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Soil Biology & Biochemistry 42 (2010) 337e346

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Soil Biology & Biochemistry

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Partitioning soil respiration and assessing the carbon balance in a Setaria italica(L.) Beauv. Cropland on the Loess Plateau, Northern China

Xudong Li a, Hua Fu a,*, Ding Guo a, Xiaodong Li a, Changgui Wan a,b

aKey Laboratory of Grassland Agro-ecosystem, Ministry of Agriculture of China, College of Pastoral Agricultural Science and Technology,Lanzhou University, P.O. Box 61, Lanzhou 730000, ChinabDept. Natural Resources Management, Texas Tech University, Lubbock, TX 79409, USA

a r t i c l e i n f o

Article history:Received 15 March 2009Received in revised form31 October 2009Accepted 10 November 2009Available online 20 November 2009

Keywords:Soil respirationMicrobial respirationRoot respirationCarbon balanceCroplandLoess Plateau

* Corresponding author. Fax: þ86 931 8663778.E-mail addresses: lixd2005@lzu.cn (X. Li), fuhua@

0038-0717/$ e see front matter � 2009 Elsevier Ltd.doi:10.1016/j.soilbio.2009.11.013

a b s t r a c t

A study was conducted in a Setaria italica (L.) Beauv. cropland on the Loess Plateau in order to partitiontotal soil respiration (Rt) into microbial respiration (Rm) and root respiration (Rr) and to determine thecarbon balance of the cropland ecosystem. A trenching method with micro-pore mesh was used to createroot-free soil cores. Differences between mesh and non-mesh treatments were used to determine rootrespiration. Similar pattern was found in the diurnal variation of Rt and Rm with the minimum values at3:00e6:00 h and the maximum at 13:00e15:00 h. The diurnal pattern of Rr was completely different, theminimum values appeared at 11:00e13:00 h and the maximum at 0:00e3:00 h. Soil temperatureexerted predominant control over the diurnal variations of Rt and Rm. The daily mean values of Rt, Rmand Rr were close to the measurements taken at 9:00 h. On the seasonal scale, Rm was stronglydependent on soil temperature, with higher correlation with 2-cm-depth temperature (r2 ¼ 0.79,P < 0.001) than with 5-cm-depth temperature. When the effects of both soil temperature and moisturewere considered, a linear model provided more accurate prediction of Rm (r2 ¼ 0.83, P < 0.0001). Rootrespiration (Rr) exhibited pronounced daily variation corresponding to changes in photosynthesis andseasonal variation related to crop phenological development. The seasonal variation in Rr was stronglycorrelated with leaf area index (LAI) (r2 ¼ 0.85, P < 0.05), and also positively, but marginally correlatedwith root biomass (RB, P ¼ 0.073). Contribution of root respiration to total soil respiration (Rr/Rt ratio)showed pronounced diurnal and seasonal variations. The daily mean values of Rr/Rt ratios were close tothe values obtained at 9:00 h. In different phenological stages, Rr/Rt ratios ranged from 22.3% to 86.6%;over the entire growing season, the mean Rr/Rt ratio was 67.3%.

Total annual loss of C due to Rm in 2007 was estimated to be 121.3 g C m�2 at the study site, while theannual NPP (net primary production) was 262.1 g C m�2. The cropland system thus showed net carboninput of 140.8 g C m�2.

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1. Introduction

Interest in soil respiration (Rs) has grown as a result of theuncertainties associatedwith the cycling of belowground carbon, aswell as the importance of soil carbon dynamics for possible feed-back mechanisms in the context of climate change (Moyano et al.,2007). On the global scale, soil respiration produces 80.4 Pg CO2eCannually, which is approximately 10-fold greater than CO2 emis-sions from fossil fuel combustion and deforestation sourcescombined (Raich et al., 2002), and thus even small changes in soil

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respiration may greatly influence atmospheric carbon and heatbalance (Veenendaal et al., 2004; Kane et al., 2005).

In contrast to fluxes of other greenhouse gases (CH4, N2O),values for total CO2 efflux from soil do not provide sufficientinformation to decidewhether the soil is a net source or net sink foratmospheric CO2. This is because not all of the CO2 coming from thesoil is soil-derived, i.e. it is not all produced by the decomposition ofsoil organic matter (Kuzyakov, 2006). Soil respiration originatesmainly from root respiration (autotrophic) and microbial (hetero-trophic) activities. Because the amount of soil respiration derivedfrom roots is independent of soil carbon pools, partitioning root andmicrobial contributions to soil respiration is important for calcu-lating the carbon budgets of vegetation and the turnover rate of soilorganic matter. It is also important for understanding sources and

Table 1Soil properties in different soil layers in the study site (n ¼ 6).

Soil layer Bulkdensity(g cm�3)

pH Soil organiccarbon(g kg�1)

Soil totalphosphorus(g kg�1)

Soil totalnitrogen(g kg�1)

0e10 cm 1.13 8.17 7.5 0.71 0.9410e20 cm 1.18 8.27 7.9 0.72 0.9120e30 cm 1.11 8.25 8.2 0.73 1.0230e40 cm 1.13 8.22 8.6 0.74 1.0340e60 cm 1.16 8.29 6.9 0.67 0.7860e80 cm 1.19 8.42 4.5 0.61 0.5280e100 cm 1.23 8.55 3.1 0.61 0.38

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346338

sinks of carbon in terrestrial ecosystems in the view of globalclimate change (Hanson et al., 2000; Jia et al., 2006). In addition,soil respiration should be analyzed as a combination of differentsources, as each has its own seasonal behavior and response toenvironmental factors (Ryan and Law, 2005; Trumbore, 2006).

Partitioning soil respiration into different components in situand defining the variables controlling each component is chal-lenging but important. Three primary methods have been used inthe field studies, including integration of components contributingto in situ soil respiration; comparison of soils with and without rootexclusion; and application of stable or radioactive isotopes (Hansonet al., 2000). Each method has its advantages and disadvantages.

The Loess Plateau is located in northern China, with a total areaof 628 000 km2. It is known for its long agricultural history andserious soil erosion. Under the pressure of the ever-growing pop-ulation, a large part of this region has been converted into cultivatedland. For a long time, land degradation, overgrazing and defores-tation have affected the ecosystems of the Loess Plateau. Someresearch work have been conducted in this region to study theeffects of land use regimes on carbon sequestration (Li et al., 2008a);the response of soil respiration to plastic film mulching (Li et al.,2004); the temporal and spatial variation and the controlling factorsof soil respiration (Li et al., 2008b); the carbon released into theatmosphere (Qi et al., 2001); and the changes of soil microbialactivities after revegetation (An et al., 2009). But no studies onpartitioning soil respiration in different growing stages includingcarbon balance assessment have been conducted in this region.

Carbon balance in the cropland ecosystems is determined as thedifference between net primary production (NPP) of vegetation andsoil heterotrophic respiration. Calculating C loss through rootrespiration would help us estimate gross primary production moreaccurately, and is a necessary step to calculate net ecosystemproduction (Kuzyakov and Larionova, 2005). Because of theimportance of the Loess Plateau in the agricultural systems ofnorthern China and its potential influence on global warming,research on C flux in this area is needed. More experimental data onmicrobial soil C fluxes in different ecosystems would contribute toimproving climate modeling. In addition, root contribution to totalsoil respiration varies with seasons and even between daytime andnighttime, but this was neglected in other studies.

This study aimed to (1) quantify the contribution of root respi-ration to total soil respiration (Rr/Rt ratios) during the differentphenological stages, and for the whole growing season withtrenchingmethod; (2) describe the diurnal and seasonal variation intotal soil respiration, microbial respiration, root respiration and Rr/Rt ratio; (3) analyze themain factors influencing each component ofsoil respiration; (4) calculate the C balance in the cropland system.

2. Materials and methods

2.1. Study site

This study was conducted in a Setaria italica (L.) Beauv. croplandat the Semi-Arid Climate and Environment Observatory of LanzhouUniversity (SACOL), located at 35�570N, 104�090E (Gansu, China)with a continental semi-arid climate. The elevation is 1966 m, themean annual air temperature is 6.7 �C and the mean annualprecipitation is about 382 mm. The soil is classified as a Sierozem,a calcareous soil which is characteristic of the China loess. Thecropland was planted with annual plants such as Solanum tuber-osum L., S. italica Beauv. and Linum usitatissimum L. in rotation, andfallowed every two or three years, and was non-irrigated.

S. italica (L.) Beauv. seeds were sown in 0.17-m rows on May 5,2007; because of severe drought the seeds were resown on June 8.The average density was measured as 309 plants m�2. Both organic

manure and chemical fertilizer were applied to the cropland exceptin the fallowing year. Organic manure (3000 kg dry matter ha�1),urea (30 kg N ha�1) and calcium superphosphate (60 kg P2O5 ha�1)were applied manually prior to sowing in spring and incorporatedinto the soil by cultivation.

The crop was harvested on October 12. In this area, millet isharvested manually by pulling it from the soil, so abovegroundtissues and most of the roots are removed from the field. The soilproperties were measured in August, 2006 (Table 1). Soil bulkdensity was measured using metal rings of known volume; soil pHwas determined in a 1:2.5 suspension of soil in distilled water(2-mm soil sample); soil organic carbon was determined with theoil batheK2CrO7 titration method (oxidization with dichromate inpresence of H2SO4, heated at 180 �C for 5 min); total nitrogen wasdetermined with Kjeldahl method, and total phosphorus withspectrophotometer after NaOH digestion.

2.2. Soil respiration measurements

Soil respiration was measured with a LICOR-6400 portablephotosynthesis system equipped with a LICOR 6400e9 soil respi-ration chamber (LICOR, Inc., Lincoln NE, USA). Polyvinyl chloridecollars 10.4 cm in diameter and 5 cm in height were used formeasurements. Collars were inserted into soil to the depth of1.5 cm. To reduce a disturbance-induced CO2 efflux, collars wereinstalled at least 12 h prior to each measurement. The plants in thecollars were clipped at ground level and litter in the collarsremoved before the measurements began. All the measurementswere taken in 2007.

2.3. Partitioning soil respiration

A trenching method was employed to partition total soil respi-ration (Rt) into microbial respiration (Rm) and root respiration (Rr).The root-free soil plots were created using micro-pore meshes withpore sizes smaller than the diameter of a fine root, which preventedroot growth into the plots and allowed the movement of water,bacteria, organic matter and minerals through the mesh and thusreduced the disturbance of natural soil conditions that could affectthe decomposition of litter and soil organic matter (Moyano et al.,2007). Root respiration is here defined as respiration by roots, theirassociated mycorrhizal fungi and other microorganisms in therhizosphere directly dependent on labile C compounds releasedfrom roots.

Twelve plots of 0.5m� 0.5mwere establishedwithin a distanceof 5e6 m and trenches 0.1 m wide and 0.5 m deep were excavatedin late March, 2007. After lining the trench with Nylon mesh of0.038 mmmesh size (Moyano et al., 2007), soil was refilled into thetrench. The plots were then kept free of seedlings and herbaceousvegetation by periodic manual removal during the measurements.Thus, it was assumed that the CO2 efflux measured in the mesh-treated plots was composed of only Rmwhile CO2 efflux measured

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346 339

in planted field was composed of both Rm and Rr. Differencesbetween mesh treatments and planted field were used to deter-mine Rr. The different treatments might result in differences in soiltemperature and soil moisture due to shading andwater absorptionby seedlings. To minimize the error, the soil respiration ratesmeasured in the mesh treatments were corrected with the differ-ence in soil temperature and soil moisture by Eq. (3). The error canbe minimized by averaging soil respiration measurements overhours of a day and over days of a year (Tang and Baldocchi, 2005),therefore, when the diurnal change of Rr/Rt ratio was measured,the Rm values for the mesh-treated plots were not corrected inthis way.

To evaluate the Rr/Rt values in the different phenological stages,soil respiration measurements were taken for both mesh-treatedplots and planted field on Jun. 29, Jul.17, Aug.11, Aug. 25, Sep.16 andOct. 6 in the growing season. For each set of measurements, onecollar was inserted into each of 12 mesh-treated plots (A); twocollars were inserted next to each plot: one in the row (B) andanother between rows of seedlings (C). For the treatment (B), theseedlings in the collars were clipped to ground level just prior tomeasurements. The measurements were made alternately in thesequence of A1eB1eC1eA2eB2eC2eA3... The measurementswere conducted between 8:00 and 11:00 h, as a study in 2006 inthe same place showed that the daily mean values of Rt, Rm and Rr/Rt ratio were close to the measurements taken between 8:00 and10:00 h (data not shown). At the same time, the leaf area index (LAI)was measured with Plant Canopy Analyzer LICOR LAI-2000 (USA)and the root biomass (RB) was estimatedwith an auger (see below).

Monthly measurements were made in the non-growing season.For each set of measurements, 12 collars were randomly set withina space of 5e6 m. All the measurements were also conductedbetween 8:00 and 11:00 h. In addition, two sets of 24 h continuousmeasurements were conducted on Aug. 21e22 and Sep. 18e19 tomonitor the diurnal variations of soil respiration components andthe Rr/Rt ratio. In the diurnal measurements, three collars were setin the mesh-treated plots and three were between rows of seed-lings. Soil respirationwas measured alternately every 2 h from 9:00to 21:00 h and every 3 h from 21:00 to 6:00 h. Each set ofmeasurements required about 20 min. Mean values of CO2 efflux ofthree replicates for each treatment represented the midpoint of themeasurement, i.e. 9:00, 11:00, 13:00 h.., thus the effect of soiltemperature on soil respirationwasminimized. Another two sets ofdiurnal measurements were taken on Jun. 3e4 and Dec. 14e15 tomonitor the diurnal variations of Rm in the non-growing season.

Soil temperature at 2 cm and 5 cm depth was measured witha soil temperature probe connected to the LICOR-6400 at the sametime the soil respirationwas measured. Volumetric soil moisture at10 cm was measured with a Trime TDR probe (IMKO, Ettlingen,Germany) at the same sites where the collars were set after soilrespiration measurements. For mesh-treated plots, soil moisturewas measured next to the collars to reduce disturbance to the soil.Soil moisturewas notmeasured inwinter when the soil was frozen.The soil moisture value in winter was calculated by the correlationbetween measured soil moisture and the soil moisture recorded bythe meteorological station (SACOL) (Huang et al., 2008).

Because negative CO2 flux was observed in the study, in order toquantify the negative flux as precisely as possible, we assumed thatthere was a relatively stable CO2 flux rate when the CO2 concen-tration in the chamber was close to the ambient CO2 concentration.We recorded the changes of CO2 concentration in the chamber atintervals of 30, 60, 90 and 120 s, respectively (the respiration valueswere all positive then), then respiration rates were calculated usingthe following equation:

R ¼ ½ðP*VÞ=ðk*TÞ*ðC90� C0Þ�=ðA*90Þ (1)

where R is the respiration rate (mmol CO2 m�2 s�1); P is the airpressure (Pa) in the chamber; V is the volume of the chamber (l)when measurements were taken; k is the gas constant(8314 Pa l mol�1 K�1); T is the air temperature in the chamber (K);C90 and C0 are the CO2 concentration (mmol/mol) in the chamberwhen the chamber was set on the collar (0 s) and 90 s afterward,respectively; A is the area of the collar (m2) and 90 is the duration ofeach measurement (s).

The correlation analysis was done between the values recordedat the different intervals and that measured by LiCOR-6400. Thevalues recorded at 90-second-interval were found to be bestcorrelated with that measured by LiCOR-6400 and close to the 1:1line (r2 ¼ 0.90, P < 0.001). So, negative CO2 flux was obtained byrecording the CO2 concentration changes in the chamber in 90 sand calculating with Eq. (1).

As the observation of negative CO2 flux in the experiment,microbial respiration measured in the study was actually the sumof two opposing fluxes (carbon absorption in the soil and carbonloss by microbial respiration), but the magnitude of which cannotbe determined specifically in this study. The negative CO2 flux maybe contributed to the carbonate precipitation and may lead tounderestimation of Rt and Rm, sequentially the overestimation ofRr/Rt ratios.

2.4. Carbon input and output in the cropland system

2.4.1. Carbon inputCarbon input in the cropland systemwas defined as net primary

production (NPP) i.e. the sum of aboveground biomass and rootbiomass at harvesting time. To measure the aboveground biomass,on Oct. 12, 12 quadrats (each 1 m2) were randomly selected. Withineach quadrat, the crop was clipped to ground level. The above-ground biomass was partitioned into three components: spike,stem and leaf. To determine root biomass, soil cores with 9.3 cm indiameter to a depth of 50 cm were taken both in the row andbetween two rows. Cores were divided into 10-cm slices andwashed over a 0.5-mm sieve (12 replicates).

All the samples were air-dried and weighed. To measure the dryweight, all the air-dried plant samples were oven-dried at 105 �Cuntil a constant weight was obtained. Sub-samples were ground topass through a 0.5 mm-sieve. The organic carbon content of theplant samples was determined by CHNS-O Analyzer (Flash-EA-1112, Thermo Fisher Scientific, Waltham, MA, USA).

2.4.2. Carbon outputCarbon output was defined as carbon loss in the form of Rm.

Although daily average CO2 efflux can be accurately calculated fromcontinuous diurnal CO2 measurements, it is often time consumingand not suitable for long-term monitoring. In this study, we usedthe daily soil temperature and moisture data at 9:00 h to estimatethe annual sum of Rm from the site (see details in Results).

2.5. Data analysis

Data analyses was performed with SPSS 13.0 for Windows(USA). Step-wise multiple regression analysis was performed toevaluate the influence of soil temperature and soil moisture on soilrespiration. Significance was defined at the 95% confidence level.

3. Results

3.1. Diurnal variations of soil respiration components

Fig. 1 shows the diurnal variations of Rt, Rm, Rr and soiltemperature at 2 cm depth (T2) on Jun. 3e4, Aug. 21e22, Sep.18e19

Fig. 1. Diurnal variations in Rm (microbial respiration), Ts (soil temperature at 2 cm) innon-growing season (Jun. 3e4 and Dec. 14e15) and Rt (total soil respiration, Rm), Rr(root respiration) and Ts in growing season (Aug. 21e22 and Sep. 18e19) in 2007.Vertical bars indicate the standard errors of the mean (n ¼ 3).

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346340

andDec.14e15, 2007 (the soil respirationmeasured in non-growingseason included only Rm). Both Rt and Rm showed strong diurnalpatterns with single maxima during daytime. The maximumvaluesof Rt and Rm occurred at 13:00e15:00 h, and the minimum at3:00e6:00 h.When the different time intervals were accounted for,the daily mean values of Rt and Rm were close to the values

measured at 9:00 and 19:00 h. Thus, Rt and Rm at 9:00 h could betaken as representative ofmeandaily values. Diurnal variations of Rtand Rm were highly associated with variations in soil temperature(r2 values ranged between 0.63 and 0.75 for all measurements,n¼ 30, P< 0.01). The variation of T2 rather thanT5 (soil temperatureat 5 cmdepth) could better explain the variations in Rt and Rm (datanot shown). The higher daily variation of Rm observed on Jun. 3e4(from�0.010 to1.372 mmol CO2m�2 s�1) and Sep.18e19 (from0.015to 1.137 mmol CO2 m�2 s�1) was in accordance with higher variationof soil temperature and relatively high soil moisture.

Negative CO2 flux was observed in nighttime on Jun. 3e4 andDec. 14e15. On Jun. 3e4, the negative CO2 flux was observed at21:00 and 3:00 h with the values of �0.008 and �0.010 mmolCO2 m�2 s�1, while on Dec. 14e15, the negative CO2 flux wasobserved between 17:00 and 9:00 h with values between �0.009and�0.057 mmol CO2 m�2 s�1. The phenomenonwas also observedin January (Fig. 3a).

Based on Rm and their corresponding Rt on Aug. 21e22 and Sep.18e19, Rr rates were calculated (Fig. 1). Root respiration showeda completely different diurnal pattern than those of Rt and Rm. Theminimum values of Rr appeared at 11:00e13:00 h and thenincreased gradually, reaching to the maximum at 0:00e3:00 h. Thedaily mean values of Rr were also close to the values calculated for9:00 h. Compared with Rt and Rm, Rr showed relatively lower dailyvariation and no significant correlation between Rr and soiltemperature was found. On Aug. 21e22, the daily mean value of Rrwas 1.084 mmol CO2 m�2 s�1, significantly higher than thatmeasured on Sep. 18e19 (0.753 mmol CO2 m�2 s�1).

3.2. Seasonal variation of microbial respirationand controlling factors

3.2.1. Responses to soil moisture and temperatureBy analyzing the data in the growing season and non-growing

season, a linear temperature function could explain most of thevariation in Rm with higher correlation with T2 (r2 ¼ 0.79,P < 0.001, n ¼ 144) (Fig. 2a):

Rm ¼ 0:026Tsþ 0:122 (2)

where Rm is the microbial respiration (mmol CO2 m�2 s�1), Ts is thesoil temperature at 2 cm (�C). As negative CO2 flux was observed inwinter, an exponential functionwas established after excluding thenegative values. The linear function, however, had higher r2 value(0.72, P < 0.001) as compared to the exponential function (0.68,P < 0.001).

The single effect of soil moisture on Rm was examined bynormalizing Rm at a reference value of 15 �C, and a linear equationhad a better fit than others (quadratic, power and exponential, etc.),accounting for 39% of seasonal variation in Rm (n ¼ 108, P < 0.001)(Fig. 2b). When both temperature and moisture effects wereconsidered, a linear model yielded better simulations (r2 ¼ 0.83,P < 0.0001):

Rm ¼ 0:024 Tsþ 0:013 Ms� 0:020 (3)

where Rm is the microbial respiration (mmol CO2 m�2 s�1), Ts is thesoil temperature at 2 cm (�C); Ms is the volumetric soil moisture at10 cm. Inclusion of soil moisture in the model improved itspredictive capacity, indicating that Rm was highly dependent onthe effects of both soil temperature and soil moisture.

3.2.2. Seasonal variation of microbial respirationTo better understand the seasonal variations of Rm, the Rm

values of each set of measurement were normalized to the soiltemperature (T2) at 9:00 hwith Eq. (2). The results showed that Rm

Fig. 2. Microbial respiration (Rm) measured in mesh-treated plots in 2007 plottedagainst (a) soil temperature at 2 cm (P < 0.001, n ¼ 144) and (b) soil moisture at 10 cm(P < 0.001, n ¼ 108) both showing significant linear relationship.

Fig. 3. Variations of (a) microbial respiration (Rm) and soil temperature at 2 cm (Ts)and (b) soil moisture at 10 cm during the whole experiment in 2007. Vertical barsindicate the standard errors of the mean (n ¼ 12).

Table 2Variations of total soil respiration (Rt), microbial respiration (Rm), root respiration(Rr) and contribution of root respiration to total soil respiration (Rr/Rt ratio) ofSetaria italica (L.) Beauv. populations in the growing season in 2007.

Date Soil respiration components (mmol CO2 m�2 s�1) Rr/Rtratio (%)

Rt Rm Rr

Jun. 29 0.515 0.401 0.115 22.3Jul. 17 0.628 0.448 0.180 28.7Aug. 11 1.426 0.347 1.079 75.7Aug. 25 1.245 0.288 0.957 76.9Sep. 16 1.209 0.216 0.993 82.1Oct. 06 0.859 0.115 0.744 86.6

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346 341

exhibited a pronounced seasonal variation with a minimum valueof �0.130 mmol CO2 m�2 s�1 in January and a maximum of0.448 mmol CO2 m�2 s�1 in July (Fig. 3a), in accordance withminimum and maximum values of T2 (�10.0 �C and 20.7 �C). Thegeneral pattern of Rm reflected the variation of soil temperatureexcept after harvest. After harvest in mid October, Rm increasedsharply for a couple of days even when soil temperature decreasedsteadily.

Soil moisture at 10 cm ranged between 8.5% on Aug. 25 and17.1% on Oct. 6 in the growing season (Fig. 3b), correlating nega-tively with both soil temperature and Rt (data not shown).

3.3. Seasonal variation of root respiration

3.3.1. Variation of root respirationThe seasonal pattern of Rr was different from that of Rm

(Table 2). Rr exhibited a higher seasonal variation, ranging from0.115 to 1.079 mmol CO2 m�2 s�1. When the plants were very young,Rr was lower, then increased rapidly in the elongation stage andpeaked in the flowering stage. It was relatively stable before theripening stage and decreased thereafter. The seasonal change of Rrwas not correlated with soil temperature and soil moisture. Theseasonal pattern of Rt was dominated by Rr, as Rm showed rela-tively small seasonal variations.

3.3.2. Factors controlling root respirationSeasonal variations of LAI and RB are shown in Fig. 4. Leaf area

index increased from June to September, with a maximum value of2.19 in mid September, and decreased thereafter. At the end ofSeptember the leaf shedding began. The maximum value of LAI

coincided with the filling stage. A parallel pattern was alsoobserved for RB with a maximum value of 152.1 g m�2 (dry matter)on Sep. 16 (filling stage). Root respiration was significantly corre-lated with LAI (r2 ¼ 0.85, P < 0.05) (Fig. 5a), while correlationbetween Rr and RB was positive but not significant (r2 ¼ 0.69,P ¼ 0.073) (Fig. 5b).

3.4. Contribution of root respiration to total soil respiration

Diurnal variations of Rr/Rt ratio were estimated on Aug. 21e22and Sep. 18e19, 2007. As shown in Table 3, the Rr/Rt ratios variedgreatly from daytime to nighttime, ranging from 49.1% to 97.3% onAug. 21e22 and from 35.4% to 98.2% on Sep. 18e19. The minimumratio appeared at 13:00e15:00 h and themaximum at 3:00e6:00 h.Calculated with the daily mean values of Rt and Rr (the differenttime intervals of measurements were accounted for), the dailymean values of Rr/Rt ratios were 74.3% and 68.5% on Aug. 21e22and Sep. 18e19, respectively, close to the values obtained at 9:00 h.Therefore, the Rr/Rt ratio obtained at 9:00 h was considered as therepresentative of the mean daily ratio.

Fig. 4. Variations of (a) leaf area index (LAI) and (b) root biomass at the 0e30 cm depth(RB) in the growing season in 2007. Vertical bars indicate the standard errors of mean(n ¼ 12).

Fig. 5. Responses of root respiration to (a) leaf area index (LAI) and (b) root biomass atthe 0e30 cm depth (RB). Measurements were done on Jun. 29, Jul. 17, Aug. 11, Aug. 25,Sep. 16 and Oct. 6 in the growing season in 2007. The correlation was significant for LAI(n ¼ 6, P < 0.05) but not significant for root biomass (n ¼ 6, P ¼ 0.073).

Table 3Diurnal variations in the contribution of root respiration to total soil respiration(Rr/Rt ratio) of Setaria italica (L.) Beauv. populations on Aug. 21e22 and Sep. 18e19,2007 (n ¼ 3).

Time Rr/Rt ratio (%)

Aug. 21e22 Sep. 18e19

9:00 70.3 71.311:00 54.1 53.913:00 49.1 36.415:00 53.2 35.417:00 61.5 49.719:00 71.6 82.721:00 87.1 84.90:00 96.2 97.43:00 96.5 98.26:00 97.3 97.6

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346342

On Jun. 29, Jul. 17, Aug. 11, Aug. 25, Sep. 16 and Oct. 6, soilrespiration was measured to evaluate the Rr/Rt ratio for thedifferent phenological stages (Fig. 6). Parallel patterns wereobserved in soil respiration dynamics against soil temperature forthe treatments: mesh-treated plots, in the rows and between therows of seedlings. For each treatment, soil respiration rates weresignificantly correlated with T2 during the whole growing season(P < 0.01, with r2 values ranging from 0.55 to 0.91). Soil respirationratesmeasured in the rows and between the rowswere higher thanthat in mesh-treated plots in different observation periods whilethe values measured in the rows were the highest. This wasattributed to the higher root density.

Table 2 shows the values of the different soil respirationcomponents and the Rr/Rt ratios at 9:00 h for different phenolog-ical stages. During thewhole growing season, the Rr/Rt ratio rangedfrom 22.3% to 86.6%. In the seedling stage, the Rr/Rt ratio was lower,and then increased rapidly during the fast growing period (elon-gation stage). After the flowering stage, the Rr/Rt ratio still keptincreasing even as Rr decreased. This was attributed to the fact thatRm declined more rapidly than Rr. Over the entire growing season,the Rr/Rt ratio was 67.3%.

3.5. Carbon balance in the cropland system

The carbon contents of root, spike, stem and leaf were525.4 � 1.0, 494.7 � 1.8, 495.0 � 5.3 and 476.6 � 4.5 g kg�1

(mean � SE, dry weight), respectively. The proportion of eachcomponent to the total plant biomass was taken as a weight tocalculate the total biomass carbon. The result showed that annualnet primary productionwas 496.8 gm�2 (dry matter), while annualcarbon input averaged 262.1 � 10.2 g C m�2.

The bivariate model (Eq. (3)) was used to calculate annualcarbon output in the form of Rm with the daily soil temperatureand soil moisture values at 9:00 h (based on meteorological data).The result showed that annual carbon output totaled 121.3 g C m�2

in the cropland system. The carbon input (262.1 g C m�2 y�1) wasabout twice as high as the output, resulting in a net carbon input of140.8 g C m�2 y�1.

4. Discussion

4.1. Diurnal variations of soil respiration components

Soil respiration is controlled by a range of biotic and abioticfactors, such as temperature, soil water content, aboveground vege-tation structure, photosynthetic activity, and plant phenologicaldevelopment (Subke et al., 2006). Different components of soilrespiration respond differently to these factors; while heterotrophicrespiration is driven mainly by soil temperature and moisture, root

Fig. 6. Soil respiration (SR) measured in the mesh-treated plots (A, triangles), in the row of seedlings (B, squares) and between the rows of seedlings (C, solid circles) plotted againstsoil temperature at 2 cm in the growing season. A include only microbial respiration while B and C include both microbial and root respiration. Temperature responses were allsignificant (r2 values ranging from 0.55 to 0.91, n ¼ 12, P < 0.01).

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346 343

respiration may be closely linked to carbon flow within the plant(Tang and Baldocchi, 2005). In the present study, soil temperatureexerted dominant control over diurnal variations of Rm when soilmoisturewas relatively stable. Root respiration showed a completelydifferent diurnal pattern with no response to soil temperature.Furthermore, the diurnal pattern of Rr was not in accordance withthat of photosynthetic activity, which was higher in daytime than atnight, while Rr was higher in nighttime than daytime, suggestinga time lag between photosynthesis and root respiration.

Ekbald and Höberg (2001) found that carbon assimilated in thecanopy of boreal conifers took one to four days to appear as carbonrespired by the soil. Tang and Baldocchi (2005) suggested that rootrespiration could immediately respond to photosynthesis withina day in an oak-grass savanna and the coupling of root withphotosynthesis outweighs the coupling between soil respirationand temperature. In Austria, Bahn et al. (2009) found that, ina mountain meadow system, freshly plant-assimilated C is rapidlytransferred belowground and respired there, and is preferentiallyused for soil respiratory processes from the late morning hoursonwards, whereas photosynthates originating from previous daysare a predominant respiratory substrate during the nighttime andearly morning hours. The different time lags between photosyn-thesis and root respiration for herbaceous and woody plants maymainly be attributed to the height of plants.

The negative CO2 flux as found here occasionally was alsoobserved inother studies (Qi et al., 2005; Zhanget al., 2008;Xie et al.,2009), but the mechanism is not well understood. It is possible torelate this to the change of the balance between soil respiration andCO2 consumption in the soil. The consumption of CO2 in the soilmaybe attributed to the formation of calcite, as the formation of pedo-genic carbonate was considered as a process of CO2 sequestration

from atmosphere in the arid and semi-arid area, especially forSierozem (Lei and Gu, 1992). Alkaline soil on land absorbs CO2 withan inorganic, non-biological process. The intensity of this CO2absorption is determined by the salinity, alkalinity, temperature andwater content of the saline/alkaline soils. In our study, the negativenighttime CO2 flux in December was probably caused by a low Rmdue to the freezing soil temperatures, while CO2 absorption by thesoilwas enhanced at lowtemperature (Xie et al., 2009). Thenegativenighttime CO2 flux in June was likely due to the dry soil and asso-ciated higher soil electrical conductivity, which were conditionsfavorable for CO2 absorption (Xie et al., 2009).

However, the magnitude of negative CO2 flux is difficult to bequantifiedwith the present facilities. To know the exact mechanismof the process and the magnitude of CO2 absorption in this area,further study is needed.

4.2. Seasonal variations of soil respiration components

The seasonal pattern of Rm indicated that Rm was correlatedwith soil temperature and moisture (Fig. 3). As reported elsewhere(Fernandez et al., 1993; Bowden et al., 1998; Conant et al., 2004),soil temperature was the main influencing factor and moisture wassecondary.

Temperature can be a strong controlling factor for respirationrates under certain conditions, but the limiting factors inmany if notmost cases are those determining substrate availability, e.g. waterstatus and assimilate supply (Högberg et al., 2001; Davidson andJanssens, 2006). A number of studies have shown that soil watercontent has a limited impact on soil respiration rate except undersoil saturation or water deficits (Edwards, 1975; Hanson et al., 1993;Jia et al., 2004). During the whole study period, volumetric soil

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346344

moisture fluctuated between 4.8% and 22.4% (Fig. 3b). Low soilmoisture can limit belowground biological activity, and Rm waspositively correlated with soil moisture throughout this study.

Residual analysis shows that the bivariate model can accuratelyestimate most of the measured data for Rm except those at highertemperature and higher moisture (Fig. 7). When soil temperaturewas lower than 15 �C and moisture lower than 14%, the residualswere small, indicating that the model accurately describes themeasured results. The exceptional pattern of Rm after harvest wasmainly attributed to the soil disturbance through ploughing activityand the decomposition of root residues, which increased soilrespiration for a period of time. Similar observations were made byMoyano et al. (2007).

The seasonal change of Rr was mainly dependent on thephenological stages (Fu et al., 2002; Jia et al., 2006), as recent carbonis the main source for Rr (Shi et al., 2006). It was reported thatseasonal patterns of soil CO2 efflux are driven by both currentphotosynthesis and photosynthate allocation to roots (Högberg et al.,2001) and are strongly correlated with biotic variables, such as rootbiomass and leaf area index (Shi et al., 2006). These biotic variablesmay influence soil respiration mainly by controlling root respiration,thus modifying the temperature response of soil respiration.

Faster growing rate of plants and higher root biomass generallyresult in higher root respiration (Schübler et al., 2000; Yi et al.,2007). During the fast growing stage, the rhizosphere respirationwas enhanced by the photosynthetic activity due to the allocationof assimilates into the roots and soil (Kuzyakov and Cheng, 2001).However, the fast growing stage did not coincide with themaximum value of root biomass in our study. Because in this stage,the relatively lower root biomass might restrict Rr, even when thephysiological activity was stronger. Thus, the seasonal change of Rrwas likely controlled by the combination of physiological activityand root biomass.

Fig. 7. Residuals (measured microbial respiration value e fitted microbial respirationvalue) plotted against (a) soil temperature at 2 cm (n ¼ 144) and (b) soil moisture at10 cm (n ¼ 108) in the study site.

4.3. Contribution of root respiration to total soil respiration

Because of the different responses of Rm and Rr to biotic andabiotic factors, the Rr/Rt ratios exhibited substantial diurnal andseasonal variations. The diurnal variation was mainly attributed tothe large variation of Rm, since the variation of Rr was relativelysmall. The much higher Rr/Rt ratio in nighttime is neglected bymany studies. This should be taken into account when assessing thecontribution of soil carbon to the atmospheric CO2.

The contribution of root respiration of different crops to the totalsoil respiration varies within a very broad range (from 8 to 85%)depending on the crop, development phase, soil types, environ-mental conditions and researchmethods employed (Andrews et al.,1999; Larionova et al., 2003; Chen et al., 2006). In the present study,the average Rr/Rt ratio in the whole growing seasonwas 67.3% with22.3% in the seedling stage and 86.6% in the reproductive stage. TheRr/Rt ratios in the studymaybe overestimated to some extent due tothe limitation of the method and CO2 absorption in the soil, butthe result was still comparable to other studies. Through the meta-analysis of the soil respiration partitioning studies from theliterature of the past 30 years, Subke et al. (2006) found that thecontribution of heterotrophic respiration of total soil respirationranged from 27 to 86% for the temperate and tropical agriculturesystems. Hanson et al. (2000) reviewed 50 reports and found thatthe Rr/Rt ratio ranged from 30 to 80%, with the mean ratio of 48%from autotrophic respiration for forest and 60% for non-forestecosystems. With root exclusion method, Larionova et al. (2006)found that the Rr/Rt ratios in corn, spring barley and bulk wheatcroplands were 69.4%, 37.6% and 88.2% in growing season, respec-tively. Singh et al. (1988) reported that the values of directmeasurements of root respiration in the laboratory accounted for10.8e37.8% of soil respiration in the growing season in a maizecropland. The result is much lower than ours. Different vegetationtypes and researchmethodsmaybe the reason. Furthermore, highersoil moisture (29.2e33.3%) might have led higher Rm in their study(1992.1e4503.9 mg CO2 m�2 d�1 in the growing season); while inour study, the lower Rm (437.2e1703.1 mg CO2 m�2 d�1) might beattributed to lower soil moisture (4.8e22.4%). The Rr/Rt ratio wasalso estimated to be 45% in awinterwheat system in growing season(Shi et al., 2006), 14% in a spring barley system (Larionova et al.,2003) and 26% in two barley fields (Paustian et al., 1990) for theentire year. Different study methods, crops, soil properties, timescales and definitions of root respiration make the results ofdifferent studies difficult to compare.

4.4. Carbon balance in the cropland system

The carbon input in the cropland ecosystem was higher thanoutputwithanetcarbon inputof140.8gCm�2y�1, suggesting that thecropland planted with S. italica (L.) Beauv. contributed to the seques-tration of atmospheric CO2 in 2007. When discuss the carbon balancein the cropland system, the after-use of the crops was not consideredhere, which is beyond the scope of the current investigation.

We also calculated the annual accumulation of Rm with dailymean soil temperature (2 cm depth) which appeared between11:00 and 12:00 h, and the carbon output was 137.0 g C m�2 y�1, orabout 13.0% higher than the former (121.3 g C m�2 y�1). It suggeststhat calculating with dailymean temperaturemay overestimate theannual carbon output on this site.

4.5. Methodological limitation

In the study, we successfully applied trenching method withmicro-pore mesh to measure different soil respiration components.This method has been confirmed as a useful tool for separating

X. Li et al. / Soil Biology & Biochemistry 42 (2010) 337e346 345

different components of soil respiration in a number of studiesreviewedbyLeakeet al. (2004).However, becauseof the limitationsofthe method, the Rr/Rt ratio might be overestimated. Firstly, thecreation of trenching plots would cause changes in soil temperatureand soil moisture. In the present study, the error was minimized bycorrecting the values with the difference between the planted andunplanted plots, but the priming effects of root to soil microbialactivitywasnot consideredand the intensitywasuncertain. Secondly,CO2 absorption in the soil may lead to underestimation of Rt and Rm,sequentially theoverestimationofRr/Rt ratios.However, the intensityof CO2 absorption in the soil is difficult to determinewith themethodtaken in the study. Further study is needed to understand themechanism of the CO2 consumption in the soil. Thirdly, anotherconcern with the trenching approach is the influence of residualdecomposing roots left in the trenchedplots and their contribution tosoil respiration (Hanson et al., 2000), but it was not likely to inducemuch influence in the cropland system. Because of the special harvestmethod, only a few fine roots in our study (15.1 g C m�2) were left insoil, which may have less effect in the next growing season.Furthermore, although root respiration is clearly a combination ofrootandmicroorganismsactivity inrhizosphere,wedidnotmake thisdistinction in the current study. In addition, the value of organiccarbon input through crop roots is an underestimation, as the rootmortality, root exudates, mucilages and sloughed cells are notconsidered. In spite of the shortcomings, it is averyuseful approach toroutinely measure soil and root respiration at low cost. Due to thisconvenience, it has beenwidely used to partition soil respiration intoautotrophic and heterotrophic components (Kelting et al., 1998;Bond-Lamberty et al., 2004; Jiang et al., 2005).

5. Conclusions

The present study for partitioning soil respiration and quanti-fying the carbon balance in a cropland on the Loess Plateau hasrevealed that:

Different components of soil respiration respond differently tobiotic and abiotic factors. The diurnal pattern of Rm was stronglyinfluenced by soil temperaturewhile Rrwas very sensitive to changesin photosynthesis. The dailymean values of Rt, Rm and Rrwere closeto those measured at 9:00 h. Calculating the annual accumulation ofRmwith daily mean soil temperature (usually occurs between 11:00and 12:00 h) would lead here to an overestimation of Rm by 13.0%.

The seasonal pattern of Rmcanbe better explained by the effects ofboth soil temperature and moisture, with soil temperature as theprimary factorandsoilmoisturesecondary.Thebivariatemodelfits themeasured resultswell, especiallywhen soil temperature andmoisturewere relatively low. The seasonal change of Rrwas likely controlled bythe combination of physiological activity and root biomass.

Large diurnal variations were observed in Rr/Rt ratios withhigher values in nighttime and lower values in daytime due to thedifferent responses of autotrophic and heterotrophic respiration tothe biotic and abiotic factors. This implies that the diurnal varia-tions in Rr/Rt ratio should be considered when other methods areemployed to partition soil respiration. In different phenologicalstages, Rr/Rt ratios ranged from 22.3% to 86.6%; while for the wholegrowing season, Rr/Rt ratios averaged 67.3%.

The annual carbon loss from the soil in the form of Rm totaled121.3 g C m�2 in the cropland system while the annual NPP (netprimary production) was 262.1 g C m�2, resulting in a net carboninput of 140.8 g C m�2 y�1 in 2007.

Acknowledgements

This study was sponsored by the National Natural Science Foun-dation of China (No. 90711002 and 30671485), the National Support

Project for Science and Technology in China (2008BAD95B03) andthe China National Key Projects for Basic Scientific Research(2006CB400501).

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