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Chemosphere 186 (2017) 928e937

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Chemosphere

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Effect of biochar and Fe-biochar on Cd and As mobility and transfer insoil-rice system

Daixia Yin a, b, Xin Wang a, *, Bo Peng a, Changyin Tan a, Lena Q. Ma b, c

a College of Resources and Environmental Science, Hunan Normal University, Changsha, Hunan 410081, Chinab State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu 210023, Chinac Soil and Water Science Department, University of Florida, Gainesville, FL 32611, USA

h i g h l i g h t s

* Corresponding author.E-mail address: hdhuanjing@163.com (X. Wang).

http://dx.doi.org/10.1016/j.chemosphere.2017.07.1260045-6535/© 2017 Published by Elsevier Ltd.

g r a p h i c a l a b s t r a c t

� Biochar reduced rhizosphere pore-water Cd, but increased As solubility.

� Fe-biochar decreased soluble As inrice rhizosphere, but enhanced Cdmobility.

� Cd and As accumulation in rice rootswas decreased by biochar and Fe-biochar, respectively.

� As and Cd transfer into roots wasenhanced respectively due to rhizo-sphere mobilization by biochar andFe-biochar.

a r t i c l e i n f o

Article history:Received 2 May 2017Received in revised form12 July 2017Accepted 25 July 2017Available online 26 July 2017

Handling Editor: X. Cao

Keywords:BiocharIron-impregnated biocharArsenicCadmiumPaddy soilsRice grains

a b s t r a c t

In this study, the effects of biochar derived from rice-straw (biochar) and iron-impregnated biochar (Fe-biochar) on Cd and As mobility in rice rhizosphere and transfer from soil to rice were investigated withdifferent application rates. 1e3% biochar reduced porewater Cd in rhizosphere but elevated soluble As,resulting in 49e68% and 26e49% reduction in the root and grain Cd, with a simultaneous increase in rootAs. Unlike biochar, 0.5% Fe-biochar decreased porewater As throughout rice growth, resulting in reducedroot As, which, however, increased Cd uptake by root. Biochar-induced soil As mobilization was probablythrough competitive desorption and Fe-biochar-induced soil Cd mobilization was probably via soilacidification. The results suggested that biochar and Fe-biochar was effective in reducing Cd and Asuptake by rice, respectively, so they may be used as emergency measures to cope with single Cd or Ascontamination in paddy soils.

© 2017 Published by Elsevier Ltd.

1. Introduction

Cadmium (Cd) and arsenic (As) are the most prominent metal

contaminants in soils in China based on 2014 national soil survey byChina Ministry of Environmental Protection and Ministry of Landand Resources. Being human carcinogens (Tully et al., 2000; Stone,2008), the prevalence of Cd and As contamination in soils is of greatenvironmental concern and has attracted much attention aboutfood safety. As the heartland of Chinese nonferrous mining sites,Hunan province is also the primary rice-producing area in China.

Table 1Basic properties of original soil, biochar and Fe-biochar (n ¼ 3).

Properties Value

Soil Sand (%) 28.5 (±3.4)Silt (%) 20.1 (±2.1)Clay (%) 51.4 (±4.1)pH (H2O) 5.35 (±0.1)CEC (cmol kg�1) 11.4 (±0.7)TOC (mg kg�1) 24.6 (±1.6)Available_P (mg kg�1) 0.40 (±0.1)Total K (g kg�1) 23.2 (±2.5)Pseudo-total Fe (g kg�1) 31.0 (±0.2)Pseudo-total As (mg kg�1) 212 (±11.3)Pseudo-total Cd (mg kg�1) 10.8 (±0.2)

Biochar pH (H2O) 10.7 (±0.1)CEC (cmol kg�1) 15.1 (±0.9)Available_P (mg kg�1) 46.9 (±5.5)Pseudo-total Fe (g kg�1) 0.74 (±0.4)Pseudo-total As (mg kg�1) 10.6 (±0.3)Pseudo-total Cd (mg kg�1) 0.00 (±0)

Fe-biochar pH (H2O) 4.87 (±0.3)CEC (cmol kg�1) 14.2 (±0.5)Available_P (mg kg�1) 55.1 (±1.3)Pseudo-total Fe (g kg�1) 35.5 (±0.1)Pseudo-total As (mg kg�1) 9.30 (±0.4)Pseudo-total Cd (mg kg�1) 0.01 (±0)

D. Yin et al. / Chemosphere 186 (2017) 928e937 929

Due to past mining and metal processing activities, paddy soils inHunan are contaminated with both Cd and As (Williams et al.,2009; Zhao et al., 2015; Zheng et al., 2015). The Cd and As con-centrations in mine-impacted paddy soils in Hunan are 0.26e37and 34e2268 mg kg�1 (Williams et al., 2009; Hu et al., 2015; Leiet al., 2015; Zheng et al., 2015; Chen et al., 2016; Yin et al., 2016),far exceeding Chinese National Environmental Quality Standardsfor agriculture soil, which is 1.0 mg kg�1 Cd and 30 mg kg�1 As inflooded soils (GB15618-1995).

Compared with other crops, paddy rice (Oryza sativa L.) is moreefficient in Cd and As uptake and translocation, leading to signifi-cant soil-to-rice transfer and grain accumulation of Cd and As (Suet al., 2010; Uraguchi and Fujiwara, 2012; Zhao et al., 2012).Consequently, Cd and As exposure from rice consumption is ofthreat to public health. Therefore, effective control of Cd and Astransfer in soil-rice system is an urgent challenge for food-safety inChina.

Biochar produced from agricultural wastes by pyrolysis at rela-tively low temperatures (<700 �C) has potential to immobilizemetals in soils (Beesley and Marmiroli, 2011; Ding et al., 2016).Biochar is effective in reducing soluble Cd in Cd-contaminated soils(Bian et al., 2013; Zheng et al., 2015; Suksabye et al., 2016; Yin et al.,2016). However, the decrease in rice grain Cd was achieved withhigh application rates of biochar at >5% (Bian et al., 2013). Tominimize its adverse effects on agriculture soils, biochar rateshould be <5% (Matovic, 2011). Therefore, it is important to deter-mine the effect of biochar at relatively low application rate on Cdtransfer from paddy soil to rice plants.

Unlike Cd, As species in most soils exist mainly as oxyanions andexhibit a high affinity for Fe oxides. Based on this fact, biochar hasbeen used as a cost-effective supporting material to producecomposite sorbents by loading nanoscale Fe oxides onto the coarsebiochar surface, which has exhibited a high capacity for As removalfrom aqueous solutions (Gu et al., 2005; Jim�enez-Cedillo et al.,2013; Zhang et al., 2016). Compared with the powder of Fe(0) orFe oxyhydroxides, Fe-biochar composite had an apparently higherporosity (Hanaoka and Okumura, 2014), which could thus mini-mize their negative effect on soil aggregate cementation. But theeffect of Fe-impregnated biochar on As mobility and transfer in thepaddy soil-rice system has yet to be unraveled. In particular, withco-occurrence of Cd contamination in paddy soil, it is not clearwhether the incorporation of Fe-loaded biochar could induce Cdmobilization and increase Cd accumulation in rice via soilacidification.

To narrow these knowledge gap, we conducted a greenhouseexperiment using a paddy soil contaminated with both Cd and As.The objective of this study was to explore the effects of biochar andFe-biochar application on rhizosphere mobility, root uptake, planttransfer and grain accumulation of Cd and As in the paddy soil-ricesystem.

2. Materials and methods

2.1. Soil collection and preparation of biochar and Fe-biochar

In this study, the soil co-contaminated with Cd and As wascollected from a paddy field near Shizhuyuan mining district inChenzhou, Hunan province (Fig. S1, Lat/Long: 25� 490 N, 113� 080 E)in June 2015. This area is known by densely-distributed mining,mineral processing and smelting plants. The nearby farmlandswere contaminated with heavymetals (Liu et al., 2005). Surface soilsamples (0e20 cm) were collected, air-dried and sieved through a5 mm sieve for the greenhouse experiment. A representative sub-samplewas further grinded to<2mm for analysis of soil properties,including texture, pH, CEC, TOC, available P, total K, pseudo-total As,

Cd and Fe (Table 1).Rice straw was obtained from a clean paddy field in Anhui

province, China. The oven-dried feedstocks were subjected to slowpyrolysis under a continuous N2 flow (Thermo Scientific, USA). Thetemperature was raised at 6 �C min�1 and kept at 450 �C for 1 h.After cooling to room temperature in a N2 atmosphere, the prod-ucts were ground and sieved to <2 mm, which is referred as bio-char. To prepare Fe-biochar (Fe-biochar), a part of biochar wasadded into 0.1 M FeCl2 at 1:15 (g/ml) solid/solution ratio and themixture was shaken for 24 h at 25 �C. During themixing, NaClOwasadded four times with a 6-h interval at ratio of FeCl2/NaClO ¼ 6.4 g/20 ml (Gu et al., 2005). The solution pH was controlled at 4.5e5.0with 1 M HCl or NaOH. At this pH, soluble Fe(II) could diffuse deepinto the internal pores of biochar to achieve homogeneous Fefollowing in-situ oxidation of Fe(II) to Fe(III) by NaClO. The Fe-biochar samples were washed thoroughly with deionized waterfollowed by drying at 60 �C for 48 h and crushed to pass through a2 mm sieve.

2.2. Greenhouse experiments

Based on our preliminary experiments, 1, 2, and 3% (w/w) bio-char and 0.5, 1, and 2% (w/w) Fe-biochar were applied into paddysoils, which were thoroughly mixed before being placed into PVCpots (24 � 28 cm dxh). Control soil was also included (CK). Eachtreatment had three replicates, with 4.5 kg soil in each pot. Inaddition, CO(NH2)2 and K2HPO4 were incorporated as the basalfertilizer at 120 mg N kg�1, 30 mg P kg�1 and 75.7 mg K kg�1 (Khanet al., 2013). The pots were placed in a nature climate greenhouseand the soils was saturated with deionized water for 5 days. Thenthree pregerminated rice seeds (Oryza sativa L. cv. Zhuliangyou 611,a hybrid cultivar commonly grown in Hunan) were planted in eachpot. Rice growth lasted for a total of 106 days from July 27th toNovember 10th with the average temperature of 28.5/21.2 �C (day/night) and humidity of 79%. Continuous flooding with ~4 cmstanding water was kept in rice seedling stage (initial 30 days) andthe pots were then allowed to dry until small, surface cracks werepresent, at which point the soils were reflooded. Before heading,

D. Yin et al. / Chemosphere 186 (2017) 928e937930

the pots were drained again followed by continuous flooding until10 days before harvest.

2.3. Porewater sampling and analysis

In each pot, one rhizon sampler (Rhizosphere Research Prod-ucts, Netherlands) was inserted to a depth of ~8 cm in the rootingzone at 20 d after planting. After 10-d equilibration, porewatersamples were extracted at 7-d intervals. In parallel with porewatercollection, the redox potential (Eh) and pH of rhizosphere soilswere measured in situ using an automated oxidation- reductionpotential analyzer with redox and pH electrodes (Nanjing Chuan-DiInstrument & Equipment CO, China). Total As in porewater wasdetermined by an atomic fluorescence spectrometer (AFS, Hai-guang 9700, Beijing), while Cd and Fe concentrations were detectedusing an atomic absorption spectrophotometer (AAS, Perkin ElmerAAnalyst 900T).

2.4. Soil sampling and analysis

At harvest, the intact rice plants were carefully dug out frompots. The soils tightly adhering to rice root was then manuallycollected by gentle tapping and referred to as rhizosphere soils. Therhizosphere soils were air-dried, and ground to <0.2 mm prior tomicrowave digestion for total Fe, As and Cd. Furthermore, twodistinct sequential extraction methods were employed to investi-gate the amendments effects on As (Lessl et al., 2014) and Cd(Tessier et al., 1979) fractionation in the rhizosphere soils, respec-tively. Detailed descriptions of the two extraction procedures canbe found in Table S1.

2.5. Plant sampling and analysis

After 106 d of cultivation, rice plants were harvested at grainmaturity. Rice roots were thoroughly washed with tap water anddeionized water. The shoots were excised and the rice grains wereseparated into husk and brown rice. They were oven-dried at 65 �Cfor 3 d and then ground before microwave-digestion (CEMMARS 6,Matthews, NC, USA) with HNO3/HCl (EPA Method 3051a) for totalAs, Fe, and Cd.

To further identify the effect of Fe-biochar on Fe plaque for-mation on root surface and associated As sequestration, excised riceroots (0.25e0.84 g, dw) were extracted using 40 ml of dithionite-citrate-bicarbonate (DCB) solution containing 0.03 M Na3C6H5O7,0.125 M NaHCO3 and 0.06 M Na2S2O4 for 30 min at room temper-ature (Zheng et al., 2012). Moreover, the middle part of a fine lateralroot was collected from the control and 2% Fe-biochar treatment form X-ray fluorescence imaging. The fresh root samples were freeze-dried after washing with deionized water. The m X-ray fluorescenceimaging was conducted at Shanghai Synchrotron Radiation Facilitybeamline 15U1, which is a hard X-ray microprobe scanningbeamline. The root sample affixed to stick tape was installed ontoan Al-sample holder placed at 45� to the incident beam. Utilizing a100 mm step size and 1.5 s dwell time per pixel, root sample wasimaged at an incident X-ray energy of 14 keV.

2.6. Quality assurance and quality control

Each treatment had three replicate pots with three plants ineach pot. Plant material from three plants in each pot was mixed,representing one replicate. One digestion blank, one spike, and onestandard reference soil GBW07403 (GSS-3) or one rice flour refer-ence material GBW10045 (GSB-23) (National Research Center forStandards in China) were included in digestion of 40 samples.

During analysis, one analytical blank, five standards, one calibrationverification standard and one continuing calibration standard wereincluded every 20 samples. The relative standard deviation (RSD)was�1% and recovery rate was 90e100% for Cdwith AAS, while theRSD was �0.8% and recovery rate 90e110% for As with AFS.

3. Results and discussion

3.1. Effects of biochar and Fe-biochar on pH and Eh in ricerhizosphere

Both pH and Eh of rhizosphere soils are important for plantgrowth and metal solubility (Husson, 2013). Alternating wettingand drying cycles was used in this work, which is widely employedin low land paddy soils with sufficient rainfall (Bouman et al., 2007;Rothenberg et al., 2014). Furthermore, it is effective in mitigating Astransfer from paddy soil to rice compared to continuous flooding(Somenahally et al., 2011).

As expected, biochar exhibited higher pH (10.7) than soil (5.35)and Fe-biochar (4.87) (Table 1). As such, soil solution pH increasedby 0.3e0.5 unit with biochar amendment, while it decreasedslightly with 2% Fe-biochar (Fig. 1). During the experiment, soil pHin rice rhizosphere increased gradually to near neutrality until theend of heading stage (~75 d). Afterwards, a steep increase in soil pHfrom 7 to 8 was determined at the grain filling stage (75e88 d) forall treatments (Fig. 1a and b). In the following 8 days, soil pHdecreased to ~7 again. During the first 38 d after rice cultivation, Ehin soil amended with biochar decreased (Fig. 1c), while its pHincreased (Fig. 1a). This was most likely due to the hydrolysis ofsoluble minerals (e.g. K, Na oxides) from biochar at this initialperiod (Wu et al., 2015; Rinklebe et al., 2016), which favored a highelectron activity and low free hydrogen (Hþ) level (Lindsay, 1979).Meanwhile, the decreased soil Eh could be caused by acceleratedsoil O2 consumption as result of the enhanced microbial respirationstimulated by the input of labile organic compounds from biochar(i.e. priming effect) (Zimmerman, 2010). In contrast, an increase insoil Eh was observed at 2% Fe-biochar with simultaneously loweredsoil pH (Fig. 1b and d), which could be due to the presence of ahigher amount of Hþ from the hydrolysis of exogenous Fe from Fe-biochar. In spite of fluctuation, rhizosphere Eh decreased to aconstant level (~0 mV) at the end of rice cultivation, except for 1%Fe-biochar treatment (Fig. 1d).

3.2. Effects of biochar and Fe-biochar on Cd and As concentrationsin porewater

Lower Cd concentrations in rhizosphere porewater wasobserved in soils amendedwith 1e2% biochar (Fig. 2a), showing theeffectiveness of biochar on Cd immobilization (Zhang et al., 2015;Yin et al., 2016). Within this process, however, an apparent in-crease in porewater Cd was noted at 45d after transplanting in CKand 1% biochar treatment, which corresponded to the increasing Ehupon drainage around 38 d (Fig. 1c and d). Cd mobilization withoxidative transformation of S2� to SO4

2� at elevated soil Ehwasmostprobably responsible for this phenomenon (Nakanishi et al., 2006;Alloway, 2012). At higher rate of 3% biochar, 3e6-fold increase inporewater Cd was observed 38 d after planting. This seeminglycontrasting result could be due to the enhanced formation of sol-uble Cd-DOM (dissolved organic matter) complexes at a higherbiochar input (Weng et al., 2002; Alloway, 2012). Antoniadis andAlloway (2002) found that higher DOC in soils resulted in higherCd solubility and uptake by root of Lolium perenne L. However, after38 d, lower porewater Cd was observed at 3% biochar (Fig. 2),possibly due to continuous consumption of DOC by soil microbes

Fig. 1. Dynamics of rhizosphere pH (a, b) and Eh (c, d) in the biochar (a, c) and Fe-biochar (b, d) treatments throughout the rice cultivation period. Data are means ± SE (n ¼ 3).

D. Yin et al. / Chemosphere 186 (2017) 928e937 931

(Kalbitz et al., 2003). Among biochar treatments, 2% showed thelowest porewater Cd. Based on the above facts, it is conceivable thatshort-term effect of biochar on porewater Cd is not only dependenton its application ratio and alkalinity, but also its introduction ofdissolved organic matter and stimulation on soil biota (Lehmannet al., 2011; Li et al., 2013; Ahmad et al., 2014). In Fe-biochartreatments, porewater Cd was generally lower, with 0.5% beingmost effective (Fig. 2b). Nevertheless, 2-fold increase in porewaterCd was observed with 2% Fe-biochar treatment during initial30e38 d after planting, which was probably resulted from Fe-biochar induced lower pH (Fig. 1b).

Unlike Cd, biochar treatments increased porewater As levels(Fig. 2), especially during the initial 45 d (Fig. 1c). Water-solublephosphate anion (0.93 mg g�1) and elevated OH� via hydrolysisof alkali metals and alkaline earth metals (~40.91 mg g�1) in thebiochar used could enhance As desorption from soil solid phasethrough ligand exchange (Wu et al., 2015). In support of thisexplanation, Beesley et al. (2013) found that soil porewater As wasup to 5-9-folder higher within one week upon biochar incorpora-tion. For 0.5e2% Fe-biochar amended soil, porewater As concen-trations did not change much until 68 d after rice planting (Fig. 2).During later half of the experiment, consistently lower porewaterAs concentrations were determined with 0.5% Fe-biochar relativeto the control throughout the heading and grain filling stages(P < 0.05; Fig. 2d), most probably due to As sorption onto Fe oxides(Sherman and Randall, 2003; Morin et al., 2008).

3.3. Relationship between Eh/pH and porewater As and Cd

Both soil Eh and pH exerted strong effects on porewater As andCd concentrations, but differed with treatments. The elevated soilpH resulted from the high ash content in biochar (37%; Fig. 1a)facilitated soil As mobilization through competitive sorption. Withincreasing soil pH, porewater As concentrations in biochar-amended soil increased more rapid than those in Fe-biochartreatments (regression slope of 0.17 vs 0.03, p < 0.05, Fig. S2). Inaddition, lower Eh helps reductive dissolution of soil As, which wassupported by the negative correlation between rhizospheric Eh andporewater As concentration for all treatments (p < 0.01) (Fig. S2cand d). Similar findings have been reported by Frohne et al.(2011) and Liu et al. (2013). With Fe-biochar application, Asretention in Fe-oxide binding pool was enhanced (Fig. 3d), favoringstronger As sequestration in solid phase with decreasing Eh(regression slope of �0.0017 vs �0.0008, p < 0.05, Fig. S2). Forexample, when soil Eh declined to ~0 mV, porewater As in biochar-amended soil was ~2-fold higher than that in Fe-biochar amendedsoil, resulting frommore efficient sorption of As by Fe-biochar thanbiochar (Cheng et al., 2008; Silber et al., 2010; Lawrinenko andLaird, 2015). In support of this, ~100% arsenate (AsV) was sorbedby a Fe-biochar compared to 8.9% by pristine biochar from solutioncontaining 118 mg L�1 AsV. Moreover, with solution pH at 3e10, AsVremoval efficiency was stable and consistently >90% (Zhang et al.,2016). Therefore, it is conceivable that high As sorption capacity

Fig. 2. Dynamics of porewater Cd (a, b) and As (c, d) concentrations in the rhizosphere throughout the rice cultivation period. Data are means ± SE (n ¼ 3). Significant differencecompared with control: *, P < 0.05; **, P < 0.01; ***, P < 0.001.

D. Yin et al. / Chemosphere 186 (2017) 928e937932

of Fe-biochar contributed As immobilization in soils.On average, lower Cd porewater concentrations were observed

in soils amendedwith biochar than Fe-biochar (Fig. 2). For example,the porewater Cd averaged 0.16 mg L�1 in the biochar treatmentscompared to 0.23 mg L�1 in Fe-biochar treatments. The data areconsistent with literature, sustaining biochar's ability to sorb Cd(Zhang et al., 2015; Rinklebe et al., 2016; Yin et al., 2016). Comparedto Fe-biochar, biochar had a higher CEC (Table 1) and ash content(52% vs 3.1%) (Wu et al., 2015; Cai et al., 2017). Enhanced Cdsequestration by biochar could be due to increased surfacecomplexation of Cd with functional groups and promoted forma-tion of insoluble Cd-containing minerals (Lu et al., 2014; Zhanget al., 2015; Cui et al., 2016).

3.4. Effects of biochar on As/Cd retention on Fe plaque

Fe plaque on rice root surface serves as a crucial buffer againstinflux of toxic metals into cortex including As (Hossain et al., 2009).For Fe-biochar treatments, increased Fe concentrations wereextracted by DCB, but with lower As concentrations (Table 2). Thisis consistent with the finding of m X-ray fluorescence (Fig. S3),showing lower As accumulation on root surface in 2% Fe-biochartreatment. This result can be largely attributed to higher Asretention in soils with Fe-biochar, which decreased As migrationtowards and thus sequestration in Fe-plaque on root surface. Forexample, 28e63% decrease in labile pool of As (soluble and

exchangeable) was observed in soils amendedwith Fe-biochar afterharvest (Fig. 3d and Table S2). In parallel, 1.1e1.3 fold increase in Asassociated with crystalline Fe/Al oxides was identified in Fe-biochar-amended soils relative to the control. Similarly, Hossainet al. (2009) also observed decreased As concentrations withhigher Fe contents in DCB extraction of root Fe-plaque from soilsspiked with Fe compared to un-amended control. In contrast, bio-char treatments resulted in 15e25% decrease in As associated withamorphous hydrous oxides of Fe/Al, possibly due to enhanceddesorption of As from Fe/Al oxides. Unexpectedly, increasedamount of As associated with well-crystallized Fe/Al oxides wasobserved in soil amended with 3% biochar (Fig. 3c and Table S2),which was most likely resulted from the biochar itself with a 2-foldhigher As/Fe ratio than the tested soil (0.014 vs 0.007, Table 1). Theformation of crystallized FeeAs oxides in biochar could be facili-tated during the feedstock pyrolysis at 450 �C.

With regard to Cd, exchangeable Cd in soil declined withincreasing biochar, which was accompanied by an increase in Cdbound to carbonates (Fig. 3 and Table S2). For example, at 3% bio-char, exchangeable Cd in soil was decreased by ~38% while a 1.4-fold increase in Cd associated carbonates was observed. In Fe-biochar treatments, exchangeable Cd was increased by 16e47%,contributing to elevated Cd in rice roots (Fig. 5a). In parallel, adecrease in Cd bound to Fe/Mn oxides was observed. The decline insoil pH with Fe-biochar (Fig. 1b) tended to decrease Cd sorptiononto Fe oxide (Alloway, 2012). Similarly, Hartley et al. (2004) also

Fig. 3. Fraction of Cd (a, b) and As (c, d) concentrations in the rhizosphere soil with and without biochar (a, c) and Fe-biochar (b, d) (n ¼ 3). As fractionation: Soluble (F1),Exchangeable (F2), Associated with amorphous hydrous Fe/Al oxides (F3), Associated with crystalline hydrous Fe/Al oxides (F4), Residual (F5). Cd fractionation: Easily exchangeable(F1), Bound to carbonates (F2), Bound to Fe and Mn oxide (F3), Bound to organic (F4), Residual (F5).

Table 2Effects of biochar and Fe-biochar on Cd/As concentrations in DCB extraction.

Treatment DCB extraction of iron plaque

Fe (g/kg) As (mg/kg) Cd (mg/kg)

2% Fe-biochar 45.9(±3.66)a 0.49(±0.03)c 1.82(±0.20)a1% Fe-biochar 32.1(±1.22)b 0.61(±0.04)b 1.55(±0.29)a0.5% Fe-biochar 41.0(±2.66)ab 0.66(±0.02)ab 1.85(±0.32)aCK 36.5(±4.71)b 0.72(±0.04)ab 1.91(±0.49)a1% biochar 38.7(±4.01)ab 0.74(±0.06)a 1.66(±0.11)a2% biochar 40.5(±4.43)ab 0.67(±0.09)ab 1.44(±0.15)a3% biochar 45.3(±5.68)a 0.63(±0.01)b 1.86(±0.01)a

Note: Different letters within a column indicate significant differences betweendifferent treatments (P < 0.05) (n ¼ 3).

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reported elevated Cd concentrations in the leachate from Fe-oxidesamended soils, substantiating that Fe amendments may increaseCd mobility through soil acidification.

3.5. Effects of biochar on As and Cd accumulation in rice

In Fe-biochar treatments, root As was decreased by ~28%compared to the control (Fig. 5a). However, increased Cd concen-trations in rice roots were obtained, consistent with porewater Cdin soils (Figs. 5a and 2b). The results suggested that Fe-biochar waseffective in reducing As uptake by rice, but it may cause enhancedCd uptake by rice. Conversely, the Cd level in rice roots wasdecreased by biochar (P < 0.05), but it increased root As by 8.1e39%(Fig. 4). As such, biochar was effective in reducing Cd uptake by rice,but it caused As mobilization.

Although both Fe-biochar and biochar were effective inreducing rice uptake of As and Cd, their effects on As/Cd

accumulation in the straw, husk or grains were less effective (Figs. 4and 5). The average Cd concentrations in brown rice weredecreased from 1.1 mg kg�1 in control to 0.5e0.8 mg kg�1 inbiochar-amended soil, and little effect was observed for Fe-biochartreatments (Fig. 5d).

Different from our results, decrease in grain As from 0.45 to0.23 mg kg�1 with Fe amendments were reported by (Matsumotoet al., 2015). In their study, Fe was applied at >0.5%, with Fe being10 times higher than this study, suggesting increased efficiency ofAs retention with increasing amount of Fe. However, high amountof Fe may result in soil aggregate cementation and reduction inporosity (Mench et al., 1999; Kumpiene et al., 2008). In a similarway, more reduction in grain Cd could be achieved by using higherrate of biochar. In a field experiment, Cd concentrations in rice grainwere reduced from 0.3-0.7 to 0.15e0.4 mg kg�1 by using biochar at40 t ha�1 to 0e15 cm depth (i.e., ~53.3 t ha�2 to the top 20 cm) (Bianet al., 2013), which was ~6-fold higher than the maximum biocharrate in present study (3% w/w, i.e. 9 t ha�2). It should be noted thatthe optimum biochar addition into agricultural soils has beensuggested to range between 1 and 5% (w/w) (Matovic, 2011),beyond which potential soil problems related with soil structure, C/N ratios and toxicants accumulation (e.g. polyaromatic hydrocar-bons) may emerge over time (Rondon et al., 2007; Kloss et al., 2012;Ku�smierz and Oleszczuk, 2014).

With regard to biochar amendment, it should also be noted thatits incorporation into the acidic paddy soils (pH 5.35, Table 1)increased porewater As (Fig. 2c), but did not translate into elevatedgrain As (Fig. 4d). This is consistent with (Beesley et al., 2013), whoreported that As leaching instead of food chain transfer is of greaterconcern from biochar application to As-contaminated soils. In theirstudy, 3e4 fold higher porewater As with quite low tomato fruit As

Fig. 4. Cd and As concentrations in the root (a), straw (b), husk (c) and brown rice (d) in the biochar treatments. Different letters indicate significant difference between differenttreatments (P < 0.05).

D. Yin et al. / Chemosphere 186 (2017) 928e937934

was determined during 4 weeks of experiment following biocharaddition. The above results could be largely attributable to Assequestration in plant roots, as evidenced by the present workshowing <0.14% translocation of As from rice roots to shoots (Fig. 4).

3.6. Relationships between grain Cd/As and porewater- or majortissue-Cd/As

There is a significantly positive correlation between brown rice-Cd and porewater Cd collected during the booting (r ¼ 0.761,P < 0.01) and grain filling stage (r ¼ 0.592, P < 0.01) for all thetreatments. According to Rodda et al. (2011), rapid Cd accumulationin rice grain mainly occurred in the first 16 days after anthesis,which accounted for ~100% of the total grain Cd. Similarly, asignificantly positive relationship between grain As and porewaterAs during the grain filling stage was determined (r ¼ 0.434,P < 0.05) for all the treatments. This is coincident with the findingof Arao et al. (2009) who reported that As accumulation in ricegrain was most sensitive within the initial 3 weeks after heading.Based on the above analysis, it is conceivable that minimizing soil

soluble Cd/As in the grain filling stage is most crucial for the miti-gation of grain Cd/As accumulation.

Furthermore, a strong and significant positive correlation be-tween brown rice- and straw-Cd (r ¼ 0.635, P < 0.01) or husk-Cd(r ¼ 0.661, P < 0.01) was noticed, while a weak and nonsignifi-cant, positive correlationwas determined between brown rice- androot-Cd (r ¼ 0.318). According to Rodda et al. (2011), there are twomajor possible pathways of Cdmovement from root to grain: (1) Cdis taken up and translocated directly through the xylem to thedeveloping grains, or (2) Cd is taken up and transported to theactively transpiring parts such as culms, rachis, flag leaves andexternal parts of the panicles, and then remobilized via the phloemto grains. The significantly positive correlation between grain-Cdand straw- or husk-Cd (P < 0.01) for all the groups suggests thatCd remobilization from the stems and husk followed by phloemtransport could probably be the main route of Cd entry into ricegrain.

A similar pattern of As transfer from rice shoot to grain was alsoindicated by a relatively low but significant correlation betweengrain- and shoot-As (r ¼ 0.419, P < 0.01) or husk-As (r ¼ 0.434,

Fig. 5. Cd and As concentrations in the root (a), straw (b), husk (c) and brown rice (d) in the Fe-biochar treatments. Different letters indicate significant difference between differenttreatments (P < 0.05).

D. Yin et al. / Chemosphere 186 (2017) 928e937 935

P < 0.01). This apparently positive relationship between grain andshoot or husk As has been corroborated by several previous studieswith either field-collected or pot experiment samples acrossdifferent rice cultivars, soil conditions and water regimes (Williamset al., 2007, 2009; Norton et al., 2010). All these results support theconclusion that phloem-derived As made a relatively highercontribution than xylem pathway to grain As accumulation (Careyet al., 2010, 2011; Zhao et al., 2012; Wang et al., 2015).

4. Conclusion

Taken together, biochar and Fe-biochar decreased porewater Cdand As concentrations, respectively, in a dose-dependent manner.As a result, remarkable decreases in root Cd and As level wereachieved, respectively, with biochar and Fe-biochar, which, how-ever, did not translate into significant decrease of grain Cd and Asaccumulation at sustainably low application rates (�3%) to avoidpotential side effects of the amendments on paddy soils over longtime scales. Therefore, biochar and Fe-biochar are suggested to bemore suitably used as short-term emergency measures mitigatingCd and As transport in soil-rice system, respectively, with

sufficiently high amount. In particular, at the co-presence of As andCd in soils, the potential mobilization of Cd by Fe-biochar and As bybiochar needs careful consideration and should be prior tested andevaluated.

Acknowledgements

This research was supported by National Natural ScienceFoundation of China (No. 41301339), the Construct Program of theKey Discipline in Hunan Province (China), Aid program for Scienceand Technology Innovative Research Team in Higher EducationalInstitutions of Hunan Province, Hunan Provincial Natural ScienceFoundation of China (No. 2017JJ2180) and the Fok Ying Tung Edu-cation Foundation for Young Teachers in Higher Education In-stitutions of China (No. 151029).

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.chemosphere.2017.07.126.

D. Yin et al. / Chemosphere 186 (2017) 928e937936

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