Evaluation of nickel toxicity and potential health implications of agriculturally diversely irrigated wheat crop varieties

2.8.1 Bioaccumulation factor (BAF)

The nickel BAF was determined as the following formula (Li et al., 2007). $$\mathrm{B}\mathrm{A}\mathrm{F}={[\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l}]}_{\mathrm{S}\mathrm{h}\mathrm{o}\mathrm{o}\mathrm{t}}/{[\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l}]}_{\mathrm{S}\mathrm{o}\mathrm{i}\mathrm{l}}$$

2.8.2 Translocation factor (TF)

The TF, which is the ability of a plant to transport stored minerals from one part to another, was calculated with the following formula in this study (Cui et al., 2007). $$\mathrm{T}\mathrm{F}={[\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l}]}_{\mathrm{S}\mathrm{h}\mathrm{o}\mathrm{o}\mathrm{t}}/{[\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l}]}_{\mathrm{R}\mathrm{o}\mathrm{o}\mathrm{t}}$$

2.8.3 Bioconcentration factor (BCF)

The BCF represents the link between trace metal concentrations in soil and the amount of heavy metals safe to eat in a portion of cereal crops. In this study, BCF was evaluated using the following formula (Cui et al., 2004). BCF = Nickel in grains / Nickel in soil

2.8.4 Enrichment factor (EF)

The EF is related to the effect of anthropogenic activity on the heavy metal content of the soil. The EF was analyzed using the following formula (Buat-Menard and Chesselet, 1979). $$\mathrm{E}\mathrm{F}={\mathrm{C}}_{\mathrm{g}\mathrm{r}\mathrm{a}\mathrm{i}\mathrm{n}}\times {\mathrm{C}}_{\mathrm{r}\mathrm{e}\mathrm{f}.\mathrm{p}\mathrm{l}\mathrm{a}\mathrm{n}\mathrm{t}}/{\mathrm{C}}_{\mathrm{s}\mathrm{o}\mathrm{i}\mathrm{l}}\times {\mathrm{C}}_{\mathrm{r}\mathrm{e}\mathrm{f}.\mathrm{s}\mathrm{o}\mathrm{i}\mathrm{l}}$$

In this study, standard reference concentrations of Ni for soil were applied as 1.5 mg/kg, respectively (Singh et al., 2010). For the wheat grains, standard metal values were applied as 9.06 mg/kg, respectively (FAO/WHO, 2001).

2.8.5 Daily intake of metals (DIM)

The DIM is determined by the regular consumption of the metal concentration in the crops and food products studied. The DIM was calculated with the following formula (Singh et al., 2010). $$\mathrm{D}\mathrm{I}\mathrm{M}={\mathrm{C}}_{\mathrm{m}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l}}\times {\mathrm{D}}_{\mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d}}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}/{\mathrm{B}}_{\mathrm{a}\mathrm{v}\mathrm{e}\mathrm{r}\mathrm{a}\mathrm{g}\mathrm{e}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}}$$

C_metal is the nickel content in wheat grains (mg/kg), D_food intake represents the daily consumption of wheat grain (mg/kg), B_{average weight} is the normal weight of the body (kg). 0.242 kg/person is the daily wheat intake, and the average weight of the body that is used is 55.9 kg (Wang et al., 2007).

2.8.6 Health risk index (HRI)

The HRI was created to assess the risks to human health associated with the ingestion of wheat grains contaminated with heavy metals. The HRI was calculated with the following formula (Sajjad et al., 2009). $$\mathrm{H}\mathrm{R}\mathrm{I}=\mathrm{D}\mathrm{I}\mathrm{M}/{\mathrm{R}}_{\mathrm{f}}\mathrm{D}$$

The R_fD (Oral reference dose) value of Ni used in this study is 9.06 mg/kg/day (USEPA, 2010).

2.8.7 Pollution load index (PLI)

The PLI was used to calculate the overall pollution level in the soil. This indicator helps assess the quality of the soil after Ni deposition (Siddique et al., 2019). The PLI was examined using the following formula (Liu et al., 2005). PLI = Ni content in soil/ Reference value of Ni in soil

The reference value of Ni in the soil is 67 mg/kg (USEPA, 2010).

3.1.1 Water

The statistical analysis showed that the water source and crop year exhibited a significant effect on Ni concentration (p > 0.05) while the interaction of water source and crop year had no influence on Ni concentration in irrigation water from various sources (p > 0.05) (Table 1). The Ni concentration in various water forms of irrigation samples fluctuated between 1.69 and 2.36 mg/L according to findings (Fig. 3). The higher Ni content was discovered in manufacturing water for one season, whereas low was found in groundwater in year two, according to data for mean Ni concentration in three water irrigation sources.

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Fig. 3

Nickel content in water from various sources.

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WWF (2007) suggested the safe limit for Ni in water as 0.20 mg/L; in the present research, all the water samples exceed this limit. In addition, all water samples contained a higher Ni concentration (1.71 mg/L) than the water used for wheat cultivation in the study by Khan et al. (2017). However, Ahmet et al. (2018) found lower Ni values (0.95, 0.89 mg/L) for groundwater and wastewater, respectively. Industrial and municipal discharge without any primary treatment is the main source of higher Ni concentration in water which also pollutes the natural reservoir of water (Alloway, 1995). The continuous use of these untreated water resources for agricultural irrigation can be considered as the reason for the high Ni contents determined in this study.

3.1.2 Soil

The present results highlight that water source, crop year and wheat variety had a significant effect on the Ni concentration in soil (p > 0.05) (Table 2). Also, the interactions of wheat variety × water source, water source × crop year and wheat variety × water source × crop year exhibited a significant effect on Ni concentration (p > 0.05). For soil samples concentration of Ni ranges between 1.35 and 2.45 mg/kg in different types of soil (Fig. 4). Ni was discovered in all soil specimens planted with varied wheat cultivars and flourished through three different waterways. However, in the second year, the maximum concentration of Ni was discovered in the variety Galaxy-2013 of soil watered with industrial water, whereas the lowest results were discovered in the soil of variety Watan.

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Fig. 4

Nickel content in soil flourishes with wheat varieties for three water sources during two seasons.

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Nickel (Ni), the 22nd most abundant element in the earth's crust, is found in trace concentrations in natural soils (Hussain et al., 2013). Nickel, a potentially toxic metal, is found in all soils at an average concentration of 20 to 30 mg/kg (Echevarria et al., 2006). The Ni values determined in this study are below these average values. Nickel contents for the soil irrigated with fresh and municipal water (1.36 and 1.61 mg/kg, respectively) given by Khan et al. (2017) were between ranges of the current findings. Yu et al. (2016) and Xiao-Rui (2016) reported the higher Ni concentration (32.08 and 36.33 mg/kg, respectively) in soil samples irrigated with wastewater in different areas of China. However, the Ni values determined in the present study exceed the values (1.30, 1.51 mg/kg) given by Khan et al. (2019) for the canal and sewage water specimens in Pakistan.

3.1.3 Root

The findings specify that the water source and wheat variety had a significant effect on the Ni concentration in the root samples (p > 0.05) (Table 3). Also, the interactions of wheat variety × water source and water source × crop year exhibited a significant effect on Ni concentration (p > 0.05). The maximum quantity of Ni (2.42 mg/kg) was defined in the Watan variety that flourished from urban water during year 2 while the minimum amount of Ni (1.17 mg/kg) was defined in varieties Watan and Galaxy-2013, both grown using groundwater for the second year (Fig. 5). The variety Galaxy-2013, which was cultivated through groundwater in year 2, had a minimum yield, whereas the variety of Watan, which was irrigated via industrial water in year 2, had a greater yield. In year 2, the Galaxy-2013 variety watered with groundwater exhibited the lesser transfer of Ni from soil to root, whereas the variety Watan irrigated with industrial water showed the greatest.

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Fig. 5

Nickel content in roots of wheat crops.

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Nickel (Ni) becomes a toxic pollutant in agricultural environments. Studying Ni bioavailability in plants is essential because of its various uses, from many common household items to industrial applications (Khan et al., 2020a, b; Rasheed et al., 2020). Nafees and Amin (2014) performed a study to evaluate heavy metal contents, their uptake and accumulation in different parts of the wheat plant in Peshawar, Pakistan and defined a lower quantity of Ni (0.60 mg/kg) in wheat roots than the present research. In a recent study, the concentrations of Ni for wheat roots sampled from the Yangtze River Delta, China were much lower than those (9.11 mg/kg) reported by Xiao-Rui et al. (2016). In addition, Yu et al. (2016) presented a higher Ni concentration (5.54 mg/kg) in wheat roots. The capability of plants to trace minerals use from soil depends on the genetic characteristics and concentration of metals inside the soil (Ye et al., 2013).

3.1.4 Shoot

Except for the interactions of wheat variety × crop year and wheat variety × water source × crop year, all the parameters showed a significant effect of Ni accumulation in wheat shoots (p > 0.05) (Table 3). Nickel concentrations in samples of shoot of wheat ranged from 1.09 to 2.10 mg/kg for different wheat varieties (Fig. 6). Variety Faislabad-2008 irrigated with industrial water had the greatest Ni concentration of 2.10 mg/kg in year 2, whereas variety Galaxy-2013 crop with canal water had a lower 1.09 mg/kg in year 1. Varieties Watan irrigated with industrial water in the first year and 2011 Punjab irrigated through built-up water in the second year had the highest and lowest Ni transfer, respectively.

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Fig. 6

Nickel content in the shoot.

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In the present study, all the shoot samples contained higher Ni concentrations than the value (0.80 mg/kg) in wheat samples grown in sewage irrigation reported by Yu et al. (2016). Neeratanaphan et al. (2017) and Nafees and Amin (2014) also documented lower Ni contents in shoot samples (0.53 and 0.06 mg/kg, respectively). Nickel concentration (1.44 mg/kg) in the wheat shoots sampled from the Yangtze River Delta, China as suggested by Xiao-Rui et al. (2016) was similar to the recent studies. The mechanism through which the heavy metals are transported to the different parts of the plants is directly related to the increase of heavy metals in these parts. It is also reliant on plant variety and concentration of metal in the soil. This might be the possible reason for the highest Ni concentration in shoot samples (Ye et al., 2013; Ma et al., 2014).

3.1.5 Grain

According to the statistical analysis of the Ni values for the wheat grain samples, except for the interactions of wheat variety × crop year and wheat variety × water source × crop year, all the parameters showed a significant effect of Ni accumulation in wheat grains (p > 0.05) (Table 3). The Ni concentration in different wheat cultivars fluctuated from 0.99 to 1.54 mg/kg, according to the findings. The maximum amount of Ni was identified in variety Faislabad-2008 cropped by manufacturing water in year 2 and the minimum amount found in variety Galaxy-2013 irrigated with groundwater during year 2 among every variety irrigated with various sources of water in two cropping years (Table 3). In year 1, the highest transfer was reported for the variety Watan irrigated with groundwater, lowest for the variety Faisalabad-2008 irrigated with groundwater (see Fig. 7).

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Fig. 7

Nickel content in grains of different wheat varieties.

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For the current study, the Ni values for wheat varieties were found lower than the values (1.69, 1.93 mg/kg) given by Khan et al. (2017) of ground and sludge water irrigated grains, respectively. The Ni range of wheat grains in the present study was found higher than the wheat grains (0.28 mg/kg) grown in the Tianjin sewage irrigation area reported by Zeng et al. (2015). Different industries like metal finishing, electroplating, circuit board production and many others are the main source of the heavy metal discharge as a pollutant to the environment, which may increase the concentration of Ni in grains (Khan et al., 2019a, b; Ugulu et al., 2021a, b). Rattan et al. (2005) reported higher values (19.07, 20.0 mg/kg) of Ni in grains irrigated with ground and sewage water. The concentrations of Ni in every specimen were within acceptable limits (67 mg/kg) (FAO/WHO, 2001). The present Ni values in grains were within the safe limits and did not show any toxic effect.

3.2.1 Pollution load index

The PLI range of Ni was between 0.15 and 0.27 (Table 4). All the soil samples showed PLI for Ni less than 1. The soil of variety Galaxy-2013 watered by way of industrial water in year 2 had the lowest PLI value for Ni, while Watan irrigated with the ground, sewage, and industrial water in year 1 and manure water in year 2 were the highest pollution load index for Ni (Table 4). PLI levels>1 indicate soil contamination, while PLI values less than 1 indicate that the soil is toxically safe (Ugulu et al., 2022a, b). The fact that the PLI values in the current findings are less than 1 indicates that the soil in the study area is not contaminated. The PLI values for Ni (0.34, 0.40) reported by Bibi et al. (2014) at two different sites (irrigated with groundwater and domestic sewage water) were found higher than all those values which were investigated in the current study. The higher PLI value for Ni (1.62) in soil samples irrigated with wastewater in Sargodha, Pakistan was also given by Ahmad et al. (2014). Khan et al. (2017) determined the PLI values for Ni (0.34, 0.40) in two types of soil irrigated with canal water and sewage water, respectively, which is found in an array of the current study. Lucho-Contantino et al. (2005) found a direct relationship between irrigation time and metal accrual in soil. The determination of various PLI values for different studies can be explained by soil–plant relationships as well as the duration of irrigation of the soil with wastewater.

3.2.2 Bioaccumulation factor for shoot-wheat

In all types of samples, the BAF values for Ni varied from 0.57 to 1.27 (Table 5). The lowest BAF value for Ni was found in variety Galaxy-2013 irrigated with groundwater in year 2, while the highest was found in variety Watan irrigated with the sewage water. Nickel BAF values in the current study were found higher than the values (0.07–0.08) reported by Khan et al. (2016). Alghobar and Suresha (2016) documented the BAF values between 0.20 and 0.32 for wastewater-irrigated rice crops and Khan et al. (2013) reported lower BAF values of 0.05–0.08 for various food crops in Pakistan. In this study, the BAF value was found to be higher than 1 for Variety Saher 2006. It has been observed that some plant species have the ability to remove heavy metals from soil and groundwater by absorbing and accumulating through their roots, adsorption at the top of the roots or precipitation at the root zone (Prasad and Freitas, 2003; Sahin et al., 2016). Differences in BAF values among the findings may be due to differences in plant species.

3.2.3 Translocation factor

The TF for Ni in various samples was lower than 1 according to the findings. The TF of Ni for diverse kinds of samples ranged from 0.76 to 0.97 (Table 6). The maximum TF for Ni was found in the variety Watan, which was grown using built-up water in year 2, while the low TF for Ni originated within the varieties Punjab-2011, which was irrigated with industrial water in cropping years 1 and 2 and Galaxy-2013, which was irrigated with groundwater in year 1. The TF values for Ni in all samples showed values below 1. These values indicate that Ni is not stored in the shoots. The TF values for Ni in Momordica charantia grown in soil irrigated with domestic sewage water in Sargodha given by Bibi et al. (2014) were found between 1.53 and 1.55 and higher than the present values. However, the Ni TF value range in Oryza sativa samples grown in a paddy field reported by Hadif et al. (2015) was between 0.3 and 0.4 and found lower compared to the current conclusion. Neeratanaphan et al. (2017) also reported a lower TF value (0.25) in rice (Oryza sativa) near electronic waste dumps.

3.2.4 Bioconcentration factor for wheat-grain

The BCF for Ni fluctuated from 0.51 to 0.88 (Table 7). The minimum concentration concluded for the variety Galaxy-2013 grown in groundwater for the second year while the maximum value was observed in the Watan variety of industrial water in the second year. The BCF values for Ni in the present research were found parallel to the values for the wheat samples irrigated with canal water and sewage water (0.62–2.60, respectively) reported by Khan et al. (2017) and the values for the wheat variety “Chagi-2” under short-term wastewater irrigation (0.45–0.73) by Ahmad et al. (2018). In all samples, the Ni range for BCF was greater than the value (0.01) reported by Sakizadeh and Ghorbani (2017). Jamali et al. (2009) also reported lower BCF values for Ni (0.11–0.17) in different varieties of wheat amended with domestic sewage sludge. The weathering process is the main reason for Ni mobilization. However, it is observed that soil pH had an inverse linkage with Ni mobility (Ugulu et al., 2020). In the present research, soil pH was high, which might be the possible reason for the lesser uptake of Ni.

3.2.5 Enrichment factor

Analysis revealed EF of Ni was less than 1 for diverse samples. The range of EF for Ni was 0.07 to 0.13 (Table 8). The results showed that varieties Punjab-2011 and Seher-2006 were cultivated in groundwater, variety Faisalabad-2008 in groundwater for the first year, and variety Watan for groundwater while Galaxy variety-2013 growing in groundwater and sludge water for both years had the lowest EF of Ni. The peak EF was examined in the variety of Watan of the second season. The EF values for Ni in the current study for all samples were lower than the values (5.0–6.53) given by Ololade (2014). Singh et al. (2010) also suggested a higher EF value (15.26) for Ni in rice plants grown at different sewage sludge amendments. Variations in the data size for all the metals in the soil and the exclusion speed of all the metals from the soil may be the possible reason for the difference in the EF of metals and metalloids (Ugulu et al., 2020; Khan et al., 2021).

3.2.6 Daily intake of metal

The DIM values for Ni varied from 0.004 to 0.007 (Table 9). The DIM values for wheat varieties were not greatly affected by water irrigation sources. The cropping year also did not affect the regular consumption of Ni in various wheat varieties. The maximum daily intake for Ni was observed in varieties Punjab-2011 and Faislabad-2008. The lower DIM values were recorded in varieties of Seher-2006 and Galaxy-2013 irrigated with groundwater for the second year. All the samples in the present study had a daily intake of Ni below the estimated daily tolerable intake value for Ni (1.400 mg/kg/day) (USEPA, 2010). Khan et al. (2013) investigated the human health risk from Ni via food crops consumption with wastewater irrigation practices in Pakistan and determined a lower DIM value (0.003 mg/kg/day) for Ni. Zeng et al. (2015) also researched the health risk of heavy metals via dietary intake of wheat grown in the Tianjin sewage irrigation area, China and reported a low DIM value (0.0006 mg/kg/day) of Ni.

3.2.7 Health risk index

The HRI values of Ni for different wheat varieties irrigated with diverse water sources ranged from 0.21 to 0.33 (Table 10). The maximum value for Ni was noticed for Punjab-2011 and Faislabad-2008 varieties irrigated with industrial wastewater in the second year while the minimum was in Seher-2006. The HRI values of wheat samples for Ni revealed less than 1. This indicated the consumption of these kinds of wheat caused no Ni toxicity to human beings. The HRI values of Ni recorded in the present research were higher than the values (0.002) recorded by Neeratanaphan et al. (2017). The HRI value (0.31) of Ni for wheat growing in groundwater-irrigated soil recorded by Khan et al. (2017) was found similar to the current findings but the HRI value (0.39) of Ni given for sewage water-grown sample was found to higher than the present results. Pollutants affect human beings in various ways but one of the important possible pathways to heavy metal exposure is the food chain (Khan et al., 2018a, b; Huma et al., 2019; Ugulu et al., 2021c, d).