Basic properties of the soil (Andisol) and sewage sludge biochar (SSB) used in this study.
Management of industrial wastes has been one of the most challenging problems in most urban municipalities due to increasing waste volume with limited disposal areas, and energy-consuming and high-cost treatment processes for disposal. In Japan, although the total volume of the industrial waste generated has been relatively constant since 1990 being approximately 400 million tons per year, remaining capacity of the final disposal for the industrial waste has decreased by approximately 20% since 1994, reaching to 172 million m3 in 2007 (Ministry of the Environment Government of Japan, 2011). This disposal capacity is predicted to be filled in the average of 8.5 years for Japan, and 3.6 years for Tokyo Metropolitan areas. Due mainly to high cost of treatment for proper disposal, illegal dumping of the industrial waste has been a new problem despite of severe regulation and monitoring of affected areas. The number and total volume of unsolved cases of illegal dumping and improper disposal of the waste were 2,610 and 1.78 million tons, respectively, in 2010 (Ministry of the Environment Government of Japan, 2011).
Sewage sludge is one of the most produced industrial wastes and comprised approximately 20% (77.2 million tons) of the total volume of industrial wastes generated across Japan in 2010 (Ministry of the Environment Government of Japan, 2011). However, the volume of its final disposal was insignificant (0.37 million tons) since the majority of sewage sludge were reclaimed and/or treated by intermediate processing such as thickening, dewatering, anaerobic digestion, composting, incineration, carbonization, and melting. On the dry solid basis, 78% of the total volume of sewage sludge (1.72 million tons) was recycled in beneficial applications mainly for construction materials (1.39 million tons), energy production (0.02 million tons), and application in agriculture and horticulture as alternative fertilizers and/or soil conditioner (0.31 million tons). Due to new technology and diversification of sewage sludge recycling techniques, further recycling avenues are expected particularly for production of energy, agriculture, forestry, livestock, and fisheries in the future.
Pyrolysis process of sewage sludge is one of the useful approaches for sewage sludge recycling, and its product called sewage sludge biochar (SSB) can be used as supplemental or alternative material to coal for thermal power plants. Some municipalities in Japan have initiated to use SSB as a part of thermal sources for energy production. In Tokyo, since 2007, 8,700 tons of SSB have been produced per year from 99,000 tons of sewage sludge and mixed with coal for energy plant to contribute approximately 1% of the total calorific value by the plant. The SSB produced is pyrolysed at 500oC for one hour and generates 2,000 kcal kg–1 of heat calorie, which is equivalent to one third of that of coal. Aichi Prefecture started a similar project as Tokyo in 2012, and uses 2,700 tons of SSB pyrolysed at 500oC from 33,000 tons of sewage sludge every year to generate 4.6 million kWh of energy, which is capable of providing electricity equivalent to annual usages of typical 1,270 households in the area.
Sewage sludge biochar can be also used for supplemental or alternative fertilizer material for crop production. Different feedstock properties and pyrolysis temperatures, however, yield SSB with different physicochemical properties, thus exhibit different degrees of effect when SSB is applied to soil as soil amendments or fertilizers for improving crop production or soil properties (Chan & Xu, 2009). An SSB produced at 800oC in Japan contained moderate amounts of macronutrients for crop production, among which P was relatively high (78.9 g P kg–1), and relatively high amounts of heavy metals (1,100 mg Cu kg–1, 1,630 mg Zn kg–1, 4 mg Cd kg–1, 126 mg Ni kg–1) which were within the limits legislated in Japan (Kawano et al., 2012). Effects of SSB application to soils up to 40% by weight on the growth of Begonia (
Agronomic effects of SSB application to soils, therefore, widely vary depending on physicochemical properties of the sewage sludge, pyrolysis temperature, and soil properties, which need to be further clarified including the heavy metal dynamics in order for the SSB application to be broadly accepted in agricultural and horticultural practices. Therefore, objectives of this study were to 1) investigate the leachability of heavy metals, particularly Cu, Zn, and Cd from SSB as applied to soil with varying rates, and 2) evaluate the effect of SSB application to soil on plants’ growth and absorption of the heavy metals, using SSB produced at two different pyrolysis temperatures.
2. Materials and methods
2.1. Soil and biochar
A soil used in this study was a forest Andisol collected from a mulberry plantation forest in Hachioji, Tokyo, Japan (35.692, 139.316) on Apr. 29, 2011. Surface 15-cm soils were sampled, dried at 45oC overnight, sieved through 2 mm, and used for physicochemical analyses and a pot study.
Sewage sludge biochars were produced in commercial plants at high (approximately 800oC; SSB-H) and low (approximately 300oC; SSB-L) temperatures, crashed by hummer, and sieved through 2-mm sieve for chemical analyses, and homogenized between 2 and 5 mm in size for the pot study.
2.2. Pot study
A pot study was performed on campus of Soka University, Tokyo, Japan. Japanese mustard spinach (
After harvest, the plants were divided into shoot, root, and bean sheath (only for common bean), and dried at 70oC overnight. The soil and SSB in the pot were separated using 2-mm sieve, and separately dried at 45oC overnight.
2.3. Soil, biochar, plant analyses
Dry weight (DW) of each part of the plants was determined after drying at 70oC overnight.
The soil, SSBs, and plant tissues after the pot study were ground to pass through 150 µm in size and digested for total elemental analyses for heavy metals. Two grams of the soil sample was heated to 180oC with 30 mL of concentrated nitric acid in a beaker with a glass watch on a hotplate until it turned like a syrup. Then, 30 mL of a perchloric acid-nitric acid mixture (1:4) was added and heated for further 10 min. After cooling, 25 mL of hydrochloric acid (1:5) was added and heated to 130oC for 1 hr. After cooling, the content was quantitatively transferred to a 100 mL flask and filtered through a Whatman No 1 paper (Committee for Analytical Methods for Soil Environment, 1997). Two grams of the SSB sample in crucible was ashed in an electric furnace at 550oC for 8 hr, and the ash was transferred to a beaker with 5 mL of concentrated nitric acid and heated to 120oC on a hotplate for 3 hr. After cooling, 25 mL of hydrochloric acid (1:5) was added and heated at 120oC for further 60 min. After cooling, the content was quantitatively transferred to a 25 mL flask and filtered through a Whatman No 1 paper (Japan Soil Association, 2010). One gram of each of the shoot, root, and sheath plant samples was heated to 140oC with 10 mL of concentrated nitric acid in a beaker with a glass watch on a hotplate until the content is reduced to approximately 1 mL. After cooling, the content was quantitatively transferred to 25 mL flask using 1% nitric acid, and filtered through a Whatman No 1 paper (Committee for Experimental Methods for Plant Nutrition, 1990).
The heavy metals extractable by 0.1
Prior to analytical determination, all filtrates were further filtered through a 0.45 µm membrane. Total and extractable concentrations of Cu, Zn, and Cd in the soil, SSBs, and plant samples were determined using ICP (ICPS-7000 ver. 2.1, Shimazu).
2.4. Statistical analyses
Significant differences of the total and extractable concentrations of Cu, Zn, and Cd in the soil, SSBs, and plant samples among different SSB application rates for each SSB type and each plant were tested by ANOVA using STATISTICA 6.1 (StatSoft Inc., Tulsa, Okalahoma, USA). Unless otherwise stated, the differences were significant at
3.1. Soil and biochar properties
The Andisol used in this study had an almost neutral pH (H2O) of 7.1 and relatively average TC and TN concentrations (Table 1). The total heavy metal concentrations in the soil were 25 mg Cu kg–1, 43 mg Zn kg–1, and 4.9 mg Cd kg–1. The SSB used in this study had slightly acidic pH levels of 6.6 (SSB-H) and 5.6 (SSB-L). The total Cd concentrations were similar for both SSB types ranging 1.4–1.5 mg kg–1, while the total Cu and Zn concentrations in the SSB-H were 5 and 1.7 times greater than those in the SSB-L, respectively. The dilute acid (0.1
3.2 Dry weight of the plants
Seeds of both plants with all treatments germinated 100% except for those of the bean with SSB-L 25% treatment being 66% of the germination rate.
The average DW of individual spinach shoot showed a significant decrease with increasing application rates of both SSB-H and SSB-L, respectively (Fig. 1a). The highest DW was 1.1 and 1.4 g with SSB-H 0% and SSB-L 5% treatment, respectively. The average DW of the bean shoot did not show significant differences among the SSB-H treatment, but a significant increase with SSB-L 5% and 15% compared with that of control.
The average DW of the spinach root showed a significant decrease with increasing application rate of SSB-H, but not among the SSB-L treatment except for SSB-L 25% showing the lowest DW among the treatment (Fig. 1b). The average DW of the bean root showed a significant decrease with the increasing SSB-H application rate, and a significant increase only with SSB-L 15% among the SSB-L treatment.
The average DW of the bean sheath was not significantly affected by the SSB application, ranging from 0.04 and 0.18 g among the SSB-H treatment, and 0.04 g for SSB-L 5% rate (the bean did not bear the sheath with SSB-L 15% and 25% rates; Table 2).
|SSB-H 0||0.07ab||5.37a||3.04a||0.58a||SSB-L 0||0.07A||5.37A||3.04A||0.58A|
|SSB-H 25||0.17ab||1.99a||2.62a||0.28b||SSB-L 5||0.04A||10.75A||5.00A||1.46A|
|SSB-H 50||0.18a||1.87a||3.36a||0.26b||SSB-L 15||na||na||na||na|
|SSB-H 75||0.04b||5.77a||3.43a||0.73a||SSB-L 25||na||na||na||na|
3.3. Total heavy metal concentrations in the plants
Copper concentrations in the spinach shoot significantly increased with both SSB treatments over the control, respectively, while, although not significantly different, those in the bean shoot were lower with both SSB treatments compared with the control, respectively (Fig. 2a). Zinc concentrations in the spinach shoot significantly increased with both SSB treatments over the control, respectively, except for SSB-L 5% rate (Fig. 2b). On the other hand, Zn in the bean shoot was not significantly affected by both SSB treatments, except for SSB-L 5% being significantly lower than the control. The shoot part of each of both plants contained significantly greater Cd concentrations with both SSB treatments over the control, respectively (Fig. 2c).
The concentrations in the plant root were generally greater than those in the shoot for all heavy metals investigated regardless of the plant, SSB type and application rate. The Cu concentration in the spinach root was greatest with SSB-H 25% rate and SSB-L 15% rate among SSB-H and SSB-L treatments, respectively, while Cu in the bean root was greatest with SSB-H 50% rate and SSB-L 25%, among each SSB treatment, respectively (Fig. 2d). The Zn concentrations in the spinach root with SSB-H 25% and 50% rates were significantly greater than that of the control, and although not significant, those with the SSB-L treatment were greater than that of the control (Fig. 2e). The bean root absorbed significantly greater Zn with SSB-H 50% and 75% rates, and not significantly but greater Zn with SSB-L 15% and 25% rates, compared with that of the control, respectively. Cadmium in the spinach root was significantly higher with SSB-H 75% rate than those at other rates, but Cd with the SSB-L treatment was lower than that of the control (Fig. 2f). The Cu in the bean root was significantly lower with SSB-H 75% rate and higher with SSB-L 0% rate compared to other rates, respectively.
Any of Cu, Zn, and Cd in the sheath was not significantly affected by either application of SSB-H or SSB-L compared with that of the control, respectively, except for Cd with SSB-H 25% and 50% rates being significantly higher than that of the control (Table 2).
3.4. Total heavy metal concentrations in the biochar after the pot study
The total Cu concentration in the SSB-H after the pot study was not significantly affected for the spinach but significantly increased with SSB-H 75% rate for the bean (Fig. 3a). The total Cu concentrations in the SSB-L were not significantly affected by the application rate for both plants. After harvest of the spinach the total Zn in the biochar was not affected by the application rate for both SSBs, but at the bean’s harvest only SSB-H 75% rate caused significantly higher total Zn among the SSB-H treatment (Fig. 3b). The total Cd in the biochar did not significantly change among each of the SSB rates and plants, respectively, except for that with SSB-H 75% rate with the spinach being significantly greater than other SSB-H rates (Fig. 3c).
3.5. Total heavy metal concentrations in the soil after the pot study
The total Cu concentration in the soil after the pot study was significantly increased only with SSB-H 75% rate among the SSB-H treatment for both plants, respectively, but not affected among the SSB-L treatment for both plants (Fig. 4a). The total Zn in the soil tended to increase with the SSB-H application rate and was significantly greater with SSB-H 75% rate compared with those with other rates (Fig. 4b). The total Zn in the soil was not significantly different among the SSB-L treatments for both plants. The total Cd in the soil was significantly increased with SSB-H 25% and 50% rates for the spinach, but not affected for the bean (Fig. 4c). The total Cd in the soil with the SSB-L treatment significantly increased compared with that of the control for both plants, respectively.
3.6. Acid-extractable heavy metal concentrations in the soil after the pot study
The dilute acid (0.1
4. Results and discussion
4.1. Heavy metal concentrations in the soil and biochar
It appears that the Andisol used in this study contained less but comparable total Cu and Zn, and greater total Cd concentrations compared with the concentration range in similar soils of Japan. The concentrations of Andisols sampled in surrounded subareas of Tokyo ranged from 97 and 140 with the average of 118 mg Cu kg–1, from 121 and 175 with the average of 143 mg Zn kg–1, and from 0.37 and 0.55 with the average of 0.44 mg Cd kg–1 (Terashima et al., 2004). Some heavy metals including Cu, Zn, and Cd have tendency of being retained thus accumulated in soils given being relatively immobile after weathering in the soil (Terashima et al., 2004). High concentrations of some heavy metals including Cd, Hg, Pb, and Sb were observed because of possible artificial interventions especially in suburb areas of Tokyo (Terashima et al., 2007). In fact, the area where the Andisol used in this study was sampled was a former forest converted to a plantation area for mulberry (
Many properties including heavy metal concentrations in SSB widely vary primarily depending on those contained in the feedstock (Chan & Xu, 2009). An SSB pyrolysed at 800oC from sewage sludge in Kyoto, Japan contained 1,100 mg Cu kg–1, 1,630 mg Zn kg–1, 4 mg Cd kg–1 (Kawano et al., 2012), while one pyrolysed at 500oC using sewage sludge in Madrid, Spain contained 222 mg Cu kg–1, 1,250 mg Zn kg–1, 1.79 mg Cd kg–1 (Paz-Ferreiro et al., 2012). It seems that both SSB used in this study fall in the low end of concentration ranges for Cu, Zn, and Cd in the SSB found in the literature. Particularly, Zn concentrations in both SSBs were exceptionally lower than those in the literature. The heavy metal concentration in the SSB appears to accumulate as the pyrolysis temperature increases (Hossain et al., 2011), to which the SSB used in this study followed a similar pattern.
4.2. Effect of biochar on plant growth
The DW of spinach shoot and root and bean root significantly decreased with increasing rates of SSB-H due mainly to a lack of soil volume in the pot. In fact, chlorosis due to N deficiency was observed with the SSB-H treatment and more pronounced on leaves of both plants with higher SSB-H rates. Although the plant was fertilized, it appeared that the lack of soil volume in the pot with high SSB-H rates limited plant root growth thus the plant growth. In addition, although the concentration was not measured in soil or plants, both plants with the SSB-L treatment showed a leave curvature due possibly to excess uptake of boron. When SSB-L was applied, however, the shoot of both plants grew more than that of the control and their DW peaked at 5% rate for spinach and 15% for bean. A similar trend was observed when a begonia (
4.3. Plant absorption of heavy metal
Some heavy metals such as Zn, Cu, and Ni are important for proper functioning of biological systems and deficiency or excess can lead to a number of disorders (Ward, 1995), while others such as Cd are dangerous pollutant due to their high toxicity to plants and inhibit growth at high absorption (Liu et al., 2006). The range of heavy metal concentrations absorbed in both shoot and root of the plants was in the order of Cd<Cu<Zn, respectively, in this study. The same order of the concentration range of heavy metals was observed in various vegetable crops including similar plants used in this study as spinach (
|Spinach/SSB-H||(DW) = –0.00097*(Cu) + 0.0048||0.651|
|(DW) = –0.00015*(Zn) + 0.0074||0.345|
|(DW) = –0.00443*(Cd) + 0.0066||0.719|
|Spinach/SSB-L||(DW) = –0.00076*(Cu) + 0.0052||0.281|
|(DW) = –0.00008*(Zn) + 0.0070||0.422|
|(DW) = –0.00129*(Cd) + 0.0051||0.121|
|Bean/SSB-H||(DW) = –0.00008*(Cu) + 0.0019||0.007|
|(DW) = –0.00001*(Zn) + 0.0021||0.038|
|(DW) = –0.00022*(Cd) + 0.0020||0.044|
|Bean/SSB-L||(DW) = –0.00053*(Cu) + 0.0041||0.082|
|(DW) = –0.00006*(Zn) + 0.0054||0.219|
|(DW) = 0.00151*(Cd) + 0.0010||0.537|
Overall concentrations of Cu, Zn, and Cd in the root were greater than those in the shoot of the plants probably because of root’s chelating exudates to solubilize heavy metals in the rhizosphere (Inaba & Takenaka, 2000) and rapid absorption by the root and slow translocation to shoot (Nada et al., 2007). Accumulation of heavy metals (Cu, Zn, and Cd) in spinach after exposure to 500 µ
4.4. Heavy metal leachability from biochar
The total concentrations of Cu, Zn, and Cd in SSB after the pot study did not greatly vary among the application rates within the same SSB type and plant, respectively, and 89–91%, 90–92%, and 98–99% of the original concentrations of Cu, Zn, and Cd were lost from the SSB during the pot study, respectively, regardless of the SSB type, application rate, and plant. While there are numerous studies that deal with sorption capacity of biochars for heavy metals when applied to soil in light of phytoremediation perspective (Cao et al., 2009; Namgay et al., 2010; Uchimiya et al., 2011), studies regarding on leachability (through desorption or dissolution) of heavy metals from biochar and their bioavailability are virtually nonexistent. The heavy metals, however, are known to be desorbed by naturally occurring organic acids such as citric, oxalic, acetic, and lactic acids (Nascimento, 2006; Marchi, 2009) and dissolved organic carbon (Antoniadis & Alloway, 2002) from soils amended with sewage sludge. Regardless of equilibrium amounts of Cd adsorbed in an Andisol, more than 80% of Cd was desorbed with one time extraction with citric acid if its concentration was more than 0.1
4.5. Heavy metal accumulation and availability in soil
The total concentrations of Cu and Zn in the soil after the pot study, regardless of the treatment, were greater and almost equal compared with those of the original soil (25 and 43 mg kg–1, respectively), while both concentrations significantly increased when SSB-H was applied at 75% rate for both plants. On the other hand, the overall concentrations of the total Cd were smaller after the pot study compared with that at pre-plant condition (4.9 mg kg–1); however those with the SSB-L treatment increased with increasing application rate for both plants. Transfer factors (TF) of heavy metal, as calculated as the ratio of the concentration of heavy metal absorbed in a plant to the concentration of heavy metal in soil, can quantify the relative differences in bioavailability of heavy metals to vegetables or to identify the efficiency of a vegetable species to accumulate a heavy metal (Uwah et al., 2011). The TF values in this study, calculated based on the sum of heavy metal concentrations of the shoot and root as the plant concentration and the sum of heavy metal concentrations in the soil and SSB as the soil concentration, were 0.77, 0.83, and 1.37 for spinach, and 0.69, 0.91, and 1.19 for bean for Cu, Zn, and Cd, respectively, regardless of the SSB application rate. These TF values may explain why Cu appeared to have been accumulated in the soil (TF less than 1 and lowest among the 3 metals for both plants), Zn seemed to have had no changes before and after the pot study (TF close to 1), and Cd appeared to have been accumulated more in the plant than in the soil (TF more than 1). The TF values widely vary depending on properties of soils and plants, however, those calculated in this study may be comparable with those found by Uwah et al. (2011), which were 0.25–0.95, 0.38–0.55, and 0.42–2.75 for Cu, Zn, and Cd, respectively, for spinach and lettuce grown on tropical soils in Nigeria. Further studies are needed to elucidate heavy metal accumulation in soil and selective absorption by plants with the SSB application.
The heavy metal concentrations extractable by 0.1
The environmental threshold concentrations in soils are 125 mg Cu kg–1, 125 mg Zn kg–1, and 0.01 mg Cd L–1 as 0.1
Biochars derived from feedstock including heavy metals such as SSB need to be thoroughly evaluated for heavy metal dynamics among SSBs, soils, and plants for environmentally safe and sound application of SSB. Both SSBs used in this study contained a low end of concentration ranges of Cu, Zn, and Cd, respectively, found in the literature, and the heavy metal concentrations accumulated in the SSB as the pyrolysis temperature increased as found in the literature. Both spinach and bean plants suffered from N deficiency due mainly to a lack of soil volume with excessively high application of SSB-H, and possibly from B toxicity especially from SSB-L application. However, when SSB-L was applied, the shoot DW of plants peaked with 5% application rate for spinach and 15% rate for bean. Therefore, it was concluded that the optimum application rates of SSB-H and SSB-L were indeterminate (lower application rates of SSB-H need to be evaluated) and 5–15%, respectively, for the best growth of the plants in this study. The concentration ranges of the heavy metals absorbed in both plants were in the order of Cd<Cu<Zn for both shoot and root. The total Cu and Zn in the shoot may have been in safe concentration ranges, and the total Cd may have been in excess range which may have caused inhibition of the growth. In fact, the plant DW showed inverse relationships with the total concentrations of the heavy metals absorbed in the plants, and the inhibitive effect of heavy metals on the plant growth was in the order of Zn<Cu<Cd. Overall concentrations of the heavy metals in the root were greater than those in the shoot for both plants. The leachability of Cu, Zn, and Cd from SSBs was 89–91%, 90–92%, and 98–99% of the original total concentrations, respectively, during the pot study regardless of the SSB type, application rate, and plant. However, the total concentrations of Cu, Zn, and Cd in the soil after the pot study were accumulated, unaffected, and reduced, respectively, compared with those before the pot study, which could be explained by the TF of each heavy metal which were less than 1, close to 1, and more than 1, respectively. Nevertheless, the percentage of the dilute acid-extractable Cu, Zn, and Cd to the total concentrations in the soil after the pot study was 0.3–0.8%, 9.4–11.8%, and 1.8–2.6%, respectively, which were lower than the environmental threshold concentrations in Japan. However, long-term effects of SSB application on heavy metal dynamics among SSBs, soils, and plants are needed to be evaluated for further acceptance of SSB application in agronomic benefits.
Abe Y Yamaguchi N Mizoguchi M Imoto H Miyazaki T 2004Effect of organic acid on transport of cadmium in soil, Proceedings for Annual Meeting of the Japanese Society of Irrigation Drainage and Reclamation Engineering, 116 117(in Japanese)
Alloway B. J Ayers D. C 1997 Chemical Principles for Environmental Pollution, 190 220Blackie Academic and Professional, London, UK.
Antoniadis V Alloway B. J 2002The role of dissolved organic carbon in the mobility of Cd, Ni and Zn in sewage sludge-amended soils, Environmental Pollution 117 515 521
Cao X Ma L Gao B Harris W 2009Dairy-manure derived biochar effectively sorbs lead and atrazine, Environmental Science & Technology 43 3285 3291
Chan K. Y Xu Z 2009Biochar: nutrient properties and their enhancement, In: Biochar for Environmental Management: Science and Technology, J. Lehmann & S. Joseph, 67 84Earthscan, 978-1-84407-658-1, London, UK.
Committee for Analytical Methods for Soil Environment 1997 Analytical Methods for Soil Environment, Hakuyusha, 978-4-8268-0168-3, Tokyo, Japan. (in Japanese)
Committee for Experimental Methods for Plant Nutrition 1990 Experimental Methods for Plant Nutrition, Hakuyusha, 978-4-8268-0118-8, Tokyo, Japan. (in Japanese)
Council on Soil Testing and Plant Analysis (CSTPA) 1980 Handbook on Reference Methods for Soil Testing, University of Georgia, Athens, Georgia, US.
Hospido A Moreira M. T Martín M Rigola M Feijoo G 2005Environmental evaluation of different treatment processes for sludge from urban wastewater treatments: anaerobic digestion versus thermal processes, The International Journal of Life Cycle Assessment 10 36 345
Hossain M. K Strezov V Chan K. Y Nelson P. F 2010Agronomic properties of wastewater sludge biochar and bioavailability of metals in production of cherry tomato ( Lycopersicon esculentum), Chemosphere 78 1167 1171
Hossain M. K Strezov V Chan K. Y Ziolkowski A Nelson P. F 2011Influence of pyrolysis temperature on production and nutrient properties of wastewater sludge biochar, Journal of Environmental Management 92 223 228
Inaba S Takenaka C 2000Remediation of heavy metal-contaminated soil in the rhizosphere, Root Research, 9 69 73(in Japanese)
Japan Soil Association 2010 Analytical Methods for Manure and Organic Matter, Japan Soil Association, Tokyo, Japan. (in Japanese)
Kashem M. A Singh B. R Kondo T Hug S. M. I Kawai S 2007Comparison of extractability of Cd, Cu, Pb, and Zn with sequential extraction in contaminated and non-contaminated soils, International Journal of Environmental Science and Technology 4 169 176
Kawano Y Yanai J Yamada H Nakajima K Yasui D Takebe K 2012Physico-chemical properties of carbonized sewage sludge and effects on plant growth, Japanese Journal of Soil Science and Plant Nutrition, 83 125 132(in Japanese)
Kuo S Jellum E. J Baker A. S 1985Effects of soil type, liming, and sludge application on zinc and cadmium availability to Swiss chard. Soil Science 139 122 130
Liu D. H Wang M Zou J. H Jiang W. S 2006Uptake and accumulation of cadmium and some nutrient ions by roots and shorts of maize ( Zea maysL.), Pakistan Journal of Botany 38 701 709
Marchi G Guilherme L. R. G Chang A. C Nascimento C. W. A 2009Heavy metals extractability in a soil amended with sewage sludge, Scientia Agricola 66 643 649
Méndez A Gómez A Paz-ferreiro J Gascó G 2012Effects of sewage sludge biochar on plant metal availability after application to a Mediterranean soil, Chemosphere 89 1354 1359
Ministry of the Environment Government of Japan 2011 Japan annual report on the environment, the sound material-cycle society and the biodiversity 2011, Ministry of the Environment Government of Japan, Tokyo, Japan.
Nada E Ferjani B. A Ali R Bechir B. R Imed M Makki B 2007Cadmium induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture, Acta Physiologiae Plantarum 29 57 62
Namgay T Singh B Singh B. P 2010Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize ( Zea maysL.), Soil Research 48 638 647
Nascimento C. W. A 2006Organic acids effects on desorption of heavy metals from a contaminated soil, Scientia Agricola 63 276 280
National Institute for Agro-Environmental Sciences 1977Database regarding the concentration of metal elements in plants, National Institute for Agro-Environmental Sciences, Ibaraki, Japan. (in Japanese)
Pandey N Pathak G. C Pandey D. K Pandey R 2009Heavy metals, Co, Ni, Cu, Zn and Cd, produce oxidative damage and evoke differential antioxidant responses in spinach, Brazilian Society of Plant Physiology 21 103 111
Paz-ferreiro J Gascó G Gutiérrez B Méndez A 2012Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil, Biology and Fertility of Soils 48 511 517
Schauer P. S Wright W. R Pelchat J 1980Sludge-borne heavy metal availability and uptake by vegetable crops under field conditions, Journal of Environmental Quality 9 69 73
Singh S Zacharias M Kalpana S Mishra S 2012Heavy metals accumulation and distribution pattern in different vegetable crops, Journal of Environmental Chemistry and Ecotoxicology 4 170 177
Teranuma M Mori T 2002Applications of carbonized sludge as soil improvement additives, Journal of Japan Sewage Works Association. Research Journal, 39 167 175(in Japanese)
Terashima S Imai N Ohta A Okai T Mikoshiba M 2004Geochemistry of soils from the southern Kanto district, Japan: Preliminary study for the soil geochemical mapping (Part 5: Generalization), Bulletin of the Geological Survey of Japan, 55 1 18(in Japanese)
Terashima S Imai N Tachibana Y Okai T Mikoshiba M Ohta A Kubota R 2007Chemical composition and background evaluation of soils and stream sediments from Kanto district, and marine sediments from Tokyo Bay, Bulletin of the Geological Survey of Japan, 58 69 91(in Japanese)
Uchimiya M Wartelle L. H Klasson K. T Fortier C. A Lima I. M 2011Influence of pyrolysis temperature on biochar property and function as a heavy metal sorbent in soil, Journal of Agricultural and Food Chemistry 59 2501 2510
Uwah E. I 2009Concentration levels of some heavy metal pollutants in soil, and carrot ( Daucus carota) obtained in Maiduguri, Nigeria, Continental Journal of Applied Sciences 4 76 88
Uwah E. I Ndahi N. P Abdulrahman F. I Ogugbuaja V. O 2011Heavy metal levels in spinach ( Amaranthus candatus) and lettuce ( Lactuca sative) grown in Maiduguri, Nigeria, Journal of Environmental Chemistry and Ecotoxicology 3 264 271
Ward N. I 1995Environmental analytical chemistry, In: Trace Elements, F.W. Fifield & P.J. Haines, 320 328Blackie Academic and Professional, London, UK.
Xue Q Harrison H. C 1991Effect of soil zinc, pH, and cultivar on cadmium uptake in leaf lettuce ( Lactuca sativaL. var. crispa), Communications in Soil Science and Plant Analysis 22 975 991
Zhou L. X Wong J. W. C 2001Effect of dissolved organic matter from sludge and sludge compost on soil copper sorption, Journal of Environmental Quality 30 878 883