Introduction

The soil ecosystem, which is contaminated with heavy metal(loid)s, is considered to be a global environmental issue. Heavy metal(loid)s have both natural (ore deposit or weathering/erosion of parent rocks) and manmade sources (mining, electroplating, energy, smelting power transmission, fuel production, sludge dumping, intensive agriculture, waste water irrigation, and dust) (Khan et al. 2015; Nawab et al. 2015a; Chanpiwat et al. 2010; Wei and Yang 2010). Mining-impacted soils are classified as poorly structured soils and lack vegetative cover due to the high toxicity associated with heavy metal(loid)s (Nawab et al. 2015b; Mench et al. 2010). In previous research, organic amendments have been used to either immobilize or mobilize heavy metal(loid)s in contaminated soils (Khan et al. 2015; Ahmad et al. 2012). In the mobilization technique, the metal(loid)s are released into the soil and are subsequently removed through the native plant species. For the immobilization technique, the metal(loid)s are rendered unavailable for plant uptake, human ingestion, and leaching into groundwater from the soil through adsorption, the formation of complex compounds, and precipitation reactions (Bolan et al. 2003). Activated carbon (AC) is generally prepared by heating carbonaceous material at a high temperature (above 600 °C) for a long period of time (>10 h) to make it extremely porous, resulting in a very high adsorptive capacity (Tomaszewski et al. 2007). Several organic materials are used to increase immobilization of heavy metal(loid)s, but AC is extremely efficient (Ucer et al. 2006; Lima and Marshal 2005).

Previously, Lyubchik et al. (2008) reported that AC was very effective in the removal of heavy metal(loid)s (50–55 %) by the precipitation of metal hydroxide and the adsorption of metal cation (15–20 %) on the negatively charged surfaces of AC. While AC is commonly used for the removal of heavy metal(loid)s from wastewater, its effects on metal immobilization in contaminated soil is rarely studied and still needs further research.

Activated carbon is a proficient and environmentally friendly material used for the removal of heavy metal(loid)s, particularly from industrial effluent (de Lima et al. 2014). AC, liquid organic fertilizers, and attapulgite clay amendments immobilize diethylene triamine pentaacetic acid (DPTA) extractable metals in soil that also affect the plant growth (Liu et al. 2012). AC has a high adsorption capacity for heavy metal(loid)s and can therefore remove more than 90 % of metal(loid)s such as Cu, Co, Cr, Mn, and Fe from landfill leachate compared with the control (Modin et al. 2011). The concentrations of organic pollutants can also be reduced by the addition of a small amount of AC into the contaminated environmental matrices (Brandli et al. 2008; Zimmerman et al. 2004). AC has a high sorption capacity due to its unique chemical composition, high porosity, and large surface area. The strong sorption capacity of AC has been shown to reduce contaminant accessibility to microorganisms (Rhodes et al. 2008). AC, both in powder (ACP) and granulated (ACG) forms, affects the growth of plants and reduces the availability of organic contaminants such as polycyclic aromatic hydrocarbons (Jakob et al. 2012). AC act as a promoter of embryogenesis in the microscopic culture of various pepper genotypes at 0.05 % concentration, while the low responsive genotype showed the most significant effect (Cheng et al. 2013).

Published literature has shown that organic amendment techniques reduced heavy metal(loid)s such as Cd, As, Pb, Cu, Zn, and Cr in the soil (Bolan et al. 2014). The farmyard manure (FYM) amendment is known to convert Cr (VI) to Cr (III), which is less toxic and mobile (Bolan et al. 2003). Most manure byproducts have comparatively low concentrations of toxic metal(loid)s and can therefore be used to immobilize these metal(loid)s in contaminated soils. Several other organic amendments such as composts, bio-solids, or bio-solid compost have effectively reduced the concentrations of heavy metal(loid)s in amended soils (Ahmad et al. 2014). Gupta et al. (2008) investigated the efficiency of 2 % FYM application and observed that the bioaccumulated concentrations of Ni decreased by 39, 40, 45, and 35 % in carrot, fenugreek, spinach, and wheat grain, respectively.

The aim of this work is to investigate the influence of ACP, ACG, and FYM amendments on the availability of heavy metal(loid)s in mine-impacted soil and their bioaccumulation in plants. Two types of fodder plant species (Penisitum americanum and Sorghum bicolor) were cultivated in mine-impacted soil amended with the selected organic materials. This was performed at different application rates for the purpose of studying the impact of these amendments on the phytoremediation of heavy metal(loid)s, such as As, Cd, Cr, Cu, Ni, Zn, Pb, Co, Mn, Al, and Fe. The effect of amendments on plant growth was also investigated.

Ethics statement

The collection of soil samples from mine sites is not a restricted activity. Therefore, no permission from any organization was required to collect soil for these control experiments. Moreover, no endangered or protected species were involved in this study. The cultivation of the selected plant seedlings did not require any permission.

Materials and methods

Chemical materials

Three types of organic materials, ACP, ACG, and FYM, were used for control experiments. The ACP and ACG were purchased from Norit Nederland BV Amersfoort. The particle size of ACP ranged from 1 to 150 μm, while ACG ranged from 1 to 3 mm. Locally produced FYM (cow manure) was used in this research. Certified seeds of fodder plant species P. americanum and S. bicolor were purchased from The Agriculture Research Center, Takhtaband Swat, Pakistan. All chemicals used were analytical grade and purchased from Merck (Merck KGaA, 64271 Darmstadt, Germany).

Soil sampling and preparation

Heavy metal(loid) contaminated soil (120 kg) was collected from 0–20 cm depth of mining-impacted sites in Khyber Pukhtunkhwa, Pakistan. The collection of soil samples from mine sites is not a restricted activity. Therefore, no permission from any organization was required to collect soil for these control experiments. First, the soil was air dried, sieved (2 mm), and homogenized into a single composite sample. The sub-sample was then stored in a paper envelope at 20 °C. The physico-chemical properties of the soil, including pH, texture, and electrical conductivity (EC), were determined (Table 1) using standard procedures (Waqas et al. 2014). The soil particle size distribution was sand (66 %), silt (16 %), and clay (18 %).

Table 1 Basic characteristics of ACP, ACG, FYM, and soil used in this study compared with the permissible limits set by SEPA (1995)
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Experimental design

The selected organic materials (ACP, ACG, and FYM) were homogenously mixed (at 2 and 5 % application rates) with the chromate mine-impacted soil on a dry weight (dw) basis. The samples were then defined as ACP2, ACP5, ACG2, ACG5, FYM2, and FYM5. All the amended (with organic materials) and control treatments (without organic materials) were prepared in triplicate. The fertilizers, such as NH4NO3 (120 mg N/kg soil) and K2HPO4 (30 mg P/kg soil and 75.7 mg K/kg soil), were thoroughly mixed with all the treatments (Khan et al. 2013). Each plastic pot was filled with 2.5 kg of sample and irrigated with deionized water. Two sets of each treatment were prepared: one set was cultivated with P. americanum and the other with S. bicolor (ten seeds in each pot). These were not endangered or protected species and their cultivation did not require any permission. These experiments were conducted in a greenhouse for 3 months, and the pots were regularly irrigated with deionized water to keep the water content at 60 %. Upon maturity, the P. americanum and S. bicolor plants were harvested and dried in an oven at 70 °C for 72 h. Dry weights of the roots and shoots were recorded.

Chemical analyses

A strong acid extraction method was used to determine total heavy metal(loid) concentrations for all treatments (amended and control soils). Oven-dried samples (1.0 g) of each material were digested in a Teflon beaker with a mixture of strong acids HNO3/HClO4 (3:1, v/v) at 70–80 °C. The solution was allowed to evaporate by raising the temperature to 105 °C until the solution became transparent. After filtration, the final volume of extract was made up to 50 ml with 0.1 N HNO3. Heavy metal(loid) concentrations in the powder fodder plants were investigated according to the method adopted by Ryan et al. (2001). Concentrated HNO3 was used to digest 1.0 g of each plant sample. After filtration, deionized water was used to make the final volume up to 50 ml. To investigate the bioavailable heavy metal(loid)s in ACP, ACG, FYM, the soil, and their amendments (ACP/ACG/FYM), a mixture of reagents comprising EDTA-Na2 (0.05 M), CaCl2 (0.01 M), and tri-ethanolamine (0.1 M) was used according to the method adopted by Zeng et al. (2011). The concentrations of Al and Fe were determined using ICP-OES (Perkin Elmer Optima 7000 DV, USA), while As, Cr, Cd, Pb, Ni, Mn, Cu, Zn, and Co concentrations were measured using ICP-MS (Agilent Technologies, 7500 CX, USA) at the Institute of Urban Environment, Xiamen, China.

Quality control

To check for contamination in the digestion and analysis processes, reagent blanks were included in each batch. The standard reference materials of plant (GBW-07602 (GSV-1)) that belonged to shrub and soil (GBW-07406 (GSS-6)) were purchased from the National Research Center for Standards in China and were included for recovery efficiency from the digestion process. The recovery rates of selected metal(loid)s were observed in the range of 91.5 ± 8.4 % to 103 ± 6.5 %.

Data analysis

For data analysis, the statistical package SPSS (version 21; IBM Corporation, USA) was used. The mean, standard deviation, and variance of the triplicates were determined using ANOVA.

Results and discussion

Characteristics of soil and organic materials

The basic properties of the organic materials (ACP, ACG, and FYM) and mine-impacted soil used in this research are given in Table 1. These selected organic amendments show differences in soil physical properties, such as pH and EC. The highest soil pH (at 8.1) was observed for ACP5, followed by ACP2 (at 7.8). The lowest pH (at 7.3) was observed for FYM2. Compared with the control, almost all the amendments resulted in an increase in soil pH. The concentrations of each heavy metal(loid) in the mine-impacted soil, ACP, ACG, and FYM are given in Table 1.

The initial pH of the mine-impacted soil was 7.1, while the corresponding EC value was 352 μS/cm (Table 1). The total metal concentrations of Cd (1.2 mg/kg), Ni (345 mg/kg), and Cr (654 mg/kg) in the soil were higher than the respective maximum guidance limits set by the State Environmental Protection Administration, China (SEPA 1995). However, the total concentrations of Pb, As, Zn, and Cu were found to be within their maximum guidance limits set by SEPA (1995).

Effects of organic amendments on soil heavy metal(loid)s

The total and bioavailable concentrations of heavy metal(loid)s in the amended soil (compared to the control) for all the organic amendments (ACP2, ACP5, ACG2, ACG5, FYM2, and FYM5) decreased (Table 2). The decrease in bioavailable concentrations of the respective metal(loid)s in ACP (2 and 5 %) amendments were observed (Table 2). These findings indicate that ACP amendments caused the lowest reduction in the availability of As followed by Cd, which could be linked with highly mobile properties of these elements (Dobran and Zagury 2006). In the ACP-amended soil, the highest reduction was observed in the available concentration of Co followed by Zn. Similarly, the concentrations of metal(loid)s in the ACG-amended soils (2 and 5 %) decreased as shown in Table 2. The treatments of ACG also showed the lowest influence on the immobilization of As and Cd in the amended soil. However, the effectiveness of ACP was comparatively greater than ACG. In FYM (2 and 5 %) amendments, the decrease in available metal(loid) concentrations were Cd (−1.42 and −4 %), Zn (−15 and −11 %), Cu (−11 and −20 %), Cr (−2 and −8 %), Ni (−8 and −13 %), Mn (−12 and −15 %), Fe (−7 and −12 %), Co (−1.2 and −3 %), Pb (−8 and −15 %), As (0 and −4 %), and Al (−18 and −24 %) (Table 2). The detailed information is given in the Supporting Information (Table S2) document.

Table 2 The characteristics of control and ACP-, ACG-, and FYM-amended soils (n = 3)
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Based on these results, ACP (2 and 5 %) was more efficient in reducing the available concentrations of heavy metal(loid)s. The decrease observed in ACP-amended soil was significantly (P ≤ 0.01) higher compared to ACG2, ACG5, FYM2, FYM5, and the control treatments. ACP had a comparatively smaller particle size (1–150 μm) than ACG (1–3 mm), as shown in Table 1. Water retention showed a strong relationship with capillary forces in the soil and provided metal solubility to the plants (Jakob et al. 2012). The ACP-amended soil capillary force was higher than the control, FYM-amended, and ACG-amended soil, thereby showing lower water availability and fewer pore spaces (Jakob et al. 2012). Soil pH plays a very important role in metal availability in soil and their bioaccumulation in plants. At soil pH greater than 6, the concentrations of free metal ions in solution decrease due to organic matter chelation, oxide surface charge enhancement, and metal hydroxide precipitation (Khan et al. 2015; Mouta et al. 2008). Precipitation processes occur between metals and anions such as OH−, SO4 2−, HPO4 2−, and CO3 2−. This process is considered to be one of the most important mechanisms for reducing the mobility of toxic metal(loid)s in soil amended with organic materials such as AC, FYM, and biochar (Ok et al. 2010). At higher pH values, different functional groups such as carbonyl, phenolic, carboxyl, and alcohol isolate organic materials were used for soil amendment. This, in turn, increases the affinity between the functional groups and metal ions (Khan et al. 2015; Ahmad et al. 2014; McGowen et al. 2001). The high concentration of P in organic matter such as FYM also reduces metal mobility through the precipitation. In previous studies, P showed a reduction in the leaching of toxic metals such as Cd, Pb, and Zn (Bolan et al. 2014). In acidic soil, the addition of organic materials, such as composts and manures, increases the soil pH, which reduces the metal availability in the soil (Walker et al. 2004). In this research, the soil pH decreased from 2.9 to 14.1 % in the organic amended soils. Compared with the control, the highest effect was observed in the ACP5 treatment followed by the ACP2 (Table 1). FYM also reduced soil pH (by 0.2–0.4) and showed effectiveness in metal availability. However, Davis and Wilson (2005) suggested that aged manure should be used for soil remediation purposes because fresh manure contains high ammonia contents, which can harm the plants. The changes in other basic properties, such as dissolved organic carbon (DOC) and EC, can also affect the availability of metals in the amended soil (Khan et al. 2013; Violante et al. 2010).

Walker et al. (2004) and Castaldi et al. (2005) have observed a decrease in heavy metal(loid) concentrations in plant shoots grown in amended soil compared with the control. Different organic composts such as biosolid, municipal solid waste, and manure have been used by various scientists for heavy metal (loid) adsorption in contaminated soils (Clemente et al. 2007; Cala et al. 2005; Rate et al. 2004; Walker et al. 2004; Cao and Ma 2004; Cao et al. 2003). In the majority of the experiments, the amendments decreased the heavy metal(loid) uptake by plants.

Effect of the organic amendments on plant biomass

The biomass of P. americanum was reduced significantly (P < 0.01) in ACP- and ACG-amended soils compared with the control (Fig. 1). ACP treatments showed a decrease from 69 to 75 %, while ACG decreased from 16 to 19 %. Inconsistently, the biomass of the plant was increased with the amendment of FYM compared with the control. The FYM treatments increased the biomass of P. americanum from 10 to 20 % compared with the control (Fig. 1). Similarly, the S. bicolor biomass decreased with the amendments of ACP (27–64 %) and ACG (4–24 %), while it increased with FYM treatments (11–26 %) compared with the control (for details see S1). These results show that the addition of FYM increases plant biomass. This increase may be due to the availability of nutrients (predominantly nitrogen) produced by the decay of FYM (Clemente et al. 2007; Nwachukwu and Pulford 2009). Higher amendments of FYM produced a higher biomass, which may be due to the release of additional nutrients, an improved buffering capacity, and enhanced nutrient cycling upon decomposition of farm manure (Clemente et al. 2007; Stewart et al. 2000; Liu et al. 2009).

Fig. 1
figure 1

The effects of ACP, ACG, and FYM amendments (2 and 5 %) on P. americanum and S. bicolor biomass yields. Error bars represent standard deviation. Similar letters indicate no significant difference (P ≤ 0.01), while different letters indicate significant differences compared with the control experiment

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The plant biomass and growth are mostly dependent on the soil’s physical and chemical parameters and, especially, the availability of water, nutrients, and oxygen. The ACG-amended soil may have aerobic conditions due to its coarse structure (1–3 mm size of particle), while the ACP may have less aerobic condition due to its compact structure (1–150 μm) (Glaser et al. 2002). Thus, ACP amendment compacted the soil and reduced aeration. These conditions affect aerobic bacteria and root penetration in the amended soil (Jakob et al. 2012). The improved plant biomass in ACG amendments can be attributed to an improvement in soil aeration and structure compared with ACP. Organic amendment usually improves the fertility of soil and enhances plant growth and biomass (Khan et al. 2015; Walker et al. 2004; Williamson and Johnson 1981). Heavy metal(loid)s are reduced in organic amendment soils by converting available fractions into those linked with organic matter, carbonates, and metal oxides (Walker et al. 2004). In the present research, FYM5 amendments significantly (P < 0.01) improved the selected plant biomasses compared with the control. These significant increases in biomass can be linked with higher concentrations of nutrients (mainly nitrogen) and the improvement in the buffering capacity of the soil amended with FYM5 materials (Clemente et al. 2007; Stewart et al. 2000; Liu et al. 2009; Nwachukwu and Pulford 2009).

Heavy metal(loid) bioaccumulation in plants

The bioaccumulation of metal(loid)s in the plant shoots was determined (Fig. 2). The ACP, ACG, and FYM amendments significantly reduced the bioaccumulation of metal(loid)s in P. americanum and S. bicolor. The effects of organic amendments on the bioaccumulation of heavy metal(loid)s in selected plants varied greatly. The concentrations of all the selected heavy metal(loid)s (except Zn and Cd with FYM5, FYM2) were reduced in the shoots of P. americanum grown in the amended soils compared with the control. Similar trends in reduction of metal bioaccumulation were also observed in S. bicolor shoots grown in ACP-, ACG-, and FYM-amended soils (Fig. 3).

Fig. 2
figure 2

Bioaccumulation of heavy metal(loid)s in P. americanum cultivated in soil amended with ACP, ACG, and FYM (2 and 5 %). Error bars represent standard deviation. Similar letters indicate no significant difference (P ≤ 0.01), while different letters indicate significant differences compared with the control experiment

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Fig. 3
figure 3

Bioaccumulation of heavy metal(loid)s in S. bicolor cultivated in soil amended with ACP, ACG, and FYM (2 and 5 %). Error bars represent standard deviation. Similar letters indicate no significant difference (P ≤ 0.01), while different letters indicate significant differences compared with the control experiments

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For P. americanum, the highest average decrease was observed in bioaccumulation of Ni (from 38 to 69 %), followed by As (from 38 to 49 %) in ACP-amended soil. For ACG2 and ACG5 applications, the highest average decrease was observed for Ni (from 30 to 43 %), followed by Cr (from 27 to 41 %), as shown in Fig. 2. For FYM2 and FYM5 applications, the highest decrease was observed in bioaccumulation of Ni (from 19 to 38 %), followed by Cr (from 24 to 37 %), while the concentrations of Cd and Zn increased (from 5 to 18 % and from 21 to 35 %, respectively) within soil amended with FYM (for detail see S3).

For S. bicolor, the highest average decrease was observed in the bioaccumulation of As (from 48 to 73 %), followed by Ni (from 46 to 64 %) in ACP treatments; in ACG2 and ACG5 treatments, the highest average decrease was observed for Ni (from 40 to 49 %), followed by Cu (from 36 to 50 %). For FYM2 and FYM5 applications, the highest average decrease was observed for Ni (from 28 to 48 %), followed by Cu (from 29 to 40 %), while the Cd and Zn concentrations increased from 3 to 8 %, and from 26 to 44 %, respectively, as presented in Fig. 3 (for detail see S4).

The aforementioned results indicate that all the amendments (ACP, ACG, and FYM) reduced the heavy metal(loid) (Ni, Pb, As, Co, Fe, Cu, Cr, Al, and Mn) bioaccumulation in the shoots of P. americanum and S. bicolor. FYM increases both Zn and Cd absorption/mobilization with the passage of time in plants particularly at high doses (Gondek 2010). The concentrations of Cd and Zn were slightly increased due to FYM amendments, which could be attributed to their high inherent concentrations in FYM compared with ACP and ACG (Table 1). In the shoots of P. americanum and S. bicolor, significant decreases were observed in heavy metal(loid) bioaccumulation for the ACP2, ACP5, ACG2, and ACG5 treatments. In all samples, the concentrations of heavy metal(loid)s were reduced in plants grown in amended soils compared with the control. However, the difference in heavy metal(loid) reduction was not significant between the treatments of the same type of AC. ACP was more effective in metal reduction than ACG (2 and 5 %). In plant shoots, the effectiveness of ACG in decreasing heavy metal(loid)s was due to the effect of growth dilution (Allard et al. 2005). In ACG-amended pots, the growth of plants was better than in the ACP treatments, which led to higher biomass production. ACP treatments were highly efficient in reducing metal bioaccumulation in plants compared with other amendments (such as ACG, FYM) and the control because of reduced concentrations of bioavailable metals in these treatments (Table 2) and soil aeration. The changes in soil pH, EC, and other basic properties could be the reason for the reduced bioaccumulation of heavy metal(loid)s in the shoots of plants grown in amended soils (Chamon et al. 2005; Gao and Collins 2009).

Organic matter decomposition limits metal mobility and releases carbonates, phosphates, and other salts, which leads to the formation of insoluble metal complexes (Walker et al. 2003; Kabata and Pendias 2001). FYM or other organic amendments enhance soil organic matter, which increases the metal’s binding capacity and reduces their mobility in the soil (Liu et al. 2007). The addition of organic amendments offers several specific and non-specific metal binding sites where desorption is not easy (Shuman 1999). The organic amendments in soil may reduce the bioavailability of heavy metal(loid)s by converting available fractions into non-available fractions, or fractions in combination with carbonates, organic matter, and metal oxides (Walker et al. 2004). This research suggests that, through the adsorption reaction of organic amendments, metals are immobilized. This result could be due to the enhancement of surface charge (Clark et al. 2007) and the availability of metal binding compounds (Gondar and Bernal 2009; Waqas et al. 2015).

Conclusion

The results of this study indicated that almost all organic amendments (ACP2, ACP5, ACG2, ACG5, FYM2, and FYM5) significantly reduced the availability of heavy metal(loid) concentrations in soil and their bioaccumulation in P. americanum and S. bicolor. The biomasses of these plants significantly (P ≤ 0.01) decreased with the application of ACP2, ACP5, ACG2, and ACG5, while the biomasses increased with application of FYM2 and FYM5. The heavy metal(loid) concentrations in P. americanum and S. bicolor shoots significantly (P ≤ 0.01) decreased (except Cd and Zn) for all amendments. The addition of ACP significantly (P ≤ 0.01) reduced the heavy metal(loid) concentrations in P. americanum and S. bicolor but negatively affected the plant growth in ACP-amended mine-impacted soil. ACG and FYM amendments were slightly less effective in reducing bioavailability of heavy metal(loid) concentrations in soil and their bioaccumulation in plants compared with ACP. Furthermore, long-term field research is needed to generalize these results to a broader variety of mine-impacted soil and plants.