Abstract

Examining the responses of root standing crop (biomass and necromass) and chemistry to soil warming is crucial for understanding root dynamics and functioning in the face of global climate change. We assessed the standing crop, total nitrogen (N) and carbon (C) compounds in tree roots and soil net N mineralization over the growing season after 6 years of experimental soil warming in a temperate deciduous forest in 2008. Roots were sorted into four different categories: live and dead fine roots (≤1 mm in diameter) and live and dead coarse roots (1–4 mm in diameter). Total root standing crop (live plus dead) in the top 10 cm of soil in the warmed area was 42.5% (378.4 vs. 658.5 g m−2) lower than in the control area, while live root standing crop in the warmed area was 62% lower than in the control area. Soil net N mineralization over the growing season increased by 79.4% in the warmed relative to the control area. Soil warming did not significantly change the concentrations of C and C compounds (sugar, starch, hemicellulose, cellulose and lignin) in the four root categories. However, total N concentration in the live fine roots in the warmed area was 10.5% (13.7 vs. 12.4 mg g−1) higher and C:N ratio was 8.6% (38.5 vs. 42.1) lower than in the control area. The increase in N concentration in the live fine roots could be attributed to the increase in soil N availability due to soil warming. Net N mineralization was negatively correlated with both live and dead fine roots in the mineral soil that is home to the majority of roots, suggesting that soil warming increases N mineralization, decreases fine root biomass and thus decreases C allocation belowground.

Introduction

Tree roots generally constitute between 15 and 30% of the total tree biomass and consume large portions of annual net primary production in forest ecosystems (Bowden et al. 1993, Janssens et al. 2002, Persson 2002). Since tree roots play a critical role in nutrient and water uptake, carbon (C) and nutrient cycling, storage of carbohydrates and synthesis of growth regulators (Jackson et al. 1997, López et al. 2001), the climate change impact on tree roots may in turn influence the structure and function of entire ecosystems.

Previous studies have found that climate warming can change root function (Pregitzer et al. 2000), dynamics (Hendrick and Pregitzer 1993, Forbes et al. 1997, Fitter et al. 1999, King et al. 1999, Gill and Jackson 2000, Tierney et al. 2003, Majdi and Öhrvik 2004, Wan et al. 2004), morphology, mass and distribution (Björk et al. 2007, Bronson et al. 2008). For example, higher soil temperature increased the root production and mortality associated with soil nitrogen (N) availability (King et al. 1999, Pregitzer et al. 2000, Majdi and Öhrvik 2004). In contrast to root production, root standing crop showed different responses to elevated temperature depending on species, research site and heating methods. In a black spruce plantation, live fine root biomass (<2 mm diameter) in the soil warming plots was decreased by 24–46% (Bronson et al. 2008). Elevated temperature decreased fine root mass of maple trees by 34, 53 and 43% for size classes <0.5, 1.0–2.0 and >2.0 mm (Wan et al. 2004). The root biomass of Agrostis scabra and Agrostis stolonifera grown at elevated temperature decreased by 8 and 15%, respectively (Lyons et al. 2007). Inconsistently with the above studies, it was reported that the fine roots (<4 mm diameter) and total root biomass either increased slightly with increasing temperature (Allen and Vu 2009) or indicated no significant change with temperature (Kandeler et al. 1998).

While changes in root productivity and biomass have been correlated with changes in temperature, another factor also influences root productivity and biomass, that is, soil N availability, which also responds to temperature. Multiple studies have shown that fine root biomass decreases with increasing soil N (Nadelhoffer 2000, Powers et al. 2005, Lee et al. 2007). It has been observed that warming increases the rate of N mineralization in the soil, affecting soil N availability (Peterjohn et al. 1994, Lükewille and Wright 1997, Melillo et al. 2002, 2011, Strömgren and Linder 2002). In a meta-analysis of soil warming experiments, Rustad et al. (2001) found that warming increased net N mineralization rate by 46%. In a decade-long soil warming experiment at the Harvard Forest, Melillo et al. (2002) reported that constant soil warming at 5 °C above ambient resulted in a cumulative increase in N availability of 41 g m−2. Therefore, we expect that root biomass decreases with warming-induced increases in soil N availability. Besides temperature and N availability, soil moisture is also a key factor that has been found to affect root mass (Meier and Leuschner 2008). For example, Dijkstra and Cheng (2007) found that root biomass increased with increased soil moisture content in a European forest. The study observing a decrease in the fine root biomass in the drier stands simultaneously found decreased fine root diameter, which may indicate that fine roots may compensate for the loss in root biomass by increased uptake area or uptake rate (Meier and Leuschner 2008).

In addition to biomass and productivity of fine roots, soil warming will likely affect C and N composition of fine roots. Root tissue chemistry plays a key role in controlling metabolic and decomposition dynamics of roots (McClaugherty et al. 1982, King et al. 2005), regulating soil microbial activity (Zak et al. 2000) and determining C inputs into soil (Brown et al. 2007). Root N concentration has been emphasized more than other chemical compounds because it is significantly correlated with root growth (Valverde-Barrantes et al. 2007), root respiration (Pregitzer et al. 1998, Burton et al. 2002) and potential decomposition dynamics (Hendricks et al. 2000). Increased soil temperatures are linked to increased N concentration of roots due to the kinetic increase in root activities and greater N availability at higher temperature (Zogg et al. 1996, BassiriRad 2000, Wan et al. 2004). A higher root N concentration is required for enzyme synthesis and activity, resulting in more nutrient uptake (Nadelhoffer 2000).

Soluble carbohydrates, holocellulose (hemicellulose and cellulose) and lignin represent three root C pools that are associated with specific root functions. Uselman et al. (2000) found that warmer temperature significantly increased root exudation of organic C. This indicates that warming might alter the C compounds of roots and soil C storage. Furthermore, increased root respiration and root turnover rates due to soil warming might potentially change root C compounds and the relationship between C and N. Burton et al. (2008) reported that root respiration rates increased with rising soil temperatures, consequently leading to decreases in C available for biomass construction. If it is true that fine root turnover rates and soil N availability increase with increased temperature, more C will be consumed in growth and respiration and less will be allocated to structural costs (Nadelhoffer 2000).

Our knowledge in understanding the interactions between root standing crop, soil N mineralization and root chemistry in response to warming is very limited. Here we use an in situ experimental warming to study the effects of soil warming on biomass and necromass of hardwood forest roots with different diameters, and changes in C compounds and N concentration in the four different root fractions, including live fine roots (≤1 mm in diameter), live coarse roots (1–4 mm in diameter), dead fine roots and dead coarse roots. We also examine the relationships between changes in fine roots, N availability, soil temperature and moisture. We hypothesize that (i) soil warming decreases root standing crop; (ii) soil N mineralization is negatively correlated with root mass; and (iii) the N concentration in roots is increased mainly due to increased soil N availability.

Materials and methods

Site description

The study was conducted in a warmed area and an adjacent control area, each 30 × 30 m, established in 2002 with heating commencing in May 2003 in the Barre Woods tract of Harvard Forest, Petersham, MA, USA (Melillo et al. 2011). The highest mean weekly air temperature is ∼20 °C and occurs in July, and the lowest, approximately −6 °C, occurs in January. Average annual precipitation is ∼1080 mm (Melillo et al. 2002). Each area is divided into 5 × 5 m subplots. The soil is warmed by resistance heating cables buried at a 10 cm depth and spaced 20 cm apart. The soil temperature in the warmed area is maintained at 5 °C above the adjacent control area. For a detailed description of the soil warming system, see Melillo et al. (2002, 2004). The study areas are within a mixed hardwood stand dominated by Quercus rubra and Acer rubrum, with lesser components of Quercus velutina and Fraxinus americana. The majority of trees in the study area have naturally regenerated after a major hurricane in 1938. The average tree diameter at breast height was 19.3 cm and the stand had a basal area of ∼31 m2 ha−1 in 2008.

This larger warming experiment (30 × 30 m) follows an earlier warming experiment established in 1991 in the Harvard Forest with multiple small (6 × 6 m) warmed plots, disturbance control plots (with buried cables but no warming) and undisturbed control plots (no buried cable, no warming) (Melillo et al. 2002). Results from the smaller warming experiment indicated that soil disturbance caused by the installation of heating cables had no significant effects on soil temperatures and only minor and insignificant impacts on soil moisture, shrub growth and N mineralization. This larger warming experiment has an advantage over the previous smaller one in that the plot can be large enough to include all roots from trees inside the warmed area. Due to the high installation and maintenance costs of this large-scale warming experiment, we do not have replicate areas or disturbance control areas. However, we made pre-treatment measurements in the present warmed and control areas in 2002, and found that there were no significant differences in tree characteristics and key soil processes between the two areas such as tree biomass, woody increment, stand basal area, species composition, soil respiration and N mineralization rates. The soil temperature at 5 cm depth measured during the sampling period is shown in Figure 1, indicating a consistent increase in soil temperature in the warmed area. For the 2008 growing season, the average gravimetric soil moisture in the organic layer was 56% in the heated and 66% in the control horizon. However, in the mineral horizon, the soil moisture was 36% in the heated and 37% in the control areas.

Figure 1.

Averaged daily soil temperature in the warmed and control areas from April to November 2008. The data from April to July were recorded every 6 h. After July, the data were collected hourly.

Figure 1.

Averaged daily soil temperature in the warmed and control areas from April to November 2008. The data from April to July were recorded every 6 h. After July, the data were collected hourly.

Separation and classification of roots

Soil cores were collected six times at approximately monthly intervals during the growing season from April to November 2008 (29 April, 27 May, 25 June, 28 July, 2 September and 4 November) from eight subplots within the warmed area and nine subplots within the control area. Soil cores of 10 cm diameter were taken to a 10 cm depth to cover the most active tree roots in the organic layers and upper mineral layers. The average organic layer depth was 1.4 cm, so the average depth of mineral soil layer sampled in each core was 8.6 cm. Gravimetric moisture content was measured for each soil core. The average bulk density was 0.373 g cm−3 in the organic layer and 0.781 g cm−3 in the mineral layer. After weighing, deionized water was put in each bag, and the bags were stored between 0 and 4 °C until sorting.

We used a 1 mm diameter threshold to define fine roots (≤1 mm) and coarse roots (1–4 mm). Only a small amount of root material was over 3 mm in diameter and roots >4 mm in diameter were not found in this study. Root diameter was measured using a digital caliper. The soil was put into a small tub with some water and roots were separated from the soil with forceps. By frequently changing water and rinsing, we were able to pick up almost all of the roots by hand. When small roots were connected to a larger root, they were cut out and separated into different size classes.

Fine roots and coarse roots were separated into live and dead categories based on visible morphological characteristics, mainly color and strength. Detailed information on how to judge live roots and dead roots has been described in the literature (Vogt and Persson 1991, Matamala and Schlesinger 2000, John et al. 2002, Persson and Stadenberg 2009). Roots from different tree species were not distinguished, but herbaceous roots were excluded. Herbaceous roots are white, light and succulent, while tree roots are slightly brown or yellow and well branched. After sorting, live and dead roots of different size classes were dried at 60 °C for at least 48 h and then weighed.

Chemical measurements

Since the amount of root material in each sample class was too small for chemical analysis, we pooled roots from all subplots after sorting and weighing. This gave us monthly chemical composition data of four categories (live fine roots, live coarse roots, dead fine roots and dead coarse roots) from each area.

Root samples were analyzed for total soluble sugars, starch, hemicellulose, cellulose, lignin, total C and total N. Total C and N were determined by combustion in a CHN analyzer (PerkinElmer 2400 Series, Waltham, MA, USA). The concentrations of the C compounds were measured in a sequential extraction process by the anthrone–sulfuric acid method (Gao 2006). Samples submerged in deionized water were extracted in a boiling water bath twice. The supernatant was used to analyze the concentration of total soluble sugars, and then the residues were extracted with hot deionized water and hydrolyzed with perchloric acid to determine starch concentration. After sugars and starch were removed, the residues were hydrolyzed with hydrochloric acid for 3 h in a boiling water bath to analyze hemicellulose concentration. The residues in the extraction tubes were washed twice with ethanol and acetone to remove lipids and pigments. Then the residues were dried and digested with concentrated sulfuric acid in a boiling water bath for 5 h to determine cellulose concentration. All final reducing sugar was measured colorimetrically using the anthrone–ethyl acetate method with a spectrophotometer at 630 nm (Shimadzu UV-1201, Shimadzu Scientific Instruments, Columbia, MD, USA). Lignin, an acid-insoluble structural component, was assessed by the weight difference.

N mineralization

We measured net N mineralization rates using the standard in situ buried bag method (Eno 1960) approximately every 5 weeks from April through November 2008. We took two 10 cm deep soil cores from each of the 10 subplots per treatment during each sampling period. We designated one core as the ‘initial’ sample, which was split into organic and mineral horizons, and each horizon was transported to the laboratory for analysis. The second core, designated as the ‘final’ sample, was placed intact inside a gas-permeable polyethylene bag and positioned back in the ground. The ‘final’ bags were incubated during April–November and then transported to the lab for analysis.

In the laboratory, soils were separated into organic and mineral layers and sieved through a 5.6 mm screen to remove rocks and roots. Approximately 10 g of soil was placed in 100 ml of 2 M KCl, incubated for 36 h and filtered. The extracts were analyzed for nitrite/nitrate (NO2/NO3-N) and ammonium (NH4+-N) using a Lachat QuikChem FIA+ 8000 Series Flow Injection Analyzer with Omnion 3.0 software (Lachat Instruments Inc., Loveland, CO, USA). Using these techniques, the detection limit for NO2/NO3-N was 0.02 mg l−1 and the detection limit for NH4+-N was 0.005 mg l−1

Statistical analyses

The statistical analysis was conducted with SPSS 13.0 (SPSS Inc., Chicago, IL, USA). The effects of soil temperature, soil depth and sample dates on root mass were tested using three-way analysis of variance (ANOVA). The effect of soil temperature on the ratio of biomass to necromass from different soil fractions was analyzed using a one-way ANOVA. We used paired-sample t-tests to analyze the difference in total N, total C and all C compounds between warming and control areas. We conducted Spearman's correlation between root mass, net mineralization and soil moisture data across each sample location after these data were averaged over the growing season.

Results

Changes in root mass

Warming decreased live plus dead root mass in the upper 10 cm of soil compared with the control (Tables 1 and 2). Significant decreases in both live and dead root mass between warmed and control areas were confined to the mineral soil (P < 0.001) (Table 1). No significant seasonal change in total root mass and four root categories was found from April to November (Table 2, Figure 2).

Figure 2.

Monthly root mass of (a) live fine roots, (b) live coarse roots, (c) dead fine roots and (d) dead coarse roots in the organic and upper mineral layers in the warmed and control areas from April to November 2008 (mean values ± SE) (n = 8). WO, organic layer in the warmed area; WM, mineral layer in the warmed area; CO, organic layer in the control area; CM, mineral layer in the control area.

Figure 2.

Monthly root mass of (a) live fine roots, (b) live coarse roots, (c) dead fine roots and (d) dead coarse roots in the organic and upper mineral layers in the warmed and control areas from April to November 2008 (mean values ± SE) (n = 8). WO, organic layer in the warmed area; WM, mineral layer in the warmed area; CO, organic layer in the control area; CM, mineral layer in the control area.

Table 1.

Averaged mass of live fine roots (LF), live coarse roots (LC), dead fine roots (DF) and dead coarse roots (DC) in the organic layer, upper mineral layer and the organic plus upper mineral layer in the warmed and control plots across all sample dates (mean values ± SE) (g m−2) (n = 8).

Soil layer Treatment LF LC DF DC 
Organic (O) Warming 22.7 ± 3.8 10.2 ± 3.7 36.7 ± 3.2 19.0 ± 8.8 
 Control 25.7 ± 3.2 20.3 ± 5.5 37.0 ± 4.6 5.3 ± 1.6 
Mineral (M) Warming 56.2 ± 7.6 43.8 ± 18.9 123.2 ± 9.6 61.3 ± 9.1 
 Control 188.0 ± 22.1 121.0 ± 30.6 172.0 ± 10.6 91.0 ± 16.7 
O + M Warming 80.9 ± 10.5 55.2 ± 16.7 161.2 ± 5.0 81.1 ± 8.3 
 Control 212.2 ± 21.8 141.8 ± 12.9 208.6 ± 15.1 96.0 ± 19.5 
Soil layer Treatment LF LC DF DC 
Organic (O) Warming 22.7 ± 3.8 10.2 ± 3.7 36.7 ± 3.2 19.0 ± 8.8 
 Control 25.7 ± 3.2 20.3 ± 5.5 37.0 ± 4.6 5.3 ± 1.6 
Mineral (M) Warming 56.2 ± 7.6 43.8 ± 18.9 123.2 ± 9.6 61.3 ± 9.1 
 Control 188.0 ± 22.1 121.0 ± 30.6 172.0 ± 10.6 91.0 ± 16.7 
O + M Warming 80.9 ± 10.5 55.2 ± 16.7 161.2 ± 5.0 81.1 ± 8.3 
 Control 212.2 ± 21.8 141.8 ± 12.9 208.6 ± 15.1 96.0 ± 19.5 
Table 2.

Statistical results (F and P values are given) of the effects of soil warming (T), sample dates (M), soil layers (SL) and their interactions on total root mass, live fine roots (LF), live coarse roots (LC), dead fine roots (DF), dead coarse roots (DC) mass and net N mineralization.

 Total mass
 
LF
 
LC
 
DF
 
DC
 
N mineralization
 
 F P F P F P F P F P F P 
Treatment (T) 13.391 <0.001 20.196 <0.001 3.657 0.058 7.119 0.008 0.394 0.531 6.934 0.012 
Soil layer (SL) 77.085 <0.001 43.185 <0.001 8.672 0.004 153.304 <0.001 28.699 <0.001 35.948 <0.001 
Month (M) 0.479 0.792 1.105 0.360 0.192 0.965 1.154 0.335 0.906 0.479 13.277 <0.001 
T × SL 14.449 <0.001 19.489 <0.001 2.286 0.133 7.762 0.006 3.464 0.065 3.495 0.070 
T × M 0.133 0.984 0.297 0.914 0.255 0.937 0.503 0.774 0.708 0.618 1.052 0.395 
SL × M 0.476 0.794 0.595 0.704 0.330 0.894 0.996 0.422 1.438 0.214 7.028 <0.001 
T × SL × M 0.109 0.990 0.183 0.969 0.361 0.875 0.433 0.825 0.563 0.728 0.866 0.534 
 Total mass
 
LF
 
LC
 
DF
 
DC
 
N mineralization
 
 F P F P F P F P F P F P 
Treatment (T) 13.391 <0.001 20.196 <0.001 3.657 0.058 7.119 0.008 0.394 0.531 6.934 0.012 
Soil layer (SL) 77.085 <0.001 43.185 <0.001 8.672 0.004 153.304 <0.001 28.699 <0.001 35.948 <0.001 
Month (M) 0.479 0.792 1.105 0.360 0.192 0.965 1.154 0.335 0.906 0.479 13.277 <0.001 
T × SL 14.449 <0.001 19.489 <0.001 2.286 0.133 7.762 0.006 3.464 0.065 3.495 0.070 
T × M 0.133 0.984 0.297 0.914 0.255 0.937 0.503 0.774 0.708 0.618 1.052 0.395 
SL × M 0.476 0.794 0.595 0.704 0.330 0.894 0.996 0.422 1.438 0.214 7.028 <0.001 
T × SL × M 0.109 0.990 0.183 0.969 0.361 0.875 0.433 0.825 0.563 0.728 0.866 0.534 

Significant differences (P < 0.05) are highlighted in bold.

Live root mass

Relative to the control, soil warming resulted in a significant decrease in live root biomass, with a 61.9% decline in fine root biomass and a 61.1% decrease in coarse root biomass (Table 1).

Dead root mass

The necromass in the warmed area was significantly lower than in the control area (242.3 vs. 304.6 g m−2) (Table 1). The fine root necromass in the warmed area was 22.7% lower than in the control area. Coarse root necromass was not significantly affected by soil warming (Table 2).

Ratio of live to dead fine roots

When we aggregated all live roots into one pool and dead roots into another (regardless of root diameter) and examined the ratios of live to dead roots, soil warming led to significantly lower ratios in the organic layer, mineral layer, and organic plus mineral layer relative to the control (Table 3). No significant differences were found in the ratios of root biomass to necromass of fine roots in the organic layer, but there was a trend toward a decreased ratio in the warmed area relative to the control (Table 3). Soil warming significantly decreased the ratios of fine root biomass to necromass by 61.5% in the mineral soil and 50.0% in the organic plus mineral soil relative to the control area (Table 3). The ratio of coarse root biomass to necromass was not significantly affected by higher soil temperature.

Table 3.

Ratios of fine root biomass to fine root necromass (FB:FN), coarse root biomass to coarse root necromass (CB:CN) and total biomass to total necromass (TB:TN) in the organic layer, upper mineral layer and the organic plus upper mineral layer for both warming and control plots across all sampling dates (mean value ± SE) (n = 8).

Soil layer Treatment FB:FN CB:CN TB:TN 
Organic Warming 0.7 ± 0.1 2.4 ± 2.8 0.7 ± 0.8 
 Control 1.0 ± 0.2 4.2 ± 5.0 1.5 ± 1.9 
 P value 0.063 0.294 0.015 
Mineral Warming 0.5 ± 0.1 0.5 ± 0.6 0.6 ± 0.9 
 Control 1.3 ± 0.2 2.5 ± 1.5 1.5 ± 1.5 
 P value 0.001 0.248 0.002 
O + M Warming 0.6 ± 0.2 1.4 ± 1.3 0.7 ± 0.3 
 Control 1.2 ± 0.4 3.4 ± 3.2 1.5 ± 0.3 
 P value 0.008 0.191 0.032 
Soil layer Treatment FB:FN CB:CN TB:TN 
Organic Warming 0.7 ± 0.1 2.4 ± 2.8 0.7 ± 0.8 
 Control 1.0 ± 0.2 4.2 ± 5.0 1.5 ± 1.9 
 P value 0.063 0.294 0.015 
Mineral Warming 0.5 ± 0.1 0.5 ± 0.6 0.6 ± 0.9 
 Control 1.3 ± 0.2 2.5 ± 1.5 1.5 ± 1.5 
 P value 0.001 0.248 0.002 
O + M Warming 0.6 ± 0.2 1.4 ± 1.3 0.7 ± 0.3 
 Control 1.2 ± 0.4 3.4 ± 3.2 1.5 ± 0.3 
 P value 0.008 0.191 0.032 

Significant differences (P < 0.05) are highlighted in bold.

Changes in C and N

Soil warming significantly increased the total N concentration in live fine roots by 10.5% (13.7 vs. 12.4 mg g−1) compared with the control area (P < 0.05, Table 4). With no change in C concentration, this led to a significant decline in C:N ratio (−8.6%) (38.5 vs. 42.1) (P < 0.05, Table 4) since there was no significant difference in total C concentration in live fine roots between the warmed and control areas. There were no significant effects of soil warming on total N concentration and C:N ratio in the other root classes.

Table 4.

Concentrations of total N, total C and C compounds in the live fine, live coarse, dead fine and dead coarse roots from the warmed and control plots. Data were averaged across all sample dates with one standard error. Different letters (a and b) of total N and C:N indicate significant differences at the 0.05 level between the warmed and control plots (mean values ± SE).

Treatment Root category Total C (mg g−1Total N (mg g−1C:N Sugars (mg g−1Starch (mg g−1Hemicellulose (mg g−1Cellulose (mg g−1Lignin (mg g−1
Warming Live fine roots 449.3 ± 6.1 13.7 ± 0. 3a 38.5 ± 1.2a 49.9 ± 4.6 52.4 ± 4.5 9.0 ± 1.5 87.4 ± 3.7 222.9 ± 16.3 
 Live coarse roots 474.5 ± 4.2 6.1 ± 0.3 91.7 ± 5.0 64.8 ± 9.6 61.3 ± 7.1 6.8 ± 1.8 168.5 ± 4.1 173.4 ± 16.8 
 Dead fine roots 431.4 ± 6.6 11.2 ± 0.3 45.2 ± 0.7 36.1 ± 4.1 40.4 ± 4.5 4.6 ± 0.4 54.4 ± 2.2 277.8 ± 31.4 
 Dead coarse roots 455.2 ± 8.6 8.6 ± 0.5 63.0 ± 3.6 36.1 ± 4.5 42.7 ± 4.7 6.2 ± 0.9 95.5 ± 12.4 227.7 ± 24.2 
Control Live fine roots 444.4 ± 4.8 12.4 ± 0.2b 42.1 ± 1.13b 52.5 ± 4.4 51.7 ± 4.6 7.8 ± 1.2 86.8 ± 5.1 203.8 ± 9.4 
 Live coarse roots 469.8 ± 5.4 6.8 ± 0.5 83.6 ± 7.4 67.6 ± 5.5 60.6 ± 4.2 9.3 ± 1.6 164. 3 ± 6.6 140.2 ± 17.9 
 Dead fine roots 425.1 ± 7.2 11.4 ± 0.2 43.6 ± 0.5 37.3 ± 3.1 44.7 ± 4.4 4.7 ± 0.4 62. 6 ± 4.0 282.0 ± 20.5 
 Dead coarse roots 451.4 ± 5.5 8.0 ± 0.9 69.4 ± 7.0 38.6 ± 4.5 46.7 ± 5.2 5.8 ± 0.8 103.5 ± 14.9 218.4 ± 29.7 
Treatment Root category Total C (mg g−1Total N (mg g−1C:N Sugars (mg g−1Starch (mg g−1Hemicellulose (mg g−1Cellulose (mg g−1Lignin (mg g−1
Warming Live fine roots 449.3 ± 6.1 13.7 ± 0. 3a 38.5 ± 1.2a 49.9 ± 4.6 52.4 ± 4.5 9.0 ± 1.5 87.4 ± 3.7 222.9 ± 16.3 
 Live coarse roots 474.5 ± 4.2 6.1 ± 0.3 91.7 ± 5.0 64.8 ± 9.6 61.3 ± 7.1 6.8 ± 1.8 168.5 ± 4.1 173.4 ± 16.8 
 Dead fine roots 431.4 ± 6.6 11.2 ± 0.3 45.2 ± 0.7 36.1 ± 4.1 40.4 ± 4.5 4.6 ± 0.4 54.4 ± 2.2 277.8 ± 31.4 
 Dead coarse roots 455.2 ± 8.6 8.6 ± 0.5 63.0 ± 3.6 36.1 ± 4.5 42.7 ± 4.7 6.2 ± 0.9 95.5 ± 12.4 227.7 ± 24.2 
Control Live fine roots 444.4 ± 4.8 12.4 ± 0.2b 42.1 ± 1.13b 52.5 ± 4.4 51.7 ± 4.6 7.8 ± 1.2 86.8 ± 5.1 203.8 ± 9.4 
 Live coarse roots 469.8 ± 5.4 6.8 ± 0.5 83.6 ± 7.4 67.6 ± 5.5 60.6 ± 4.2 9.3 ± 1.6 164. 3 ± 6.6 140.2 ± 17.9 
 Dead fine roots 425.1 ± 7.2 11.4 ± 0.2 43.6 ± 0.5 37.3 ± 3.1 44.7 ± 4.4 4.7 ± 0.4 62. 6 ± 4.0 282.0 ± 20.5 
 Dead coarse roots 451.4 ± 5.5 8.0 ± 0.9 69.4 ± 7.0 38.6 ± 4.5 46.7 ± 5.2 5.8 ± 0.8 103.5 ± 14.9 218.4 ± 29.7 

There were no significant differences in the concentration of total C or any of the C compounds analyzed in four root categories in the warmed area compared with the corresponding chemistry observed in the control area (P > 0.05). Although soil warming resulted in lower concentrations of total soluble sugars in four different root categories and higher starch concentrations in live roots compared with control, the differences were not statistically significant. The total non-structural carbohydrate content (the sum of soluble sugars and starch) of live roots, especially live coarse roots, was significantly higher than that of dead roots, regardless of treatment (Table 4). Since the absolute concentration of hemicellulose in roots was very low (<10 mg g−1) and hemicellulose and cellulose have similar structure, we combined hemicellulose and cellulose. The holocellulose (hemicellulose plus cellulose) concentrations in live roots in the warmed area were very close to those in the control area. However, soil warming resulted in a decreased trend in holocellulose concentration in dead roots relative to the control. Soil warming caused a slight increase in lignin concentration in live fine, live coarse and dead coarse roots compared with the control area, although the difference was not statistically significant.

Soil N mineralization

Soil net N mineralization showed pronounced seasonal patterns during the sampling period in both warmed and control areas, with highest values in July and lowest values in November (Table 2, Figure 3). Net N mineralization was also affected by warming treatment and soil layer (Table 2, Figure 3). Net N mineralization in the upper mineral soil was over four times higher than that in the organic layer for both warmed and control areas from April to November. Soil warming increased soil net N mineralization by 60.9% (13.3 vs. 8.3 kg N ha−1) in the organic layer, by 83.7% (65.2 vs. 35.5 kg N ha−1) in the mineral layer and by 79.4% (78.5 vs. 43.7 kg N ha−1) in the organic plus upper mineral layer compared with the control area.

Figure 3.

Seasonal change in net N mineralization in the organic layer, upper mineral layer and the organic plus upper mineral layer for both warmed and control areas from April to November 2008 (mean values ± SE) (n = 10). WO, organic layer in the warmed area; WM, mineral layer in the warmed area; CO, organic layer in the control area; CM, mineral layer in the control area.

Figure 3.

Seasonal change in net N mineralization in the organic layer, upper mineral layer and the organic plus upper mineral layer for both warmed and control areas from April to November 2008 (mean values ± SE) (n = 10). WO, organic layer in the warmed area; WM, mineral layer in the warmed area; CO, organic layer in the control area; CM, mineral layer in the control area.

Relationship between soil N mineralization, root mass, soil temperature and moisture

Soil net N mineralization was significantly correlated (negatively) with both fine root biomass (P = 0.0018, correlation coefficient =  − 0.70) and fine root necromass (P = 0.0093, correlation coefficient =  − 0.61) in the mineral soil that is home to the majority of root mass. In the mineral soil, moisture was significantly correlated with fine root necromass (P = 0.0467, correlation coefficient = 0.49), but not with other root categories. The soil net N mineralization in the warmed and control areas was linearly correlated with soil temperature, and the slope of net mineralization against temperature was higher in the warmed area than in the control area (Figure 4).

Figure 4.

Linear relationship of net N mineralization to soil temperature in the warmed and control areas (n = 8).

Figure 4.

Linear relationship of net N mineralization to soil temperature in the warmed and control areas (n = 8).

Discussion

Effects of warming on root mass and net N mineralization

Fine roots (≤1 mm) made up the majority of the root biomass in the heated and control areas to a depth of 10 cm. We did not find any roots >4 mm in diameter due to the shallow depth of our sampling. Our results indicate that soil warming does not alter seasonal patterns of root biomass and necromass.

The root mass in this study is within the range of global estimations of root mass in other forest ecosystems. Jackson et al. (1997) estimated that the average total and live fine root (≤2 mm in diameter) mass in the upper 30 cm of soil of global temperate deciduous forest were 780 and 440 g m−2. The two values are a little higher than the values in the control area (658.5 and 354.0 g m−2) because the sampling depth was only 10 cm in our study. However, the percentage of live roots to total root mass is similar, 56% for global average and 54% in the control area. In the warmed area, the absolute values of total and live fine roots and the percentage of live roots are significantly lower than the average global values or our control. Soil warming resulted in a >60% decrease in fine root or coarse root biomass, while fine root and coarse root necromass decreased by <23%, consistent with previous research (Bronson et al. 2008).

Results from our study support the first hypothesis that soil warming leads to a decrease in root standing crop, but the decline is probably not the direct effect of elevated soil temperature. Correlation analysis shows that decreased fine root mass is mainly attributed to the increase in soil N mineralization rates and thus soil N availability, and therefore supports our second hypothesis. The C allocation theory indicates that plants maximize growth rates by partitioning C to optimize the capture of limiting resources (Tilman 1988, Cannell and Dewar 1994, McConnaughay and Coleman 1999). When soil N availability is increased by warming, the demand for C allocation to roots decreases, leading to a decline in fine roots, the functional tissue for N uptake. Here we used net N mineralization rates to indicate soil N availability, but we acknowledge that plant roots and associated mycorrhizal fungi may directly use organic N such as amino acid (Schimel and Bennett 2004). Given the difficulty in directly measuring total N availability, N mineralization remains a useful index to indicate N availability (Schimel and Bennett 2004). In addition, the seasonal pattern of soil N mineralization in the warmed and control areas is positively correlated with soil temperature, which is consistent with many previous publications (Hill and Shackleton 1989, Tietema and Verstraten 1992, Zak et al. 1999, Rustad et al. 2001, Strömgren and Linder 2002, Owen et al. 2003, Pajuste and Frey 2003) and this research site at Harvard Forest (Melillo et al. 2002, 2011).

Compared with N availability changed by soil warming, soil moisture does not strongly affect live fine root mass. Although gravimetric soil moisture was lower in the organic horizon in the warmed area compared with the control (56% in the warmed area vs. 66% in the control), there was little difference between the soil moisture measured in the upper mineral horizon in the warmed and control areas (36 and 37%, respectively). Since significant decreases in live and dead root mass between warmed and control areas were confined to the mineral soil, we have concluded that the warming-induced change in soil moisture had little effect on root mass in this temperate forest with an average annual precipitation of 1080 mm. However, it has been found in other studies that root mass decreases with soil water availability (Cavelier et al. 1999, Vanguelova et al. 2005, Metcalfe et al. 2008).

The ratio of live to dead root mass is considered a useful index of root turnover (Persson and Stadenberg 2009). The biomass:necromass ratio of fine roots has been reported to be 0.4–3.0 in a beech and Norway spruce stand (Stober et al. 2000), 1.4–2.2 in a coniferous forest (Persson and Stadenberg 2009) and 0.3–2.9 collected from various natural stands (Persson 2000). In the present study, we found that the biomass:necromass ratio of fine roots ranged from 1.0 to 1.3 in the control area and from 0.5 to 0.7 in the warmed area, within the range of previous studies. If the low biomass:necromass ratio indicates reduced fine root longevity (Leuschner et al. 2004, Persson and Stadenberg 2009), the significant decrease in the biomass:necromass ratio in the warmed area implies that fine roots at elevated temperature have a higher turnover rate relative to the control. As expected, we also found that the biomass:necromass ratios of fine roots were lower than those of coarse roots for both warming and control areas, since coarse roots have a longer life span or a lower turnover rate (Gill and Jackson 2000, Gill et al. 2002, King et al. 2002).

Effects of warming on root chemistry

The most pronounced changes in the chemical composition of roots in the warmed area are the increased N concentration and the decreased C:N ratio in the live fine roots. It has been observed in some forests that fine root N concentration increases with increased soil N availability (Majdi and Rosengren-Brinck 1994, Zogg et al. 1996, Högberg et al. 1998, Burton et al. 2000). In addition to inorganic N, trees also have the capability to directly take up organic N such as amino acid (Schimel and Bennett 2004, Finzi and Berthrong 2005). If warming stimulates root activity, we reason that organic N uptake via live fine roots will be increased. Thus, our third hypothesis is supported only for live fine roots.

In contrast to N, total C of roots was not significantly changed with soil warming. The ratio of C:N is an important predictor of root longevity or decomposition rates (Müller et al. 1988, Entry et al. 1998, Hishi and Takeda 2005, Withington et al. 2006). In the current study, only the C:N ratio of live fine roots was decreased by soil warming (−8.6%) compared with the control area due to the significant increases in total N and no change in total C. The decrease in C:N ratios with warming, indicating an increase in root mortality (Withington et al. 2006), is consistent with our earlier discussion that soil warming decreases root longevity based on the biomass:necromass ratio. The C:N ratios found in our study are between 38 and 92, a range consistent with previously published values. For example, Jackson et al. (1997) reported that the global average is 42 for live roots <2 mm in diameter. The C:N ratio is 22–32 in tropical tree species (Valverde-Barrantes et al. 2007). Gordon and Jackson (2000) found that the C:N was 43 in live roots <2 mm in diameter and 79 in live roots 2–5 mm in diameter by analyzing 56 published studies. Relatively higher C and lower N concentrations in coarse roots resulted in higher C:N ratios (63 in dead coarse roots and 92 in live coarse roots) in our study. In the control area, we found no difference in the C:N ratio of live and dead fine roots, which is consistent with the results of Valverde-Barrantes et al. (2007).

There are no significant changes in non-structural and structural C concentrations of roots due to soil warming. Thus, the lack of change in chemical composition of roots suggests that the intrinsic decomposition rate of dead roots may not be affected by warming. However, kinetic theory indicates that higher soil temperature increases the decomposition rate as an external driver (Fierer et al. 2005, Davidson and Janssens 2006). A confirmed conclusion on temperature sensitivity of root decomposition in response to warming cannot be reached by our study since soil moisture, C availability, microbial community and other conditions may also influence temperature sensitivity of decomposition (Tang et al. 2005, Tang and Baldocchi 2005, Davidson and Janssens 2006).

Long-term soil warming experiments show that soil respiration increases over the first few years of soil warming, and then the stimulatory effect decreases due to the decrease in the labile soil C pool or microbial acclimation to warming (Luo et al. 2001, Melillo et al. 2002). Our results of an ∼40% decline in root standing crop and previous reports of decreased root metabolic capacity (Burton et al. 2008) due to soil warming suggest that the contribution of root respiration to total soil respiration decreases in response to warming. To understand the mechanisms underlying the belowground dynamics in response to warming, root respiration, root production and turnover, microbial decomposition using various pools of C, and microbial community composition should be further studied. Future soil warming experiments could involve manipulation of soil moisture as well because these two environmental factors are so closely related.

Funding

This study was funded by the US National Science Foundation (NSF-AGS-1005663) and the Marine Biological Laboratory (to J.T.), China Scholarship Council (to Y.Z.), Harvard Forest Long Term Ecological Research (NSF-DEB-0620443) and the National Institute for Climate Change Research (DOE-DE-FCO2-06-ER64157) (to J.M.M.).

Acknowledgments

We would like to express special gratitude to Matthew Erickson for the help in using the CHN analyzer and to Don Burnette for lab work. We thank Lifen Jiang and Junqiang Zheng for the suggestion of statistical analysis. We also thank Rose Smith and Lindsay Scott for revising the final version of the manuscript.

References

Allen
L.H.
Vu
J.C.V.
2009
.
Carbon dioxide and high temperature effects on growth of young orange trees in a humid, subtropical environment
.
Argic. For. Meteorol
 .
149
:
820
830
.
BassiriRad
H.
2000
.
Kinetics of nutrient uptake by roots: responses to global change
.
New Phytol
 .
147
:
155
169
.
Björk
R.G.
Majdi
H.
Klemedtsson
L.
Lewis-Jonsson
L.
Molau
U.
2007
.
Long-term warming effects on root morphology, root mass distribution, and microbial activity in two dry tundra plant communities in northern Sweden
.
New Phytol
 .
176
:
862
873
.
Bowden
R.D.
Nadelhoffer
K.J.
Boone
R.D.
Melillo
J.M.
;Garrison
J.B.
1993
.
Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest
.
Can. J. For. Res
 .
23
:
1402
1407
.
Bronson
D.R.
Gower
S.T.
Tanner
M.
Linder
S.
Herk
I.V.
2008
.
Response of soil surface CO2 flux in a boreal forest to ecosystem warming. Glob
.
Change Biol
 .
14
:
856
867
.
Brown
A.L.P.
Day
F.P.
Hungate
B.A.
Drake
B.G.
Hinkle
C.R.
2007
.
Root biomass and nutrient dynamics in a scrub-oak ecosystem under the influence of elevated atmospheric CO2
.
Plant Soil
 
292
:
219
232
.
Burton
A.J.
Pregitzer
K.S.
Hendrick
R.L.
2000
.
Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests
.
Oecologia
 
125
:
389
399
.
Burton
A.J.
Pregitzer
K.S.
Ruess
R.W.
Hendrick
R.L.
Allen
M.F.
2002
.
Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes
.
Oecologia
 
131
:
559
568
.
Burton
A.J.
Melillo
J.M.
Frey
S.D.
2008
.
Adjustment of forest ecosystem root respiration as temperature warms
.
J. Integr. Plant Biol
 .
50
:
1467
1483
.
Cannell
M.G.R.
Dewar
R.C.
1994
.
Carbon allocation in trees—a review of concepts for modeling
.
Adv. Ecol. Res.
 
25
:
59
104
.
Cavelier
J.
Wright
S.J.
Santamaría
J.
1999
.
Effects of irrigation on litterfall, fine root biomass and production in a semideciduous lowland forest in Panama
.
Plant Soil
 
211
:
207
213
.
Davidson
E.A.
Janssens
I.A.
2006
.
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
.
Nature
 
440
:
165
173
.
Dijkstra
F.A.
Cheng
W.
2007
.
Moisture modulates rhizosphere effects on C decomposition in two different soil types
.
Soil Biol. Biochem
 .
39
:
2264
2274
.
Eno
C.F.
1960
.
Nitrate production in the field by incubating the soil in polyethylene bags
.
Soil Sci. Soc. Am. Proc
 .
24
:
277
279
.
Entry
J.A.
Runion
G.B.
Prior
S.A.
Mitchell
R.J.
Rogers
H.H.
1998
.
Influence of CO2 enrichment and nitrogen fertilization on tissue chemistry and carbon allocation in longleaf pine seedlings
.
Plant Soil
 
200
:
3
11
.
Fierer
N.
Craine
J.M.
McLauchlan
K.
Schimel
J.
2005
.
Litter quality and the temperature sensitivity of decomposition
.
Ecology
 
86
:
320
326
.
Finzi
A.C.
Berthrong
S.T.
2005
.
The uptake of amino acids by microbes and trees in three cold-temperature forests
.
Ecology
 
86
:
3345
3353
.
Fitter
A.H.
Self
G.K.
Brown
T.K.
Bogie
D.S.
Graves
J.D.
Benham
D.
Ineson
P.
1999
.
Root production and turnover in an upland grassland subjected to artificial soil warming respond to radiation flux and nutrients, not temperature
.
Oecologia
 
120
:
575
581
.
Forbes
P.J.
Black
K.E.
Hooker
J.E.
1997
.
Temperature-induced alteration to root longevity in Lolium perenne
.
Plant Soil
 
190
:
87
90
.
Gao
J.F.
2006
.
Experimental guidance for plant physiology
.
Higher Education Press
,
Beijing
, pp
144
148
.
Gill
R.A.
Jackson
R.B.
2000
.
Global pattern of root turnover for terrestrial ecosystems
.
New Phytol
 .
147
:
13
31
.
Gill
R.A.
Burke
I.C.
Lauenroth
W.K.
Milchunas
D.G.
2002
.
Longevity and turnover of roots in the shortgrass steppe: influence of diameter and depth
.
Plant Ecol
 .
159
:
241
251
.
Gordon
W.S.
Jackson
R.B.
2000
.
Nutrient concentration in fine roots
.
Ecology
 
81
:
275
280
.
Hendrick
R.L.
Pregitzer
K.S.
1993
.
Patterns of fine root mortality in two sugar maple forest
.
Nature
 
361
:
59
61
.
Hendricks
J.J.
Aber
J.D.
Nadelhoffer
K.J.
Hallett
R.D.
2000
.
Nitrogen controls on fine root substrate quality in temperate forest ecosystems
.
Ecosystems
 
3
:
57
69
.
Hill
A.R.
Shackleton
M.
1989
.
Soil N mineralization and nitrification in relation to nitrogen solution chemistry in a small forested watershed
.
Biogeochemistry
 
8
:
167
184
.
Hishi
T.
Takeda
H.
2005
.
Dynamics of heterorhizic root systems: protoxylem groups within the fine-root system of Chamaecyparis obtuse.
New Phytol
 .
167
:
509
521
.
Högberg
P.
Högbom
L.
Schinkel
H.
1998
.
Nitrogen related root variables of trees along an N-deposition gradient in Europe
.
Tree Physiol
 .
18
:
823
828
.
Jackson
R.B.
Mooney
H.A.
Schulze
E.-D.
1997
.
A global budget for fine roots biomass, surface area and nutrient contents
.
Proc. Natl Acad. Sci. USA
 
94
:
7362
7366
.
Janssens
I.A.
Sampson
D.A.
Curiel-Yuste
J.
Carrara
A.
;Ceulemans
R.
2002
.
The carbon cost of fine root turnover in a Scots pine forest
.
For. Ecol. Manage
 .
168
:
231
240
.
John
B.
Pandey
H.N.
Tripathi
R.S.
2002
.
Decomposition of fine roots of Pinus kesiya and turnover of organic matter, N and P of coarse and fine pine roots and herbaceous roots and rhizomes in subtropical pine forest stands of different ages
.
Biol. Fert. Soils
 
35
:
238
246
.
Kandeler
E.
Tscherko
D.
Bardgett
R.D.
Hobbs
P.J.
Lampichler
C.
Jones
T.H.
1998
.
The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem
.
Plant Soil
 
202
:
251
262
.
King
J.S.
Pregitzer
K.S.
Zak
D.R.
1999
.
Clonal variation in above- and below-ground growth responses of Populus tremuloides Michaux: influence of soil warming and nutrient availability
.
Plant Soil
 
217
:
119
130
.
King
J.S.
Albaugh
T.J.
Allen
H.L.
Buford
M.
Strain
B.R.
;Dougherty
P.
2002
.
Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine
.
New ;Phytol
 .
154
:
389
398
.
King
J.S.
Pregitzer
K.S.
Zak
D.R.
Holmes
W.E.
Schmidt
K.
2005
.
Fine root chemistry and decomposition in model communities of north-temperate tree species show little response to elevated atmospheric CO2 and varying soil resource availability
.
Oecologia
 
146
:
318
328
.
Lee
E.H.
Tingey
D.T.
Beedlow
P.A.
Johnson
M.G.
Burdick
C.A.
2007
.
Relating fine root biomass to soil and climate conditions in the Pacific Northwest
.
For. Ecol. Manage
 .
242
:
195
208
.
Leuschner
C.
Hertel
D.
Schmid
I.
Koch
O.
Muhs
A.
Hölscher
D.
2004
.
Stand fine root biomass and fine root morphology in old-growth beech forests as a function of precipitation and soil fertility
.
Plant Soil
 
258
:
43
56
.
López
B.
Sabaté
S.
Gracia
C.A.
2001
.
Annual and seasonal changes in fine root biomass of a Quercus ilex L. For
.
Plant Soil
 
230
:
125
134
.
Lükewille
A.
Wright
R.F.
1997
.
Experimentally increased soil temperature causes release of nitrogen at a boreal forest catchment in southern
Norway. Glob. Change Biol
 .
3
:
13
21
.
Luo
Y.Q.
Wan
S.Q.
Hui
D.F.
Wallace
L.L.
2001
.
Acclimatization of soil respiration to warming in a tall grass prairie
.
Nature
 
413
:
622
625
.
Lyons
E.M.
Pote
J.
DaCosta
M.
Huang
B.
2007
.
Whole-plant carbon relations and root respiration associated with root tolerance to high soil temperature for Agrostis grasses
.
Environ. Exp. Bot
 .
59
:
307
313
.
Majdi
H.
Öhrvik
J.
2004
.
Interactive effects of soil warming and ;fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden
.
Glob. Change Biol
 .
10
:
182
188
.
Majdi
H.
Rosengren-Brinck
U.
1994
.
Effects of ammonium sulphate application on the rhizosphere, fine root and needle chemistry in a Picea abies (L.) Karst. stand
.
Plant Soil
 
162
:
71
80
.
Matamala
R.
Schlesinger
W.H.
2000
.
Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem
.
Glob. Change Biol
 .
6
:
967
979
.
McClaugherty
C.A.
Aber
J.D.
Melillo
J.M.
1982
.
The role of fine roots in the organic matter and nitrogen budgets of two forested ecosystems
.
Ecology
 
63
:
1481
1490
.
McConnaughay
K.D.M.
Coleman
J.S.
1999
.
Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients
.
Ecology
 
80
:
2581
2593
.
Meier
I.C.
Leuschner
C.
2008
.
Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 ;mature stands across a precipitation gradient
.
Glob. Change Biol
 .
14
:
2081
2095
.
Melillo
J.M.
Steudler
P.A.
Aber
J.D.
et al
2002
.
Soil warming and carbon-cycle feedbacks to the climate system
.
Science
 
298
:
2173
2176
.
Melillo
J.M.
Steudler
P.A.
Aber
J.D.
et al
2004
.
Soil warming—a major consequence of global climate change. In
Forests in Time: The Environment Consequences of 1000 Years of Change in New ;England. Eds
 .
Foster
D.
Aber
J.
Yale University Press
,
New ;Haven, CT
, pp
280
295
.
Melillo
J.M.
Butler
S.M.
Johnson
J.
et al
2011
.
Soil warming, carbon-nitrogen interactions and forest carbon budgets
.
Proc. Natl Acad. Sci. USA
 
108
:
9508
9512
.
Metcalfe
D.B.
Meir
P.
Aragão
L.E.O.C.
et al
2008
.
The effects of water availability on root growth and morphology in an Amazon rainforest
.
Plant Soil
 
311
:
189
199
.
Müller
M.M.
Sundman
V.
Soininvaara
O.
Merilfiinen
A.
1988
.
Effect of chemical composition on the release of nitrogen from agricultural plant materials decomposing in soil under field conditions
.
Biol. Fert. Soils
 
6
:
78
83
.
Nadelhoffer
K.J.
2000
.
The potential effects of nitrogen deposition on fine-root production in forest ecosystems
.
New Phytol
 .
147
:
131
139
.
Owen
J.S.
Wang
M.K.
Sun
H.L.
King
H.B.
Wang
C.H.
Chuang
C.F.
2003
.
Comparison of soil nitrogen mineralization and nitrification in a mixed grassland and forested ecosystem in central Taiwan
.
Plant Soil
 
251
:
167
174
.
Pajuste
K.
Frey
J.
2003
.
Nitrogen mineralisation in podzol soils under boreal Scots pine and Norway spruce stands
.
Plant Soil
 
257
:
237
247
.
Persson
H.
2000
.
Adaptive tactics and characteristics of tree fine roots. In
The Supporting Roots of Trees and Woody Plants: Form, Function and Physiology.
  Eds.
Stokes
A.
Kluwer Academic Publishers
,
Dordrecht, The Netherlands
, pp
337
346
.
Persson
H.
2002
.
Root system in arboreal plants. In
Plant Roots: The Hidden Half. Eds
 .
Waisel
Y.
Eshel
A.
Kafkafi
U.
Marcel Dekker
,
New York, NY
, pp
187
204
.
Persson
H.Å.
Stadenberg
I.
2009
.
Spatial distribution of fine-roots in boreal forests in eastern Sweden
.
Plant Soil
 
318
:
1
14
.
Peterjohn
W.T.
Melillo
J.M.
Steudler
P.A.
Newkirk
K.M.
1994
.
Responses of trace gas fluxes and N availability to experimentally elevated soil temperatures
.
Ecol. Appl
 .
4
:
617
625
.
Powers
J.S.
Treseder
K.K.
Lerdau
M.T.
2005
.
Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances
.
New Phytol
 .
165
:
913
921
.
Pregitzer
K.S.
Laskowski
M.J.
Burton
A.J.
Lessard
V.C.
Zak
D.R.
1998
.
Variation in sugar maple root respiration with root diameter and soil depth
.
Tree Physiol
 .
18
:
665
670
.
Pregitzer
K.S.
King
J.S.
Burton
A.J.
Brown
S.E.
2000
.
Responses of tree fine roots to temperature
.
New Phytol
 .
147
:
105
115
.
Rustad
L.E.
Campbell
J.L.
Marion
G.M.
Norby
R.J.
Mitchell
M.J.
;Hartley
A.E.
Cornelissen
J.H.C.
Gurevitch
J.
2001
.
A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming
.
Oecologia
 
126
:
543
562
.
Schimel
J.P.
Bennett
J.
2004
.
Nitrogen mineralization: challenges of a changing paradigm
.
Ecology
 
85
:
591
602
.
Stober
C.
George
E.
Persson
H.
2000
.
Root growth and response to nitrogen. In
Carbon and Nitrogen Cycling in European Forest Ecosystems: Ecological Studies.
  Ed.
Schulze
E.-D.
Springer
,
Heridelberg
,
Vol. 142
, pp
99
121
.
Strömgren
M.
Linder
S.
2002
.
Effects of nutrition and soil warming on stemwood production in boreal Norway spruce stand
.
Glob. Change Biol
 .
8
:
1195
1204
.
Tang
J.
Baldocchi
D.D.
2005
.
Spatial-temporal variation in soil respiration in an oak-grass savanna ecosystem in California and its partitioning into autotrophic and heterotrophic components
.
Biogeochemistry
 
73
:
183
207
.
Tang
J.
Misson
L.
Gershenson
A.
Cheng
W.X.
Goldstein
A.H.
2005
.
Continuous measurements of soil respiration with and without roots in a ponderosa pine plantation in the Sierra Nevada Mountains
.
Argic. For. Meteorol
 .
132
:
212
227
.
Tierney
G.L.
Fahey
T.J.
Groffman
P.M.
Hardy
J.P.
Fitzhugh
R.D.
;Driscoll
C.T.
Yavitt
J.B.
2003
.
Environmental control of fine root dynamics in a northern hardwood forest
.
Glob. Change Biol
 .
9
:
670
679
.
Tietema
A.
Verstraten
J.M.
1992
.
Nitrate cycling in an acid forest ecosystem in the Netherlands under increased atmospheric nitrogen input
.
Biogeochemistry
 
15
:
21
46
.
Tilman
D.
1988
.
Plant strategies and the dynamics and structure of plant communities
.
Princeton University
,
Princeton, NJ
.
Uselman
S.M.
Qualls
R.G.
Thomas
R.B.
2000
.
Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.)
.
Plant Soil
 
222
:
191
202
.
Valverde-Barrantes
O.J.
Raich
J.W.
Russell
A.E.
2007
.
Fine-root mass, growth and nitrogen content for six tropical tree species
.
Plant Soil
 
290
:
357
370
.
Vanguelova
E.I.
Nortcliff
S.
Moffat
A.J.
Kennedy
F.
2005
.
Morphology, biomass and nutrient status of fine roots of Scots pine (Pinus sylvestris) as influenced by seasonal fluctuations in soil moisture and soil solution chemistry
.
Plant Soil
 
270
:
233
247
.
Vogt
K.A.
Persson
H.
1991
.
Measuring growth and development of roots. In
Techniques and Approaches in Forest Tree Ecophysiology. Eds
 .
Lassoie
J.P.
Hinckley
T.M.
CRC Press
,
Boca Raton, FL
, pp
477
501
.
Wan
S.
Norby
R.J.
Pregitzer
K.S.
Ledford
J.
O'Neill
E.G.
2004
.
CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots.
New Phytol
 .
162
:
437
446
.
Withington
J.M.
Reich
P.B.
Oleksyn
J.
Eissenstat
D.M.
2006
.
Comparisons of structure and life span in roots and leaves among temperate trees
.
Ecol. Monogr
 .
76
:
381
397
.
Zak
D.R.
Holmes
W.E.
MacDonald
N.W.
Pregitzer
K.S.
1999
.
Soil temperature, matric potential, and the kinetics of microbial respiration and nitrogen mineralization
.
Soil Sci. Soc. Am. J
 .
63
:
575
584
.
Zak
D.R.
Pregitzer
K.S.
King
J.S.
Holmes
W.E.
2000
.
Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis
.
New Phytol
 .
147
:
201
222
.
Zogg
G.P.
Zak
D.R.
Burton
A.J.
Pregitzer
K.S.
1996
.
Fine root respiration in northern hardwood forests in relation to temperature and nitrogen availability
.
Tree Physiol
 .
16
:
719
725
.