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Ecology
Fine-root production dominates response of a deciduous forest to atmospheric CO₂ enrichment

Richard J. Norby ^*, , Joanne Ledford ^*, Carolyn D. Reilly ^*, Nicole E. Miller ^*, , and Elizabeth G. O'Neill ^*

^*Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6422; and Department of Biology, Loyola University, Chicago, IL 60626

Communicated by William H. Schlesinger, Duke University, Durham, NC, May 17, 2004 (received for review April 1, 2004)

	Abstract

Top Abstract Methods Results and Discussion References

 
Fine-root production and turnover are important regulators of the biogeochemical cycles of ecosystems and key components of their response to global change. We present a nearly continuous 6-year record of fine-root production and mortality from minirhizotron analysis of a closed-canopy, deciduous sweetgum forest in a free-air CO₂ enrichment experiment. Annual production of fine roots was more than doubled in plots with 550 ppm CO₂ compared with plots in ambient air. This response was the primary component of the sustained 22% increase in net primary productivity. Annual fine-root mortality matched annual production, and the mean residence time of roots was not altered by elevated CO₂, but peak fine-root standing crop in midsummer was significantly higher in CO₂-enriched plots, especially deeper in the soil profile. The preferential allocation of additional carbon to fine roots, which have a fast turnover rate in this species, rather than to stemwood reduces the possibility of long-term enhancement by elevated CO₂ of carbon sequestration in biomass. However, sequestration of some of the fine-root carbon in soil pools is not precluded, and there may be other benefits to the tree from a seasonally larger and deeper fine-root system. Root-system dynamics can explain differences among ecosystems in their response to elevated atmospheric CO₂; hence, accurate assessments of carbon flux and storage in forests in a globally changing atmosphere must account for this unseen and difficult-to-measure component.

We used minirhizotron observation tubes and video imaging (9, 10) to quantify fine-root production and mortality in a FACE experiment in an established deciduous forest. Minirhizotrons permit observations of the production and disappearance of individual fine roots over frequent sampling intervals without the repeated disturbance effects associated with coring techniques. Although the problem of high spatial variability remains (and the labor-intensive nature of the analysis precludes optimal replication), spatial and temporal variation are not confounded. We assumed that the root system in this closed-canopy forest stand had fully occupied the soil volume and was no longer expanding, and an initial hypothesis for the FACE experiment was that full soil occupancy would constrain the N cycle (5). Here we present fine-root dynamics for six growing seasons and evaluate their role in the integrated response of the forest to CO₂ enrichment of the atmosphere.

	Methods

Top Abstract Methods Results and Discussion References

 
Experimental Site. The experimental site is a planted sweetgum (Liquidambar styraciflua L.) forest stand, which was established in 1988 at the Oak Ridge National Environmental Research Park in Roane County, TN (35°54'N, 84°20'W). One-year-old, bare-rooted sweetgum seedlings were planted at a spacing of 2.3 x 1.2 m. Herbicide was used in 1989 and 1990 to control competition from weeds; no fertilizer has been added. The soil at the site, which is classified as an Aquic Hapludult, developed in alluvium washed from upland soils derived from a variety of rocks including dolomite, sandstone, and shale, has a silty clay loam texture, and is moderately well drained. The soil is slightly acidic (water pH, 5.5–6.0) with high base saturation largely dominated by exchangeable Ca. The mean annual temperature (1962–1993) is 13.9°C, and the mean annual precipitation is 1,371 mm, with a generally even distribution of precipitation throughout the year (11).

Five 25-m-diameter plots were laid out in 1996, and FACE apparatus (8) was assembled in four of them; site disturbance was minimized during construction. When pretreatment measurements were made in 1997, the trees (90 per plot) were 12 m tall with an average diameter of 11 cm and a stand basal area of 28 cm²·m^-2 (11). The trees were in a linear growth phase, leaf area index was 5.5 m²·m^-2, and the canopy was no longer expanding (12). Exposure to elevated CO₂ commenced in two plots in April 1998 and has continued during the growing season (April to November) since then. The average daytime CO₂ concentrations during the 1998–2003 growing seasons were 528, 538, 546, 548, 552, and 549 ppm in the two CO₂-enriched plots, including periods when the exposure system was not functioning, and 384–398 ppm in ambient plots. The standard deviation of 1-min averages in the CO₂-enriched plots was 60 ppm. The site and experimental design has been fully described in ref. 11, and operating and meteorological conditions are documented at http://face.ornl.gov and http://cdiac.ornl.gov/programs/FACE/ornldata/ornldata.html.

Minirhizotron Analysis. Five minirhizotron tubes were installed in each FACE plot in July 1997. Cellulose acetate butyrate minirhizotron tubes (Bartz Technology, Santa Barbara, CA) were installed in each plot at a 60° angle from vertical and to a depth of 60 cm by using a hand auger (10). The tubes were stabilized with rebar and wrapped above the soil surface with black foam insulation, the upper ends sealed with a rubber stopper. Video images of the root systems were recorded beginning in February 1998 and continued biweekly during the growing seasons through November 2003. Video images were collected with a BTC-2 minirhizotron camera with a Smucker handle (Bartz Technology). Images were not collected during the winter because shrinkage of the tubes in cold soil precluded movement of the camera in the tubes. Each tube had 90 viewing windows (12.4 x 18.0 mm) for a total viewing area of 0.0201 m². From 1998 to 2002, individual frames on the videotape were captured by using a Targa+ video board (True Vision, Indianapolis) and digitized by using ROOTS software (Michigan State University, Lansing). In 2003, digital images were captured in the field by using the I-CAP system (Bartz Technology) and analyzed with ROOTRACKER software (Duke University, Durham, NC). The length and width of each root segment were measured, and the incremental growth, death, or disappearance was recorded. Root-length production, mortality, and standing crop were calculated as described in ref. 9. Roots were not included in mortality until they disappeared; although a few roots that were most likely dead were observed in the minirhizotron windows, they always disappeared quickly, and we equate "disappearance" with "mortality."

Cohort analysis was used to estimate fine-root longevity. We measured survivorship on an annual basis for all roots produced between the first filming of the year to June 1 of that year. Roots present at the first filming were excluded, as were all roots >1.0 mm in diameter. Survival data were analyzed (13) and tested for significance by using Peto and Peto's log-rank test (with 1° of freedom and = 0.05) for censored data, where not all individuals followed begin the treatment at the same time. Half-lives for the root cohorts were calculated from regressions of log-transformed data by year and CO₂ treatment.

Soil Cores. Five soil cores were extracted from each plot in July 2002 by using a 10-cm-diameter hole saw. The cores were 15 cm deep and collected in 5-cm increments. Roots were picked from the cores first by hand, and then the soil was washed through a 590-µm sieve. Roots were sorted into diameter classes (<0.5 mm, 0.5–1.0 mm, 1.0–2.0 mm, and >2.0 mm). A subsample of different diameter classes from each plot and depth was removed and kept cold and moist; the remaining roots were oven-dried and weighed. The subsampled roots were laid out individually on a minirhizotrom tube in the laboratory and filmed and digitized to determine length by using the same techniques as used in the field. These roots were then dried and weighed, and specific root lengths (SRLs) (length/mass) were determined. Additional soil cores (two per plot) were collected in October 2003 to compare a direct measurement of fine-root mass with the estimate from minirhizotron analysis.

	Results and Discussion

Top Abstract Methods Results and Discussion References

 
The seasonal pattern of fine-root production varied from year to year, and peaks of activity occurred throughout the growing season (Fig. 1A). Generally, root productivity was higher in March to June than in July to October. The large majority of root length (80%) observed in the minirhizotrons was in roots <0.5 mm in diameter, and <5% was in roots >1 mm in diameter. This pattern did not change with time or CO₂ treatment. CO₂ enrichment began to have an effect on root productivity during the third year, and the response was strongest in midsummer (June to August). The CO₂ effect on annual production (Fig. 2A) was highly significant, with production 2.2-fold higher in CO₂-enriched plots from 2000 to 2003. This large and significant effect of CO₂ on fine-root productivity would not have been seen if the measurements had been maintained for only the first 2 years of the experiment. Mortality was highly variable, with peaks occurring throughout the year (Fig. 1B), but generally mortality was highest in late summer and fall. Annually, mortality (Fig. 2B) matched production in both ambient and elevated CO₂.

View larger version (37K): [in this window] [in a new window]   Fig. 1. Seasonal dynamics of fine roots were determined by analysis of minirhizotron images collected biweekly during the growing seasons from February 1998 to November 2003. (A) Production during an observation interval was calculated as the length of new roots plus increases in length of existing roots. (B) Mortality is the disappearance of roots during an interval, with corrections made for roots that subsequently reappear. (C) Standing crop is the total length of root visible; changes in standing crop generally reflect production minus mortality. Data are expressed as the length of root per square meter of observation window. Pooled SEs for each year are shown.

View larger version (38K): [in this window] [in a new window]   Fig. 2. Fine roots comprised an increasing fraction of NPP in CO2-enriched trees. Annual budgets of production (A), mortality (B), and maximum standing crop (C) were expressed in grams of dry matter per square meter of ground. Increases in root mass between the last measurement in the fall and the first measurement in the spring of the next year were attributed to production in the spring, whereas decreases were attributed to mortality in the fall. Data are the means ± SE of three ambient or two elevated CO2 plots. Analysis of variance indicated the main effect of CO2 on production, mortality, and peak standing crop to be significant at P < 0.013, P < 0.068, and P < 0.010, respectively. Probability levels for the effect of year were P < 0.157 (production), P < 0.057 (mortality), and P < 0.028 (standing crop); CO2–years interaction was never significant (P > 0.20). (D) The contribution of fine-root production to total annual NPP (grams of C per square meter of ground area). NPP was calculated through allometric relationships, leaf litter trap collections, and the data in A, following methods described in ref. 20. Conversion of dry matter units to C units was based on measured C concentration values of 47.1% in wood (open), 46.3% in leaf litter (vertical hatching), and 39.6% in fine roots (diagonal hatching). The percentage increase in NPP is shown above the bars. The effects of CO2 on leaf litter C mass and NPP are statistically significant (P < 0.001 and P < 0.002, respectively), but, excluding 1998, there is no statistically significant difference in wood C mass production.

Elevated CO₂ can increase standing root crop by accelerating whole-plant development, as in a young, developing tree stand (15), through a specific change in plant allocation or indirectly through its effects on transpiration and soil moisture (16). Separation of these often confounded mechanisms can be difficult, but it is important for prediction of long-term responses in fully developed stands (5). Our initial assumption was that the sweetgum trees had fully occupied the site. This assumption was verified above ground in that peak leaf area index did not increase from 1998 to 2003 (12), but the root system may have still been expanding during this period. Peak root length (Fig. 1C) and mass (Fig. 2C) in ambient CO₂ were 150% greater in 2003 than in 1998, although the trend through time was not statistically significant (R² = 0.19, P = 0.07). However, there was little change in peak length during the last 3 years in either ambient or elevated CO₂, so the effect of CO₂ cannot be ascribed simply to an acceleration of ontogeny. Indirect effects of CO₂ through soil moisture can be discounted. Although stomatal conductance of upper canopy leaves was usually lower in elevated CO₂, canopy conductance and stand-level evapotranspiration were little affected (17). Hence, soil moisture was not significantly different between plots. Our results suggest that CO₂ enrichment significantly increased peak-standing root crop by altering allocation such that the potential for root occupancy of the soil volume was increased. This response was manifested especially in the deeper distribution of roots in the soil profile (Fig. 3). In 1998 most of the root length was in the upper soil (40% in the top 15 cm and 79% in the top 30 cm). Five years later 63% of the root length was still at 0–30 cm depth in ambient CO₂, but the root distribution was distinctly different in elevated CO₂ plots. CO₂ enrichment increased root length in the upper profile, but the largest increases occurred in deeper soil: 3-fold more length at 30–45 cm and 4-fold more at 45–60 cm. This response, although statistically significant, was highly variable: 3 of the 10 minirhizotron tubes in elevated CO₂ accounted for 90% of the root length deeper than 45 cm. Soil cores collected in October 2003 confirmed the presence of fine roots at 60 cm, but not enough cores were collected to verify the effect of CO₂ on depth distribution given the high spatial variability. High variability in root distribution is not surprising and cannot be dismissed as a sampling artifact: morphological plasticity of root systems, including spatially explicit root proliferation, is considered a major mechanism whereby plants cope with the heterogeneity of soil resources (2, 18). Other reports of effects of CO₂ on root distribution include an upward shift in a grassland ecosystem (16), a downward shift in a developing Populus stand (15), and stimulation of both surface and deep roots in a scrub oak system (19).

View larger version (16K): [in this window] [in a new window]   Fig. 3. Distribution of fine-root length by depth in soil at the time of peak standing-root length in 1998 and 2003. Data are the means ± SE of three ambient and two elevated plots, based on analyses of five minirhizotron tubes per plot and expressed as length per square meter of observation window. CO2 had a significant effect on root length at 0–15 cm (P < 0.035), 30–45 cm (P < 0.001), and 45–60 cm (P < 0.013) but did not at 15–30 cm. The patterns in intervening years were intermediate to those shown here.

The additional C taken up and converted to organic matter by trees in CO₂-enriched plots (average 22% increase in NPP) was allocated primarily to fine-root production (Fig. 2D). After the first year of treatment, there was no significant increase in aboveground woody dry matter production (stem growth). Because fine-root turnover is much faster than turnover of woody stems, the preferential allocation to fine roots should significantly reduce the potential for additional C sequestration in trees in elevated CO₂ (20). However, sequestration of some of that C in the forest remains a possibility. As fine roots die, their C enters the soil system where there is the potential for movement into long-lived organic matter pools. Although the efflux of CO₂ from the soil surface has been higher in the CO₂-enriched plots (21), the response is inconsistent and smaller than the increase in fine-root production and mortality. Soil analysis indicates that there is increased accumulation of new C in CO₂-enriched plots (E. Hanlon and W. M. Post, personal communication), particularly in microaggregate fractions (at 0–5 cm in depth) that facilitate movement of C into pools with long residence times (J. Jastrow, personal communication). It may become especially important that the greatest increases in root production in elevated CO₂ occur in deeper soil, where sequestration into longer-lived pools may be more likely (22). Construction of a complete C budget for the stand is a clear need and a formidable challenge.

These results contrast with those from the similar FACE experiment in a loblolly pine stand (23). There, the enhancement in NPP was allocated primarily to aboveground stem increment. The C in pine fine roots has a 3-fold-higher MRT than in sweetgum roots (3) (similar to the difference in MRT of the evergreen vs. deciduous canopy); therefore, annual fine-root production and mortality rates are much lower than in our sweetgum stand, and the pine root system is less responsive to elevated CO₂ (24). There has been no evidence for increases in soil C content in the pine stand (25). Hence, the inherent difference in fine-root dynamics between these two contrasting tree species is a key ecosystem attribute controlling how C flux and storage respond to rising CO₂.

The substantial response of fine-root productivity to CO₂ enrichment in the sweetgum stand may be a mechanism for increasing N uptake to meet the increased demand associated with additional C uptake in elevated CO₂. Long-term effects of elevated CO₂ on tree growth and C sequestration in forests are highly dependent on the availability and cycling of N (7, 26), and N availability is considered a major factor regulating fine-root production in elevated CO₂ (27). In grasslands, microbial N processes that control the supply of N to plants have been responsive to elevated CO₂, with N availability increasing because of an indirect effect of CO₂ on soil moisture (28) or declining because of reduced quality of litter inputs (29). Microbial N cycling and N availability have not responded to elevated CO₂ in this or other forest stands (30); therefore, the N needed to meet the requirement for increased NPP must be met through increased access to soil N. To assess this possibility, we calculated fine-root-length duration as an integrative measure of the capacity for N uptake by the root system during the growing season. N uptake has been linearly associated with fine-root-length duration (Fig. 4) in support of the premise that the fine-root response is important in the interaction between C and N cycles. Our hypothesis that full soil occupancy in this forest stand would constrain the N cycle is not supported. Elevated CO₂ increased the capacity of roots to occupy the soil volume, and there was a concomitant increase in N uptake. However, increased fine-root production may represent a futile mechanism for improving N nutrition in this forest stand. The increased C supply in CO₂-enriched plots was used to support more root production, but the resulting increase in N uptake has so far supported only increased root production and not whole-tree N nutrition or aboveground growth (31).

View larger version (13K): [in this window] [in a new window]   Fig. 4. Relationship between N uptake and root-length duration. N uptake per plot for each year (1998–2002) was calculated as the N content (dry matter production times N concentration) of woody increment, leaf litter, and annual fine-root production plus net foliar leaching (31). Root-length duration is the area under the plots of fine-root standing crop (Fig. 1C). Regression line: N uptake = 5.74 x root-length duration - 36.3; R2 = 0.80.

The potential for CO₂ enhancement of root productivity mandates that analyses of ecosystem responses to atmospheric change take a whole-ecosystem approach. Analyses based solely on aboveground production will possibly miss a significant fraction of C and underestimate the potential of the ecosystem for additional C storage. Deciduous forest ecosystems with highly dynamic root systems will exhibit different relationships between C uptake, allocation, storage, and cycling than forests with less dynamic root systems, and generalizations about the potential for forests to sequester additional C and provide a negative feedback to the rising atmospheric concentration must account for these differences. Although current methods for quantifying root dynamics are cumbersome and not appropriate for documenting compliance to C sequestration management (33), methodological limitations should not be an excuse for ignoring this critical ecosystem response to global change.

	Acknowledgements

 
We thank Stan Wullschleger, Roser Matamala, Julie Jastrow, and four anonymous reviewers for helpful comments on the manuscript. This work was supported by the Oak Ridge Institute for Science Education (C.D.R.), Summer Undergraduate Research Experience of the Department of Energy Global Change Education Program (N.E.M.), and the Department of Energy's Office of Science, Biological, and Environmental Research. Oak Ridge National Laboratory is managed by UT-Battelle for the Department of Energy (Contract DE-AC05-00OR22725).

	Footnotes

 
Abbreviations: FACE, free-air CO₂ enrichment; MRT, mean residence time; NPP, net primary productivity; SRL, specific root length.

To whom correspondence should be addressed. E-mail: rjn{at}ornl.gov.

© 2004 by The National Academy of Sciences of the USA

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