REGULAR ARTICLE

Impact of biochar application on nitrogen nutrition of rice,greenhouse-gas emissions and soil organic carbon dynamicsin two paddy soils of China

Zubin Xie & Yanping Xu & Gang Liu & Qi Liu &

Jianguo Zhu & Cong Tu & James E. Amonette &

Georg Cadisch & Jean W. H. Yong & Shuijin Hu

Received: 19 September 2012 /Accepted: 4 February 2013# Springer Science+Business Media Dordrecht 2013

AbstractAims Two field microcosm experiments and 15N label-ing techniques were used to investigate the effects ofbiochar addition on rice N nutrition and GHG emissionsin an Inceptisol and an Ultisol.

Methods Biochar N bioavailability and effect ofbiochar on fertilizer nitrogen-use efficiency (NUE)were studied by 15N-enriched wheat biochar (7.8803atom% 15N) and fertilizer urea (5.0026 atom% 15N)(Experiment I). Corn biochar and corn stalks were

Plant SoilDOI 10.1007/s11104-013-1636-x

Responsible Editor: Per Ambus.

Zubin Xie, Yanping Xu and Shuijin Hu contributed the same tothe paper.

Z. Xie (*) :Y. Xu :G. Liu :Q. Liu : J. ZhuState Key Laboratory of Soil and Sustainable Agriculture,Jiangsu Biochar Engineering Center, Institute of SoilScience, Chinese Academy of Sciences,Nanjing 210008, People’s Republic of Chinae-mail: zbxie@issas.ac.cn

Y. Xue-mail: wshxyp@126.com

G. Liue-mail: gliu@issas.ac.cn

Q. Liue-mail: liuq@issas.ac.cn

J. Zhue-mail: jgzhu@issas.ac.cn

Z. Xie :C. Tu : S. HuSoil Ecology Lab, Department of Plant Pathology,North Carolina State University,Raleigh, NC 27695, USA

C. Tue-mail: congtu62@yahoo.com

S. Hue-mail: shu4@ncsu.edu

Y. Xu :Q. LiuGraduate School of Chinese Academy of Sciences,Beijing 100039, People’s Republic of China

J. E. AmonetteChemical and Materials Sciences Division,Pacific Northwest National Laboratory,PO Box 999, MSIN: K8-96, Richland, WA 99352, USAe-mail: jim.amonette@pnl.gov

G. CadischInstitute of Plant Production and Agroecologyin the Tropics and Subtropics, University of Hohenheim,70593 Stuttgart, Germanye-mail: georg.cadisch@uni-hohenheim.de

J. W. H. YongLife Science, Singapore Universityof Technology and Design,20 Dove Drive, Singapore 138682, Singaporee-mail: jyong@sutd.edu.sg

applied at 12 Mgha−1 to study their effects on GHGemissions (Experiment II).Results Biochar had no significant impact on riceproduction and less than 2 % of the biochar N wasavailable to plants in the first season. Biochar additionincreased soil C and N contents and decreased ureaNUE. Seasonal cumulative CH4 emissions withbiochar were similar to the controls, but significantlylower than the local practice of straw amendment.N2O emissions with biochar were similar to the con-trol in the acidic Ultisol, but significantly higher in theslightly alkaline Inceptisol. Carbon-balance calcula-tions found no major losses of biochar-C.Conclusion Low bio-availability of biochar N did notmake a significantly impact on rice production or Nnutrition during the first year. Replacement of strawamendments with biochar could decrease CH4 emis-sions and increase SOC stocks.

Keywords Biochar . Greenhouse gases . Carbonsequestration . Nitrogen use efficiency . Rice

Introduction

Increases in atmospheric carbon dioxide (CO2), meth-ane (CH4), and nitrous oxide (N2O) concentrationscontribute to the increase of total radiative forcing(2.63 Wm−2) by 63 %, 18 % and 6 %, respectively(IPCC 2007a), raising concerns of associated climatechange. Of the global anthropogenic emissions in2005, agriculture accounts for about 60 % of N2Oand about 50 % of CH4 (IPCC 2007b). Judicious waysare needed to balance greenhouse-gas (GHG) sourcesand sinks in order to stabilize global mean surfacetemperatures (Mathews and Caldeira 2008), whilenot impairing the capacity of ecosystems to ensurefood security.

Amendment of soils with biochar (a solid materialobtained from biomass pyrolyzed under low/no oxy-gen environment) has been proposed as a potentialtechnique to abate climate change by sequesteringcarbon and reducing concomitant CH4 and N2O emis-sions (Lehmann 2007; Woolf et al. 2010). Woolf et al.(2010) estimated that biochar application can mitigateup to 12 % of the current annual anthropogenic CO2-Cequivalent emissions. Biochar materials, depending onthe production conditions, vary in their properties and,as a consequence, have potentially contrasting

behavior and impact on agro-ecosystems and the en-vironment. Shindo (1991) reported that the total CO2

flux from a soil amended with biochar from fire burn-ing was similar to that without biochar after 280 daysof incubation, indicating that biochar decomposedvery slowly. Similarly, after 2.9 years incubation underanaerobic conditions, 8.5 % of a rice-husk biochar C(made by farmer’s burning plus water spray) and2.9 % of a wheat straw biochar (pyrolyzed at 525 °C)at 35 % water holding capacity was mineralized(Knoblauch et al. 2011; Bruun et al. 2012). In contrast,Nguyen and Lehmann (2009) reported that the C loss ofbiochar derived from corn straw (pyrolyzed at 350 °C)was approximately 21 % after being incubated at 30 °Cin unsaturated water conditions for one year. Liu et al.(2011) further showed that amendments (equivalent to27 Mgha-1) of bamboo biochar and rice-straw biochar(pyrolyzed at 600 °C) were able to decrease CH4 emis-sions by up to 51 % and 91 %, respectively, whenincubated in a waterlogged paddy soil at 25 °C in thelaboratory for 7 weeks. In a separate study, however,Zhang et al. (2010a) reported that amendments (40 Mgha−1) with wheat-straw biochar (pyrolyzed at 350–550 °C) increased CH4 emissions by 37 % from a ricepaddy in the Tai Lake plain of China. These sparse andcontrasting results involving a wide variety of biocharshighlight the need for more studies to assess the stabilityof biochar C and the role of biochar in mitigating green-house gas emissions.

Plant growth is often limited by the availability ofN, and the production, transportation and utilization ofN fertilizer consumes large quantities of energy (e.g.,CO2-equivalent emission from 1 kgN manufacturingof calcium ammonium nitrate is 6.29 kg CO2 (Kern etal. 2010)). Amendment of biochar to soils was foundto increase soil fertility and enhance crop production,especially on soils with low fertility (Asai et al. 2009;Major et al. 2010; Jones et al. 2012; Solaiman et al.2012). However, no noticeable increase in productionfollowing biochar amendments has been reported insoils with high fertility, and some studies evenreported inhibition of plant growth (Gaskin et al.2010; van Zwieten et al. 2010; Zhang et al. 2010b;Haefele et al. 2011; Jones et al. 2012). The growth-stimulating effects are generally attributed to biochar’scapacity to supply nutrients, improve soil physicalstructure, increase soil pH (in acidic soils), and en-hance fertilizer-use efficiency stemming from its highsurface area and high cation-exchange capacity

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(Glaser et al. 2002; Asai et al. 2009; van Zwieten et al.2010). Recent observations by Taghizadeh-Toosi et al.(2012), which show that ammonia adsorbed at biocharcould be released to the soil and become available toryegrass, further illustrate biochar’s potential to en-hance fertilizer N-use efficiency by decreasing lossesof ammonia. Unfortunately, little work has been doneon the effect of biochar on fertilizer N-use efficiency.The N content of biochar is often higher than that of itsfeedstock (Knoblauch et al. 2011; Bruun et al. 2012),but the fraction of this N that is available for uprake byplants (N bioavailability) is not well known yet.Experiments are needed to assess the bioavailabilityof biochar N (i.e. the total N contained in biochar) andthe impact of biochar on fertilizer N-use efficiency(NUE) to better understand the factors of biochar thatpromote crop growth.

In this paper, field-microcosm and 15N-labelingtechniques were used to study biochar-N bioavailabil-ity and the effects of biochar on non-CO2 GHG emis-sions and soil-C dynamics, and to test the hypothesisthat biochar can enhance NUE of fertilizer urea duringthe first cropping season after its incorporation intosoil.

Materials and methods

Two microcosm experiments were carried out on twocontrasting soils. Experiment I used 15N-labeledwheat-straw biochar to assess the bioavailability ofbiochar-N to rice and to determine the effect ofunlabeled wheat-straw biochar on NUE of 15N labeledfertilizer. Experiment II investigated the impact ofcorn biochar on CH4 and N2O emissions and SOCdynamics.

15N labeling of wheat straw

Two 15N-enriched wheat straw materials were producedby applying 15N-enriched urea at 5 atom% 15N (herein-after referred as 15N−5 % wheat straw) or at 20 atom%15N (hereinafter referred as 15N−20 % wheat straw) togrowwheat plants in the field. To obtain a more uniform15N enrichment, 200 kgN ha−1 urea were split-applied 5times: at the seed-sowing stage (40 kgN ha−1), at the re-green stage (20 kgN ha−1), at the transition between thetillering stage and the jointing stage (40 kgN ha−1), atthe jointing stage (60 kgN ha−1), and at the heading

stage (40 kgN ha−1), respectively. Phosphorus (P)21.83 kgha−1 and potassium (K) 27.46 kgha−1 wereapplied at the seed-sowing stage as the normal practiceof local farmers. The wheat growth period was Nov. 16.2009 to Jun. 15, 2010. At crop maturity, wheat strawwas harvested. Wheat straw labeled with 15N−5 % ureawas subsequently used as a direct soil amendment;while straw labeled with 20 % 15N-enriched urea wasused for biochar production.

Biochar production

Biochar was produced under “no-oxygen” conditionsusing a patented slow-pyrolysis process (China patentNo. ZL200920232191.9). Before pyrolysis, unlabeledand 15N-20% wheat straw and unlabeled corn stalkswere oven-dried for 12 h at 80 °C, and then transferredinto the biochar reactor. The reactor was heated by astep-wise procedure. The temperature was set at 200 °Cinitially, and then elevated stepwise to 250 °C, 300 °C,350 °C and 400 °C. At each temperature step (except for400 °C), the process was maintained for 1.5 h. Thewhole process was flushed by N2 and terminated afterabout 10 h when there was no visible smoke emissionfrom the gas vent. Selected chemical properties of thedifferent biochars are listed in Table 1.

Paddy soil characteristics

Two contrasting soil types were used in these experi-ments. Soil classified as an Inceptisol (using the US SoilTaxonomy) was collected at Xiaoji town (119°42′E, 32°35′N), Jiangdu city, Jiangsu Province. This soilcontained 13.6 % clay (<0.002 mm), 28.5 % silt(0.002–0.05mm), and 57.8% sand (0.05–2 mm), whichcorresponds to the sandy loam textural class accordingto the US classification. An Ultisol was obtained fromLiujia station town (116°55′E,28°15′N), Yingtan city,Jiangxi Province, China. This soil contained 28.9 %clay, 34.7 % silt, and 37.3 % sand, corresponding to aclay loam textural class. Selected chemical properties ofthe two soils are presented in Table 1.

Microcosm experiments

Two microcosm experiments were conducted, one fo-cused on N bioavailability and NUE, and the other onemissions of non-CO2 greenhouse-gases and SOC dy-namics. The experiments were carried out in microcosms

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containing the two soils installed in a field in Xiaoji town(119°42′E, 32°35′N), at an elevation of 5 m above sealevel. Local climate data for Jiangdu City, JiangsuProvince include a mean annual precipitation of 1100–1200 mm, mean annual evaporation of >1100mm,meanannual temperature of 14–16 °C, more than 2000 h ofsunshine annually, and a frostless growing season ofabout 220 d.

Experiment I The objective of this experiment was toassess the bioavailability of wheat-biochar N to rice anddetermine the effect of biochar on NUE of 15N labeledfertilizer in a paddy rice system. The microcosms weremade from 5-mm-thick PVC (polyvinyl chloride) andhad inner dimensions (length×width×height) of200×150×250 mm. In Experiment I, the bottom of eachmicrocosm was sealed with the PVC to prevent 15Nleaching and gas exchange with the field soil. Theexperiment consisted of two soils (Inceptisol, Ultisol)each with 6 treatments: CK1 (non-amendment control),WBC (wheat straw biochar at 36 g microcosm−1 (12Mgha−1 equivalent)), 15N-WBC (15N-enriched wheat strawbiochar (7.8803 atom% 15N) at 36 g microcosm−1), 15N-WS (15N-enriched dry wheat straw (2.4867 atom% 15N)at 18 g microcosm−1 (6 Mgha−1 equivalent)), 15N-N(15N-enriched urea (5.0026 atom% 15N) at 0.75 gNmicrocosm−1 (250 kgN ha−1 equivalent)), and 15N-N +WBC (15N-enriched urea at 0.75 gN microcosm−1 andunlabeled wheat biochar at 36 g microcosm−1) (see de-tails in Table 2). The experiment was replicated threetimes in a completely randomized design with a distanceof about 10 cm between two microcosms.

Experiment II In this experiment the impact of corn-stalk biochar on CH4 and N2O emissions and SOCdynamics was determined. The microcosms used wereof the same dimensions and material as in Experiment I,but the bottom of each microcosm was wrapped withnylon mesh cloth (48-μm pore size) to allow free verti-cal movement of water and gas while preventing soil inthe microcosm from mixing with the field soil. Therewere two soils (Inceptisol, Ultisol) and 3 treatments inExperiment II: CK2 (0.75 gN microcosm−1 urea(250 kgN ha−1), but no biochar, no stalk), CS (dry cornstalk at 36 g microcosm−1 (12 Mgha−1)) and 0.75 gNmicrocosm−1 urea (250 kgN ha−1)), CBC (corn biocharat 36 g microcosm−1 and 0.75 gN microcosm−1 urea)(Table 2). Corn stalk material was obtained from localfarmer. As in Experiment I, Experiment II was replicat-ed three times in a completely randomized design.

The microcosms in both experiments contained5.4 kg of soil (oven-dried basis) that had been passedthrough a 4.76-mm mesh stainless steel sieve. Wheat-straw biochar, corn-stalk biochar, wheat straw andcorn stalks were cut to <2 cm in length, and thenwell-mixed with the respective soil in each micro-cosm. The mixtures were packed in the microcosmsto achieve a bulk density of 1.2 gcm−3 similar to thatof the local fields. The microcosms were placed intothe field soil at a depth of 15 cm and flooded on June20, 2010. On the next day, two 22-day-old rice seed-lings of cultivar ‘Wuxiangjing 14’ (inbred japonicacultivar) were transplanted to each microcosm. Thewater management was the same as local practice

Table 1 Selected chemical properties of the soils, straw (S) and biochar (BC) materials used in the experiment a

C N P K AP AK pH C/N 15N atom%gkg-1 gkg-1 gkg-1 gkg-1 mgkg-1 mgkg-1

Inceptisol 18.30 1.67 0.56 –b 9.2 47.8 7.60 13.56 0.3702

Ultisol 6.35 0.65 0.19 – 3.5 55.5 4.40 9.77 0.3685

Natural WS 423.5 4.70 0.35 22.57 238.8 – – 92.49 0.3765

WBC 632.7 5.70 0.89 48.93 473.4 – 10.12 111 0.372415N-WS 425.3 5.20 – – – – – 81.78 2.486715N-WBC 667.2 9.10 – – – – – 73.32 7.8803

CS 412.0 8.50 – – 803.8 – 6.50 48.47 –

CBC 597.7 13.4 2.47 13.42 806.7 – 9.6 44.60 –

a AP available phosphorus; AK available potassium;WS wheat straw;WBC biochar from wheat straw; CS corn stalk; CBC biochar fromcorn stalk;b not determined

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(i.e., flood-drainage-reflooding-moist). The microcosmswere kept waterlogged during the first 20 days (June 20to July 10, 2010). From July 10, the water in the micro-cosms began to be drained to keep rice from ineffectivetillering. From August 1 onwards, the microcosms wereflooded and kept moist alternatively. Nitrogen fertilizer asurea was applied in three applications: 90 kgha−1N wasapplied at the seedling transplantation, 60 kgha−1 was top-dressed during late June at the jointing stage and 100 kgha−1 in early August at the heading stage. Compoundphosphorus (P, 30.56 kgha−1) and potassium (K,38.45 kgha−1) were applied at seedling transplantation asbeing normal practice of local farmers. Rice was harvestedon Oct. 15, 2010 after a growing period of 117 d.

CH4 and N2O measurements

In order not to influence rice growth in Experiment I,CH4 and N2O fluxes were measured only in ExperimentII in the morning between 07:30 and 10:00, for every 6 to14 days during the rice growing season of 2010 using thestatic opaque chamber technique as described by Wangand Wang (2003). Briefly, PVC chambers with insidedimensions (length×width×height) of 20×15×50 cmwere attached to the tops of the microcosms and usedwhen the rice stalks were less than 50 cm in height. Taller

chambers (20×15×110 cm) were used when rice stalkswere higher than 50 cm. The chambers were wrappedwithinsulation (foamed plastic), and contained a battery-drivenfan and a silicon sampling septum. Four 20-mL air sam-ples from each chamber were collected with a plasticsyringe at 0, 15, 30 and 45 min after enclosure with fanrunning during the sampling period. Sampleswere injectedinto pre-evacuated 18-ml glass vials fitted with butyl rub-ber stoppers for subsequent analysis in the laboratory. Theair temperature inside the chamber was simultaneouslymeasured during sampling. The CH4 and N2O concentra-tions in the gas samples were determined using a Varian3380 gas chromatograph equipped with flame ionization(FID) and electron capture (ECD) detectors (VarianAmerica Inc., USA). The CH4 and N2O fluxes werecalculated using linear-regression analysis of the temporalchanges in CH4 and N2O concentrations in the chamberheadspace at the average chamber temperature.

Soil and plant analysis (C, N and 15N analysis)

At crop maturity, rice biomass (aboveground and be-lowground), grain and soil material were collected fromthe microcosms. Rice biomass and grain were oven-dried at 80 °C and soils were dried at 105 °C untilconstant weight was obtained (Lu 2000). Rice roots

Table 2 Treatments and their description

Treatment Material added

Biochar Straw Urea

15N labeled a 15N unlabeled b 15N labled c 15N unlabeled d 15N labelede 15N unlabeled

EX I CK1

WBC Wheat 1215N-WBC Wheat 1215N-WS Wheat 615N-N Urea 25015N-N+WBC Wheat 12 Urea 250

EX II CK2 Urea 250

CS Corn 12 Urea 250

CBC Corn 12 Urea 250

a Wheat-straw biochar with 7.8803 atom% 15 N at 12 Mgha−1 (=36 g microcosm−1 )b Wheat-straw biochar without 15 N labeling at 12 Mgha−1

c Wheat straw with 2.4867 atom% 15N at 6 Mgha−1 (=18 g microcosm−1 )d Corn stalks without 15 N labeling at 12 Mgha−1

e Urea with 5.0026 atom% 15 N at 250 kgha−1 (=0.75 g microcosm−1 )

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were separated, washed and oven-dried in Experiment I.Before soil C and N determination, visible plant residueswere carefully removed by hand from the soils. Toremove inorganic C, excess HCl was added to 20 g soil(in the form of a 10 % HCl [v/v] and 9.2 % FeSO4 [w/v]solution) until effervescence ceased. The soil sampleswere washed with deionized water and centrifuged at300 rpm (relative centrifugal force = 15g) several timesuntil the pH was similar to that of deionized water, andthen dried in an oven (Nelson 1982; Lu 2000). Total Cand N of soil and plant samples were analyzed by drycombustion (Perkin Elmer 2400, Series II CHNS/Oanalyzer, Perkin Elmer Inc., USA). Available phospho-rus (AP) of the Ultisol was extracted by HCl+NH4F(Bray method), AP of the Inceptisol and the biocharby NaHCO3 (Olsen method) and AK (availablepotasium) was extracted by CH3COONH4 (Lu 2000).The 15N abundance was determined using an isotope-ratio mass-spectrometer (Flash-2000 Ea-Delta VAdvantage, Thermo Finnigan, Germany).

Calculations and statistical analysis

The bioavailability of biochar-N to rice was estimatedby assessing the 15N recovery of 15N labeled biocharN (Nbioa) by rice as:

Nbioa% ¼ Nrb � 15Nrb�excess

Nb � 15Nb�excess� 100 ð1Þ

While the fertilizer NUE (NUEf) was calculated as15N recovery of 15N labeled urea as:

NUEf% ¼ Nrf � 15Nrf�excess

Nf � 15Nf�excess

� 100 ð2Þ

where Nrb (g) and Nrf (g) are total rice N uptake inbiochar and N-fertilizer treatments, respectively,15Nrb-excess and

15Nrf-excess are rice plant 15N abundanceexcess from the background rice 15N abundance inbiochar and N fertilizer treatments, respectively, Nb andNf are the total applied N in biochar and N fertilizer,respectively; and 15Nb-excess and

15Nf-excess are15N abun-

dance excess from background rice 15N abundance inbiochar and N fertilizer treatments, respectively.Background rice 15N abundance is the rice plant 15Natom% in the unlabeled control treatment (NWAC andSCAC 1980; Kaewpradit et al. 2009).

Soil-N retentions were calculated as corresponding15N recoveries:

NRRb% ¼ Nsb � 15Nsb�excess

Nb � 15N 0b�excess

� 100 ð3Þ

NRRf% ¼ Nsf � 15Nsf�excess

Nf � 15N 0f�excess

� 100 ð4Þ

where NRRb% and NRRf % are the proportion of appliedN retained in the soil after one rice season in biochar andN fertilizer treatments, respectively; Nsb and Nsf are totalsoil N pools in the 5.4 kg soil used in this experiment inbiochar and N fertilizer treatments after one rice season,respectively; 15Nsb-excess and

15Nsf-excess are soil15N abun-

dance excess from background soil 15N abundance inbiochar and N fertilizer treatments, respectively; and15N’b-excess and

15N’f-excess are15N abundance excess from

background soil 15N abundance in biochar and N fertil-izer, respectively. Background soil 15N abundance is thesoil 15N atom% in the unlabeled control treatment.

Statistical analyses of the results were performedusing the Univariate-Custom in General Linear Modelof SPSS (SPSS Inc. 2001) to test the effects of biocharon plant growth, biochar N bioavailability, fertilizerNUE, soil C, and CH4 and N2O emissions. Differenceswere considered significant only when P values werelower than 0.05.

Results

Influence of biochar on rice growth and total soil N

Application of biochar without urea did not significantlyaffect rice biomass relative to the control in theInceptisol (p=0.203) or the Ultisol (p=0.615) (Table 3).Comparing average biomass and grain yield in ureatreatments (15N-N, 15N-N+WBC) with non-urea treat-ments (CK1, WBC, 15N-WBC), revealed that N appli-cation significantly increased rice biomass by 45.8 %(p=0.017) and grain yield by 77 % (p=0.046) in theInceptisol. However, corresponding biomass increasesin the Ultisol were not statistically significant (p=0.085).Comparison of biomass and grain yields also showedthat the fertility of the Inceptisol was significantly higherthan that of the Ultisol (p<0.001, Table 3). Applicationof wheat-straw biochar or of wheat straw did not

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significantly change the N concentration in the ricebiomass (p=0.439 Inceptisol, and p=0.562 Ultisol,Table 4) relative to the control (CK1) treatment.

Results showed that wheat-straw biochar (15N-WBC), wheat straw (15N-WS), and urea-N applicationsignificantly increased soil-N content in the Inceptisol(p<0.001) and in the Ultisol (p<0.001) (Table 4).Although soil N content of the Inceptisol was signifi-cantly higher than that of the Ultisol (p<0.001), nosignificant difference in the N content of the rice grownin these two soils was seen (p=0.667).

Biochar N bioavailability and NUE

After the application of 15N-enriched wheat-strawbiochar (15N-WBC), 15N-enriched wheat straw(15N-WS) and 15N-enriched urea, soil 15N abundanceincreased significantly. Rice 15N abundance was signifi-cantly increased by the applications of 15N-enrichedwheat-straw biochar, 15N-enriched wheat straw and15N-enriched urea (Table 5).

The bioavailability of wheat-straw biochar N to rice Nnutrition was 1.5 % and 0.67 % over one season in theInceptisol and the Ultisol, respectively, while wheat-strawN bioavailability was 33.5 % and 23.3% in the Inceptisol

and the Ultisol, respectively. The mixed application ofbiochar and N (15N-N+WBC) significantly decreasedNUE in the Inceptisol, but not in the Ultisol comparedto the urea-N alone treatment (15N-N) (Table 5).

CH4 and N2O flux dynamics and cumulativeemissions during rice season

Under flooded conditions, CH4 emission by theInceptisol increased dramatically, especially in thecorn-stalk treatment. With drainage, the CH4 emis-sions in the corn-stalk treatment decreased butremained higher than in corn-stalk biochar and controltreatments until 69 days after transplanting (Fig. 1a).The corn-stalk amendment also increased CH4 emis-sions by the Ultisol more than the corn-stalk biocharand control treatments, but CH4 emission intensitywas lower than in the Inceptisol (Fig. 1).

N2O emissions by the Inceptisol were higher in thecorn-stalk biochar treatment than in the corn-stalk andcontrol treatments after drainage commenced (i.e.,20 days after transplanting) and during the late drain-age periods (69 to 116 days after transplanting). In theUltisol, no obvious differences in N2O emissionamong the treatments were found (Fig. 2).

Table 3 Rice biomass and grainyield (kgm−2) as affected bywheat-straw biochar (WBC),wheat-straw (WS), and nitrogen(N) application

a Mean±1standard error. Datawith the same lower letter in thesame column are not statisticallydifferent at p≤0.05, n=3

Treatments Inceptisol Ultisol

Biomass Grain yield Biomass Grain yield

CK1 2.98±0.48aa 0.96±0.33a 1.04±0.11ab 0.41±0.06a

WBC 2.06±0.25a 0.60±0.16a 0.96±0.11ab 0.36±0.10a15N-WBC 2.74±0.18a 1.05±0.12ab 0.84±0.18ab 0.29±0.08a15N-WS 2.79±0.25a 1.26±0.31ab 0.75±0.15b 0.35±0.12a15N-N 3.74±0.41b 1.73±0.37b 1.20±0.28ab 0.36±0.10a15N-N + WBC 3.82±0.5b 1.35±0.42b 1.25±0.30a 0.42±0.11a

Table 4 Nitrogen contents ofsoil and of rice plants afterwheat-straw biochar (WBC),wheat straw (WS), and urea-Namendments to an Inceptisol andan Ultisol

a Data with the same lower letterin the same column are not sta-tistically different at p≤0.05

Inceptisol Ultisol

Treatments Soil Ng/kg Rice N% Soil Ng/kg Rice N%

CK1 1.66±0.02aa 0.86±0.07ab 0.52±0.01a 0.81±0.06a

WBC 1.67±0.04a 0.88±0.07ab 0.59±0.03b 0.71±0.05a15N-WBC 1.94±0.00bc 0.74±0.06a 0.68±0.01cd 0.75±0.03a15N-WS 1.87±0.02b 0.85±0.05ab 0.60±0.01b 0.85±0.12ab15N-N 1.90±0.03bc 1.00±0.09b 0.63±0.01bc 1.05±0.08b15N-N +WBC 1.96±0.02c 0.83±0.15ab 0.70±0.02d 0.86±0.08ab

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Gas flux measurements revealed that the seasonalcumulative CH4 emissions from the corn-stalk amendedInceptisol (932 kgha−1) were about 4 times as high asthose from the corn-stalk biochar amended Inceptisol(230 kgha−1). The seasonal cumulative CH4 emissionsin corn-stalk amendments were significantly higher thanthose in the corn-stalk biochar amendments for bothsoils. The corn-stalk biochar amendment decreased cu-mulative CH4 emissions by both soils when comparedto the control treatment, but the difference was notstatistically significant (Fig. 3a).

The corn-stalk amendment had no significant im-pact on N2O emissions by the Inceptisol or the Ultisol.The corn-stalk biochar amendment also had no signif-icant impact on N2O emissions by the Ultisol.However, in the Inceptisol, the corn-stalk biocharamendment significantly increased N2O emissionscompared to those of the corn-stalk amendment aswell as to those from the corn-stalk biochar amend-ment to the Ultisol (Fig. 3b).

SOC dynamics

Wheat-straw and corn-stalk amendments caused on-ly minor changes in the SOC stocks. Biocharamendments, on the other hand, significantly in-creased SOC. The apparent C losses (estimated asdifference of added biochar C and SOC stockchange before and after biochar amendment in onerice season) from biochar were 15.8 % in theInceptisol and undetectable in the Ultisol treatments(Table 6).

Table 5 15N dynamics in soil and rice, biochar N bioavailability (Nbioa), N use efficiency (NUE) and soil N retention from wheat-strawbiochar (WBC), wheat straw (WS), and nitrogen (N) in the Inceptisol and the Ultisol by 15N labeling technique

Treatments Inceptisol Ultisol

Soil 15Natom %

Plant 15Natom %

Nbioa% orNUE %

Soil N retentionrate %

Soil 15Natom %

Plant 15Natom %

Nbioa% orNUE %

Soil N retentionrate %

CK1 0.372aa 0.380a 0.381aa 0.393a

WBC 0.370a 0.400ab 0.381a 0.457ac15N-WBC 0.688c 0.442b 1.50a 111.5a 1.311b 0.478ad 0.67a 99.98a15N-WS 0.385b 0.476b 33.53b 60.49b 0.413c 0.642bcd 23.35b 52.42b15N-N 0.449d 1.761c 41.74c 21.69c 0.553d 2.780e 24.32b 16.05c15N-N+WBC

0.461d 1.859d 33.77d 23.87c 0.587d 2.642e 18.75b 19.84c

a Data with the same lower letter in the same column are not statistically different at p≤0.05, n=3

CH

4 fl

ux (

mg

m-2

h-1

)

-50

0

50

100

150

200CK2CSCBC

Days after transplanting

0 20 40 60 80 100 120

CH

4 fl

ux (

mg

m-2

h-1

)

-10

0

10

20

30

40

50

CK2CSCBC

a

b

Fig. 1 CH4 flux dynamics after corn-stalk biochar (CBC) andcorn stalk (CS) amendments during rice season in Inceptisol (a)and Ultisol (b). CK2 indicates control treatment without CS andCBC. Single arrow indicates the day when drainage began. Dou-ble arrow indicates the day when flooding and moist water man-agement began. Error bars indicate one standard error (n=3)

Plant Soil

Discussions

Biochar N bioavailability and fertilizer NUE

The low biochar N bioavailability (<2 %) was likelycaused by the formation of heterocyclic compoundssuch as pyrroles, imidazoles and pyridines (black N)during the heating process involved in making biochar(Knicker 2010). The results indicated that once plantbiomass is converted to biochar, N inherited from theplant biomass does not directly improve soil fertility,at least in the short-term. Thus, biochar is clearly not aN fertilizer in the usual sense. However, because near-ly all biochar N remained in the soils after one ricecrop season (Table 5); the long-term effects of biocharN need further investigation.

Contrary to our hypothesis, biochar application de-creased urea NUE in both soils, although the decrease

was statistically significant only for the Inceptisol(Table 5). Possible mechanisms for this biochar-induced decrease in NUE include retention of N bybiochar, inhibition of plant development by increasedpH, volatilization of NH3, and losses of other N gasesas a result of nitrification and denitrification (Cassmanet al. 2002; Liang et al. 2006; Steiner et al. 2008;DeLuca et al. 2009). Although Taghizadeh-Toosi etal. (2012) observed that NH3 adsorption was muchhigher on acidic biochar than on alkaline biochar, nosignificant effect of biochar on fertilizer-N retention insoils was found in our experiment (Table 5), and wethus, discounted this possibility.

One reason for a biochar-induced decrease of NUEmight be an inhibitory effect of biochar on early plantdevelopment. Zhang et al. (2010b) observed a slowingof plant development when biochar was applied to thesame Inceptisol and attributed it to the possible effects

N2O

flu

x (m

g m

-2 h

-1)

-.5

0.0

.5

1.0

1.5

CK2CSCBC

Days after transplanting

0 20 40 60 80 100 120

N2O

flu

x (m

g m

-2 h

-1)

-.5

0.0

.5

1.0

a

b

Fig. 2 N2O flux dynamics after corn-stalk biochar (CBC) and cornstalk (CS) amendments during rice season in Inceptisol (a) andUltisol (b). CK2 indicates control treatment without CS and CBC.Single arrow indicates the day when drainage began.Double arrowindicates the day when flooding and moist water managementbegan. Error bars indicate one standard error (n=3)

Sea

son

al c

um

ula

tiv

e C

H4

em

issi

on

s

(k

g h

a-1

)

0

300

600

900

1200

Inceptisol

Ultisol

a

b

aa

a

b

Corn stalk (CS) and corn biochar (CBC) amendment

CK2 CS CBC

Sea

son

al c

um

ula

tiv

e N

2O

em

issi

on

s

(k

g h

a-1)

0

1

2

3

4

5

a

a

b

a a

a

Inceptisol

Ultisol

a

b

aa

a

b

a

b

Fig 3 Impacts of corn stalk (CS) and corn-stalk biochar (CBC)amendment on seasonal cumulative CH4 (a) and N2O (b) emis-sions in Inceptisol and Ultisol. CK2 indicates control treatmentwithout CS and CBC. The same lower letter on the bars with thesame legend indicates that the data are not statistically differentat p≤0.05. Error bars indicate one standard error (n=3)

Plant Soil

of secondary compounds associated with the biochar.A similar effect was noted by Deenik et al. (2011),who attributed a temporary decrease in plant growth tohigh contents of volatile matter in one of the biocharsthey tested. The volatile matter was bioavailable andlikely caused N immobilization which would havedecreased NUE.

Another reason for decrease NUE might bebiochar-enhanced NH3 volatilization. Volatilizationof NH3 in the already alkaline soil (pH=7.6, Table 1)would certainly be enhanced by amendments withhighly alkaline wheat-straw biochar (pH= 10.12) witha resultant decrease in the N balance and slowing ofearly development of the plant. Increased NH3 emis-sions stemming from biochar amendments were notedby DeLuca et al. (2009) and, this mechanism, togetherwith the observed elevated N2O emissions (nitrifica-tion and denitrification) (Fig. 3b), likely reduced plant-available fertilizer-N. Eventhough biochar amended toeach microcosm in the 15N+WBC treatment contained0.2 gN (equivalent to 68 kgN ha−1), due to its lowbioavailability of nitrogen in the biochar (Table 5), theN in the biochar might not play a significant role onsoil N transformation. To better understand the mech-anisms involved in the decrease in NUE by biochar,more research is needed.

Effect of biochar on rice growth

Biochar often enhances crop growth in poor soils, butexhibits either no effect or a slight negative effect infertile soils (Asai et al. 2009; Haefele et al. 2011; Uzoma

et al. 2011). However, we observed no significant effectof wheat-straw biochar amendments on rice biomassand grain yield in both the fertile Inceptisol and therelatively infertile Ultisol (Table 3). Asai et al. (2009)found biochar enhanced upland rice yield at sites withlow P availability. Similarly, Uzoma et al. (2011) ob-served that the highest corn yield was obtained at abiochar application rate of 15 Mgha−1, and the yieldincreases were attributed to greater P availability. Incontrast, Blackwell et al. (2010) did not find steadyenhancement of wheat-grain yield following increasingbiochar amendments under different climate conditions,and even reported some negative effects (p > 0.1) at thehighest biochar application rates (10 Mgha−1).Enhanced yields resulting from biochar amendmentcoupled with application of 7 kgha−1 of water-soluble-phosphate were interpreted as the result of an improvedP supply due to increased colonization by arbuscularmycorrhizal fungi (Blackwell et al. 2010). In our exper-iment, P might not have been a limiting factor to ricegrowth due to the application of 30.56 kgha−1 P. Inaddition, water-soluble phosphate and P availabilityincrease under the reducing environment of a floodedpaddy soil (Kyuma 2004). Thus, high P availabilitymight, in part, explain why no significant influence ofbiochar on rice growth was seen in our experiment.

Nitrogen is generally the main limiting nutrient indetermining rice growth and productivity. The increasein rice biomass production by both the Inceptisol and theUltisol soil in response to urea-N application highlightsthe importance of N supply in these two soils (Table 3).Even though there was sufficient total N in the biochar

Table 6 Effects of biochar and straw amendments on SOC stocks in the microcosms (0–15 cm) after one rice season (kgm−2), mean±se

CKb Wheat straw Wheat-straw biochar Corn stalk Corn-stalk biocharkgm−2

Inceptisol 3.26±0.14aa 3.33±0.10a 3.93±0.08b 3.25±0.07a 4.03±0.14b

Ultisol 1.18±0.03a 1.12±0.03a 1.94±0.01b 1.21±0.02a 1.90±0.06b

C inputc 0 0.25 0.76 0.49 0.72

Cincrementd

Inceptisol −0.03±0.14a 0.04±0.10a 0.64±0.08b −0.04±0.07a 0.74±0.14b

Ultisol 0.04±0.03a −0.03±0.02a 0.80±0.01b 0.06±0.02a 0.76±0.06b

a Data with the same lower letter in the same row are not statistically different at p≤0.05, n=3b Data in CK are average of data in treatment CK1 and CK2c C input = straw (or biochar) amendment quantity ×C contentd C increment = the difference between the final C stocks and the initial C stocks (i.e., Cfinal-Cinitial) before the experiment. Before theexperiment, the soil C stocks in the Inceptisol and the Ultisol were 3.29 kgm−2 and 1.14 kgm−2 , respectively

Plant Soil

(equivalent to 68.4 kgha−1), this N did not play anymajor role on rice growth due to its low bioavailability(<2 %, Table 5), and even decreased fertilizer-N acces-sibility during the first year after amendment.

Emissions of CH4 and N2O and SOC dynamics

In Experiment II, applying biochar pyrolyzed from cornstalks rather than applying corn stalks significantly de-creased CH4 emissions by both soils tested. This wassubstantiated by calculations of the net CH4 emissionsper unit of C applied (i.e., the difference between thetotal CH4 emission from the treatments with biochar orstraw and the control treatment divided by the amount ofC in the biochar or straw amendment). Net CH4 emis-sions by the Inceptisol with biochar were 133 kg lowerper Mg C applied than those with the corn-stalk amend-ment. For the Ultisol, the comparable decrease withbiochar was 24 kg per Mg C applied relative to amend-ment with corn-stalks. There have been several reportson the influence of biochar on CH4 emissions in paddysoils in recent years (Singh et al. 2010; Zhang et al.2010a; Knoblauch et al. 2011; Wang et al. 2011; Zhanget al. 2012). Paddy-soil CH4 emission is strongly affect-ed by SOC availability (Watanabe et al. 1998; Majumdar2003; Yan et al. 2005; Xie et al. 2010). Our results thusindicate that, due to the recalcitrance of biochar (Jones etal. 2011; Knoblauch et al. 2011; Zimmerman et al. 2011),no significant alterations in C availability are induced bybiochar addition. In contrast, addition of fresh cerealstraw materials generally enhance C availability andhence CH4 emissions (Khalil and Inubushi 2007; Xieet al. 2010). Hence, our results largely confirm observa-tions by Knoblauch et al. (2011) who found no majorincrease in CH4 emissions after biochar amendmentunder field conditions. Additionally, Feng et al. (2012)using PCR-DGGE and real-time quantitative PCR(qPCR) techniques, found that the observed decrease inCH4 emission by biochar addition was due to an increaseof methanotrophic bacteria, and a decrease in the ratio ofmethanogenic to methanotrophic bacterial abundances.

The influence of corn-stalk amendment on CH4

emission was much larger in the Inceptisol than inthe Ultisol (Fig.3). Methane emissions in paddy soilare the result of the balance of methanogenic andmethanotrophic processes (Feng et al. 2012) andCH4 production is initiated at a soil Eh of −150 mV(Majumdar 2003). Ultisols contain large amounts ofoxidizing minerals (i.e., Fe2O3 and MnO2) (Wang and

Cai 2008) and little organic matter (Table 1). Due tothis large redox buffer capacity, once an Ultisol isflooded, it will take several days longer to reach a soilEh of −150 mV than an Inceptisol. Hence, we specu-late that in our experiment the lower CH4 emissions inthe Ultisol might be related to maintenance of a highersoil Eh than in the Inceptisol due the combination ofmore oxidizing minerals in the soil and a relativelyshort period (20 d) of continuous flooding.

Previous studies have demonstrated that N fertiliza-tion suppresses CH4 oxidation and results in higher CH4

emissions (Dubey 2003; Hanson and Hanson 1996). Ameta-analysis by Banger et al. (2012) find that theresponse of CH4 emission per kgN fertilizer was signif-icantly higher at <140 kgN ha−1yr−1 (0.51 kg CH4-Cha−1kg−1N) than at > 140 kgN ha−1yr−1 (−0.04 kgCH4-C ha−1kg−1N) in the rice-production soils. Theseresults indicate that eventhough N availability washigher in the Inceptisol than in the Ultisol (Table 1), itwould not be the main factor inducing higher CH4

emissions by the Inceptisol than by the Ultisol.While the corn-stalk biochar amendment decreased

CH4 emissions it significantly increased N2O emis-sions by the Inceptisol compared to the control treat-ment (Fig. 3). Kammann et al. (2012) found that at80 % water holding capacity, biochar amendment sig-nificantly increased N2O emission, during an 18-month incubation, especially when fertilizer N wasincorporated. Yanai et al. (2007) also observed in-creased N2O emissions with biochar-amended soil at83 % water filled pore space (WFPS), but at lowerWFPS they reported a significant reduction. However,Wang et al. (2011) reported that a 50 Mgha−1 rice-husk biochar amendment decreased N2O emission by73 % over a 60-day anaerobic incubation period.Similarly, Zhang et al. (2012) observed decreasedN2O emissions after biochar amendments in a two-year rice season field experiment. The increased N2Oemissions by the Inceptisol receiving the corn-stalkbiochar amendment might be due to the lower bulkdensity of this soil and hence faster water drainage,which would tend to increase nitrification of ammonia(Suratno et al. 1998) and decrease N2O reduction toN2 (Yao et al. 2012). In paddy fields during water-logged periods, inorganic N mainly exists as NH4

+,however, during drainage periods, NO3

- and NO2-

concentrations increase greatly (Yan et al. 2000; Li etal. 2009). Yao et al. (2012) found drainage greatlyincreased N2O emission whereas, under flooded

Plant Soil

conditions, N2O emissions were negligible in threecontinuous years. Sharp increases of N2O emissionin rice fields have been well-documented during thedrainage periods (Bronson et al. 1997; Cai et al. 1997;Seneviratne and van Holm 1998). In the Ultisol, thebiochar amendment did not significantly increase N2Oemissions. The reason for this result probably was dueto the high clay content of the soil, which preventedflood water from drainage and thus kept N2O produc-tion from increasing. But the mechanisms of biocharamendment affecting N2O emission need furtherinvestigation.

Estimated C losses from biochar were negligibleover the 117-d experimental period, apart from the15.5 % wheat-straw biochar C loss in the Inceptisol.Although, C-balance calculations are not highly accu-rate, the low degradability of biochar was confirmedby Knoblauch et al. (2011) who found that after2.9 years of incubation, a rice-husk biochar lost only4.4 % and 8.5 % of its C by mineralization to CO2

under aerobic and anaerobic conditions, respectively.Also, Kuzyakov et al. (2009) incubated rye grassbiochar under aerobic conditions and found that after3.2 years, about 4 % of the rye grass biochar C wasdegraded to CO2, and in the first 2 months the degra-dation rate of biochar C was 1.8–2.1 %. It is thusevident that biochar C amendments can increase soilC pools and greatly mitigate CH4 emissions duringrice production compared with the conventional strawamendment.

Conclusions

The bioavailability of N in a wheat-straw biochar isvery low and amendment with this biochar does notincrease fertilizer NUE or rice growth during the firstyear after application. Biochar amendments can in-crease SOC pools due to the slow degradation rate ofbiochar in soil. The replacement of conventional strawamendments to paddy rice soils with amendments ofbiochar made from the same straw can significantlydecrease CH4 emissions. Corn biochar was found toenhance N2O emission in the Inceptisol during thedrainage period, and its mechanisms need to be stud-ied. However, to properly evaluate the effects ofbiochar on greenhouse gas mitigation, crop productionand food security, it is important to address the nega-tive effects induced by biochar application in

agricultural fields, such as polycyclic aromatic hydro-carbons (PAHs) and phenols.

Acknowledgments We wish to express our gratitude to theNatural Science Foundation of China (41171191, 40871146),Chinese Academy of Sciences (KZCX2-YW-Q1-07, KZCX2-EW-409), Ministry of Science and Technology of China(2008BAD95B05) and Blue Moon Fund, USA for financialsupport. The constructive comments of the two anonymousreviewers are highly appreciated.

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