Effects of biochar addition on toxic element

STOTEN-24446; No of Pages 8 Science of the Total Environment xxx (2017) xxx–xxx

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Effects of biochar addition on toxic element concentrations in plants: A meta-analysis Xin Peng a,b, Yinger Deng a,b,⁎, Yan Peng c, Kai Yue d a

State Key Laboratory of Geohazard Prevention and Geoenvironment Protection, Chengdu University of Technology, Chengdu 610059, PR China College of Environment and Civil Engineering, Chengdu University of Technology, Chengdu 610059, PR China Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, DK, 1958, Frederiksberg C, Denmark d Long-term Research Station of Alpine Forest Ecosystems, Institute of Ecology and Forestry, Sichuan Agricultural University, Chengdu 611130, China b c

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Biochar addition to soil noticeably decreased TE concentrations in plants. • Feedstock and pyrolysis temperature were main controlling factors. • Biochar addition significantly decreased TE concentrations in edible parts. • Mechanisms were hypothesized based on the observed effects of biochar addition.

a r t i c l e

i n f o

Article history: Received 16 August 2017 Received in revised form 17 October 2017 Accepted 21 October 2017 Available online xxxx Editor: F.M. Tack Keywords: Soil contaminants Feedstock Pyrolysis temperature Plant parts Bioaccumulation Health risk

a b s t r a c t Consuming food contaminated by toxic elements (TEs) could pose a substantial risk to human health. Recently, biochar has been extensively studied as an effective soil ameliorant in situ because of its ability to suppress the phytoavailability of TEs. However, despite the research interest, the effects of biochar applications to soil on different TE concentrations in different plant parts remain unclear. Here, we synthesize 1813 individual observations data collected from 97 articles to evaluate the effects of biochar addition on TE concentrations in plant parts. We found that (1) the experiment type, biochar feedstock and pyrolysis temperature all significantly decreased the TE concentration in plant parts; (2) the responses of Cd and Pb concentrations in edible and indirectly edible plant parts were significantly more sensitive to the effect of biochar than the Zn, Ni, Mn, Cr, Co and Cu concentrations; and (3) the biochar dosage and surface area, significantly influenced certain TE concentrations in plant tissues as determined via correlation analysis. Moreover, the only exception in this study was found for metalloid element (i.e., As) concentrations in plants, which were not significantly influenced by biochar addition. Overall, the effects of biochar on TE concentrations in plant tissues were negative, at least on average, and the central trends suggest that biochar has a considerable ability to mitigate the transfer of TEs to food, thereby reducing the associated health risks. Our results provide an initial quantitative determination of the effects of biochar addition on multifarious TEs in different plant parts as well as an assessment of the ability of biochar to reduce TE concentrations in plants. © 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: 1#, Dongsanlu, Erxianqiao, Chengdu 610059, Sichuan, China. E-mail address: [email protected] (Y. Deng).

https://doi.org/10.1016/j.scitotenv.2017.10.222 0048-9697/© 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Peng, X., et al., Effects of biochar addition on toxic element concentrations in plants: A meta-analysis, Sci Total Environ (2017), https://doi.org/10.1016/j.scitotenv.2017.10.222

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X. Peng et al. / Science of the Total Environment xxx (2017) xxx–xxx

1. Introduction Soil contamination with toxic elements (TEs) has become a global and widespread problem, and it is primarily caused by anthropogenic activities (Tóth et al., 2016; Li et al., 2014; Duruibe et al., 2007; Zhang et al., 2009). Common TEs in soil include arsenic (As), cadmium (Cd), chromium (Cr), cobalt (Co), copper (Cu), lead (Pb), manganese (Mn), nickel (Ni) and zinc (Zn) (Shu et al., 2016; Williams et al., 2009; Nannoni et al., 2016). All of these TEs pose a great risk to human health because of most of them or their compounds are highly toxic carcinogenic substances, especially As, Cd, and Pb. These highly carcinogenic substances, accumulate in various human organs, and can induce organ (e.g., brain, kidney, gastrointestinal tract and lung) lesions and even failure after long-term intake, even at levels below the acceptable daily intake (Satarug and Moore, 2004; Horiguchi et al., 2013; Landrigan et al., 2002 Türkdoğan et al., 2003; Fu and Boffetta, 1995). Chromium, Co, Cu, Mn, Ni and Zn are essential trace elements that are linked to human metabolism at strictly limited concentrations (Nielsen, 1990; Chowdhury and Chandra, 1987; Fraga, 2005). Such TEs accumulate in soil and are transferred into the human body through soil-plant (i.e., crop and vegetable) food chains or soil-plant (i.e., residuum of crops, including the hull, stems, leaves, and some grasses utilized for silage or forage)-poultry/livestock food chains (Hang et al., 2009; Fu et al., 2008). Inhibiting the TEs in food to minimal concentrations is desired for highly toxic elements (e.g., Cd, As, Pb) and to maximum permissible concentrations for toxic but essential elements (e.g., Cu, Zn). Biochar, which is an effective, low-cost and eco-friendly soil ameliorant, has received increasing attention because of its ability to immobilize TEs and reduce their bioavailability in soil, which suppresses the bioaccumulation of TEs (Malińska et al., 2017). Biochar is a carbon-rich porous material that can be derived from agricultural waste or forestry biomass and treatment plant residuum via thermolysis in the absence of oxygen (Lundberg and Sundqvist, 2011). Biochar is recognized for its ability to improve soil properties and safely sequester carbon (Woolf et al., 2010). Biochar has been investigated to determine its ability to reduce the bioaccumulation of TE concentrations through several mechanisms. For example, in terms of soil, biochar can enhance the immobilization of TEs in soil by altering soil physical and chemical conditions, and such changes decrease the bioavailability of TEs, thereby reducing plant bioaccumulation of TEs (Jiang et al., 2012; Khan et al., 2014; Gul et al., 2015). Previous studies (Bruun et al., 2008; Lundberg and Sundqvist, 2011; Lehmann and Joseph, 2009) have shown that the immobilization of TEs in soil via biochar relies on several factors: (1) the feedstock, ash content and constituents, which refer to the mineral fraction; (2) preparation conditions, particularly the pyrolysis temperature; and (3) soil properties. From the perspective of plants, biochar additions reduce the translocation of TEs in plants, thereby decreasing the TE concentrations in different plant tissues. Moreover, experimental conditions (e.g., biochar application rate, experimental type and duration) also influence the uptake of TEs by plants (Rizwan et al., 2016; Beesley et al., 2011). Thus, numerous experimental studies have been performed to determine the response of different TE concentrations in various plant species and different parts to biochar treatments (derived from various feedstocks with different pyrolysis temperature). However, considerable differences and even contradictory findings have been observed among these studies. For instance, herbal biochar has been shown to increase Cd concentrations in plant tissues (Prapagdee et al., 2014; Hossain et al., 2010; Moreno-Jiménez et al., 2016), though the same type of biochar decreased Cd bioaccumulation in plants, even drastically (Cui et al., 2011; Jones et al., 2016). Some have also reported that biochar has no significant effect on Cd bioaccumulation in plants (Xu et al., 2016a, 2016b), and inconsistent results have been observed for several TEs (e.g., Pb, As) (Gartler et al., 2013; Houben et al., 2013; Moreno-Jiménez et al., 2016). Biochar application has been frequently reported to increase certain TEs and decrease others under the same

experimental conditions. For example, in field applications, herbal biochar (850 °C) could decrease Zn and Cd concentrations and increase Cu and Pb concentrations in plants (Wagner and Kaupenjohann, 2015), whereas biowaste biochar (500 °C) had insignificant effects on Pb, Cu, and Ni concentrations in plants but caused a significant decrease in Cd (Bian et al., 2014). All these results suggest that it is crucial to evaluate the effects of moderator factors (i.e., feedstock, pyrolysis temperature, soil properties, plant species, and experimental conditions) to better understand and utilize biochar to decrease the bioaccumulation of TEs. Currently, a knowledge gap is observed regarding whether the effects of all types of biochar (mainly affected by feedstock or pyrolysis temperature) on the bioaccumulation of TEs in plants may or may not be significantly negative and whether the magnitude of the response of TE concentrations in different plants and plant parts varies according to the biochar additions. Moreover, an overall perspective on the ability of biochar to the decrease the bioavailability of different TEs in soil and reduce the bioaccumulation of TEs in plants is difficult to obtain because of the different or contradictory datasets. In this study, the mean effect of biochar addition on the bioaccumulation of TEs was quantitatively analyzed using data extracted from primary studies. We applied a comprehensive meta-analysis and synthesized data from 97 articles. The main objective of our study was to determine and compare the magnitude of the direct effects of biochar additions on different TE concentrations in plants and to ascertain the underlying mechanism based on different types of biochar. The mechanisms were evaluated according to how the biochar addition influenced the bioavailability of TEs in soil. Furthermore, because TEs threaten human health through the food chain, we also evaluated the effect of biochar addition on the bioaccumulation of TEs in different plant parts in terms of their edibility. In particular, the response of the bioaccumulation of TEs (including As, Cd, Pb, Cr, Co, Cu, Ni, Mn, and Zn) in plants to experimental biochar addition was evaluated. We hypothesized that (1) TE concentrations in plants would be significantly reduced by biochar addition; (2) the ability of biochar to decrease the bioaccumulation of TEs would not be influenced by higher pyrolysis temperatures; and (3) the effects of biochar addition on TE concentrations in plants would be significantly influenced by moderator variables (e.g., experimental conditions). 2. Methods 2.1. Data compilation Peer-reviewed articles evaluating the effects of biochar additions on the bioaccumulation of TEs were identified by searching the Web of Science and Google Scholar on 23 December 2016 using the keywords “biochar”, “trace element”, “heavy metal”, “TE”, and “bioaccumulation”, and Chinese searches were conducted using CNKI (Chinese National Knowledge Infrastructure). There were no restrictions on the publication year. To minimize publication bias as much as possible, the following criteria were applied to the primary studies: (i) the treatment and control groups were the same in all aspects except biochar application; (ii) experiments used a randomized design; (iii) the standard deviation (SD) was provided directly or could be calculated by the standard error (SE); and (iv) the culture medium was soil. After extraction, 97 published articles were included in our database. Measurements from the last sampling period were collected if multiple measurements were performed throughout the experimental period in the same primary study, because this criterion was required for the statistical assumption of independence among each observation in the meta-analysis (Hedges et al., 1999). Different biochar application rates and/or TEs and/or plants species and/or plant parts under treatment and control conditions were considered individual variables; therefore, several effect sizes were often obtained in a single primary study, even though such effect sizes may not be independent.



Nevertheless, the important available information could be reduced, which was subject to a limited analysis by the moderators if it was obtained only from a case study in a primary study. To address this issue of data compilation, sensitivity analysis was performed to evaluate the independence of the multiple observations in each study (Yue et al., 2015) (Table S2). The data were collected from tables presented in the articles or from figures using the free Engauge Digitizer software (Free Software Foundation, Inc., Boston, MA, USA). During data extraction, the biochar application rate was presented in mass per area in certain studies, and these data were converted to the mass percentage by assuming that 15,000 kg/ha was equivalent to 1% unless otherwise provided (Ping et al., 2016). The soil pH(CaCl2) values were transformed to pH(H2O) by the equation pH(H2O) = 1.65 + [0.86 × pH(CaCl2)] (Augusto et al., 2008). Whenever feasible, the soil pH and nutrient (C, N, and P) concentrations were recorded as auxiliary information and considered as background values in this analysis. There were 1813 pairwise comparisons in total extracted from the 97 primary study articles (Table S1). Various experimental factors affected the level of TE bioaccumulation under biochar application. Thus, several variables, which were treated as moderators, were categorized into the following groups to facilitate the analysis according to the methods of previous studies (Yue et al., 2015, 2016, 2017b; Cayuela et al., 2014): experimental type (field or pot studies); biochar feedstocks, grouped as biowaste (municipal solid waste), biosolid (sewage sludge from water treatment plants), manure (manures or manure-based materials from livestock and poultry), wood (multifarious wood, and unidentified wood mixtures), herbaceous (greenwaste, bamboo, various straws including rice, corn, cotton and so on), lignocellulosic wastes (rice husk, nuts shells, paper and olive mill waste); edibility, grouped as edible (i.e., plants parts that are often directly consumed), indirect edible (pastures and plants parts that are usually utilized for silage, including straws, husk, and leaves), inedible (plants parts that explicitly could not be esculent, e.g., most roots); pyrolysis temperature (≤400, 400–500 including 500, 500–600 including 600, N600 °C); and plant function type (PFT) (woody or herbaceous) according to the growth form. Moreover, some moderators were considered continuous variables (biochar application rate (w/ w); Brunauer, Emmett and Teller (BET) surface area (m2/g); soil pH, and C, N, total P or available P concentrations; experimental duration). A Pearson correlation analysis was used to test the correlation between these moderators and the response of TE bioaccumulation to the biochar addition. 2.2. Calculation and analysis The data for different TEs in the above groups were analyzed by employing a meta-analysis, and the impacts of biochar addition on the TE concentrations in the plant parts were calculated by using the natural log-transformed response ratio (lnRR) based on the following equation: ln RR ¼ ln ðXXec Þ, where Xe represents the treatment mean of the biochar and Xc represents the control mean (Lajeunesse and Forbes, 2003). The SD of the biochar treatments and controls was employed to calculate the S2

S2

variance (ν) of each lnRR using the following equation: ν ¼ ne Xe e þ nc Xc c , where Se and Sc represent the standard deviations, ne and nc represent the sample size in the treatment (e) and control (c) groups, respectively. The weighted mean response ratio (lnRR++) was calculated using equation: ln RRþþ ¼

m

k

∑i¼1 ∑ j¼1 wij ln RRij m

k

∑i¼1 ∑ j¼1 wij

, where m is the number of groups,

k is the number of comparisons in the ith group, and w is the weight of each response ratio (Yue et al., 2017a). To evaluate the effects of the moderators on the magnitude and direction of the responses of the bioaccumulation of TEs to the biochar addition, we calculated the grouped effect sizes using a categorical random effects model. The significance of each categorical moderator was also evaluated by employing mixed models by comparing the heterogeneity within and between moderator

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levels (Koricheva et al., 2013). Significant differences were not observed between two groups if their 95% confidence intervals (CIs) overlapped. The mean percentage of the change in response to the bioaccumulation of different TEs in different plant parts under the biochar addition treatment was calculated and compared with that of the control. Moreover, the equation [exp (lnRR++) − 1] × 100% was used to convert the effect sizes into mean percent changes, and the effects of moderators could be considered significant if their 95% (CIs) did not overlap zero. We used the meta-analysis software MetaWin 2.1 to calculate the lnRR and its 95% CI (Rosenberg et al., 2000).

3. Results Results showed that the bioaccumulation of different TE concentrations under biochar treatments was affected by the experimental conditions and forcing factors. The data from pot or field studies were analyzed separately, and a further categorized analysis was performed (Fig. 2) if the between-group heterogeneity (Qbetween) for the experimental type was significant at P b 0.05, which could indicate that a significant difference occurred between the pot and field groups. However, categorized analyses of Ni, Mn, Cr and Co were performed using only the database for the pot studies (Fig. 1d–f) because field experiments were absent from the primary studies.

3.1. Effects of biochar addition on the bioaccumulation concentrations of Zn, Cd, As, Ni, Mn, Cr, and Co In pot studies, the effects of biochar addition on the bioaccumulation of TEs were revealed to be significantly suppressive except on As (Fig. 1), and considerable decreases were observed for Cr and Co. Compared with the control groups, the Cr and Co concentrations in plants decreased significantly by an average of −64.13%, which was a substantially greater effect than that observed for Zn, Cd, As, Ni, Mn. Cd decreased significantly in both the pot and field studies by − 30.24% and − 32.54%, respectively, under biochar addition conditions (Fig. 1b, f). The effects of moderators were considered for the different TEs. In terms of interactions with feedstock sources, the largest number of studies were completed using wood and herbaceous feedstocks for different TEs, and in both cases, the effects were significant for Cd, Ni, and Mn. In particular, the effect of biochar produced from herbaceous feedstocks was more pronounced on Mn (− 44.43%) than the other TEs, as shown in Fig. 1, and biochar produced from wood feedstocks produced the same results on Cr (−49.43%). However, biosolids and lignocellulosic waste were also common feedstocks used to prepare biochar. Biochar produced from biosolids and lignocellulosic waste produced more significant reductions in Co (− 67.52%) and Cd (− 43.09%) than the other elements. In addition, biochar produced from manures significantly increased the Zn concentration by 91.32%, whereas it decreased the Cd concentration (−65.37%) in plants (Fig. 1a, b). With respect to edibility, the TE concentrations in the inedible plant parts significantly decreased with the biochar treatments. Moreover, the Cd concentrations in the edible and indirectly edible plant parts significantly decreased by −33.90% and −35.42%, respectively, under the biochar treatments (Fig. 1b). The temperature of pyrolysis, which is considered an important factor, also had an effect. Biochar produced at higher temperatures (N600 °C) had more pronounced effects on Ni (−83.42%) and Mn (−81.23%) than biochar produced at different pyrolysis temperatures. The largest number of studies were performed using a temperature range (i.e., 400–500 °C), and the impacts were significant for Zn, Cd, and Ni. Additionally, the biochar treatments did not significantly affect the As concentration across all case studies (Fig. 1c), whereas they had significant effects on Ni across all pot studies (Fig. 1d).


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Fig. 1. Effect of biochar addition on the (a) Zn, (b) Cd, (c) As, (d) Ni, (e) Mn, (f) Cr and Co concentrations in different plant parts expressed as the percentage change (%) relative to the control. The values represent mean values with 95% bootstrap confidence intervals (CIs), and the sample sizes are shown in parentheses. The mean percentages of the changes in the TE concentrations in plant tissues were estimated as (elnRR++ −1)× 100%, where lnRR++ is the weighted mean response ratio across studies. The effect of biochar is significant when the 95% CI does not overlap zero. The results are not presented for sample sizes b2; thus, the sum of the numbers of the case studies for subgroups may be smaller than the total number in such cases. Legend: PFT = plant function type; total represents the experimental type, including pot and field studies.

3.2. Effects of biochar addition on the bioaccumulation concentrations of Cu and Pb Cu and Pb were analyzed separately in the field and pot studies because the significance of the Qbetween value was P b 0.05. Compared

with the control groups, the effects of biochar addition on all field studies were scarcely significant, whereas the opposite results were observed for the pot studies (Fig. 2). When the effects of the moderators were considered, biochar produced from manure significantly decreased the Pb concentrations in plants by − 85.32% [− 92.13% −

Fig. 2. Effect of biochar addition on the (a) Cu and (b) Pb concentrations in different plant parts expressed as the percentage change (%) relative to the control. The values represent mean values with 95% bootstrap confidence intervals (CIs), and the sample sizes are shown in parentheses. The mean percentages of the changes of the TE concentrations in plant tissues were estimated as (elnRR++ −1)×100%, where lnRR++ is the weighted mean response ratio across studies. The effect of biochar addition is significant when the 95% CI does not overlap zero. The results are not presented for sample sizes b2; thus, the sum of the numbers of the case studies for subgroups may be smaller than the total number in such cases. Legend: PFT = plant function type; total represents the experimental type, including pot and field studies.



72.60%]. It is important to note that the Cu and Pb concentrations in the edible plant parts were both significant decreased by −18.49% and − 48.93%, respectively, after biochar addition. 3.3. Influences of moderator variables The correlation analysis indicated that the biochar addition level, biochar BET surface area, soil properties (including pH, C, N, total P and available P), soil TE concentrations, and experimental duration could represent important moderators of the TE bioaccumulation concentration response to biochar treatment (Table 1). Overall, different TEs showed a greater response based on the biochar application rate, BET surface area, and soil TE concentrations (i.e., background concentrations). The responses of Mn and Co to biochar were significantly affected by the soil pH (P b 0.01), although other TEs were nearly unaffected. Similarly, the experimental duration affected the response of Zn to biochar. 4. Discussion Experimental biochar addition was found to dampen the concentrations of TEs in plant tissues, and this response varied according to the biochar characteristics, soil properties, plant species and experimental conditions. The effects of biochar application on the bioaccumulation of TEs varied according to the experimental type. Our study found a significant negative response in the pot studies but not in most field studies, which may be attributed to uncontrollable factors (e.g., rainfall). For example, although DOC is known to act as a chelator, and shows the ability to immobilize TEs in soil and reduce the bioavailability of TEs via physical absorption and formation of stable clathrates (Zheng et al., 2012; Khan et al., 2014), DOC can only show a short-term increase after biochar addition, perhaps due to the dissolution and leaching of DOC under field condition (Chen et al., 2016). However, the response of Cd to the biochar treatment was less influenced by field factors, and the average of the difference between the pot studies and field studies

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was minor (Fig. 1b). These results suggest that biochar treatments had a significant effect on the Cd bioaccumulation concentration and could contribute to amending soil under Cd stress in practice. The major mechanisms that immobilize TEs in soil are likely “formation” and “absorption” via a series of reactions (e.g., redox, precipitation, and absorption) (Joseph et al., 2010; Kumpiene et al., 2008; Zhang et al., 2017). The high heterogeneity of biochar resulted from differences in feedstock and pyrolysis temperature (Zhao et al., 2016; Kloss et al., 2012). In addition, the variety of biochar characteristics to the different mechanisms by which TE bioavailability was suppressed (Yu et al., 2016; Zhang et al., 2016). The feedstock type plays an important role in the physical and chemical properties of biochar and its nutrient and toxicant contents (Downie et al., 2009; Spokas and Reicosky, 2009). Among all the biochar feedstock sources, the herbaceous and wood sources were more extensively utilized for the experimental studies. However, the effect of biochar derived from herbaceous materials was more pronounced than that of biochar derived from wood across all TEs, whereas the effect of biochar produced by manures was larger than that of other sources. Manure biochar had a distinctly higher ash content and presented a greater potential cation exchange capacity (CEC) and more exchangeable cations than biochar produced from wood, and herbaceous biochar generally fell between these two types (Singh et al., 2010; Kloss et al., 2012). The CEC was dominated by H+, Ca+ and K+ on the biochar surface, which can be attributed to decreasing the bioavailability of TEs, especially for Cd and Pb.(Gul et al., 2015; Yousaf et al., 2016; Namgay et al., 2010). Simultaneously, the ash content affected the mineral content in the soil, which could retain certain TEs to reduce plant uptake through precipitation or by furnishing sites of potential adsorption (Uchimiya et al. 2010). For instance, phosphates (higher content in manure biochar) or silicate (higher content in herbaceous biochar) reacted with Pb to form an insoluble material (Lu et al., 2014; Mukome et al., 2013; Cao et al., 2011), and the results of both the meta-analysis and correction analysis (R2 = −0.624, P b 0.01) demonstrated that the Pb concentrations in the plant tissues were significantly decreased via

Table 1 Coefficient of determination (R2) for the correlation analyses of the response ratios (lnRR) of biochar addition to the TE concentrations in plant tissues under various experimental conditions and values (i.e., biochar application rate, biochar BET surface area, soil properties, experimental duration). TE

Biochar application rate

BET surface area

Soil pH

Soil C

Soil N

Soil P

Soil available P

Soil TE concentrations

Experimental duration

Zn

−0.16⁎⁎ (269) −0.247⁎⁎ (567) −0.08 (167) Pot −0.025 (137) Pot 0.159 (78) Pot −0.148 (53) Pot −0.301 (20) Field Pot 0.552⁎ −0.29⁎⁎ (193) (17) Field Pot 0.338 −0.223⁎⁎ (15) (286)

0.045 (115) −0.009 (258) 0.086 (85) Pot −0.636⁎⁎

−0.035 (258) 0.001 (525) 0.15 (115) Pot −0.037 (131) Pot 0.582⁎⁎ (70) Pot −0.063 (51) Pot 0.678⁎⁎ (14) Field 0.192 (16) Field −0.463 (15)

−0.303⁎⁎ (204) 0.107⁎ (380) 0.027 (111) Pot 0.036 (94) Pot 0.132 (55) Pot 0.472⁎⁎

−0.033 (187) 0.06 (318) 0.107 (89) Pot −0.127 (64) Pot 0.431⁎⁎ (37) Pot −0.093 (26) Pot 0.782⁎⁎ (14) Field Pot 0.108 −0.27⁎⁎ (16) (106) Field Pot 0.45 0.122 (15) (140)

0.43 (109) −0.23⁎⁎ (177) −0.728⁎⁎

−0.117 (59) −0.149 (89) −0.417⁎

(47) Pot 0.145 (54) Pot 0.115 (32) Pot 0.102 (17) Pot −0.578 (8) Field Pot −0.164 (71) Field Pot −0.06 (92)

(37) Pot −0.528 (10) Pot

−0.296⁎⁎ (240) −0.16⁎⁎ (550) 0.176 (110) Pot −0.368⁎⁎

0.211⁎⁎ (258) 0.054 (541) 0.057 (167) Pot 0.133 (121) Pot −0.185 (62) Pot −0.084 (53) Pot −0.327 (20) Field 0.12 (17) Field −0.397 (15)

Cd As Ni

Mn

Cr

Co

Cu

Pb

(24) Pot −0.559⁎⁎ (35) Pot −0.874⁎⁎ (14) Pot 0.817⁎⁎ (12) Field Pot 0.014 (76) Field Pot 0.108 (122)

Pot −0.002 (189) Pot −0.075 (234)

(38) Pot 0.817⁎⁎ (12) Field 0.733⁎⁎ (16) Field 0.274 (15)

Pot −0.52⁎⁎ (137) Pot 0.128 (178)

Pot −0.761⁎ (9) Pot

Field 0.655⁎ (11) Field

Pot −0.16 (32) Pot −0.624⁎⁎ (38)

(123) Pot −0.026 (58) Pot −0.793⁎⁎ (51) Pot 0.817⁎⁎ (12) Field Pot 0.046 −0.048 (15) (174) Field Pot 0.223 −0.165⁎ (15) (236)

Pot 0.02 (193) Pot −0.003 (228)

Field and pot represent the experimental type, and unspecified values include field and pot studies; negative relationships are indicated by “−”; values in parentheses are the sample size. Correlation analyses were not performed when the sample size was less than eight; thus, results were not available for some variables. ⁎ P b 0.05. ⁎⁎ P b 0.01.


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complexation reactions (Fig. 2b, Table 1). A possible explanation for the significant positive effect of manure biochar on Zn was the increased Zn content from the addition of several manure biochar because Zn uptake is dependent on external Zn levels and its intrinsic metabolic characteristics (Ishimaru et al., 2011). Certain properties of lignocellulosic waste biochar were reported to be between that of herbaceous and wood biochar and even significantly lower than that of herbaceous biochar (e.g., surface area) (Uchimiya et al., 2012a), although the ability of lignocellulosic waste biochar to decrease the Zn, Cu, Pb, and Cd concentrations in plant tissues was more pronounced than that of herbaceous biochar. The hypothetical mechanism is the ability of lignocellulosic waste biochar to exploit the advantages of both herbaceous biochar and wood biochar. Numerous previous studies have reported that the pyrolysis temperature is an important factor that determines the biochar properties, such as the pH and surface area (as well as the CEC) (Gaskin et al., 2008; Mukome et al., 2013; Singh et al., 2010). Biochar is known to modify the soil pH and generally increases the soil pH because of the alkaline nature of biochar produced under increased pyrolysis temperatures (Ehsan et al., 2014; Singh et al., 2010). With increases in soil pH, the bioavailability of TEs, such as Cd, Pb, Cu, Zn, and As, generally decreases (Rees et al., 2014; Houben et al., 2013; Venegas et al., 2015). In addition, the surface area is strongly influenced by the pyrolysis temperature, especially temperatures N500 °C, which could lead to a drastic magnification because of the disintegration and volatilization of thermally unstable substances within the biochar matrix under higher temperatures (Mukome et al., 2013; Kloss et al., 2012). Similarly, studies have reported that the surface area had a large effect on the retention of TEs via adsorption (e.g., Cd, As, and Pb) (Beesley et al., 2011). Nevertheless, the results were inconsistent, and biochar produced at temperatures N600 °C had a reduced effect on the Cd and Pb concentrations in plant tissues than biochar produced at lower temperatures, likely because of the polar functional group, especially oxygen-containing surface functional groups, which also play important roles in binding TEs and are reduced at higher pyrolysis temperature (Zhang et al., 2017; Gaskin et al., 2008; Li et al., 2016a, 2016b). Increasing the pH seemed to facilitate an increase in the CEC in the soil; however, the extent of the response might depend on certain prerequisites (e.g., soil organic matter content) (Sylvia et al., 2004). Furthermore, the correlation analysis suggested that the Ni (R2 = −0.636, P b 0.01), Mn (R2 = −0.559, P b 0.01) and Cr (R2 = −0.874, P b 0.01) bioaccumulation concentrations were significantly influenced by the biochar surface area (Table 1). It is reasonable to assume that Cr was likely influenced by absorption to the surface via π electron donor-acceptor interactions and diffusion within pores of biochar, which were linked to a high surface area (Herath et al., 2015). Cu had a high affinity for the organic functional groups on the biochar because of the specific absorption capacity, which led to increased stability of complexes between Cu and organic functional groups compared with complexes involving Pb and Cd. In addition, the increasing pH contributed to the increased hydrolysis of metals and the creation of weak hydrogen bonds of OH—H, which promoted the formation of metal hydroxides (Jiang et al., 2012; Gul et al., 2015). The mechanisms underlying the reduced bioavailability in soil of Ni and Mn were likely analogous to that of Cr because of the increased surface area of biochar. A remarkable difference was observed in the response of plant parts stressed by different TEs under the biochar treatments (Figs. 1 and 2). Soil-to-plant was the major exposure pathway to TEs via direct and indirect consumption by humans. Both the edible and indirectly edible parts represented aboveground parts, whereas the inedible parts represented underground parts (i.e., roots). However, we did not directly analyze and discuss the effects of biochar on the aboveground and underground parts, which was observed in the overwhelming majority articles, because the edible and indirectly edible parts might be more directly and closely relevant to human health and more beneficial in an evaluation of the effect of biochar on the health risk induced by TEs.

The effects of biochar on highly toxic elements (e.g., Cd and Pb) in the edible and indirectly edible parts were significantly negative and greater than that in the inedible parts, which was an important finding. The results suggested that biochar can contribute to decreases in Cd and Pb concentrations in the food chain and human health risks. Moreover, biochar inhibited the translocation of Cd and Pb among plant tissues. It was hypothesized that internal Cd transport in plants may be linked with the low affinity cation transporter, and roots were the first barrier for Pb transport to other tissues because Pb was restrained in the cell walls through ion exchangeable sites, formed precipitates (e.g., phosphate) outside of cells, and combined with pectin and cysteine inside root cells (Raskin and Ensley, 1999; Peralta-Videa et al., 2009; Li et al., 2016a, 2016b; Xu et al., 2016a, 2016b). For example, the Pb-cysteine concentration was found increased about 21.6% in the roots of plants with biochar addition (Li et al., 2016a, 2016b). Silicate decreased the bioavailability of TEs in soil, thereby reducing plant uptake, and it also restrained translocation of TEs in plant, perhaps due to the thickening of plant tissues (e.g., increased cell wall thickness), protecting plant tissues via antioxidants simulation, and enhancing expression of TE transporter genes (Li et al., 2012; Li et al., 2016a, 2016b; Cunha, 2009). Moreover, the TE bioaccumulation concentrations were mediated by moderator variables in the biochar treatments. In this study, the As concentration in plants was significantly influenced by and negatively correlated with phosphate, which was likely because arsenate is similar to phosphate and both of these elements enter the plants through a common transporter (Khan et al., 2014; Zhao et al., 2010). According to the third assumption, significant (P b 0.01) negative correlations were observed between the Zn, Cu (pot studies), Pb (pot studies), and Cd concentrations in plants and the biochar application rate, which may have been related to increases in the soil CEC and pH with increases in the dosage of biochar (Jiang et al., 2012). However, with respect to economic feasibility, plant growth and crop yields, the biochar application rate should be kept below a threshold because excessive application rates lead to reduced growth (Biederman and Harpole, 2013; Liu et al., 2013). However, the deficiencies and uncertainties that still remain were attributed to experimental limitations and the lack of complete data. For example, the effects of biochar addition on decreases in TE concentrations could be overestimated using pot experiments. According to our results, the effects of biochar addition on decreases in As concentrations in plant tissues were all insignificant, although the use of manure biochar might obtain satisfactory results. In addition, the experimental duration was considered another important moderator variable (Rizwan et al., 2016). However, in our study, only the Zn concentration in plant tissues was significantly influenced by the experimental duration, and it presented a negative correlation with duration, which was likely because the majority of experiments were short term and the durations were similar. Therefore, long-term experiments, particularly long-term field experiments, should be performed. 5. Conclusions Our integrated study showed that the majority of types of biochar added to soil generally decreased the bioaccumulation concentration of different TEs. These findings suggest that the use of biochar as a soil ameliorant might have a crucial effect on the eco-environment and agriculture and could reduce human health risk by decreasing the daily intake of TEs. Our results also showed that (1) TE concentrations presented greater reductions in pot studies than in field studies; (2) manure, herbaceous, and wood biochars significantly decreased the Cd, Cu, and Pb concentrations in plants, with manure biochar presenting a significant effect on Cd and Pb; (3) compared with biochar generated under other pyrolysis temperatures, biochar generated under lower pyrolysis temperatures (≤400 °C) significantly decreased the TE contents (except for As), although the effects were weak; (4) TE concentrations, especially Cd and Pb concentrations, in the edible and indirect edible parts were clearly decreased by biochar addition; and (5) moderator



variables, including the biochar application rate, surface area, soil P and original TE concentrations in soil, were all important factors that mediated the ability of biochar to decrease TE concentrations in plant tissues. Our study provides the first insights into one of the main functions of biochar, which can promote the security of terrestrial ecosystems and food.

Acknowledgements We are thankful to all the scientists whose primary studies were used to perform this meta-analysis. This work was financially supported by the National Natural Science Foundation of China (40202036, 40572163, and 41172277) and the Opening fund of State Key Laboratory of Geohazard Prevention and Geoenvironment Protection (Chengdu University of Technology) (SKLGP2018K0). The authors declare no conflict of interest. Appendix A. Supporting Information Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2017.10.222.

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