Urbanization influences the distribution, enrichment, and ecological health risk of heavy metals in croplands

General characteristics of study soils

Table 2 presents the descriptive statistics regarding the soil characteristics. Significant changes were observed in the distribution of sand (110–850 g kg⁻¹), silt (50–530 g kg⁻¹), clay (100–610 g kg⁻¹), and soil textural class (7 texture classes) showing the diversity of natural and human processes involved in the formation and development of these soils²⁸. Almost all soil samples were alkaline (with reaction at a range of 7.4–8.1) and calcareous (with CCE at a range of 5.5–35%). The EC of some soils was > 4 dS/m (about 7% of the soil samples), indicating the partial salinity of the study soils. The organic carbon and total N contents of the soils were, on average, 2% (0.8–3.1%) and 0.28% (0.05–0.51%), respectively, placing them within the range of the moderate class. Likewise, the mean CEC of the soil, which is an effective indicator of soil fertility and quality, was in the moderate class of 12–25 cmol kg⁻¹²⁹. The CEC was found to be highly correlated with clay (r = 0.76 P < 0.01) content and organic carbon (r = 0.54 P < 0.05) significantly. This result implies that CEC variations may accord with clay and carbon distribution. Most soil characteristics have a high coefficient of variations (CV) of > 35%, implying a wide variability of the soils in the study area.

Soil heavy metals

The concentrations of Zn, Cu, Cd, Pb, and Ni varied in the ranges of 55.4–185, 22.9–121.5, 0.49–1.59, 29.1–122.1, and 21.8–99.5 mg kg⁻¹, respectively (Table 2). Their mean concentrations descended in the order of Zn (80.2 mg kg⁻¹) > Pb (58 mg kg⁻¹) > Ni (55.4 mg kg⁻¹) > Cu (38.8 mg kg⁻¹) > Cd (0.88 mg kg⁻¹). In most soil samples, these ranges are comparable with data reported for other urban soils around the world—e.g. Ref.³⁰ in Poland, Ref.³¹ in China, and Ref.³² in Greece. The values of Cd, Cu, and Zn were below their acceptable ranges as per the international standards⁴ in all soil samples. Nonetheless, the Pb and Ni contents were higher than their acceptable ranges in 13.1% and 17.4% of the samples, respectively. Furthermore, the concentrations of the five elements were higher than their background values in all urban soil samples. This difference was considerable for Cd, Pb, and Ni. The heavy metals had CV in the order of Cd (53%) > Pb (51%) > Ni (46%) > Zn (21%) > Cu (18%). This CV variation implies great variations in Cd, Pb, and Ni, which is linked to anthropogenic activities³³. The background values of the metals, estimated by the median absolute deviation method^10,14, were 52.3, 18.7, 0.45, 29.1, and 30.8 mg kg⁻¹ for Zn, Cu, Cd, Pb, and Ni, respectively.

We compared the concentrations of the heavy metals between urban and non-urban soils and found significant increases in the concentration of the metals in most soil types (Fig. 2). The urban soils had 17–36%, 14–21%, 41–70%, 43–69%, and 13–24% higher Zn, Cu, Cd, Pb, and Ni contents than the non-urban soils. The effluent and waste entry from multiple food processing and storage units, dying plants, metal plating facilities, and plastic production in close proximity of the study area is believed to be the reason for the high concentration of these trace elements. Research in various parts of the world, e.g., Ref.³⁴ in India, Ref.³⁵ in Brazil, and Ref.³⁶ in China, has documented that the facilities have introduced significant quantities of heavy metals to soils. However, traffic and agrochemicals also play a key role in the accumulation of heavy metals in this region¹⁰.

Soil pollution indices

The pollution ranges of Zn, Cu, Cd, Pb, and Ni were assessed by calculating enrichment factor (EF), pollution index (PI), and ecological risk for each metal (E_i) and for all metals (ER). The EF values were in ranges of 1.47–2.13, 1.1–2.2, 2.3–3.6, 1–2.13, and 1.1–2.1 for Zn, Cu, Cd, Pb, and Ni whereas they were in ranges of 1.3–1.8, 1–1.6, 1.9–2.2, 1–1.8, and 1–1.4 in the non-urban soils, respectively. The mean comparisons reveal an increase of 12–25% for Zn, 9–37% for Cu, 18–82% for Cd, 8–22% for Pb, and 7–48% for Ni in the urban soils versus the non-urban soils (Fig. 3). These increases upsurged the EF severity class from minimal enrichment (EF < 2) in the non-urban soils to moderate enrichment (2 ≤ EF < 5) in the urban soils. The shift in enrichment class occurred in 25% of the samples for Cu, 33% of the samples for Ni, 50% of the samples for Zn, 62% of the samples for Pb, and 100% of the samples for Cd. As a result, urban activities resulted in the enrichment of heavy metals in the order of Cd > Pb > Zn > Ni > Cu. These findings are comparable to the results reported by³⁷ and¹². The highest EF for all five elements was observed in the Fluvisols soil type, reflecting that this soil type had been exposed to element pollution induced by urban activities to a greater extent than the other soil types. In a study on the pollution potential of four soil types in Central Greece, Ref.³⁸ reported different ranges of element pollution across different soil types.

As shown in Table 3, the mean PI of the urban soils decreased in the order of Cd (1.97) > Pb (1.89) > Ni (1.86) > Cu (1.73) > Zn (1.51). Mean PI for non-urban soils followed the order Cd (1.5) > Zn (1.4) > Cu (1.33) > Pb (1.31) > Ni (1.29). Nearly 7% and 16% of the urban soils showed moderate pollution (MP, PI = 2–3) and high pollution classes (HP, PI > 3) of PI for Cd and 39% and 4% showed the MP and HP class of PI for Pb, respectively. However, the PI class was low pollution (PI = 1–2) for all soil samples and soil types in the non-urban soils. The results on the pollution index indicate a widespread intensification of soil pollution in urban soils across all studied heavy metals.

Ecological risk, E_i was similarly found to be significantly higher in the urban soils than in the non-urban soils, even though the concentration of all elements except Cd fell within the low-risk class (E_i ≤ 40) in both urban and non-urban soils (Table 3). The mean E_i for Cd was 58.7 (moderate-risk class) and 39.2 (low-risk class) in the urban and non-urban soils, respectively. This means that urban activities have enhanced the ecological risk class of Cd by one grade. Overall, Cd had the highest EF, PI, and E_i among all heavy metals and in all soil samples, indicating a greater risk potential by Cd than Zn, Cu, Pb, and Ni across the water-soil–plant-human domain. Elevated Cd pollution by anthropogenic activities has been widely reported in the literature^10,12,39. Cadmium as a Group 1 carcinogen element⁴⁰ can accumulate in plant tissue without exhibiting visual symptoms. Therefore, Cd generally transfers from soil to the food chain covertly. Cadmium pollution can also influence soil quality and reduce crop yields and grain quality³.

Similar to EF, PI, and E_i, the mean ER was significantly elevated in all urban soil types than the non-urban soils (Fig. 4). Among different soil types, the ER magnitude was in the order of Fluvisols (66.6%) > Regosols (66.1%) > Cambisols (59.8%) > Calcisols (47%). These results indicate that Fluvisols carry a higher ecological risk potential for heavy metal accumulations than other soil types. In the study region, Fluvisols due to higher fertility and productivity are subject to more intense and extensive agronomic operations than other soil types¹³. Heavy application of agrochemicals (e.g., pesticides, herbicides, insecticides, and chemical fertilizers), accelerate the heavy metal input to the Fluvisols. Widespread application of nitrogen fertilizers and subsequent reduction in average soil pH markedly increases the solubility of certain heavy metals (e.g., Zn, Cu, Cd) which can be another factor increasing the ecological risk of heavy metal contamination in Fluvisols⁴¹. In addition, these Fluvisols are located on the margin of open urban wastewater channels, which are sometimes used for irrigation. A combination of mentioned processes can be implicated for higher ER of Fluvisols than that of other soil types as for BF, PI, and E_i.

The concentration of heavy metals in corn roots and grains

Table 4 presents the minimum, maximum, mean, and standard deviation of the metals in corn roots and grains. The concentrations of Zn, Cu, Cd, Pb, and Ni in the corn roots were in ranges of 4.3–21, 3.2–12.6, 0.4–0.74, 0.2–0.84, and 0.29–2.8 mg kg⁻¹ with means of 9.9, 6.4, 0.55, 0.4, and 1.1 mg kg⁻¹, respectively. The minimum, maximum, and mean values of these metals in the corn grains were 3.3, 16.6, and 7.9 mg kg⁻¹ Zn, 2.4, 10.1, and 5.1 mg kg⁻¹ Cu, 0.08, 0.15, and 0.11 mg kg⁻¹ Cd, 0.05, 0.26, and 0.13 mg kg⁻¹ Pb, and 0.06, 0.2, and 0.12 mg kg⁻¹ Ni, respectively. Metal concentration was in the order of Zn > Cu > Ni > Cd > Pb in the roots, partially differing from that of the grain—Zn > Cu > Pb > Ni > Cd. Heavy metals concentrations observed in the corn roots and grains are almost comparable with those reported by⁴² in China and⁴³ in Peru.

The accumulation of heavy metals in the edible parts of corn is of higher importance. In the present study, the concentrations of these metals were lower than the acceptable level in the corn grains based on international references⁴⁴. So, the consumption of corns grown in the regions should not threaten human and animal health in the short term, but caution should be exercised in their long-term consumption because some of these elements, especially Cd and Pb, which have long decomposition half-lives, gradually accumulate in body organs, especially in kidneys and livers⁴⁵. Besides, the ratio of Zn, Cu, Cd, Pb, and Ni of the corn grain to their acceptable standard concentration, known as the pollution index of crop heavy metals, Ref.¹² was lower than 0.7 for most corn samples, indicating the unpolluted risk class.

The mean concentrations of Cd, Pb, and Ni were 5, 3.1, and 9.2 times as great in the corn roots as in their grains. This observation exhibits a notable phytoremediatory function of corn roots through restriction of radial translocation of heavy metals to the xylems and eventually into the grains. A similar trend of heavy metal accumulation in different plant organs has been reported in previous observations^46,47. Based on Kabata-Pendias⁴ and Adriano²², plant cells can use the defensive tools of the roots to cope with heavy metals, especially Cd and Pb—highly toxic metals to plant cytosols. Accordingly, plant cells can fix these elements in the root system by such approaches as precipitating on cell walls, storing in vacuoles, and/or chelating by phytochelatins, thereby alleviating their toxic effects and inhibiting their translocation to plant shoots. For Zn, Cu, and Cd metals, a significant correlation was observed between their concentration in corn roots and grains. But, a less significant correlation (P < 0.05) was recorded for Pb and Ni with r = 0.52 and r = 0.38 (Table 5). These correlations indicate that a major part of Zn, Cu, and Cd in the corn grains may have been mobilized by their soil-root system, while a combination of atmospheric precipitation and root-soil system may be implicated for Pb and Ni⁴.

Bioconcentration factor (BCF) and translocation factor (TF)

The values of BCF and TF were calculated considering the concentrations of heavy metals in the soil, corn roots, and corn grains (Table 4). The mean BCF of the elements was in the descending order of Cd (0.68) > Cu (0.17) > Zn (0.12) > Ni (0.02) > Pb (0.01). This implies that Cd, and to a smaller extent Cu is taken up by corn roots from the soil more readily, but Pb and Ni are less absorbable. These results are consistent with the reports of⁴⁸ and⁴⁶. The greater value of BCF-Cd may be related to a combination of the specific factors e,g., Cd concentration and chemistry, as well as soil characteristics (e.g., soil texture, pH, and calcium carbonate content)⁴. As was already discussed, the examined soils were characterized by high alkaline (pH = 7.4–8.1) and calcareous properties (CCE = 5.5–35%) with a high concentration of Soluble salts (EC = 0.7–6.6 dS m⁻¹). These characteristics can result in the formation of complex Cd ions, especially CdOH⁺, CdCl₂⁰, CdCl⁺, CdSO₄⁰, and CdHCO₃^+4,22. These ions are plant-available, resulting in a further increase in Cd BCF. Regarding Ni and Pb, the alkaline and calcareous properties of the soils may have motivated insoluble compounds such as NiHCO₃⁺ and NiCO₃⁰ (for Ni) and Pb(OH)₂, PbCO₃, PbSO₄, and PbO (for Pb)^4,22. These compounds cannot be uptake by plant roots, which may have resulted in a significant decrease in the BCF of these metals versus the other analyzed elements.

Like BCF, the heavy metals had TF of < 1, which is similar to some previous studies that reported TF < 1 for the translocation of heavy metals from roots to grains for crops such as wheat, corn, and rice^49,50,51. The mean TF of the metals decreased in the order of Zn (0.8) > Cu (0.78) > Pb (0.21) > Cd (0.2) > Ni (0.15). This implies that Zn and Cu are translocated from roots to grains readily, about four times as great as the other metals, while Ni, Cd, and Pb are translocated in smaller concentrations.

The comparison of BCF and TF of Cd showed that less than 30% of Cd, on average, accumulated in the corn roots were translocated to the grains. This states that Cd is immobilized by various mechanisms before it can find its way into the grains. Some of the important mechanisms include (i) the antagonistic effects of Cd with other equivalent elements, especially Zn, Fe, and Ca, in the vascular system of corn, which reduces its mobility in the corn root-stem-grain system²², (ii) Cd sequestration in active exchange sites on the cell wall in the corn root-stem pathway¹⁰, and (iii) the binding of Cd with some specific compounds, e.g., phytochelatins of root vacuoles, which immobilizes it before its translocation to grains^4,22. Lin and Aarts⁵² remarked that Cd mostly tends to be trapped in root vacuoles, which reduces its translocation to the upper parts of the plants. In general, it was found that corn plants have a high potential to absorb and accumulate Cd in their roots and Zn in their grains, which is consistent with previous studies⁴¹. For the majority of heavy metals, the values of BCF and TF in different soil types were in the order of Fluvisols > Regosols > Cambisols > Calcisols, indicating that the great variety of soil types for the uptake and translocation of heavy metals in the soil-root-grain of the corn (Fig. 5).

Multivariate analysis of metals concentration and accumulation in root and grain corn

The relationship of the heavy metals concentration in root and grain of cron with soil characteristics was explored by multivariate regression models. These models can be used as an easy tool to predict the concentration of heavy metals and the risk of their accumulation in various crops¹⁰. Significant relationships were observed between Zn, Cu, Cd, and Pb concentrations in soil and associated concentrations in corn root and shoots(Table 6) while the relationship was non-significant for Ni. This implies that a considerable value of corn Ni might be attributed to non-soil sources—e.g., atmospheric depositions, or metal-bound dust. Among different properties of soil, CCE, CEC, and concentration of Cd and Cu were the key factors influencing Cd accumulation in the roots and grain of corn, accounted for 81% and 67%, of the variance, respectively. For Pb, the values of soil CCE, Pb, and Cd had a significant impact on Pb-root and Pb-grain, accounted for 94% and 63%, of the variance, respectively. The models indicated that the predicted Cd content in the root and grain of corn increased with an increase in soil Cd content, calcium carbonate, CEC. However, an increase in soil calcium carbonate and Cd concentration decreased the predicted Pb content in the corn root and grain. As previously discussed, the positive and negative impact of calcium carbonate on corn Cd and Pb, respectively, is likely due to the formation of the complexes of Cd with carbonate which is readily uptake by plant roots, and the formation of insoluble compounds of Pb which cannot be absorbed by plant roots⁴. Besides, the regression model Pb showed an antagonistic interaction between soil Cd and Pb which might have resulted in a decrease in Pb uptake by roots crop²².

Commonly, organic carbon was an important factor influencing Zn and Cu accumulation in corn root (capturing 85 and 72% of the variance, respectively) and grain (capturing 84 and 74% of the variance, respectively). This may be explained by the synthesis of organometallic complexes of Zn and Cu that enhance the availability of two metals and protect them from precipitation reactions, resulted in an increase in their uptake by crops^22,52.

Health risk assessment

Non-carcinogenic risk

Since corn grains have traditionally been a staple food for Iranians, the daily intake (DI), hazard quotient (HQ), and hazard index (HI) of heavy metals translocated by corn ingestion were calculated to different demographic groups, including children, adult women, and adult men (Table 7). The mean DI was varied in ranges from 0.0012 (Cd) to 0.084 (Zn), from 6.27 E−05 (Ni) to 0.004 (Zn), and from 4.78E−05 (Cd) to 0.0034 (Zn) for children, women, and men, respectively. So, Zn had the highest DI for all demographic groups. Nonetheless, the DI values are within the acceptable range for all metals and demographic groups according to WHO/FAO (2017). The comparison of the mean DI among the three demographic groups showed that DI of Zn, Cu, Cd, Pb, and Ni in children was 21, 20.7, 21.4, 20.4, and 20.7 and 24.7, 24.5, 25.1, 23.9, and 24.3 times of woman and men, respectively, which accords with previous research by⁵¹. These differences may be due to the different nutritional behaviors of the demographic groups. The result for higher DI of the children is related to the fact that although children consume lower volumes of food, their body weight is lower than that of the other groups¹⁰. These data also mean that the effects of an environmental threat, like heavy metals, by food consumption is not similar across different demographic groups.

HQ for different metals was in the order of Cd > Zn > Cu > Pb > Ni for children, differing from that for adults (Cu > Cd > Pb > Zn > Ni). The values of HQ was < 1 for all metals, except for Cd, in all three demographic groups, reflecting the negligible risk of Zn, Cu, Pb, and Ni to cause non-cancerogenic diseases among corn consumers in the study region⁵³. Similar to DI, HQ of the metals was the highest for children followed by women and men. So, children are more exposed to non-carcinogenic risks than adult females and males. Regarding Cd, HQ was > 1 in over 87% of the samples, implying the low non-carcinogenic risk of this metal for corn-consuming children in the study region⁵³. Rapidly developing children’s nervous system are highly sensitive to environmental factors, including heavy metals, so even a relatively low concentration of Cd in children’s blood may irreversibly affect their mental growth and functioning⁵⁴.

The highest HI was observed in children (min = 1.16, max = 2.31, mean = 1.63) followed by women and men which was similar to the found pattern of HQ (Table 7). These data show a moderate non-carcinogenic health risk (1 ≤ HI < 4) for corn-consuming local children. In contrast, the local adults, including both females and males, exhibited a low non-carcinogenic health risk (0.1 ≤ HI < 1) caused by corn grain consumption (USEPA, 2004). Similarly, a study in western Iran⁵⁵ reported the HI values higher and lower than the acceptable levels for Cd, Pb, Zn, Cu, Ni, and Hg in grains and other cereals (corn, wheat, rice, peas, and beans) for children and adults, respectively. In all demographic groups, Cd and Cu had the highest contribution in HI followed by Zn and Pb. The contributions of these three elements in HI were 37–72.5%, 8.3–42%, and 8.7–27.2%, respectively. As a result, the highest HQ for the demographic groups consuming corn grains was related to Cd, so it had the highest impact on the HI value. Such a pattern of Cd may cause its long-term accumulation in vital organs, especially in kidneys and liver of corn-consuming individuals, thereby leading to severe damages in neural systems, skeletons, lungs, and enzymatic and immune systems^56,57.

Carcinogenic risk

Since the cancer slope factor was available for Cd and Pb, the carcinogenic risk (CR) of these two metals by corn grain consumption was calculated for different demographic groups. The values of CR of the two metals for children, women, and men were in ranges from 1.1E−04 to 1.5E−04, 6.21E−05 to 8.53E−05, and 5.84E−05 to 8.03E−05 for Cd and from 4.82E−06 to 1.13E−05, 2.33E−07 to 5.48E−07, and 2.19E−07 to 5.16E−07 for Pb, respectively. These data mean that CR is almost within the acceptable range (from 1.00E−04 to 1.00E−06) for corn-consuming adults in the region, but children are exposed to the low to moderate risk of cancer⁵³. Regarding Cd, the mean CR was 1.40E−04, 8.53E−05, and 8.03E-5 for children, adult females, and adult males, respectively (Fig. 6). This implies that occurrences of 14 and 8 cases out of 1,000,000 of children and adults are exposed to the risk of cancer caused by Cd. The lead had lower CR than Cd and its risk of cancer was one child and five adults cases out of 1,000,000 individuals. The comparison of these data shows that the risk of Cd-caused cancer through corn ingestion among different demographic groups was 13.5 for children and 155 times for adults higher than that caused by Pb in the region. This corroborates the findings of⁴¹ and⁴³, who reported higher CR for Cd than for other metals taken up by grain consumption.

Total carcinogenic risk (TCR) for Cd and Pb was the highest for children (min = 1.20E−04, max = 2.30E−04, mean = 1.60E−04) followed by females (min = 6.24E−05, max = 1.20E−04, mean = 8.59E−05) and males (min = 5.88E−05, max = 1.10E−05, mean = 8.09E−05). Therefore, TCR for women (more than 86% of samples) and men (more than 95% of samples) are almost within the acceptable range (1.00E−04 to 1.00E−06), but considering the TCR data, children are exposed to a moderate level of carcinogenic risk (more one case of cancer after every 1,00,000 inhabitants). These findings are supported by the findings of³⁴ and⁵⁸ for the CR of Cd and Pb metals. The highest values of HI, CR-Cd, CR-Pb, and TCR were observed in Fluvisols (Fig. 7), showing that this soil type is more polluted than the other types and has a higher potential to cause cancerous and non-cancerous risks.

Our study provides insight into the urbanization impact on heavy metal contamination in the soil system to the food chain and the associated health risks across a range of soil types, metals, age, and gender groups. Our finding is expected to aid policymakers and NGOs with hands-on information regarding the state of heavy metal contamination and associated health risks in northwestern Iran. It should be acknowledged that further studies are required to fully understand the mechanisms of absorption, mobility, translocation, and accumulation of heavy metals in different parts of grains (roots, stems, leaves, and grains) using bioclinical models that are dependent on animal and human health. At present, the studies on the analyses of human health risk caused by heavy metals merly rely on thresholds and prediction models defined by the Environmental Protection Agency of the US. While the local data supporting the validity of those standards around the world is lacking.

Source: Ecology - nature.com