Measured forest soil C stocks and estimated turnover times along an elevation gradient

Geoderma 136 (2006) 342 – 352 www.elsevier.com/locate/geoderma

Measured forest soil C stocks and estimated turnover times along an elevation gradient☆ Charles T. Garten Jr. ⁎, Paul J. Hanson Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA Received 4 March 2005; received in revised form 27 March 2006; accepted 30 March 2006 Available online 8 May 2006

Abstract The purpose of this research was to measure forest soil C stocks and estimate turnover times along a 1.3 km rise in elevation in the southern Appalachian Mountains. Turnover times were calculated based on estimated soil C inputs and near steady state soil C stocks in the O-horizon and the mineral soil to a 30-cm soil depth. Monte Carlo methods were used in the calculations to accommodate uncertainties in model parameterization. Measured mean stocks and calculated median turnover times of soil C ranged from 4.4 to 12.2 kg C m− 2 and 11 to 31 years, respectively. The predicted turnover times reflect a high proportion of labile soil C over the selected sampling depth. Both forest soil C stocks and the predicted turnover time of soil C increased with altitude. There were no consistent trends for stand basal area and forest soil C inputs along the elevation gradient suggesting that altitudinal changes in soil C stocks and turnover times could be attributed to different rates of soil organic matter decomposition. Soil respiration flux did not vary significantly with altitude, but soil respiration normalized for existing soil C stocks indicated decreasing rates of soil organic matter decomposition with increasing elevation. Measured soil N stocks and differences in Ohorizon litter chemistry indicated increasing N availability from low-elevation to high-elevation forests. Soil C storage and turnover time increased from warmer, drier, less N-rich forests to colder, wetter, more N-rich forests. Considered together, these data support assumptions of a declining rate of soil organic matter decomposition with increasing elevation in the southern Appalachian Mountains. Representative characterization of long-term litter C inputs is one of the most challenging aspects of the present analysis. © 2006 Elsevier B.V. All rights reserved. Keywords: Forests; Soil C; Soil N; Turnover times; Temperature; N availability; Litter chemistry; Mountainous terrain

1. Introduction

☆

The submitted manuscript has been authored by a contractor of the U.S. Government under contract DE-AC05-00OR22725. Accordingly, the U.S. Government retains a nonexclusive, royalty-free license to publish or reproduce the published form of this contribution, or allow others to do so, for U.S. Government purposes. ⁎ Corresponding author. Tel.: +1 865 574 7355; fax: +1 865 576 8646. E-mail address: [email protected] (C.T. Garten Jr.). 0016-7061/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2006.03.049

The role of soil C dynamics in the exchange of CO2 between the terrestrial biosphere and the atmosphere is at the center of many science questions related to global climate change. However, large uncertainties remain about the mean residence time or turnover time of total soil organic C (Six and Jastrow, 2002; Pendall et al., 2004). Uncertainties in estimates of total soil C turnover time arise, in part, because of differences between

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studies in vegetation type, climate, soil type, and methods of measurement. Recent reviews (e.g., Six and Jastrow, 2002) indicate the need for additional data on turnover times of forest soil C stocks because there are relatively few studies on which to base such estimates for total soil C in forest ecosystems. Furthermore, recent state-of-the-science reports have recognized the need to fill gaps in our knowledge of soil C stocks, particularly forest soil C dynamics in mountainous regions (Wofsy and Harriss, 2002). Various studies indicate that soil C concentrations or stocks increase with altitude in mountainous terrain (Townsend et al., 1995; Trumbore et al., 1996; Conant et al., 1998; Garten et al., 1999; Bolstad and Vose, 2001). The differences along elevation gradients reflect a changing balance of soil C inputs and soil C losses that are potentially related to changes in both abiotic (e.g., temperature) and biotic (e.g., litter quality) factors. Mean residence times of soil C can be inferred directly from measurements of soil CO2 efflux when steady state soil C stocks and the contribution of heterotrophic and autotrophic components of soil CO2 efflux are well characterized. However, measurements of soil CO2 efflux may disproportionately reflect the decomposition of labile soil organic matter (Janzen et al., 1992; Janssens et al., 2001) and thereby bias estimates of the mean residence time for total soil organic C stocks. Furthermore, seasonal variations in the relative contribution of root respiration and heterotrophic microbial respiration to soil CO2 efflux (Dorr and Munnich, 1987; Wang et al., 2000), as well as technical difficulties in distinguishing both sources, are serious limitations to estimating the turnover time of soil C based solely on measurements of soil respiration. The turnover time (T, years) of total soil C can also be estimated from measurements of soil C inputs and near steady state soil C stocks using the following simple equation: T ¼ 1=ðCi =Cs Þ

ð1Þ

where Ci is the soil C input (g C m− 2 yr− 1) and Cs is the soil C stock (g C m− 2). Long-term soil C inputs are difficult to quantify directly because of uncertainties associated with the measurement of belowground processes. However, recent studies indicate that annual soil respiration in mature forest ecosystems (45+ years of age) can be predicted from annual aboveground litterfall C flux (Raich and Nadelhoffer, 1989; Davidson et al., 2002). The studies concluded, where forest soil C stocks are near steady state, belowground production of root detritus (i.e., belowground soil C inputs) can be

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approximated from estimates of aboveground litterfall production across divergent ecosystems, but not necessarily within an ecosystem. The purpose of this report is to describe trends in amounts of forest soil C and turnover along an elevation gradient in the southern Appalachian Mountains of eastern Tennessee and western North Carolina, USA. Using measured soil C stocks in mature and undisturbed forest ecosystems and Monte Carlo type calculations to estimate soil C inputs, the turnover time of soil C was calculated for different sites over a 1335 m rise in elevation. Calculations indicated that differences in forest soil C storage along the elevation gradient arise from varying rates of soil organic matter decomposition rather than changes in soil C inputs. 2. Methods 2.1. Field measurements Three sites (NG, BB, and SP) were closed canopy, evergreen stands located in high-elevation spruce (Picea rubens) and fir (Abies fraseri) forests in the Great Smoky Mountains National Park (GSMNP). One site (TD) was a closed-canopy, northern hardwood forest also located at high elevation in the National Park. The five remaining study sites (WB, MC, MB, SB, and MH) were closed canopy, mixed hardwood forests (Table 1): WB was a low-elevation forest located on the Oak Ridge Reservation (ORR), near Oak Ridge, TN, and the remaining four sites were closed-canopy, low- and mid-elevation forests in the GSMNP. There was little woody understory at all of these sites. Forest sites on federal lands, like the ORR and the GSMNP, have been protected from direct human disturbance and land cover change for more than 55 years. Soil C stocks at these undisturbed and mature forest sites were assumed to be near steady state. Both theoretical (West et al., 2004) and empirical (Switzer et al., 1979) studies indicate that surface soil C stocks in aggrading, temperate forest ecosystems can approach equilibrium conditions over a period of ≈60 years. Soil samples were collected in August 2001 and August 2003 at five forest sites (WB, SB, MH, BB, and SP). An additional four sites (MB, MC, TD, and NG) along the altitudinal gradient were sampled in August 2003. At each soil sampling event, 8 to 10 mineral soil samples (30 cm deep) were collected per site using a stainless steel soil recovery probe with hammer attachment and 2.4 cm diameter butyrate plastic liners (AMS, American Falls, ID). The O-horizon was removed from a 214-cm2 area, above where mineral soil samples were taken with the soil recovery probe, and placed in plastic

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Table 1 Longitude, latitude, elevation, mean annual temperature (MAT), mean annual precipitation (PPTN), stand basal area (BA), and the ratio of sand to silt + clay content at study sites in the southern Appalachian Mountains Site b

WB MBb MCb SBb MHb TDb NGc BBc SP c

Longitude (W)

Latitude (N)

Elevation (m)

MATa (°C)

PPTNa (cm)

BA (m2 ha− 1)

Sand/(silt + clay)

84°16′55ʺ 83°39′06ʺ 83°38′22ʺ 83°27′44ʺ 83°27′58ʺ 83°23′40ʺ 83°26′08ʺ 83°26′55ʺ 83°27′03ʺ

35°57′51ʺ 35°40′50ʺ 35°40′52ʺ 35°41′02ʺ 35°40′51ʺ 35°34′43ʺ 35°36′39ʺ 35°36′27ʺ 35°36′21ʺ

335 530 560 940 1000 1430 1570 1650 1670

12.8 11.9 11.8 10.0 9.7 7.7 7.1 6.7 6.6

147 158 159 181 184 208 216 221 222

21.7 40.4 55.7 63.4 58.3 52.0 38.5 55.1 43.6

0.60 ± 0.07 0.34 ± 0.02 0.43 ± 0.01 0.63 ± 0.06 0.71 ± 0.04 0.74 ± 0.05 1.01 ± 0.14 0.74 ± 0.04 0.91 ± 0.08

a Mean annual temperature and precipitation were predicted at each site using regressions between temperature and elevation (r2 = 0.97) or precipitation and elevation (r2 = 0.97). Regressions were developed using data from studies by Stephens (1969) and Garten et al. (1999) and summarized in Garten (2004b). b Closed canopy, deciduous, mixed hardwood forest stand. c Closed canopy, evergreen forest stand.

bags. Samples were transported to the laboratory on the day of collection and stored in a refrigerator (5 °C) prior to sample processing. Prior to leaf senescence in 2003, four litter baskets (0.128 m2) were randomly placed at each study site. Broadleaf litterfall was collected in each forest stand on two occasions (October 22 and November 3) in late 2003 to determine C:N ratios in aboveground leaf litter inputs. Because of a coarse mesh size, most small needleleaf litterfall passed through the baskets. This led to an under-representation of needleleaf litterfall (which means that the samples are not representative of the entire forest stand), but also made the samples more comparable across the nine study sites by limiting them to primarily deciduous, broadleaf species. The leaf litterfall samples from each basket were dried in an oven (70 °C) prior to sample processing. Basal area (i.e., the cross sectional area of tree stems at breast height) was measured in each forest stand during the summer of 2004 using a JIM-GEM® Cruz-All gauge (Forestry Suppliers, Jackson, MS). Tree counts from multiple sampling points were combined and converted to stand basal area measurements (m2 ha− 1). Measurements of soil respiration were made prior to the present study at five of the forest sites during field campaigns in May, June, July, August, September, and November of 1996. Soil respiration, or net forest floor CO2 efflux (Rs), was measured with the LiCor 6200 closed-gas-exchange system and a custom-designed aluminum chamber having a surface area of 594 cm2 and a volume of 5227 cm3 (Hanson et al., 1993). The open bottom of the chamber was pressed into the litter layer to form the closed cuvette for measurements that lasted from 1.5 to 3 min depending on the season (i.e., shorter observations in the summer when rates were

high). Permanent soil collars were not used to avoid inappropriate trapping of precipitation on the litter layers. Soil temperature and soil water content were monitored simultaneously with each observation. Soil moisture (%, cm3 cm− 3) was measured with a time-domain reflectometer (Soil Moisture Equipment Corporation, Santa Barbara, CA) to a depth of 15 cm (Topp and Davis, 1985). Soil temperature (°C) was measured to ≈10 cm with an OMEGA digital temperature probe. 2.2. Laboratory analyses The dry mass of the O-horizon was determined after drying at 70 °C. The O-horizon samples were ground and homogenized in a sample mill and stored in airtight glass bottles prior to analysis for C and N concentrations. Mineral soil samples collected with the soil probe were extruded from the plastic liners and cut into 10cm increments. The various increments were air-dried at room temperature (21 ± 1 °C) in a laboratory equipped with a dehumidifier. The air-dry soil samples were crushed using a rubber mallet and passed through a 2mm sieve to remove stones, gravel, and coarse debris (e.g., large roots). The N 2-mm fraction was discarded. Soil passing the 2-mm sieve was ground and homogenized using a mortar and pestle, and stored in an airtight glass vial prior to analysis for C and N concentrations. A portion of each sieved soil sample was dispersed by shaking overnight in an aqueous solution of sodium hexametaphosphate (5 g L− 1) and further sieved (0.053 mm). The sand (≥ 0.053 mm) and silt + clay (≤ 0.053 mm) fractions were oven dried (70 °C) and weighed. Samples were analyzed for total C and N concentrations using a LECO CN-2000 elemental analyzer (LECO Corporation, St. Joseph, MI). The

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instrument was calibrated using a LECO soil standard traceable to the National Institute of Standards and Technology (NIST), Gaithersburg, MD. 2.3. Calculation of soil carbon stocks Carbon stocks (g C m− 2) in the O-horizon were calculated as the product of concentration (g C g− 1) and dry mass per unit area (g m− 2). Carbon or N stocks in the 0–10, 10–20, and 20–30 cm mineral soil increments were calculated as the product of concentration (g element g− 1), soil density (g m− 3), and increment length (m). Soil density (g cm− 3) was calculated from the mass of soil (b 2 mm) in each depth increment. Cumulative mineral soil C or N stocks to a 30-cm soil depth were calculated by summing the respective stocks in the 0–10, 10–20, and 20–30 cm increments. In a small number of cases, deeper soil core increments (20– 30 cm) were missing from samples collected in 2001 and 2003. Earlier measurements (Garten et al., 1999) of soil C and N stocks in the same depth increment and at the same sites were substituted for the missing data. 2.4. Calculation of turnover time A critical step in solving for the turnover time of forest soil C based on Eq. (1) is estimation of annual soil C inputs (Ci). Steps for the calculation of Ci are summarized in the following equations. Soil respiration (Rs, g C m− 2 yr− 1) at each site was calculated from an equation developed by Davidson et al. (2002) that was demonstrated to have utility for comparisons across divergent ecosystems: Rs ¼ a þ bðA½CL Þ

ð2Þ

where A is aboveground litterfall input (g m− 2 yr− 1), CL is the litterfall C concentration (0.45 g C g− 1), and a and b are, respectively, the intercept and slope of the regression between annual soil respiration and annual aboveground litterfall C inputs (g C m− 2 ) (Raich and Nadelhoffer, 1989; Davidson et al., 2002). The forest soil respiration flux (Rs) is comprised of CO2 originating from both heterotrophic (soil organic matter decomposition) and autotrophic (root respiration) sources. The heterotrophic component (Rh, g C m− 2 yr− 1) was calculated from: Rh ¼ Rs ðHf Þ

ð3Þ

where Hf is the fraction of the annual soil respiration flux that can be attributed to heterotrophic respiration.

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In forests with near steady state soil C stocks, belowground C inputs (Pb, g C m− 2 yr− 1) can be calculated as the difference between heterotrophic soil respiration and aboveground soil C inputs (Raich and Nadelhoffer, 1989), or: Pb ¼ Rh −ðA½CL Þ:

ð4Þ

Annual soil C inputs (Ci) were then calculated from: Ci ¼ ðA½CL Þ þ Pb ;

ð5Þ

and soil C stocks to a 30-cm soil depth (Cs, g C m− 2) at each study site were calculated from: Cs ¼ Co þ Ca ;

ð6Þ

where Co is the measured C stock in the O-horizon (g C m− 2) and Ca is the measured C stock in the mineral soil (g C m− 2). Monte Carlo methods were used to predict the turnover time of forest soil C because some parameters in the foregoing model (Eqs. (1)–(6)) are not precisely known. The Monte Carlo method incorporates errors in the estimation of both Ci and Cs into the calculation of soil C turnover. A probability density function (i.e., normal distribution) was specified for parameters in the previous equation set based on either field measurements (e.g., Cs) or literature data (e.g., estimation of Ci). Parameter variance for a specific site along the elevation gradient may be overestimated from literature data that includes multiple sites or studies; hence, errors in the final estimate of soil C turnover at each study site are probably less than the predicted variance. Soil C stock and the turnover time for soil C at each site were estimated from 1000 individual calculations where estimates of A, Hf, a, b, Co, and Ca were varied simultaneously. The approach assumed zero covariance among the various model parameters and thus maximized variation in predicted turnover times. The basis of each parameter distribution for Monte Carlo sampling is discussed in the following paragraphs. Litterfall mass (A) — Mean (±SD) annual leaf litterfall in the southeastern USA, based on 252 USDA study plots, is 405 ± 63.5 g m− 2 yr− 1, with no significant difference among forest types (Sharpe et al., 1980). This regional estimate for aboveground leaf litterfall mass corresponds reasonably well with measurements of annual leaf litterfall inputs at Walker Branch Watershed, TN (378 g m− 2 from Edwards et al., 1989; 537 g m− 2 from Hanson et al., 2003), Coweeta, NC (399 g m− 2 from Johnson and Lindberg, 1992), Duke, NC (377 g m− 2 from Johnson and Lindberg, 1992), and measured mean annual forest litterfall inputs for sites in the southeastern US during

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Table 2 Measured mean (±SD) C or N stocks in the O-horizon or mineral soil, and total soil C stocks (to a 30-cm soil depth) at nine forest sites along an elevation gradient in the southern Appalachian Mountains Site

WB MB MC SB MH TD NG BB SP a

n

17 9 9 17 17 9 9 18 17

O-horizon (kg C m− 2) 0.51 ± 0.17 1.33 ± 0.36 1.47 ± 0.37 0.67 ± 0.30 1.23 ± 0.62 1.96 ± 0.42 1.33 ± 0.35 1.30 ± 0.50 2.27 ± 0.49

Mineral soil −2

−2

gNm

kg C m

152 ± 41 281 ± 24 220 ± 36 684 ± 81 347 ± 59 337 ± 63 367 ± 70 478 ± 72 496 ± 121

3.83 ± 0.57 4.91 ± 0.70 5.38 ± 0.79 11.01 ± 1.63 7.08 ± 1.62 7.49 ± 1.74 6.43 ± 1.30 8.52 ± 1.58 9.91 ± 2.35

Total soil Ca (kg C m− 2) 4.35 ± 0.60 6.24 ± 0.79 6.84 ± 1.02 11.68 ± 1.68 8.32 ± 1.97 9.45 ± 1.60 7.76 ± 1.42 9.83 ± 1.71 12.18 ± 2.61

Total soil C = O-horizon + mineral soil stocks.

the International Biological Program (422 g m− 2 from Cole and Rapp, 1981). Most of the foregoing measurements are within 10% of the estimate derived by Sharpe et al. (1980). Prior short-term (3-year) measurements of leaf litterfall inputs at various sites along the elevation gradient (≈460 ± 48 g m− 2 yr− 1 from Garten et al., 1999) were somewhat greater, but within 15% of the same estimate. In the Monte Carlo calculations, values for leaf litterfall mass at each site were randomly drawn from a normal distribution with a mean and standard deviation (SD) of 405 and 63.5 g m− 2 yr− 1, respectively. Heterotrophic fraction of soil respiration (Hf) — Based on a review of numerous studies (Hanson et al., 2000), root respiration contributes 46%, on average, to the total annual forest soil CO2 efflux. This estimate was derived from measurements over varying time intervals (i.e., daily, monthly, and annual measurement periods) in forests of different ages. Studies conducted in mature forests indicated that the annual fractional contribution of heterotrophic sources to soil CO2 efflux could be approximated by randomly drawing values from a normal distribution with a mean and SD of 0.50 and 0.075, respectively. This produced in a wide range of values for Hf (0.2 to 0.8) in Monte Carlo calculations of soil C turnover times and may overestimate the true variance. Variation in predicting soil respiration (Rs) — Based on studies in mature forest ecosystems (Davidson et al., 2002), values for b (the slope of the regression between annual Rs and annual leaf litterfall C inputs) were randomly drawn from a normal distribution with a mean and SD of 2.8 and 0.49, respectively. Values for the intercept, a, were randomly drawn from a normal distribution with a mean and SD of 287 and 130, respectively.

Soil C stocks (Cs) — Values for C stocks (g m− 2) in the O-horizon (Co) and surface mineral soil (Ca) in the Monte Carlo calculations were drawn from normal distributions defined by the mean and SD of measured soil C stocks at each study site (Table 2). 3. Results 3.1. Site characterization The sampling sites ranged in elevation from 335 to 1670 m (Table 1). Mean annual temperature declined from 12.8 to 6.6 °C and mean precipitation increased from 147 to 222 cm yr− 1 with increasing altitude. Stand basal area ranged from 22 to 63 m2 ha− 1, but there was no significant relationship between stand basal area and study site elevation (r 2 = 0.08). Soil sand content increased with altitude (Table 1). The sand:silt + clay ratio in the surface 30-cm of mineral soil at each study site was significantly related to elevation (r = + 0.83, P ≤ 0.01). This change is partly caused by predominantly sandstone parent material at the higher elevations. 3.2. Soil respiration Across the five study sites, forest floor CO2 efflux showed strong seasonal patterns with maximum emissions in July or August and minimum emissions in November (Fig. 1). This pattern was related to the seasonal pattern of temperatures with maximum forest floor CO2 efflux occurring during the warmest period on all sites. Flux data for all sites and dates yielded an increasing temperature response with an estimated Q10 value of ≈ 1.9. Although the warmest temperatures were associated with the low elevation site (WB) on all dates (Fig. 1), this site did not always support the highest rate of soil CO2 efflux. Notably, in July the highest rates of CO2 efflux were observed at the high elevation spruce and fir forest (SP). Variable rates of belowground root growth and activity are a likely cause for such patterns of CO2 efflux that appear unrelated to temperature. During the wet 1996 growing season soil water contents (0–15 cm depth) were always high at all sites and did not appear to contribute to site-to-site differences in soil respiration (data not shown). Repeated measures analysis of variance indicated that soil respiration was significantly different among sites (F4,25 = 6.5; P ≤ 0.001) and time of the year (F5,125 = 84.1; P ≤ 0.001). The interaction between site and month of the year was also statistically significant (F20,125 = 4.2; P ≤ 0.001). Post hoc comparisons of site

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Fig. 1. Mean (± SE) soil respiration at five forest sites along an elevation gradient in the southern Appalachian Mountains. Statistics during each sampling period are based on 6 measurements per site. Site codes are explained in Table 1.

means (with Scheffé's Test) indicated soil respiration at four of the five study sites (WB, SB, MH, and SP) was not significantly different. Over all six sampling periods, the mean ± SE (n = 36) soil respiration at WB, SB, MH, BB, and SP was, respectively, 3.1 ± 0.23, 3.2 ± 0.21, 3.0 ± 0.24, 2.3 ± 0.16, and 3.3 ± 0.34 μmol C m− 2 s− 1. Estimates of annual soil respiration (heterotrophic + autotrophic) for each site were obtained by fitting a sitespecific temperature response function to the efflux values presented in Fig. 1. These relationships were then applied to measured annual patterns of soil temperature obtained at each site, and the values summed to yield annual CO2 loss from the forest floor. Calculated annual CO2 fluxes at WB, SB, MH, BB, and SP were, respectively, 863, 940, 852, 646, and 890 g C m− 2 yr− 1. There was no statistically significant association between soil CO2 flux and study site elevation. However, when calculated annual soil CO2 efflux was normalized for existing soil C stocks, the rate of soil CO2 flux (yr− 1) decreased with increasing elevation (r = − 0.88; P ≤ 0.05).

site (MH) produced leaf litterfall with low mean N concentrations (0.58% to 0.66%) and high mean C:N ratios (74 to 85). Three high-elevation sites (NG, BB, SP) and another mid-elevation site (SB) produced leaf

3.3. Litterfall chemistry There were statistically significant differences between sites in leaf litter N concentrations (F8,63 = 18.8; P ≤ 0.001) and C:N ratios (F8,63 = 17.1; P ≤ 0.001) in 2003. Both mean leaf litterfall N concentrations and mean C:N ratios were correlated (P ≤ 0.05) with study site elevation (r = +0.76 and r = − 0.77, respectively). Most of the sites could be binned into one of two groups based on leaf litterfall chemistry (Fig. 2). Three lowelevation sites (WB, MB, MC) and one mid-elevation

Fig. 2. Mean (±SE) leaf litterfall N concentrations and C:N ratios in forests along an elevation gradient in the southern Appalachian Mountains. Site codes are explained in Table 1.

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litterfall with high mean N levels (1.15% to 1.23%) and low mean C:N ratios (40 to 44). There were also statistically significant between site differences in O-horizon N concentrations (F9,126 = 35.7; P ≤ 0.001) and C:N ratios (F9,129 = 18.8; P ≤ 0.001). Mean O-horizon N concentrations and C:N ratios were correlated (P ≤ 0.01) with study site elevation (r = + 0.95 and − 0.88, respectively). The correlations between elevation and O-horizon chemistry (Fig. 3) were markedly stronger than those observed for leaf litterfall. Elevation accounted for 90% of the variance in mean O-horizon N concentrations and 78% of the variance in mean Ohorizon C:N ratios across the nine study sites. 3.4. Soil nitrogen and carbon stocks There were statistically significant between site differences in O-horizon C stocks (F9,120 = 26.5; P ≤ 0.001), surface (0–30 cm) mineral soil C stocks (F9,120 = 38.2; P ≤ 0.001), total C stocks to a 30-cm soil depth (F9,120 = 38.9; P ≤ 0.001), and surface mineral soil N stocks (F9,120 = 73.7; P ≤ 0.001). Total soil C stocks (Cs) include

Table 3 Predicted mean (± SD) total soil respiration (Rs, g C m− 2 yr− 1), heterotrophic soil respiration (Rh, g C m− 2 yr− 1), soil C inputs (Ci, g C m− 2 yr− 1), and the geometric mean of predicted turnover times for total soil C stocks to a 30-cm soil depth (Cs, kg C m− 2) at nine sites along an elevation gradient in the southern Appalachian Mountains Site

Rs

Rh = Ci

Cs

Predicted turnover time (years)

WB MB MC SB MH TD NG BB SP

794 ± 180 801 ± 184 802 ± 184 787 ± 174 796 ± 177 810 ± 180 794 ± 180 784 ± 175 795 ± 173

400 ± 111 398 ± 113 400 ± 113 394 ± 105 396 ± 106 402 ± 107 398 ± 110 391 ± 104 397 ± 106

4.37 ± 0.56 6.21 ± 0.80 6.86 ± 0.88 11.63 ± 1.71 8.34 ± 1.79 9.56 ± 1.79 7.75 ± 1.37 9.82 ± 1.63 12.15 ± 2.33

11.3 (11.0–11.6) 16.1 (15.7–16.5) 17.7 (17.3–18.2) 30.3 (29.5–31.2) 21.3 (20.7–22.0) 24.2 (23.5–24.9) 20.0 (19.4–20.5) 25.7 (25.1–26.4) 31.1 (30.3–32.0)

At steady state, Rh = Ci in undisturbed forests. Values in parenthesis indicate the 99% confidence interval for predicted turnover times at each site based on 1000 Monte Carlo type calculations.

both the O-horizon and the mineral soil C stocks. Mean O-horizon C stocks tended to increase with altitude (P ≤ 0.10). Mean O-horizon C stocks ranged from 6% to 21% of the total soil C stock (Table 2). Across all 9 sites, measured total soil C stocks increased with elevation (r2 = 0.52; P ≤ 0.05), but site SB exhibited a large deviation from the regression line. When site SB was excluded from the dataset, surface soil N (r2 = 0.83; P ≤ 0.01) and C stocks (r2 = 0.75; P ≤ 0.01) were strongly correlated with altitude. 3.5. Calculated soil carbon turnover times

Fig. 3. Mean (± SE) O-horizon N concentrations and C:N ratios in forests along an elevation gradient in the southern Appalachian Mountains. Site codes are explained in Table 1.

Table 3 presents predicted mean (± SD) total soil respiration (Rs), heterotrophic soil respiration (Rh), and total soil C stocks (Cs) based on calculations with the model at each study site. At near steady state, the predicted soil C input (Ci) should equal predicted heterotrophic soil respiration (Rh) in undisturbed forest stands. Predicted mean values of Rh and Rs were not different among the study sites because the model assumed no trend between soil C inputs and elevation. Predicted soil respiration (Rs) was within ≈ 10% to 20% of annual estimates from field data collected at select sites along the elevation gradient (see Section 3.2), and the assumption of no relationship between elevation and Rs was consistent with field measurements. When Rs and Rh were normalized for calculated soil C stocks (i.e., Rs/Cs and Rh/Cs, respectively), both parameters exhibited a significant negative association with study site elevation (r = − 0.75; P ≤ 0.05). Predicted soil C stocks (Cs) were normally distributed at each study site. However, there was significant

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positive skewness in predicted soil C turnover times. A geometric mean, which estimates the median value, and the 99% confidence interval about the geometric mean were used to summarize predicted turnover times from the 1000 model calculations at each site (Table 3). Mean predicted soil C stocks (Cs) and median predicted soil C turnover times increased with elevation (P ≤ 0.05). When all 9 sites were considered the coefficient of determination (r2) was ≈0.51 for both predicted Cs and soil C turnover. However, sites SB and NG exhibited large deviations from the regression line. When sites SB and NG were excluded from the dataset, elevation accounted for ≈ 90% of the variance in both mean Cs and median soil C turnover times (Fig. 4). Across all 9 sites, ≈ 72% of the variation in median predicted turnover times was explained by a multiple regression against elevation and stand basal area (F2,6 = 7.7; P ≤ 0.05) indicating that soil C inputs were possibly

Fig. 4. Mean predicted soil C stocks (Cs) and median predicted turnover times of forest soil C along an elevation gradient in the southern Appalachian Mountains. Sites SB and NG (open symbols) were excluded from the linear regression against elevation (see Results). Site codes are explained in Table 1.

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misestimated at sites SB and NG by values used in calculations with the model. 4. Discussion The present study indicated that both soil C stocks and the turnover time of forest soil C increase with altitude in the southern Appalachian Mountains. Increasing soil C stocks with elevation could be caused by greater soil C inputs in combination with a relatively constant rate of C loss through decomposition of soil organic matter. However, available data suggest that soil C inputs do not increase with altitude. First, there was no association between stand basal area and elevation across the nine study sites (Table 1). Second, studies in North Carolina forests indicate a decline in aboveground net primary production and leaf area index with increasing altitude (Bolstad et al., 2001) and no significant elevational trend in aboveground litterfall inputs (Bolstad, personal communication). Prior studies at five of nine sites along the elevation gradient indicated no significant site differences in litterfall C inputs (Garten et al., 1999). Other studies along elevation gradients in mountainous areas report declines in annual aboveground litterfall with increasing altitude (Reiners and Lang, 1987; Joshi et al., 2003). Considered together, these data indicate that soil C inputs do not increase significantly from low- to highelevation forests, however representative characterization of long-term leaf litterfall inputs is one of the most challenging aspects of the present analysis. If we have systematically overestimated annual leaf litterfall inputs at high elevations (≥1400 m) with the regional estimate of 405 g m− 2, then calculated turnover times of forest soil C at sites TD, NG, BB, and SP are longer than those presented in Table 3. If soil C inputs do not increase with elevation, then differences in organic matter decomposition must be the cause of altitudinal variation in forest soil C stocks and turnover driven by elevation gradients of environmental factors. Field measurements of soil CO2 efflux at five of the study sites, when normalized for soil C stocks, indicated declining soil organic matter decomposition rates with increasing altitude. Calculations with the model also indicated that soil respiration measurements decline with increasing elevation when normalized for existing soil C stocks (i.e., the fraction of soil C respired annually decreases with elevation). Recently published studies of the disappearance of 13C-labelled glycine along the same gradient also indicate decreasing decomposition rates with increasing altitude (Garten, 2004a). These data support assumptions of a declining rate of soil organic matter decomposition with increasing elevation.

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Multiple environmental factors (temperature, precipitation, N deposition, litter quality, and soil type) vary with altitude in the southern Appalachian Mountains and each factor can potentially affect soil C storage and turnover. Numerous studies indicate that both decomposition of labile soil organic matter (Tate et al., 1995; Trumbore et al., 1996; MacDonald et al., 1999; Kirschbaum, 2000) and soil respiration (Raich and Schlesinger, 1992; Kirschbaum, 1995; Raich and Potter, 1995) increase with temperature. Mean annual temperature shows a significant inverse correlation with elevation (Table 1). Nevertheless, in addition to changes in climate, trends in soil N stocks and leaf litter chemistry indicate N availability increases with elevation. Prior studies show an increase in both potential net soil N mineralization (Garten and Van Miegroet, 1994) and atmospheric N deposition (Johnson and Lindberg, 1992) with increasing elevation in the southern Appalachians. Litter quality varies strongly with altitude and reflects a gradient of forest N status. In addition, although less soil organic matter decomposition is indicated at cool, high-elevation sites, low substrate C:N ratios in these N-rich forests result in more N release (net soil N mineralization) for each unit of C converted to CO2 by soil microorganisms (Garten, 2004a). Current theory suggests there is more soil organic matter remaining at the terminus of decomposition and greater accumulation of forest soil humus when litter inputs have high N concentrations or low C:N ratios (Berg, 2000; Berg and Meentemeyer, 2002). High substrate N concentrations inhibit lignin-degrading enzymes, promote humification, and thereby limit soil organic matter decomposition (Berg, 2000; DeForest et al., 2004). Declining mean annual temperatures and increasing N availability may contribute individually or collectively to greater soil C storage and longer soil C turnover times with increasing altitude. Further studies of soil organic matter decomposition are needed to differentiate mechanisms that underlie the observed trends. At this time, we can only conclude that soil C storage and turnover times increase as one proceeds from warmer, drier, less N rich forests to colder, wetter, more N rich forests. Two sites along the elevation gradient (SB and NG) deviated from the general relationships between elevation and soil C stocks or turnover times (Fig. 4) possibly because of an error in estimated soil C inputs (Ci). Underestimation of Ci at site SB would cause the soil C turnover time to be overestimated. Similarly, overestimation of Ci at site NG would cause soil C turnover time to be underestimated. Given the large basal area at site SB, soil C inputs may be greater than those estimated from the model. Soil C inputs are possibly overestimated at site NG because the measured basal area is

less than that for other forests at the same elevation. The foregoing interpretation is supported by a significant multiple regression of soil C turnover times against elevation and stand basal area. Whenever elevation does not adequately explain existing forest soil C stocks or predicted soil C turnover, stand basal area appears to account for an additional part of the unexplained variance. Results from studies of other forests indicate that fine root biomass is directly associated with tree basal area (Chen et al., 2004) and that aboveground net primary production increases (r = +0.72; P ≤ 0.01) with stand basal area (Bolstad et al., 2001). Although errors in the estimation of Ci are an apparent likely cause of residual variation about the regression of turnover time against elevation (Fig. 4), other factors may also contribute. For example, leaf litter N concentrations were elevated at site SB (Fig. 2) and may contribute to reduced soil organic matter decomposition rates (see Berg, 2000). Other unmeasured edaphic or environmental factors could also cause the deviation of particular study sites from a general relationship between soil C turnover and elevation. Calculations of soil C turnover time using Eq. (1) are dependent on soil depth. In general, 50% of the forest mineral soil C stock (to a 1-m soil depth) is found in the upper 20 cm of mineral soil and 71% is found in the upper 40 cm (Jobbagy and Jackson, 2000). For meaningful crosssite comparisons, C stocks must be normalized for soil depth. We chose a 30-cm soil depth and measurements were not extrapolated to 1-m. The measurements probably include ≈75% or more of the total soil C stock to a 1-m depth because C stocks decline exponentially with depth (Jobbagy and Jackson, 2000) and surface litter layers were included in our measurements of total forest soil C stocks (Cs). Increasing the size of forest soil C stocks (by including additional C below 30-cm) would increase the model estimates of turnover time. Numerous studies (Harrison et al., 1995; Tate et al., 1995; Townsend et al., 1995; Garten et al., 1999; Perruchoud et al., 1999; Six and Jastrow, 2002) indicate that forest soils contain a high proportion of active or decomposable soil C with turnover times in the range of ≈4 to 50 years. Predicted median turnover times (11 to 31 years) for soil C along our elevation gradient reflect a high proportion of active soil C over the selected sampling depth and the influence of labile soil C stocks on surface soil C turnover. The partitioning of C between O-horizons and the mineral soil (Table 2) suggests that the relatively fast soil C turnover times are not simply caused by a preponderance of C in the forest floor. Carbon at greater soil depths may be older, more “protected”, and add to the soil C stock, but not necessarily be more active in the rate of total soil C turnover.

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5. Conclusion Studies of soil C under forests that have been protected from human disturbance for many decades, such as those in the Great Smoky Mountains National Park or on the Oak Ridge Reservation (Table 1), can be used to estimate the turnover time of soil C stocks and associations with elevation or changing environmental factors. For the C pools of interest in this paper, that will likely turnover within years or decades (rather than centuries), these sites can be considered to approximate near steady state conditions with respect to soil C stocks. Having said that, we acknowledge that such stocks may fluctuate around an average pool size in conjunction with temporal trends in weather and other environmental drivers. The three environmental factors that have potentially significant effects on soil C dynamics (temperature, precipitation, and N availability) vary in a predictable manner with altitude in the southern Appalachian Mountains. Past studies along elevation gradients have contributed to a better, but not complete, understanding of how environmental factors or processes potentially affect forest soil C balance. In addition to advantages of convenience and economy, studies along elevation gradients can be a legitimate approach to climate change research when hypotheses are placed in a strong theoretical or mechanistic framework. Most importantly, ecosystem processes and attributes affecting soil C dynamics along elevation gradients reflect the long-term interactions between numerous abiotic and biotic factors such as climate, vegetation, and soil type. Acknowledgements This research was sponsored by the U.S. Department of Energy, Office of Science, Biological and Environmental Research/Terrestrial Carbon Processes Program under contract DE-AC05-00OR22725 with Oak Ridge National Laboratory (ORNL), managed by UT-Battelle, LLC. We wish to thank Bonnie Lu (retired) and Deanne Brice (ORNL) for their valuable technical assistance with laboratory and field aspects of the research. References Berg, B., 2000. Litter decomposition and organic matter turnover in northern forest soils. Forest Ecology and Management 133, 13–22. Berg, B., Meentemeyer, V., 2002. Litter quality in a north European transect versus carbon storage potential. Plant and Soil 242, 83–92. Bolstad, P.V., Vose, J.M., 2001. The effects of terrain position and elevation on soil C in the southern Appalachians. In: Lal, R., Kimble, J.M., Follett, R.F., Stewart, B.A. (Eds.), Assessment Methods for Soil Carbon. Lewis Publishers, Boca Raton, FL, pp. 45–51.

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