Soil properties
Previous studies confirmed that the application of CMR (Ma et al., 2019), SS (Eid et al., 2019b; Lin et al., 2018), and CM (Watanabe et al., 2019) significantly increased SOM, which was consistent with the current study. Increased SOM is an important index of soil fertility. SS was the most effective in increasing SOM, followed by CM, and then CMR, although the organic matter carried by CMR was highest. This might be attributed to that SS might have led to the formation of the most stable soil aggregate that prevents SOM from decomposition.
Soil pH values showed a slight reduction after OA application in the present experiment. The decreased pH values also occurred in the soils improved by biosolids (Zuo et al., 2019a), traditional Chinese medicine residues (Ma et al., 2019), and municipal solid waste compost with 50% recommended doses of fertilizer (Meena et al., 2016). The decreased pH after OA application might be attributed to the humic acid resulting from the degradation of OAs (Moreno, Garcia et al. 1997), the oxidation of N and S compounds (Logan, Lindsay et al. 1997) and the neutralization of relatively low pH OAs, particularly at high application rates (Bai, Zuo et al. 2017).
Soil salinity decreased after OA application, which was also reported by Zuo et al. (2019a). OA application can improve the soil structure by binding mineral particles to organic polymers (Leogrande and Vitti 2019), which contributes to reduced bulk density and increased porosity, water holding capacity (Shi, Zhao et al. 2016) and hydraulic conductivity. The improvement of soil structure makes the water infiltration faster, bolstering salt leaching (Grigg, Sheridan et al. 2006). As a result, soil salinity decreases. SS was most effective in lowering soil salinity probably because SS-amended soils had the highest SOM, which promotes soil aggregate formation. There was a negative correlation between organic matter and salinity (SS: r=-0,922, MR: r=-.873, CM: r=-0.614, P<0.01). Unlike saline mudflat soil, OA application generally increased soil salinity in nonsaline soils due to the high salinity of OAs. For example, Eid et al. (2019b) reported that the salinity of original soils (EC: 0.06 mS cm-1) significantly increased after applying SS (EC: 2.07 mS cm-1) at rates of 0 to 50 g kg-1.
Maize growth
OA application significantly increased the maize yield. OAs have been found to increase the yield of maize (Zhang et al., 2012) and rice (Chen et al., 2017) . The improved soil quality, such as increased SOM and other nutrients (data not shown), and decreased salinity and pH may contribute to the increased crop yield. In addition, OAs had a positive impact on soil microbial activities and nutrient supply, which was beneficial for crop growth (Yadav et al., 2000). In the current experiment, the biomass of maize increased with the increasing CMR application. Though CMR application introduced massive HMs into mudflats, it did not decrease the growth of maize, which is consistent with the findings of previous studies (Ma et al., 2019). Jin et al. (2018) found that the application of CMR significantly increased the yield of Pleurotus ostreatus and nutrients in growing substrates. As SS application increased SOM the most, it might have led to the greatest increase in the maize yield. The absence of further increases in maize biomass at higher application rates suggested that the massive HMs caused by SS application may have inhibited the maize growth, which was previously reported by Watanabe et al. (2019).
Heavy metals in the soil
OA application was considered an additional source for soil HMs (Chaney, 2012). In SS-amended soils, soil total HM contents (Zn, Cu, and Cd) increased with the increasing SS application rates, but soil Mn and Ni contents were unchanged because their concentration differences between SS and mudflat soil were small (Table 1), which was also demonstrated by Bai et al. (2017b). Liang et al. (2010) found that SS application significantly increased Mn and Cu contents in soils and Zn contents in crops. In CMR-amended soils, soil total metal contents (Mn, Zn, and Cd) increased with increasing CMR application, except Cu and Ni. Previous studies have found that CMR application significantly increased soil total heavy metals (Cr, Cd, Pb, As, and Hg) (Ma et al., 2019). The Zn and Cd contents increased significantly after CM application. Soil total HM contents in amended soils complied with the limitations of the Chinese soil risk control standard (GB15618-2018), except soil total Zn above 150 t ha-1 SS application rates. The Zn contents in SS-amended soils were much higher than those in CMR- and CM-amended soils at the same application rates, which may have resulted from the excessive Zn in SS (Table 1). The HM contents of CMR and CM-amended soils were similar in the current study due to the similar HM contents in CMR and CM. In general, the highest level of HMs in SS led to the highest HM contents in the amended soil.
The risk of HM contamination depends on not only the total soil HM concentration but also the bioavailable HM concentrations (Liu & Sun, 2013). The bioavailability of HMs was in the order of SS> CMR>CM, except for Mn (SS>CM>CMR), indicating that SS is the most effective in increasing HM bioavailability. The order of the average BRs of HMs was Cd>Mn>Cu>Zn>Ni in CMR- and CM-amended soils, while in SS-amended soils, the average BRs of HMs followed the order of Cd> Zn > Cu > Mn>Ni , suggesting that bioavailable fractions of Cd, Mn, Cu, Zn are high and therefore might lead to more plant bioconcentration. Mobile Cd was found to account for approximately 40~50% of Cd forms, contributing to the highest average BR values among all HMs (Ramos et al., 1994). For example, 37% and 45% of the total Cd was leached with 0.1 M of NaCl from two soil columns (Norrström, 2005). The responses of the BRs of HMs to OA application rates varied with the kind of OAs. The bioavailability of HMs (Zn, Cu, Cd, Mn, and Ni) increased significantly with the increasing SS application in the present study, consistent with the results of a previous study (Kidd et al., 2007). CMR application increased the bioavailability of Ni and decreased the bioavailability of Mn and Cd, and only the bioavailability of Zn increased with the CM application rates.
The bioavailability of HMs is associated with some chemical processes, such as sorption/desorption and precipitation/dissolution (Skrbic & Durisic-Mladenovic, 2010), which are regulated by environmental factors such as pH, SOM, and salinity (Du Laing et al., 2002).
The bioavailability of HMs was positively related to SOM, except for Ni and Mn in this study (Table 4 Figure 5 A). Bai et al. (2017a) reported that the bioavailability ratio of HMs showed a positive correlation between SOM after SS application in mudflats, except for Zn. Increased organic acid resulting from the decomposition of SOM can enhance the bioavailability of HMs (Ma et al., 2020; Zuo et al., 2019b). SOM, acting as a chelate, can form soluble complexation with HMs, thus enhancing the bioavailability of HMs (Vega et al., 2004). For example, OA application increased dissolved soil organic matter, which complexed with soil Cd, promoting the mobilization of Cd at alkaline pH by forming water-soluble Cd contents (Fang et al., 2018). The degree of correlation between the bioavailability of HMs and SOM is higher for SS than for CMR and CM, which may be attributed to the fact that the binding capacity for heavy metals varies with organic acid molar weight and functional group (Ma et al., 2020).
The chemical forms of heavy metal were strongly impacted by salinity. Soil salinity increased the bioavailability of soil HM (Wang & Song, 2019). The effects of salinity on HM bioavailability are regulated by two main opposite processes: (1) the competition between salt-derived cations and positively charged heavy metals over sorption sites on the solid phase and (2) the complexation capacity of salt-derived anions with heavy metals (Zhou et al., 2019). Mujeeb et al. (2020) reported that soil salinity increased the bioavailability of Cu, Mn, Zn, and Pb. However, the bioavailability of HMs mostly decreased with the increasing soil salinity. The negative correlation between soil salinity and HM availability may be attributed to the fact that salinity was negatively related to SOM and that the effect of salinity was masked by that of SOM (Fig. 5). In addition, previous studies mainly focused on the influence of single salts, such as NaCl (Wang & Song, 2019), ignoring the effects of other salts or the specific mixing ratio of salts. Nevertheless, salt types and concentrations in real soils are extremely complex, and the effect of salinity varied with the kind of salt. For example, due to the low stability of Cu-chloride complexes, NaCl had no significant impact on Cu mobility (Du Laing et al., 2008),
Correlations between pH and the bioavailability of HMs vary with OAs and HM species. The effect of pH on the bioavailability of HMs was most significant in CMR, followed by SS and then CM treatments. The BRs of HMs had positive correlation with pH when all OA treatments were combined, except Ni and Mn. In general, the bioavailability of HMs increased with the decreasing pH because lower pH values enhance the transformation from the immobile form to the bioavailable form (Yu et al., 2016), for example, through decreased adsorption of dissolved ions of HMs by a negative surface with decreasing pH (Sungur et al., 2014).
The accumulation and bioconcentration of heavy metals in maize
The HM contents in maize straw, grain, and leaf were mostly amplified with increasing OA application, which was consistent with the results of previous studies (Bose & Bhattacharyya, 2008; Eid et al., 2019b; Taghipour & Jalali, 2019) that had demonstrated that OA application increased the uptake of HMs in wheat (Eid et al., 2019a), spinach (Eid et al., 2017), and sugarcane (Nogueira et al., 2013). The HM concentrations in aboveground parts of maize were lower than the threshold of the national standards for food safety, although Cd contents in the grain and leaf of maize surpassed the threshold (GB2762-1017) at the 150 and 300 t ha-1 SS application rate. Thus, except for the SS application rate of 150 and 300 t ha-1, mudflat soil amendment by SS, CMR, and CM may be practical and safe. In addition, the HM contents in maize grown in SS-amended soil is the highest due to the highest HM contents is SS.
The responses of BCFs of HMs to OA application varied with the OA types (Fig.4). The BCFs of Zn in SS-amended soils were also much higher than those of other OA treatments, which may be attributed to the high bioavailability of Zn in SS-amended soil. The bioconcentration of HM in maize generally followed the order SS>CMR>CM, which is consistent with the order of bioavailability of HM. The impact of OA on BCFs of HMs varied with HM and tissue types. The BCFs of Cu and Ni in aboveground tissues were not affected by SS amendment, while the BCFs of Cd, Mn, and Zn increased with the increasing SS application rates. Eid et al. (2019b) reported that the BCFs of Cu and Mn in root decreased with the increasing SS application, while the BCFs of Ni and Zn in root increased after SS application. Kidd et al. (2007) reported that the bioaccumulation factors for Mn and Zn decreased after SS application. In general, the bioconcentration of Cd and Zn by maize was highest, followed by Cu, Mn, and Ni,, which was consistent with the results of many studies of wheat straw (Ul Hassan et al., 2017), and wheat grain (Chen et al., 2018), indicating that Zn and Cd are preferably absorbed by plants, so the potential risk of Zn and Cd accumulation in plants is high.
The main aboveground reservoirs of HM varied with the type of HMs (Bai et al., 2017b). For example, the BCFs of Cu and Zn in the straw were higher than those of other HMs, suggesting that Cu and Zn accumulate more easily in the straw. The bioconcentration and transfer of HM in plants vary with plant tissues (Taghipour & Jalali, 2019; Zhang et al., 2018). The BCFs of HMs (Mn, Cu, and Ni, ) in the straw, grain and leaf were lower than 1 in all treatments, which implied the limited accumulation ability of these HMs in aboveground parts of maize (Yoon et al., 2006). Orman et al. (2014) showed that the BCFs of HMs (Mn, Cu, Ni, and Zn) in shoot and root of Alfalfa were lower than 1 after SS application (0-80 t ha-1). However, the BCFs of Cd in the grain and leaf in SS-amended soils at the 300 t ha-1 application rate were higher than 1, suggesting that the grain and leaf absorb Cd more easily, which poses a great risk for grain consumption or straw return to field. Compared to other HMs, Cd easily transfers from soils to grain, and Cd, Cu, and Mn easily accumulate in leaf. However, Li et al. (2012) demonstrated that the BCF of straw (49.5%) for Cd was higher than the BCF of grain (3.6%) in maize, which implied that there was more Cd accumulation in straw than in grain. Carbonell et al. (2011) reported that the grain of maize accumulated the least Ni and Cd. This discrepancy may be attributed to the different physicochemical properties of soil and OAs from the current study.
The HM contents in the maize tissues showed a significantly positive correlation with soil bioavailable HM contents, which is consistent with the results of previous studies (Bai et al., 2013; Bai et al., 2017b) (Table 5). The soil bioavailable HM contents could accurately predict HM uptake by plants (Wan et al., 2020)Generally, SS is associated with stronger correlation than CMR and CM, and Zn and Ni showed better correlation than other HMs. The differences may be attributed to the various accumulation potentials of tissues for different HM species. In addition to soil properties, such as pH, SOM, and salinity, the interactions of multiple HMs in soils, such as coexistence and antagonistic or synergistic actions, may multiply, suppressing the effect of single heavy metals on soils or crops (Puschenreiter et al., 2005). For example, the increase in bioavailable Cd may lead to a decrease in the bioconcentration of Zn under saline conditions (Taghipour & Jalali, 2019).