Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydrocarbons and ecotoxicity of soils

STOTEN-20018; No of Pages 9 Science of the Total Environment xxx (2016) xxx–xxx

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

Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydrocarbons and ecotoxicity of soils Michał Kołtowski a, Isabel Hilber b, Thomas D. Bucheli b, Patryk Oleszczuk a,⁎ a b

Department of Environmental Chemistry, Maria Curie-Skłodowska University, 3 Maria Curie-Skłodowska Square, 20-031 Lublin, Poland Agroscope Institute for Sustainability Sciences ISS, Reckenholzstrasse 191, 8046 Zürich, Switzerland

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 produced from willow, coconut and wheat straw were steam activated. • Non- and activated biochars were added to three different soils. • Bioavailable (Cfree) and bioaccessible (Cbioacc) PAHs content was investigated. • Biochar activation resulted in more pronounced reduction of Cfree and Cbioacc PAHs. • Activation of biochars decreased the toxicity of leachates from the soils.

a r t i c l e

i n f o

Article history: Received 22 March 2016 Received in revised form 11 May 2016 Accepted 17 May 2016 Available online xxxx Editor: Sarmah Ajit Keywords: Bioaccessibility Remediation Soil amendment Contamination Biochar Activation

a b s t r a c t The aim of this study was to determine the effect of steam activation of biochars on the immobilization of freely dissolved (Cfree) and bioaccessible fraction (Cbioacc) of PAHs in soils. Additionally, the toxicity to various organisms like Vibrio fischeri, Lepidium sativum and Folsomia candida was measured before and after the amendment of biochars to soils. Three biochars produced from willow, coconut and wheat straw were steam activated and added to three different soils with varying content and origin of PAHs (coke vs. bitumen). The soils with the addition of the biochars (activated and non-activated) were incubated for a period of 60 days. Steam activation of the biochars resulted in more pronounced reduction of both Cfree and Cbioacc. The range of the increase in effectiveness was from 10 to 84% for Cfree and from 50 to 99% for Cbioacc. In contrast, the effect of activation on the toxicity of the soils studied varied greatly and was specific to a particular test and soil type. Essentially, biochar activation did not result in a change of phytotoxicity, but it increased or decreased (depending on the parameter, type of biochar, contaminant source, and soil and soil type) the toxic effect to F. candida, and decreased the toxicity of leachates to V. fischeri. © 2016 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Department of Environmental Chemistry, University of Maria Skłodowska-Curie, pl. M. Curie-Skłodowskiej 3, 20-031 Lublin, Poland. E-mail address: [email protected] (P. Oleszczuk).

http://dx.doi.org/10.1016/j.scitotenv.2016.05.114 0048-9697/© 2016 Elsevier B.V. All rights reserved.

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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1. Introduction Soil contamination in industrial areas is a serious problem in many countries. Contaminated sites should be remediate, otherwise it may lead to negative consequences such as exclusion of soils from plant production. Due to the significant area of impact of different manufacturing plants, conventional remediation of such soils is not undertaken. Traditional remediation method of heavy contaminated soil is incineration. This method is fast, however technically difficult, mainly due to the transportation of contaminated soil and advanced infrastructure. It makes this method expensive and not feasible everywhere. Our preliminary calculations have shown that the cost of remediation using biochar is several times cheaper than using traditional methods. Contaminants present in a soil are not subject to any control and they often migrate in a natural way to the adjacent grounds, negatively affecting the environment. Polycyclic aromatic hydrocarbons (PAHs) are a common environmental hazard (Srogi, 2007). Due to their mutagenic and carcinogenic properties, they pose a threat to living organisms, including humans. The coking and bitumen industries are some of the sources of PAHs (Mastral and Callén, 2000). The soils in the surroundings of these types of plants are characterized by high levels of PAH contamination ranged even from 920 to 3330 mg/kg (Ahn et al., 2005; Wang et al., 2015). In situ techniques, whose action mechanism is based not on complete elimination of contaminants but on binding the bioavailable and mobile fraction of these contaminants, currently attract a great interest in the area of soil remediation (Ghosh et al., 2011; Kupryianchyk et al., 2015). It is assumed that this fraction determines the toxicity of contaminants. Adsorbents characterized by strong affinity for contaminants are used to immobilize them. Thereby, their mobility in the environment and the exposure to living organisms is reduced (Cornelissen et al., 2006; Gomez-Eyles et al., 2013; Zimmerman et al., 2004). The most popular material used for this purpose is activated carbon (AC) (Ghosh et al., 2011). The efficiency of AC has been successfully confirmed in sediments, where reduction of the bioavailable fraction of various organic contaminants (Cornelissen et al., 2008; Gomez-Eyles et al., 2013) and their bioaccumulation (Cornelissen et al., 2006; Zimmerman et al., 2004), as well as in soils (Jakob et al., 2012; Kupryianchyk et al., 2016) and sewage sludges was observed (Oleszczuk et al., 2012). Nevertheless AC is considered to be very expensive, thus there is still need to find a more cost-effective material. Besides AC, biochar is a more and more used adsorbent to immobilize contaminants (Khan et al., 2015; Kupryianchyk et al., 2016; Oleszczuk et al., 2014). Biochar is a solid material obtained from the carbonization of biomass in an oxygen-limited environment. The research showed that biochar can effectively bind both heavy metals and organic contaminants (Ahmad et al., 2014; Beesley et al., 2014). Advantages of this type of material over AC include its lower production cost and its positive influence on the physical, chemical and biological properties of soils (Ok, 2016). Moreover, biochar may be also a source of nutrients (Lehmann, 2007), which are necessary for plants grow. Nevertheless, comparative studies revealed that the biochar is less effective in organic contaminants binding than AC (Jia and Gan, 2014; Kupryianchyk et al., 2016; Oleszczuk et al., 2012). This is mainly due to the worse surface properties of biochar, especially lower surface area (Kupryianchyk et al., 2016). Therefore, increasing the surface area of biochar as a result of activation can be a factor enhancing its effectiveness. In particular, activated biochar is usually produced via chemical or physical activation. Among these methods, steam activation enjoys great interest. The activation may affect other parameters of biochar concerning the surface chemistry. During the steam activation process decrease of the acidic and increase of phenolic functional groups occurs. Moreover, steam activation may affect other parameters like elemental composition or particle size distribution. Recent research has shown that steam-activated biochars can efficiently remove contaminants from water. For example, Ippolito et al. (2012) demonstrated the potential of steam-activated pecan shell biochar to sorb excess Cu ions from wastewaters. Shim et

al. (2015) also used steam activation to improve sorption capacity of biochar to Cu ions. Rajapaksha et al. (2015) observed a 55% increase in sorption capacity of sulfamethazine on steam-activated biochar compared to the non-activated biochar. Steam activation of biochar may therefore be an efficient method for increasing its sorption capacity, thereby representing a cost-effective alternative to immobilize contaminants in waters or soils. However, in the literature there is a lack of studies on the use of activated biochar for this purpose. Moreover, our preliminary research concerning the comparison between different method of biochar activation (activation by microwaves, carbon dioxide and steam) showed the best results (the highest specific surface area, volume, etc.) for steam activated biochar. Biochars can differ in their properties, hence it is important to determine the influence of activation on the sorption capacity of biochars to contaminants and on the toxicity of polluted soils that were amended with activated biochars. The most recent research (Shim et al., 2015) showed that activation may indicate the biochar toxicity, because of aromaticity increasing and decrease of polarity index. Our previous study (data not showed) showed that, depending on the soil type and contaminant source (coke vs. bitumen plants), the effectiveness of bioavailable PAHs binding by AC or biochar and the toxicity reduction can vary markedly (Kołtowski and Oleszczuk, 2016). However, there is still a lack of data that would provide comprehensive information in the context of the above considerations. The aim of this study was to determine the effect of biochar activation on the effectiveness of immobilization of PAHs in soils with different properties and with a varying content and origin of PAHs (coke vs. bitumen plants). The study evaluated immobilization of freely dissolved (Cfree) and bioaccessible (Cbioacc) PAHs. Furthermore, the effect of activated biochar on the toxicity of PAH polluted soils to different terrestrial organisms was studied. 2. Materials and methods 2.1. Soils and biochars Three different soils (KOK, POPI and KB) and three types of biochar (produced from: 1) wheat straw (WS), 2) coconut (CS) and 3) willow (WI)) were selected. Soils KOK and KB were sampled from a coking plant area (Dąbrowa Górnicza, Poland) and soil POPI from the vicinity of a bitumen processing plant (Wólka Łańcuchowska, Poland). Biochar WS was provided by Fluid S.A. (Sędziszów, Poland) and biochars CS and WI were provided by Mostostal (Wrocław, Poland). All biochars were produced by pyrolysis of the biomass at a temperature from 350 °C (start of pyrolysis) to 650 °C (max. pyrolysis temperature) in an oxygen-poor atmosphere. The physico-chemical properties of soils and non-activated biochars were determined as described in the SI and presented in Table S1 and S2. 2.2. Activation of the biochars Biochars were activated by the superheated steam, which was identified as a most effective activation in a previous study (data not showed). The biochars were activated in quartz fluidized bed reactor (heating rate: from 20 to 800 °C 10 °C/min in N2 atmosphere with a flow rate of 100 mL/min for 78 min, isothermal heating at 800 °C in a superheated steam atmosphere at (steam was generated in evaporator at temperature 200 °C and flow rate of liquid water 0.6 ml/min ). Physicochemical properties of non-activated and activated biochars are presented in Table 1. 2.3. Experiment Soils were milled with a ball mill (SM1 Retsch GmbH, Germany) and dried at 40 °C to constant weight. Dry soil aliquots (100 g) were transferred into 100 mL bottles (SIMAX, Czech Republic). Then, dried non-

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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Table 1 The parameters of porous structure of initial and steam activated biochars. Biochars/activated biochars

SBET

Smic

Vp

Vmic

R

pH

WS WS-H2O CS CS-H2O WI WI-H2O

26.3 246.2 3.1 626.8 11.4 840.6

10.8 140.4 2.3 472.4 4.5 509.3

0.0256 0.1587 0.0009 0.3361 0.0061 0.5765

0.0046 0.0622 0.0087 0.2094 0.0016 0.2245

1.95 1.02 0.60 0.85 1.08 1.09

9.9 8.8 8.0 7.2 9.1 8.2

SBET – surface area [m2/g]; Smic – surface of micropores [m2/g]; Vp – volume of pores [cm3/g]; Vmic – volume of micropores [cm3/g]; R – average pore radius [nm], pH – reactivity in KCl.

activated or activated biochars were added to each bottle at the dose of 5% (w/w). One bottle of each treatment was produced. Pure soil samples without biochar amendment were used as a control. To homogenize, samples were rolled end over end at 10 rpm (Rotax 6.8. VELP, Poland) for 24 h. Milli-Q water (Spring 15 UV/UF, Hydrolab, Poland) was added to each bottle at 40% water holding capacity (WHC) to rehydrate the treatments. The biochar-soil mixtures were rolled end over end at 10 rpm for 2 months in the dark and at a room temperature of 21 ± 1 °C. 2.4. Freely dissolved (Cfree) PAHs content The freely dissolved (Cfree) PAH in suspensions was determined as described in Cornelissen et al. (2008). Two POM strips (about 0.35 g) were put into an each conical flask containing prepared samples - 1 g of dry soil or dry soil-biochar-mixture and 40 mL of Milli-Q with 0.2 g/L NaN3. Samples with POM strips were prepared in triplicates. Samples were mixed for 30 days, after which the strips were removed, cleaned in Milli-Q and dried with some lint free tissue (Kleenex), wrapped in aluminium foil, and kept in the fridge until extraction. POM strips were extracted with 20 mL acetone/heptane (20:80 v/v) for 48 h by horizontal shaking and the extract was then concentrated to 1 mL. Samples were spiked with deuterated standards into the acetone/heptane at the beginning of extraction. The concentrated extracts were quantified for PAHs by gas chromatography – mass spectroscopy (GC–MS) using the internal standard method. Blanks with POM only and without adsorbents and soils were run to assess the level of contamination from other sources, which was found to be negligible. 2.5. Bioaccessible (Cbioacc) PAH content Bioaccessible concentration (Cbioacc) of PAHs, was determined using silicon rods according to Gouliarmou and Mayer (2012). The silicon rods were cleaned before use by Soxhlet extraction with ethyl acetate for 100 h. Hydroxylpropyl-β-cyclodextrin (HPCD) solution was prepared by adding 75 g of HPCD and 200 mg of NaN3 in 1 L of Milli-Q water. HPCD was used as a diffusive carrier to enhance desorption from the matrix (Gouliarmou and Mayer, 2012). Clean and dry silicone rods (3 m) were placed in empty 100 mL Pyrex bottles. Then 100 mg of sample (soil or soil/biochar mixtures) and 50 mL of HPCD-solution were added to each bottle. The samples were prepared in triplicates. Next, the samples were shaken in horizontal, orbital shaker at N200 rpm at room temperature for 30 days. Recovery standards were spiked and extraction was carried out using 2 × 100 mL of acetone without shaking once for 6 h and once overnight. The acetone was added and concentrated to 1 mL. 2.6. Gas chromatography–mass spectroscopy (GC–MS) Separation of PAHs was carried out with a Thermo Scientific Trace 1300 gas chromatograph equipped with a Restek Rxi-5 ms Column (length 30 m, 0.25 mm id and 0.25 μm film thickness). Detection was performed with a Thermo Scientific ISQ LT mass spectrometer in the electron impact mode. Detailed information about the PAHs analysis is presented in the supporting information (SI).

2.7. Toxicity evaluation Samples were evaluated by two solid phase tests (Collembola and Phytotoxkit F tests) and one test with eluates (Microtox®). Mentioned tests were selected because of the fact that the PAHs toxicity mechanisms are different with respect to selected test organisms. In relation to springtails PAHs may lead to decreasing of the Folsomia candida reproduction or death of adult organisms. PAHs presence in soil also may negatively affect the root and shoot grow, as well as seeds germination, especially during the early stage of plant development. Contaminants like PAHs may also provoke the bioluminescence inhibition of marine bacteria Vibrio fischeri, because of PAHs negative influence on their metabolism. Tests were performed to evaluate the toxicity of both control and biochar-amended soils to different endpoints. To evaluate the toxicity to springtails, the test was carried out with Folsomia candida according to the ISO guideline 11,267 (ISO, 1999). Mortality and reproduction of F. candida were monitored. The presented results were compared to the OECD control soil. Samples were prepared in triplicates and incubated for 4 weeks. To evaluate the effect on soil phytotoxicity, Lepidium sativum was selected as a test plant and test was performed according to test manual (Phytotoxkit, 2004). Germination and root growth inhibition were measured. OECD artificial soil was used in solid phase toxicity tests as a reference. OECD soil has been recommended as a medium for ecotoxicological tests and it is a “reference soil” in the testing of complex solid samples. The bioassays were performed in six replicates and incubated for 3 days. Detailed information about Phytotoxkit F and F. candida tests are presented in the SI. To evaluate the effect of BC on bacteria (Microtox®), eluates from control soils and non-activated and activated biochar-amended soils were tested. They were obtained according to the EN 12457-2 protocol (EC, 2002). The Microtox® toxicity test was used to evaluate the inhibition of the luminescence of Vibrio fischeri according to the test protocol (SDI, 1992). The values of inhibition were presented in relation to control, which was sample with bacteria and diluent. Samples were prepared in triplicates. Detailed information about the Microtox® test is presented in the SI.

3. Results and discussion 3.1. Effect of biochars and activated biochars in soils on Cfree of PAHs The soils were characterized by different levels of the sum of 16 (Σ16) PAHs content (Fig. 1). In soil POPI, the highest concentration of Cfree was noted (172 ng/L). Soil KOK was characterized by an equally high content of Cfree PAHs (153 ng/L) as POPI soil. The level of Cfree in KB soil was the lowest (52 ng/L). The non-activated and activated biochars amendment to investigated soils were effective in context of soil remediation, resulted in high efficiency of bioavailable PAHs binding. Nevertheless, the bioavailable fraction of PAHs (Cfree as well as Cbioacc) in soil is not a key factor in context of remediation strategy legislation. Hence, it is still problematic to relate the remediation effectiveness to any regulations. Amendment of biochar and activated biochar had different effects on the Cfree of Σ16 PAHs, which depended on the feedstock and soil type or

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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Fig. 1. Freely dissolved concentration (Cfree) of the sum (Σ) of the 16 PAHs in control soil and biochar-amended soil. KOK, KB and POPI – soil are shown in panels A, B, C, respectively. Amendments are biochars from wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 3.

contaminant source. In case of non-activated biochars, the most pronounced reduction of Cfree PAHs was obtained in KOK soil after application of the biochars WS (by 57%) and WI (by 48%) (Fig. 1A), in KB soil after application of WS biochar (by 47%) (Fig. 1B), whereas in POPI soil after application of CS biochar (by 86%) (Fig. 1C). In relative terms, the highest reduction of Cfree PAHs was observed in POPI soil for most of the biochars, whereas the weakest reduction was observed in KB soil (Fig. 1). No significant effect on the Cfree content was found in KOK soil in the case of CS (Fig. 1A) and in KB soil for CS and WI (Fig. 1B). In POPI soil, all the biochars significantly reduced Cfree PAHs (Fig. 1C). Generally, the relative reduction of Cfree as a result of different biochar amendments corresponded for both individual PAHs and their sum (Tables S3–S5). All three non-activated biochars were the most efficient in reduction of dibenz(a,h)anthracene in all investigated soils. No clear trends in reduction of the individual PAH groups were observed depending on the above-mentioned factors (Tables S3–S5). The level of the reduction, observed after non-activated biochar application was similar to the studies of other authors (Beesley et al., 2010; Gomez-Eyles et al., 2013, 2011; Khan et al., 2015). For example, Beesley et al. (Beesley et al., 2010) observed a N40% reduction of bioavailable PAHs after 60 days of soil incubation with hardwood-derived biochar. A clearly lower reduction of freely dissolved PAHs (b 34%) was observed by Gomez-Eyles et al. (2011) after 56 days of incubation of soil contaminated with these compounds, also using hardwood-derived biochar for PAH immobilization. The reduction of bioavailable PAHs observed by Khan et al. (2015) after application of biochars derived from sewage sludge, soybean straw, rice straw and peanut shells ranged from 27 and 80% depending on biochar dose and type. However, in most cases, these values are still distinctly lower, both in the present study and in the studies of other authors (Beesley et al., 2010; Gomez-Eyles et al., 2011; Khan et al., 2015; Kupryianchyk et al., 2016), than the results obtained for activated carbon (Jakob et al., 2012; Oleszczuk et al., 2012). Steam activation of all the biochars caused a significant decrease of the Cfree PAHs relative to non-activated biochars (Fig. 1). However, this effect varied depending on soil type or contaminants source. Relatively the highest effect of biochars activation was found in KOK soil (Fig. 1A). In this soil, activation had the greatest influence on the effectiveness of CS biochar (its effectiveness was higher by 84% than in the case of non-activated biochar), followed by WS (69%) and WI (53%). In KB soil, activation increased the efficiency of immobilization of Cfree PAHs in the range from 28% (CS) to 61% (WI). However, in the POPI soil, activation had an effect on increasing the effectiveness of immobilization of Cfree PAHs only after application of the biochars WS (by 63%) and WI (by 41%). Activation of CS biochar had no influence on the Cfree

PAHs in the POPI soil. In KOK soil, the Cfree reduction of PAHs after adding activated biochars was ranged from 76 to 87%, in KB soil from 29 to 69%, while in POPI soil from 76 to 88%, depending on biochar type. Similar to non-activated biochars, the effectiveness of immobilization of the individual Cfree PAH groups depended on soil type/contaminant source and material used (Tables S3–S5). However, a clear trend was observed where the efficiency of immobilization of the individual PAHs increased with the increasing of their molecular mass. All activated biochars reduced completely 6-ring PAHs, regardless of soil type (Tables S3–S5). In context of individual PAHs, application of WI-H2O and WS-H2O biochars caused 100% reduction of anthracene, benzo(a)pyrene, indeno(1,2,3-cd)pyrene, dibenz(a,h)anthracene and benzo(ghi)perylene in all investigated soils. In case of CS-H2O, the best reduction of indeno(1,2,3-cd)pyrene, dibenz(a,h)anthracene and benzo(ghi)perylene was observed in all investigated soils. The increase of the biochars effectiveness as a result of developing their specific surface area (Table 1) is confirmed by previous observations on AC and biochars, in which a relationship between sorption capacity and surface area was often observed (Hale et al., 2016; Kupryianchyk et al., 2016). Comparing our results to previous studies, it can be concluded that the level of reduction of Cfree PAHs after application of activated biochars is similar to that for AC (Cornelissen et al., 2006; Gomez-Eyles et al., 2013; Hale et al., 2013; Jakob et al., 2012; Jia and Gan, 2014; Kupryianchyk et al., 2016; Oleszczuk et al., 2012) and considerably exceeds the binding of contaminants efficiency in comparison to non-activated biochars (Beesley et al., 2010; Gomez-Eyles et al., 2011; Oleszczuk et al., 2014). Nevertheless, in the literature there is a lack of research related to the effect of biochar activation on the contaminants binding in various soils contaminated by different PAHs sources. In the present study, it was observed that the PAH immobilization after biochar application was substantial in some soils, but less pronounced in others. It is assumed that the surface area of the adsorbent has a major influence on the effectiveness of Cfree reduction (Jakob et al., 2012; Kupryianchyk et al., 2015), but this can be impaired by the presence of some components in the soil (e.g. dissolved organic matter, DOC) (Hale et al., 2009). The range of Cfree PAH reduction after application of non-activated biochars in KOK and KB soils was in many cases related with the surface area of biochar (Table 1, Tables S3 and S4). After application of activated biochars, these relationships were only observed in few cases in KOK and KB soils. This indicates that the lowest surface area found (which was 246 m2/g for WS-H2O biochar) was sufficient to fully bind Cfree PAHs in these soils. Any further increase in SBET of the biochars seemed to be irrelevant and in this case the range of reduction of Cfree PAHs would only be determined by soil type and contaminant source.

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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It should however be noted that in POPI soil the reduction of Cfree was inversely proportional to the surface area (Table S5) of non-activated biochars and the highest efficiency of binding of Cfree PAHs was observed for CS biochar, characterized by the lowest SBET (Table 1). A several dozen-fold increase in the surface area of CS biochar did not increase the effectiveness in binding Cfree PAHs in this soil comparing to the non-activated analogue. A significant reduction of Cfree PAHs related to the non-activated biochar after activation was only obtained for WSH2O (Fig. 1C), but it was still smaller than that observed for CS/CS-H2O. Nevertheless, both non-activated and activated biochars reduced Cfree PAHs in relation to POPI soil. The absence of a Cfree reduction in the POPI soil comparing to the non-activated biochars suggests that in this soil other mechanisms (than pore filling) play a major role in the sorption of PAHs. Such a different behavior of POPI soil, compared to KOK and KB after application of adsorbents depended on the one hand, from a different source of contaminants in this soil, and on the other hand from the properties of these soils. The KOK and KB soils were both contaminated by a coking plant (which essentially does pyrolysis of coal and probably emits recondensates of pyrosynthesis products, which are primarily soots or soot-like materials). In contrast, the POPI soil was contaminated by a bitumen plant (basically a distillation of crude oil, where different oily to bituminous fractions may be emitted, which are essentially amorphous). This is confirmed by the significantly higher content of black carbon in KOK and KB soils than in POPI soil (Table S1). PAHs originating from this latter fraction are probably more mobile and are adsorbed more readily on the biochar surface than in the pores of biochar/activated biochar. Moreover, POPI soil contained significantly more DOC than KOK and KB soils. It is conceivable that bituminous materials release more DOC than soot-like materials. DOC is a commonly known factor that contributes to a decrease in the efficiency of carbon adsorbents (Hale et al., 2009; Oen et al., 2012) as a result of pore blocking (Pignatello et al., 2006). Therefore, it may be presumed that the surface processes play the major role in this soil.

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was characterized by the highest surface area, and showed the highest reduction of Cbioacc. No clear trends were observed in the reduction of the Cbioacc of individual PAHs (SI Tables S6–S8), which was most probably associated with the small overall effect of the biochars on Cbioacc PAHs in comparison to the Cfree. Biochar activation had a significant effect on Cbioacc PAHs, substantially reducing their content (Fig. 2). This effect was however completely different depending on the investigated biochar than that observed for Cfree PAHs (Fig. 1). In KB and POPI soils, the Cbioacc PAHs concentration decreased almost below detection. In KOK soil, such a high level of Cbioacc reduction was only obtained in WI-H2O. In the case of WSH2O and CS-H2O, the reduction of Cbioacc was lower: 61.1 and 63.7%, respectively. Activation of biochar proofed most effective in KB soil (92– 96%), followed by POPI (93–99%), while it was weakest in KOK soil (50–98%). In context of individual PAH groups, the range of reduction increased with increasing molecular mass (Tables S6–S8), similarly as in the case of Cfree PAHs. This relationship was observed for most of the biochars in KB and POPI soils, but not in KOK soil (Tables S6–S8). Moreover, strong correlation between Cfree and Cbioacc PAHs in all experimental variants concentration was observed for Σ16 PAHs in soil KB (r = 0.914, P ≥ 0.01). In soil KOK (r = 0.736) and POPI (r = 0. 737) the relationship was lower but also statistically significant (P ≥ 0.1). Nevertheless, the correlation for individual PAHs between Cfree and Cbioacc in each soil was not always observed (Table S9). Depending on the type of PAH fraction (Cfree vs Cbioacc), the reduction of PAHs varied. This shows that other mechanisms are responsible for the bioaccessibility than for the Cfree of PAHs. Activation had a more pronounced impact (in particular in KB and POPI soils) on the reduction of Cbioacc than of Cfree. This may indicate that the pore filling mechanism, which requires long time, is important in reducing Cbioacc, whereas in the case of Cfree these are surface responses which are characterized by quicker achievement of the balance, as suggested previously. 3.3. Solid phase toxicity (L. sativum, F. candida)

3.2. Effect of biochars and activated biochars on Cbioacc PAHs The effect of non-activated biochars on the content of Cbioacc PAHs also varied, as in the case of Cfree PAHs (Fig. 2). No statistically significant differences were found in the concentration of Cbioacc PAHs in KOK soil between control and amended soil with non-activated biochars (Fig. 2A). In KB soil, only the WS biochar significantly reduced the level of the Cbioacc PAH fraction, whereas CS and WI non-activated biochars did not reduce the Cbioacc in this soil. All the biochars substantially reduced Cbioacc PAHs in the POPI soil; similarly as in KB soil, WS biochar,

In general, tests on both, plant and springtail, showed responses in toxicity provoked by soil, amended soil and even on activated biochar amended soil. Root growth of L. sativum was generally inhibited up to 30% irrespective of the amendment, biochar treatment and feedstock, except for the WI biochar (Fig. 3A-C). In all the soils amended with WI biochar root growth was enhanced. In the POPI soil the amendment of biochar in some cases increased the root growth inhibition (Fig. 3C). Biochar activation did not result in a change of the toxicity in most cases. No significant differences were found between the biochars WI,

Fig. 2. Bioaccessible concentration (Cbioacc) of the sum (Σ) of the 16 PAHs in control soil and biochar amended soil. KOK, KB and POPI – soil are shown in panels A, B, C, respectively. Amendments are biochars from wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 3.

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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Fig. 3. Root growth inhibition [%] of Lepidium sativum in control soil and biochar-amended soil. KOK, KB and POPI – soil are shown in panels A, B, C, respectively. Amendments are biochars from wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 6.

CS and WS and their activated equivalents in the context of L. sativum roots stimulation. The mortality of F. candida remained the same in KOK soil irrespective to the amendment (Fig. 4A). In KB soil, an increase in F. candida mortality was observed after using the tested materials. Similarly as in KOK soil no significant differences were observed between biochars and activated biochars (except of WS and WS-H2O) (Fig. 4B). The highest variation was, however, observed in POPI soil. Application of non-activated biochars WS and WI to this soil caused a significant increase in the mortality of F. candida relative to the control soil. Activated WS-, CS-, and WI-derived biochars amendment to POPI soil, caused significant reduction of the F. candida toxicity in comparison to the control soil (Fig. 4C). F. candida's reproduction was also tested (Fig. 5). In KOK soil, non-activated biochars significantly stimulated F. candida reproduction relative to the control soil (Fig. 5A). Activation of WS biochar reduced its stimulating effect on F. candida reproduction, though it was still higher than in the control soil. Activation of CS and WI negatively affected the reproduction, which fell below the level observed for the control soil. In the KB soil, all biochars stimulated the reproduction of F. candida, except for the non-activated WS biochar (Fig. 5B). The biggest effect was the CS biochar (activated and non-activated) and activated-WI biochar. In the POPI soil, CS biochar (activated and non-activated) and activated WI biochar stimulated F. candida reproduction (Fig. 5C). In the other

cases, the reproduction of F. candida was completely inhibited (WS, WI) or substantially reduced (WS-H2O). Even though in the case of F. candida mortality no significant differences were observed between activated and non-activated biochars, activation had a significant effect on F. candida reproduction in all the soils: in the KOK soil, it reduced the reproduction in relation to non-activated biochars, whereas an opposite trend was observed in KB and POPI soils. The effect of biochar on living organisms has been described quite extensively in the literature (Lehmann et al., 2011). But there are fewer studies on the effect of AC (Hale et al., 2013; Jakob et al., 2012; Jonker et al., 2009; Kołtowski and Oleszczuk, 2016), while studies on activated biochars are exceptionally scarce (Shim et al., 2015), in particular together with their non-activated forms. The diverse results observed in this study in relation to various organisms in different soils most probably indicate the effect of variable factors affecting the stimulation or inhibition of their development. It is important to emphasize that the reduction of bioavailable PAHs was not associated with a change in the toxicity of the soils investigated, which may indicate that the toxicity observed in the present study is not related with the Cfree or Cbioacc of the PAHs. Moreover chemical proxies of pollutant exposures may be less indicative in case of soil than in case of sediment. Nevertheless, we cannot rule out the fact that in some cases the reduction in the toxicity can be partially associated with a reduction of these contaminant's concentrations. As far as AC and biochar are concerned,

Fig. 4. Folsomia candida mortality [%] in control soil and biochar-amended soil. KOK, KB and POPI – soil are shown in panels A, B, C, respectively. Amendments are biochars of wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 6.

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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Fig. 5. Number of Folsomia candida juveniles in control soil and biochar-amended soil. KOK, KB and POPI – soil are shown in panels A, B, C, respectively. Amendments are biochars of wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 6.

inconsistent data on their effects on living organisms are found in the literature. A negative effect (Hale et al., 2013; Jonker et al., 2009, 2004; Oleszczuk et al., 2013), a positive effect (Domene et al., 2015; Hale et al., 2013; Zielińska and Oleszczuk, 2015), and no effect (Domene et al., 2015; Millward et al., 2005; Sun and Ghosh, 2007) on living organisms have been observed. These results confirm the previous information concerning the different effects of biochars on organisms depending on the feedstock of biochar (Anjum et al., 2014; Domene et al., 2015; Oleszczuk et al., 2013). It was, however, observed that, depending on soil, the effects of both non-activated and activated biochars varied. This may be due to the different effects of biochar amendment on soil properties (Ok, 2016). A negative effect may result from the reduced bioavailability of nutrients and water (Hale et al., 2013; Jośko et al., 2013) as well as from the presence of contaminants occurring in biochar and soil (Table S1 and S2) (Oleszczuk et al., 2013; Zielińska and Oleszczuk, 2015). Other factors could be e.g. changes in soil and/or

eluent pH, changes to essential plant nutrients, the possibility of other chemical agent in the eluents used to screen toxicity with Vibrio (metals, phenols, etc.), physical agitations associated with sharp biochar F. candida. A positive effect is associated with the supply of nutrients and carbon as well as with a reduction of the negative effect on living organisms as a result of binding contaminants present in the soil. Biochar activation did not affect L. sativum. This confirms our previous observations where materials with a high surface area (activated carbon, carbon nanotubes) (Jośko et al., 2013) did not affect negatively plants, either. The absence of the effect of activation potentially excludes the binding of nutrients as a factor in the possible toxic effect observed in POPI soil (Fig. 3C), which is frequently suggested as a possible factor of biochar phytotoxicity (Ok, 2016). However, biochar activation reduced the negative effect of the biochars on the mortality and reproduction of F. candida in KB and POPI soils, whereas in KOK soil activation negatively affected the

Fig. 6. Vibrio fischeri luminescence inhibition [%] in control soil and biochar and biochar-amended soil. KOK and POPI – soil are shown in panels A and B, respectively. Amendments are biochars from wheat straw (WS), coconut (CS), and willow (WI) and the activated biochars are indicated by H2O. Error bars indicate the standard deviation of n = 3.

Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114

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reproduction of F. candida (no significant influence on its mortality was found in this soil). On the one hand, the reduction of the toxic effect towards F. candida may be associated with a decrease in the pH of the biochars due to their activation (Table 1). Greenslade and Vaughan (2003) observed that an increase in pH is unfavorable to the growth of F. candida and acidic pH is most optimal. Liesch et al. (2010) also reported that the high earthworm toxicity of a poultry litter biochar was suggested to be related by the high pH and gaseous NH3 emissions. A significant (positive) relationship between biochar pH and toxicity to F. candida was observed in our previous study. On the other hand, however, biochar activation undoubtedly increased the affinity of the biochars for organic contaminants occurring in the soil (Fig.1, Fig. 2), thus reducing their negative effect on the organisms, which has been frequently observed for sediments with AC (Millward et al., 2005; Zimmerman et al., 2004). Biochar activation had a completely different effect on F. candida in KOK soil than in KB and POPI (Fig. 5). The inhibition of F. candida reproduction after biochar activation observed in KOK soil most probably resulted from a change in the soil pore water chemistry and/or a change in the availability of essential compounds such as soluble organic carbon or nutrients, which can be adsorbed by the biochar (Gomez-Eyles et al., 2011; Jonker et al., 2009). Nutrients were introduced into KOK soil together with the unmodified biochars, which evidently caused an increase in the number of juveniles relative to the soil that did not contain the biochars. Biochar activation contributed to the elimination of these compounds from the biochars and additionally increased surface area of the biochars promoted the binding of nutrients present in the soil, which in consequence resulted in a decrease of reproduction.

of dissolved carbon (DOC), as already suggested previously. The DOC content in POPI soil was three times higher than in KOK soil (Table S2). DOC is a commonly known as a fouling agent that can limit the sorption capacity of AC/biochar by blocking the carbon pores. 4. Conclusion In the present study, four observations should be stressed. Firstly, steam activation of the biochars significantly increased the immobilization of the bioavailable and bioaccessible fraction of PAHs (both Cfree and Cbioacc) present in contaminated soils. However, the PAH reduction of Cfree and Cbioacc varied in different soils and the activation in general worked. Nevertheless, among the activated ones, surface area was not decisive. Secondly, significant differences were found in the reduction of Cfree and Cbioacc. Activation reduced more effectively Cfree in KOK soil and Cbioacc in KB and POPI soils which could be related with different source of PAHs and soil properties. Thirdly, apart from few exceptions, biochar activation had no effect or had a positive effect on the toxicity of the soils studied. To conclude, it should however be emphasized that the multifaceted effect of biochars and activated biochars, as manifested in increased toxicity relative to the control soil, may result from indirect effects caused by biochars and activated biochars. Acknowledgements This work was conducted in a BCAMEND project PSPB-135/2010 supported by a grant from Switzerland through the Swiss Contribution to the enlarged European Union.

3.4. Toxicity of leachates (V. fischeri) Appendix A. Supplementary data KB soil did not exhibit toxicity to V. fischeri and amendment of nonactivated and activated biochars to this soil did not result in a change of the toxicity level (data not shown). However, a significant effect was found in KOK and POPI soils (Fig. 6). The addition of the all types of biochars to KOK soil caused a significant reduction in the toxicity of leachates in the following order: WS (by 100%) N WI (by 86%) N CS (by 27%) (Fig. 6A). The addition of CS to POPI soil did not affect significantly the toxicity of leachates in comparison to the control, whereas WS and WI reduced the toxicity, respectively by 67% and 79% (Fig. 6B). That is interesting, because amendment proofed successful in terms of reducing PAH bioavailability/bioaccessibility, indicating that other toxicants (with lower biochar affinity) in the eluate may be responsible for toxicity (e.g. potentially more polar ones). In both soils, activation of the biochars increased their effectiveness in reducing the toxicity of leachates. Activated biochars caused a total reduction of the toxicity in KOK soil. In POPI soil, the reduction of the toxicity after activation was less pronounced than that observed in KOK soil. Compared to non-activated biochars, the effectiveness of reduction of luminescence inhibition was higher by 15% (WS), 23% (CS), and 9% (WI). The purpose of adding biochars/activated biochars to soils was to reduce the soluble fraction of contaminants that exhibit a toxic effect towards organisms. The efficiency of biochar amendment was confirmed by the results regarding to the inhibition of V. fischeri luminescence. As a result of the decreased solubility of contaminants by introducing adsorbents, the toxic effect caused by these contaminants was reduced. In KOK soil, this effect was clearly dependent on the surface area in the case of non-activated biochars (Table 1, Fig. 6A). However, a similar relationship was not found in POPI soil (Fig. 6B), which confirms the previous suggestions that in POPI soil the surface interactions play more important role than the surface area. The observed differences between KOK and POPI soils were most probably due to the different origin and composition of the contaminants in these soils and the different level of their toxicity (Table 1, sum of the total PAHs) to V. fischeri. The toxicity could also have been reduced by the presence

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Please cite this article as: Kołtowski, M., et al., Effect of steam activated biochar application to industrially contaminated soils on bioavailability of polycyclic aromatic hydroca..., Sci Total Environ (2016), http://dx.doi.org/10.1016/j.scitotenv.2016.05.114