However, when data were subdivided into ecosystem types elevated CO2 had no significant effect on root production and mortality in the desert (Fig. 4a, b). Moreover, the decrease was significant only for OTC (−13.6%) when data were subgrouped into experimental facilities, for grassland (−19.2%) when data were subgrouped into ecosystem types, and for less than 5-year CO2 enrichment (−4.5%) when data were subgrouped into durations.

figure

Figure 4. The weighted response ratios for the responses to elevated CO2 of root production (a), root mortality (b), root respiration (c), and rhizodeposition (d). Bars represent the weighted response ratio ± 95% confidence interval. Values near each variable indicate the numbers of cases synthesized. FACE, free-air CO2 enrichment; OTC, open top chamber.

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Elevated CO2 stimulated root respiration by an average of 58.9% (Fig. 4c). However, opposite responses of FACE (–11.0%) and OTC (+117.7%), and agriculture (−19.8%) and forest (+115.1%) to elevated CO2 was found when data were subdivided into facilities and ecosystem types, respectively.

Overall, elevated CO2 had significant effects on rhizodeposition (+37.9%; Fig. 4d). Because only one study in grassland using OTC limited the power of this analysis, the significant response of forest (+26.1%) using FACE for elevated CO2 was probably more realistic.

Fungal colonization

Elevated CO2 increased fungal colonization by an average of 3.3% across all studies (Fig. 5). The effect was most pronounced for FACE (+30.6%) in comparison with OTC (+1.0%). When data were subgrouped into ecosystem types, the increases were significant for grassland (+1.5%) and forest (+5.3%).

figure

Figure 5. The weighted response ratios for the responses to elevated CO2 of fungal colonization. Bars represent the weighted response ratio ± 95% confidence interval. Values near each variable indicate the numbers of cases synthesized. FACE, free-air CO2 enrichment; OTC, open top chamber.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Despite the highly diverse results from individual experiments, the effects of CO2 on plant root traits can be detected because meta-analysis reduces the statistical power in studies with small sample sizes and increases the precision of the effect estimator. This meta-analysis demonstrates that root morphology, biomass accumulation and allocation, rooting depth and fungal colonization responded positively to changes in atmospheric CO2 concentration across a wide array of terrestrial ecosystems. In addition, our results also indicate that respiration and rhizodeposition significantly increased at elevated CO2 in comparison with ambient CO2. Such widespread regulation of ecosystem C and N cycling is consistent with conceptual and numerical models (Luo et al., 2004; Pendall et al., 2004b). Our meta-analysis indicates that elevated CO2 would increase soil C sequestration by promoting the morphological development of roots, expanding root systems and increasing C input to soils. This study enables us to better predict changes in future terrestrial C dynamics under rising atmospheric CO2 concentration.

Morphology and biomass response to elevated CO2

The positive responses of root length and diameter to elevated CO2 suggests that plant roots would change their metabolism and storage of nutrients (Berntson & Woodward, 1992; Crookshanks et al., 1998) and have a higher surface area for conducting and exchanging of resources across the plant–soil interface (Eissenstat, 1992; Stover et al., 2010). The overall CO2-induced stimulation of root length (+26.0%) was much stronger than that of root diameter (+8.4%) in this meta-analysis. In addition, elevated CO2 caused similar increases in root length and total root biomass (+26.0% vs. +28.8%), suggesting that root length growth plays a key role in root biomass accumulation.

The total increase in root biomass was close to the 28.3% augmentation in total root biomass due to elevated CO2 reported by de Graaff et al. (2006). Our meta-analysis suggests that fine root biomass was responsible for nearly all of the increase in biomass (Fig. 1d). Fine roots control ecosystem C and N cycling as plants obtain water and nutrients and release exudates mainly through fine roots (Brunner & Godbold, 2007; Bader et al., 2009). It should be noted that most data for fine root biomass from our database were extracted from studies performed in forest ecosystems. Norby et al. (1999) found that elevated CO2 increased fine root density (biomass per unit volume) from 60 to 140% in OTC experiments with sapling hardwoods. The stronger response of fine root biomass to elevated CO2 than that of this meta-analysis (+33.4%) may be explained by highly sensitive response of fine root biomass of young trees to elevated CO2 relative to old ones (de Graaff et al., 2006). In addition, this meta-analysis showed that fine root biomass of trees had a significantly stronger response to elevated CO2 in OTC experiments (+35.8%; 95% CI = 0.31 ± 0.03) than in FACE experiments (+30.5%; 95% CI = 0.27 ± 0.03).

One of the most crucial issues in forecasting future plant responses to rising atmospheric CO2 is how plants allocate belowground biomass and alter C distribution in ecosystems (Cotrufo & Gorissen, 1997; Iversen, 2010). Because of a significantly higher root:shoot ratio in elevated CO2 treatments (Fig. 2a), our results suggest that elevated CO2 has greater stimulatory effects on root biomass than aboveground biomass (de Graaff et al., 2006). The increased biomass allocation to roots and deeper rooting distribution would lead to enhanced potential for roots to store C and acquire nutrients from the soil to meet plant growth demand at elevated CO2 (de Graaff et al., 2006; Luo et al., 2006; Iversen, 2010).

Altered C and N pools and turnover at elevated CO2

Our results are consistent with previous meta-analyses which found that root productivity and the C pool increased with CO2 enrichment (de Graaff et al., 2006; Luo et al., 2006; Ainsworth, 2008). Our results also demonstrated that the root C pool of all ecosystems significantly increased under elevated CO2 (Fig. 3d), resulting in increased root respiration (Fig. 4c) and more new organic C input to soil through rhizodeposition (Fig. 4d). The N uptake efficiency under long-term elevated CO2 partly determines the roles of plant roots in terrestrial C cycling (Luo et al., 2004; Johnson, 2006). In our meta-analysis, elevated CO2 increased the root C pool by 29.6% but the root N pool by just 9.4%, consistent with the widening C:N ratio of roots with elevated CO2 in all facilities, ecosystems and experimental durations. The positive N accumulation of roots revealed in this meta-analysis would support ecosystem C sequestration in response to rising atmospheric CO2 concentration. Additional mechanisms that could alleviate N demands and support increased C pools identified here include increases in N uptake through increasing fine root biomass (Fig. 1d) (Brunner & Godbold, 2007; Bader et al., 2009), adjustments of chemical components through increasing C:N ratio (Fig. 3c) (Luo et al., 2004, 2006), optimizing root systems through increasing the root:shoot ratio and deeper rooting distribution (Fig. 2a, b) (de Graaff et al., 2006; Iversen, 2010), and through increasing fungal colonization (Fig. 5) (Gamper et al., 2004).

Root turnover is considered as one of the most important allocation pathways of C fluxes into the soil. Elevated CO2 significantly increased both root production and mortality in this meta-analysis. The increases in root mortality (+56.7%; Fig. 4b) were larger than the increases in production (+38.8%; Fig. 4a), but it would be unrealistic to compare their estimates because they were derived from data on root production and mortality obtained from non-uniform time periods. Root production is usually higher than mortality in the earlier growing season but lower than mortality in the later growing season (King et al., 2002; Wan et al., 2004). For example, Wan et al. (2004) obtained the mini-rhizotron data from the early growing season, while Pregitzer et al. (2000) mainly obtained data from the late growing season. Although seasonal differences from the selected works limit the precision of the results, this meta-analysis does clearly show that both root production and mortality significantly increased with elevated CO2.

Although measurements of root respiration from selected studies were mainly based on individual roots or root respiration per unit area of control and fumigated plots, these measurements can be scaled to an annual flux of the entire ecosystem using daily measurements of average soil temperature, soil moisture and root biomass (Jackson et al., 2009). An increase in C:N ratio may contribute to low root quality and decomposability at elevated CO2 (Curtis & Wang, 1998; Long et al., 2004). Several mechanisms also may underlie lower root decomposability, including increased root diameter (Wells & Eissenstat, 2001; Iversen et al., 2008), increased fungal colonization (Eissenstat et al., 2000) and deeper vertical root distribution in the soil. Root longevity increases with increasing soil depth (Milchunas et al., 2005). The growth dynamics and physiological state of plant roots partly determine the capacity for long-term belowground C storage (Trumbore, 2000; Beedlow et al., 2004; Pendall et al., 2004b). As a consequence, increase in root biomass and root:shoot ratio and a decrease in root decomposability under elevated CO2 contribute to an increased C pool in root biomass and a subsequent increased amount and stability of soil organic matter.

Effects of experimental method and ecosystem type on root trait responses to elevated CO2

In most cases, root trait responses to elevated CO2 were consistent across fumigation methods and ecosystems. However, we highlight some contrasts here. Elevated CO2 had significantly higher effects on total root biomass and root:shoot ratio in FACE experiments than in OTC experiments (Figs 1c & 2a). In addition, a higher level of stimulation of deeper rooting by elevated CO2 was observed in FACE experiments than OTC experiments (Fig. 2b). These results suggest that CO2-induced increase in belowground biomass and root expansion is stronger in plants grown in FACE experiments relative to OTC experiments. This discrepancy may be due to the possible constraints of root growth in OTC experiments (Norby & Zak, 2011). FACE plots can be set up as large as 30 m in diameter (Gielen et al., 2005; Jackson et al., 2009), but most of the OTC plots are only about 3 m in diameter (e.g. Crookshanks et al., 1998; Milchunas et al., 2005). Plot size may constrain plant growth. For example, tree saplings can be grown in unconstrained soil for several growing seasons in OTCs (Norby & Zak, 2011).

Elevated CO2 has significantly higher effects on root length and root:shoot ratio in grassland plants than forest trees (Figs 1a & 2a), and root C accumulation shows a stronger response to elevated CO2 in grasslands than in forests (Fig. 3d). That is possibly because root expansion of forest trees partly depends on the growth of buttress roots, which have relatively slow growth rates (Fitter, 1991). Across ecosystems, however, elevated CO2 produced a stronger stimulating effect on fine root biomass of forest ecosystems than grasslands, and had no effects on agricultural ecosystems (Fig. 1d). Fine roots play a critical role in absorbing and competing for nutrients (e.g. nitrogen), which in turn mediate the growth of fine roots. The high level of fertilizer application in agricultural ecosystems increases the efficiency of fine roots to take up nutrients, possibly resulting in no extra growth of fine roots of agricultural plants under elevated CO2. Previous studies suggest that forest trees had lower uptake efficiency of nutrients and more intense competition with soil microbes than grasses (Kaye & Hart, 1997; Cheng & Bledsoe, 2004). Therefore, a sensitive response of forest fine roots to elevated CO2 may increase uptake efficiency and increase competition with soil microbes in the responses to elevated CO2 (Nambiar & Sands, 1993; Dybzinski et al., 2011).

We found that root respiration decreased with elevated CO2 in FACE experiments but increased in OTC experiments (Fig. 4c). However, in our compiled database, all root respiration data for agricultural systems were obtained from the FACE experiments while most of the root respiration data of forests (9 of the 13 cases) came from OTC experiments. Because root respiration decreased in agricultural systems and increased in forests, the effects of elevated CO2 on root respiration compared with other root traits may be more dependent on the fumigation method and ecosystem type.

Implications for modelling terrestrial ecosystems

Limited knowledge of belowground processes, including root traits, constrains a predictive understanding of feedbacks between climate change and terrestrial ecosystems (Pendall et al., 2004b). Ecosystem models (e.g. Biome-BGC) representing terrestrial vegetation as biomes require root ecophysiological parameters such as root turnover rate and C:N ratio (White et al., 2000). Our data on shifts in these traits at elevated CO2 will improve development and parameterization of this type of model for predicting future climate. In models such as the Community Land Model (CLM), terrestrial vegetation is considered as patches of plant functional types (Bonan et al., 2002), in which root distribution depends on parameterization of the soil water potential at different soil depths (Zeng, 2001). Our work suggests elevated CO2 would accelerate deeper rooting, which should be considered as another important parameter in the CLM in a high-CO2 world. For other biogeochemical models, such as DAYCENT, data on fine and coarse root production which determine plant belowground allocation and root function dynamics are required for simulating transfers of C and N at the atmosphere–soil–vegetation interface (Del Grosso et al., 2001; Parton et al., 2007). Increased root biomass under elevated CO2 is important for the potential utility in modelling root contribution to CO2 fluxes at local to global scales under climatic change. Our synthetic analysis additionally provides uncertainty estimates of the responses of roots to elevated CO2, demonstrating the potential range of variability within and across ecosystems.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Elevated CO2 generates complex responses of ecosystem structure and function, but this study suggests coherence in many root trait responses. Results from this study and previous meta-analyses (de Graaff et al., 2006; Luo et al., 2006) have revealed that the simultaneously enhanced root C and N pools probably support long-term negative feedbacks of plants to rising atmospheric CO2 concentration. Our meta-analysis further revealed that both root morphology and function were substantially altered under elevated CO2. Root length, diameter, rooting depth and fungal colonization are expected to increase with rising atmospheric CO2 concentration. These responses could potentially increase absorption and transportation of soil nutrient and water for sustaining ecosystem productivity. Moreover, an enhanced C pool with lower root decomposability could potentially facilitate sequestration of atmospheric CO2 in root biomass. In addition, plant root systems supply more organic C to the soil through root litter and rhizodeposition at elevated CO2 (Trumbore, 2000; Lorenz & Lal, 2005). Incorporating these results into ecosystem models will improve predictions of ecosystem C sequestration under future scenarios of global change.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

We thank Xuhui Zhou for technical support with the data analysis. This research was supported by the US Department of Energy's Office of Science (BER), by the National Science Foundation (DEB no. 1021559), and by the China National Natural Science Foundation for Young Scholars (No. 31100352).

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
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Ming Nie, Meng Lu and Elise Pendall are interested in exploring the responses of ecosystem processes to climate change and ecological disturbance, and predicting mechanisms driving feedbacks between the terrestrial biosphere and the atmosphere.

Jennifer Bell and Swastika Raut are undergraduates and interested in characterizing root dynamics in response to climate change.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
FilenameFormatSizeDescription
geb12062-sup-0001-si.doc58K

Appendix S1 A list of 110 papers from which the data were extracted for this meta-analysis.

geb12062-sup-0002-si.xls53K

Appendix S2 Geographic, climatic and experimental information of papers from which the data were extracted for this meta-analysis.

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.