Assessment of Heavy Metals Accumulation in Soil and Native Plants in an Industrial Environment, Saudi Arabia

Abstract

Industrial activities are associated with various heavy metals (HMs) being emitted into the environment, which may pose a threat to humans and animals. The rapid increase in an industrial activity in major cities in Saudi Arabia (SA) has raised concerns regarding the accumulation of HMs in the environment. The aim of this study is to assess the accumulation of HMs in soil and native plants in an industrial environment. We collected 36 surface soil samples and 12 plant species from 12 sites in an industrial city in central SA. The results showed that the HMs content in the soil followed a descending order of (Fe > Ni > Zn > Pb > Cu> Cr > Cd). The enrichment factor (EF) of HMs in the soil ranged from 0.20 to 7336. Up to 100%, 16.6%, and 6.2% of soil samples were extremely highly enriched with Cd, Ni, and Pb, respectively. Plant species Cyperus laevigatus accumulate Cd, Pb, and Ni. Citrullus colocynthis accumulate Cd and Pb in significantly (p < 0.001) higher amounts than other studied species. The Pollution Load Index (PLI) values for the 12 sites ranged from 0.52–1.33 with S5 and S2 PLI >1.0 indicating progressive deterioration of these sites. The Bioaccumulation Factor (BF) ranged from 0.04–2.76 and revealed that some plant species may be candidates for phytoextraction potential. The most promising plant species for phytoextraction and remediation were annuals or perennials such as Malva parviflora, Sisymbrium irio and Citrullus colocynthis, especially for Cr and Cu. This study suggests that these native plant species may be useful for phytoremediation in the area.

1. Introduction

Soil pollution with heavy metals (HMs) is one of the most pressing environmental problems worldwide. HMs refer to elements with large atomic weight and relatively high densities [1,2]. After being discharged, HMs can stay in the environment for a long time due to their non-degradability, and as a result, they can adversely affect soils, plants, and humans [3,4]. HM pollution may originate from the soil parent material (lithogenic source) and/or from various anthropogenic sources [5]. For example, soils at industrial sites can have distinct groups of HM contaminants, which depend on the respective industries and their raw materials and products. However, HM pollution is mainly related to human activities, including mining and processing of metal ores, fertilizers, and pesticides, sewage sludge, transportation, and others industrial processes [6].

HM pollution mainly results from anthropogenic activities, such as industrial activities, mining, use of agrochemicals, and automobiles. However, industrial activities are considered the major source of HMs that accumulate in our environment and reach toxic levels, thereby causing health risks and adversely affecting ecosystems [7,8,9,10]. Mining and industrial zones are pointed to as sources of global deterioration of environmental quality due to the release of HMs. HM pollution is considered to be one of the most serious and dangerous hazards affecting humans and animals [11,12]. Moreover, HMs are non-biodegradable elements that exist in the soil for a period of time longer than any other contaminants of the biosphere [13]. Human activities could be responsible for the environment’s contamination by high concentrations of toxic metals, including Zn, Cu, and Cd. Various manufacturing activities in industrial areas have led to a marked increase in the total amount of HMs in nearby soils. HMs such as As, Cd, Cr, Ni, Pb, etc., have been classified as carcinogenic to humans and wildlife [13,14,15]. The result of poor solid and liquid waste disposal from industrial activities in soils alongside Buddha Nullah, Ludhiana, (Punjab) India caused increases in the concentration of HMs, such as Cd, Co, Cu, Pb, and Zn, which can directly influence human health and ecological systems [16]. The soil’s microbial diversity and function are also affected by HMs contamination [17,18]. In samples collected from urban and suburban areas of Belgrade, HM contamination of soils and water caused by industrial and traffic actives in the urban environment were arranged in the order Zn > Ni > Pb > Cr > Cu > As > Hg > Cd [19]. In most cases, the maximum concentrations of metals were found in the surface (0.0–30 cm) in the order (Fe > Mn > Zn > Ni > Pb > Cu > Co). A pot experiment conducted with EDTA showed that some plant species, including Lamium purpureum, accumulated a relatively higher amount of As, while the Amaranthus reflexus accumulated higher Cd compared to the other plant species studied. It was also concluded that chelates can improve phytoremediation of HMs from contaminated soils through increasing solubility and uptake by high biomass plants and accelerating the remediation process [20,21]. After evaluation of the efficiency of different diluted chelate solutions to mobilize HMs—namely, Cd, Pb, Cr, and As—upward by capillary force in soil under greenhouse conditions, mobilization of specifically Cd and Pb upward to the surface layer was greater than 35% of the added concentration [22]. For a plant to be a hyperaccumulator of As, Pb, Cu, Ni, and Co, it should be greater than 1000 mg·kg⁻¹ dry shoot mass, while for Cd it should be greater than 500 mg·kg⁻¹ [23,24]. Different plants, such as S. lycopersicum and B. juncea, have been found to tolerate and accumulate HMs, which can used to eliminate the HMs soil contamination. However, plants that grow in aridic soil are subjected not only to HMs, but also to alkaline and saline conditions due to high pH and EC. These chemical and environmental stresses do not allow the survival of HMs accumulator plants. Thus, the best option is to use native plants, which are able to thrive and grow in their native environment, for phytoremediation of HMs contaminated sites [23,25]. However, information regarding the use of plant species indigenous to this region of extreme environmental conditions is lacking. Therefore, the objectives of this study were (1) to assess HM pollution in soil in the vicinity of the industrial zone in Riyadh city and (2) to assess the content of HMs in the native plants growing in the study area and their potential use for remediating HMs contaminated sites in the region.

2. Materials and Methods

2.1. Study Area

The study area is an industrial city located south of Riyadh Capital in central SA (Figure 1). The Second Industrial City, which is located 12 km south of Riyadh City, capital of Saudi Arabia, was established in 1976. It has been developed in four stages to a total area of more than 18 million square meters. It houses more than 1115 different industrial units including smelting, metal chemical industries, electroplating, energy, fuel production, and cement factories. The area of study is in a desert region, where the climate is dominated by high temperatures and limited rainfall with an annual precipitation range of 90–100 mm and a high evaporation rate.

2.2. Soil Sampling and Analyses

Surface soil samples from depths of 0 to 20 cm were randomly collected from 12 sites of the study area using a soil auger. The global positioning system (GPS) device was used to point to sample locations (Figure 1). Each site was divided into three sections, and three soil samples were collected from each section and combined to provide a composite sample. Soil samples were then air-dried at room temperature (20–25 °C) for one week and sieved through a 2-mm sieve. The soil was analyzed for basic chemical and physical properties. The hydrometer method was applied to determine the particle size distribution [26]. A calcimeter method was used to estimate the soil calcium carbonate (CaCO₃) content [27]. The content of the soil organic matter (SOM) was measured following the method of Nelson and Sommers [28]. The soil pH and electrical conductivity (EC) were measured in distilled water extracts in the soil and distilled water ratio of 1:1 after equilibration for 24 h [29]. The chemical and physical characteristics of the soil are provided in (

Table 1. Chemical and physical properties of the study area.

Parameters	Minimum	Maximum	Mean (SD a)
Sand%	55	60	58.1 (1.4)
Silt%	18	26	22.4 (2.6)
Clay%	16	23	19.4 (2.1)
pH (1:1)	7.4	8.7	8.2 (0.4)
EC b dsm−1	6.6	12.8	9.19 (2.0)
% O.M c	0.43	0.98	0.74 (0.2)
CaCO3%	28.5	42.2	35 (5.1)

^a Standard deviation. ^b Electrical conductivity. ^c Soil organic matter.

. A 0.5 g of oven dry soil was accurately weighed and digestated using a Teflon beaker following the addition of a mixture of acids (HF + HCl) at 130–140 °C for complete digestion. The digested extract was diluted with double distilled water and filtered into 100 mL volumetric flasks using a Whatman no. 42 filter and analyzed for HMs using ICP-AES.

2.3. Plant Sampling and Analyses

According to their importance for adaptation to the environment, 12 native plant species were identified and sampled from the 12 sites of the study area (Figure 1). Three individuals of each species were randomly selected from each sampled site. It was found that the identified 12 plant species belong to 11 families (

Table 2. The species characteristic of the study areas.

Family	Species	Classification
Apocynaceae	Calotropis procera	Perennial
Cucurbitaceae	Citrullus colocynthis	Annual
Fabaceae	Cassia italica	Perennial
Cyperaceae	Cyperus laevigatus	Perennial
Papaveraceae	Argemone mexicana	Annual
Apocynaceae	Rhazya stricta	Perennial
Combretaceae	Conocarpus lancifolius	Perennial
Zygophyllaceae	Zygophyllum simplex	Annual
Amaranthaceae	Salsola imbricata	Annual or perennial
Malvaceae	Malva parviflora	Annual or perennial
Brassicaceae	Sisymbrium irio	Annual or winter-annual
Poaceae	Phrgmites australis	Annual or perennial

). All plants were washed and cleaned with distilled water, oven dried at 70 °C, and ground into powder with an electric grinder. Plant samples of 2.0 g were taken in a Pyrex beaker and digested with a mixture of acids (HNO₃ + HClO₄ and aqua regia). The mixture of acids (HNO₃ + HClO₄) extract was analyzed for HMs using ICP-AES [30].

2.4. Data Precision and Accuracy

All reagents were of analytical grade. Stock standard solutions of 1000 µg/mL for all seven elements were prepared either from salts or pure metals supplied by J. T. Baker (Deventer, The Netherlands), Merck (Darmstadt, Germany), and Aldrich Chemical Company (Milwaukee, WI, USA). Working multi-elemental standard solutions were prepared by appropriate dilution with deionized water from stock solutions and by the addition of 8 mL of concentrated nitric acid (s.p. Merck) per 100 mL of standard solution. The calibration curve was prepared for each of the metals investigated by least square fitting.

2.5. Quantification of Soil Contamination of the Study Area

2.5.1. Enrichment Factor (EF)

A common approach to estimate how much the sediment is impacted (naturally and anthropogenically) by HMs is to calculate the Enrichment Factor (EF) for metal concentrations above un-contaminated background levels [31]. The EF normalizes the measured HMs content with respect to a sample’s reference such as Fe, Al, or Zn [32]. The Fe is used to determine the relative degree of metal contamination, and the comparisons in this study were made using Fe background concentrations in the earth’s crust as a reference element with the assumption that iron content in the crust is not affected by anthropogenic activity [33]. The EF of an HM in soil can be calculated with the following formula:

$$\mathrm{EF}=\frac{\raisebox{1ex}{${\mathrm{C}}_{\mathrm{metal}}$}\!\left/ \!\raisebox{-1ex}{${\mathrm{C}}_{\mathrm{normalizer}}$}\right. \left[\mathrm{soil}\right] }{\raisebox{1ex}{${\mathrm{C}}_{\mathrm{metal}}$}\!\left/ \!\raisebox{-1ex}{${\mathrm{C}}_{\mathrm{normalizer}}$}\right.\left[\mathrm{control}\right]}$$

(1)

where C_metal and C_normalizer are the concentrations of HMs and normalizer in the sediment and the unpolluted control [34]. The EF can be used to differentiate between the metals originating from anthropogenic activities and those from natural processes, and to assess the degree of anthropogenic influence. Five contamination categories are recognized, and they are (1) EF < 2 is deficiency to minimal enrichment; (2) EF 2–5 is moderate enrichment; (3) EF 5–20 is significant enrichment; (4) EF 20–40 is very high enrichment; and (5) EF > 40 is extremely high enrichment [35].

2.5.2. Contamination Factor (CF)

The contamination factor (CF) for the sediment samples was calculated by the equation below, where CF is the ratio obtained by dividing the concentration of each metal in the soil (C_metal) by the baseline or background (C_background) value (average earth crust abundance or concentration in unpolluted soil):

$$\mathrm{CF}=\frac{{\mathrm{C}}_{\mathrm{metal}}}{{\mathrm{C}}_{\mathrm{background}}}$$

(2)

Contamination levels may be classified based on their intensities on a scale ranging from 1 to 6 (0 = none, 1 = none to medium, 2 = moderate, 3 = moderate to strong, 4 = strongly polluted, 5 = strong to very strong, 6 = very strong) [36].

The highest number indicates that the metal concentration is 100 times greater than what would be expected in the crust.

2.5.3. Pollution Load Index (PLI)

For the entire sampling site, the PLI has been determined as the nth root of the product of the n CF in this study to measure the PLI in the studied sites. The PLI for a single site is the nth root of n number of the contamination factor (CF) values multiplied together [37]. The CF is the quotient obtained as follows:

PLI = (CF₁ × CF₂ × CF₃ × ··· × CF_n)^1/n

(3)

This provides a simple, comparative means for assessing the level of HM pollution. For the all-sampling site, the PLI has been calculated as the nth root of the product of the n CF [38].

2.5.4. Bioaccumulation Factor for Plants (BF)

The Plants Bioaccumulation Factor (BF) is a useful tool to evaluate whether a specific plant is an HM hyperaccumulator. The bioaccumulation factor is defined as the ability of a plant to accumulate HM concentrations. The ability of a plant to accumulate HMs from soils can be estimated using the BF, which is the ratio of HM concentrations in plants and soil [39,40,41]. The BF is computed according to the following formula:

$$\mathrm{BF}=\frac{{\mathrm{C}}_1}{{\mathrm{C}}_2}$$

(4)

where C₁ and C₂ are the average concentrations of metal in plants and soil, respectively.

2.6. Statistical Analyses

Statistical analyses were made for all of the data using (SPSS; IBM Corp., New York, NY, USA) and Microsoft Excel. The figures were drawn using Microsoft Excel. Data mean and standard deviation were calculated using Microsoft Excel. Comparison of the mean of HMs in plants across all sites was made with Statistical Package for Social Studies (SPSS; IBM Corp., New York, NY, USA) using one-way ANOVA.

3. Results and Discussion

3.1. Soil

3.1.1. Physicochemical Parameters

The soil’s basic physical and chemical properties are shown in Table 2. In the topsoil from the different sampling sites in the area investigated, 58% had sandy clay loam and 42% sandy loam. The average soil texture class for all sites was sandy clay loam texture with very low organic matter content ranging from 0.43% to 0.98% with an average of 0.65%. The soil pH values ranged between 7.4 and 8.7 with an average of 8, indicating a high alkalinty for all sites. For electrical conductivity (EC), the value ranged between 6.65 and 12.80 dsm⁻¹ and with an average of 9.19 dsm⁻¹, and for CaCO₃%, the value ranged between 28.5% and 42.2% and with an average of 35%. Results revealed that all sites are saline and alkaline soils. The soil’s chemical proprieties indicate that HMs in such environments would precipitate in the topsoil surface with limited movement and bioavailability for plants due to high calcium carbonate content in addition to alkaline pH.

3.1.2. Heavy Metal Concentration in Soils

The concentrations of HMs (Cd, Cr, Cu, Fe, Pb, Zn, and Ni) in the soil samples collected from the 12 sites (S) of the study area are summarized in

Table 3. Mean and standard deviation of heavy metal concentrations in soil of study areas (12 site, n = 36; mg·kg⁻¹).

Sites No.	Mean (SD a)
	Heavy Metal
	Cd	Cr	Cu	Fe	Pb	Ni	Zn
S1	1.7 (0.34)	15.85 (0.32)	14.6 (1.87)	4035.5 (207.7)	16.7 (1.12)	26.65 (1.08)	33.95 (0.11)
S2	22 (1.41)	20.55 (2.38)	11.1 (0.88)	5218 (163.8)	25.5 (5.12)	21.7 (2.22)	32.5 (0.40)
S3	3.1 (1.43)	15.55 (15.55)	18.7 (2.31)	4848 (183.5)	18.05(1.65)	60.1 (5.94)	20.1 (2.52)
S4	16 (0.62)	1.25 (0.36)	12.55 (2.67)	655.5 (19.7)	5.1 (1.28)	72.8 (5.32)	22.8 (4.05)
S5	12.9 (1.79)	34.2 (3.37)	16.95 (1.12)	6478.5 (162.8)	10.9 (1.53)	45.0 (8.64)	42.6 (2.13)
S6	5.5 (0.51)	16.75 (1.15)	22.4 (1.64)	1660.8 (76.9)	10.75 (1.54)	48.8 (1.51)	20.1 (2.56)
S7	15.1 (0.67)	11.7 (0.57)	12.4 (0.36)	1303.5 (30.3)	12.55 (1.52)	66.5 91.16)	21.15 (0.94)
S8	5.9 (0.57)	4.5 (0.59)	17.9 (0.23)	6262 (186.6)	22.55 (2.19)	38.75 (0.32)	14.35 (0.10)
S9	7.7 (0.96)	18.1 (0.36)	14.9 (0.23)	4860 (60.8)	3.35 (0.26)	29.3 (0.93)	21.7 (0.17)
S10	1.1 (0.08)	5.7 (0.37)	22.35 (0.32)	2003.7 (7.57)	16.25 (0.24)	34.5 (1.08)	11.55 (0.66)
S11	8.3 (90.36)	2.75 (0.10)	8.2 (0.29)	1829.2 (117.1)	22.55 (0.88)	32.5 (0.50)	15.25 (0.07)
S12	3.6 (0.22)	1.6 (0.15)	9.25 (0.07)	3117.5 (181.0)	25.5 (0.45)	64.93 (2.12)	16.65 (0.11)

^a Standard deviation.

. The values of the contents of the eight HMs in the soils of the study area followed a descending order of Fe > Ni > Zn > Pb > Cu> Cr > Cd. The average value for Cd in all sites was 8.58 mg·kg⁻¹ with ranges between 1.1–22 mg·kg⁻¹ and for Cr the value was 12.38 mg·kg⁻¹ with ranges between 1.25 to 34.2 mg·kg⁻¹. The Cu value was 15.11 mg·kg⁻¹ with ranges between 8.2 to 22.4 mg·kg⁻¹ and for Fe the value was 3522.7 mg·kg⁻¹ with ranges between 655 to 6479 mg·kg⁻¹. The Pb value was 15.81 mg·kg⁻¹ with ranges between 3.35 to 25.5 mg·kg⁻¹ and for Zn the value was 22.73 mg·kg⁻¹ with range between 11.55 to 42.6 mg·kg⁻¹, while for Ni the average value was 45.13 mg·kg⁻¹ with a range from 21.7 to 72.8 mg·kg⁻¹. The soil’s physical and chemical properties have a strong influence on the environmental fate and the mobility of HMs in soils [42]. However, the soils of the study area have 35% CaCO₃ and pH value of 8.2, which indicate that HMs in such environments would precipitate in the topsoil surface with limited movement and bioavailability for plants. Cement and stone factories may produce pollutants that are widely dispersed and exceed the standard limit. In addition, the harmful chemical gases and dusts from cement factories, power plants, and vehicles in the this study area cause a pollution risk [43]. The comparison of the mean values showed that contents of Cd in S2 and S4 and Ni in S4 and Pb in S2 and S12 in the study area were found to be significantly (p < 0.001) higher than those in other sites. The high level of Cd and Pb on S2, S4, and S12 indicate a higher accumulation load from adjacent factories as well as due to the contamination by other sources such as oil refineries, petrochemicals, battery, and cement factories as well as heavy vehicle traffic. The correlation between HM content and soil’s physico-chemical properties is given in (

Table 4. The Pearson correlation matrix for HMs and soil physicochemical characteristics.

	Zn	Pb	Ni	Fe	Cu	Cr	Cd
Sand%	0.486	−0.07	−0.03	0.362	−0.627 *	0.244	0.195
Silt%	−0.544	0.611 *	−0.127	−0.234	0.103	−0.373	−0.194
Clay%	0.326	−0.753 **	0.193	0.016	0.373	0.296	0.099
pH	0.474	−0.527	−0.086	−0.095	0.447	0.462	0.071
EC	−0.486	0.475	0.528	−0.457	−0.452	−0.549	−0.035
O.M%	0.05	−0.119	−0.449	−0.241	0.157	0.307	0.188
CaCO3%	0.126	−0.03	0.357	0.067	−0.266	−0.188	0.02

* Correlation is significant at the 0.05 level. ** Correlation is significant at the 0.01 level.

). Significant negative correlations between the percent of sand and Cu concentration (p > 0.05) were observed. Silt content was positively correlated with Pb (p > 0.05), while clay was negatively correlated with Pb (p > 0.01). Dragović also found silt to be positively correlated (p > 0.01) with concentrations of Pb in soils in the Zlatibor mountains [44]. Soil pH, organic matter, EC, and calcium carbonate in soil showed no significant correlation with HM content in the soil in the study area.

3.2. Indices of Pollution

In this study, the enrichment factor (EF), contamination factor (CF), and pollution load index (PLI) have been applied to assess HM contamination in the soil of the study area. In addition, the bioaccumulation factor (BF) for each plant was applied and investigated in this study.

3.2.1. Enrichment Factor (EF)

The most common indices of pollution are deaccumulation and enrichment factors (EF). The EF was used in this study to differentiate between the metals originating from anthropogenic activities and those from natural processes in order to assess the degree of anthropogenic influence. The results of the calculated EF of HMs in soil samples are shown in

Table 5. Percentage of contaminated samples according to Enrichment factor (EF) of the studied metals in sites (S1–S12).

Enrichment Factor (EF)	Cd	Cr	Cu	Pb	Zn	Ni
Deficiency to minimal enrichment	0	66.6	0	0	8.33	8.33
Moderate enrichment	0	33.4	58.33	8.33	50	33.33
Significant enrichment	0	0	33.34	41.66	33.33	33.33
Very high enrichment	0	0	8.33	33.3	8.33	8.33
Extremely high enrichment	100	0	0	8.33	0	16.66

and

Table 6. Enrichment factor (EF) between the studied metals of the studied metals in sites (S1–S12).

Enrichment Factor (EF)
Soil Sites	S1	S2	S3	S4	S5	S6	S7	S8	S9	S10	S11	S12
Cd	266	2670	405	15,457	1261	2097	7336	596	1003	347	2873	731
Cr	1.5	1.5	1.2	0.7	2	3.8	3.4	0.3	1.4	1.1	0.6	0.2
Cu	4.6	2.7	4.9	24.2	3.3	17.1	12	3.6	3.9	14.1	5.7	3.8
Pb	15.7	18.6	14.1	29.6	6.4	24.6	36.6	13.7	2.6	30.8	46.8	31.1
Zn	6.4	4.7	3.2	26.4	5	9.2	12.3	1.7	3.4	4.4	6.3	4.1
Ni	6.3	4	11.8	105.5	6.6	27.9	48.5	5.9	5.7	16.4	16.9	19.8

. The EF of HMs ranged from 0.20 to 7336. The low values of EF indicate that the enrichment of soils by HMs is due to a natural process while high values indicate enrichment by anthropogenic activities. Based on contamination categories, 100%, 16.6%, and 6.2% of the samples fell under extremely high enrichment for Cd, Ni, and Pb, respectively. Of the soil samples, 33.3% showed very high enrichment for Pb, and 8.3% of soil samples showed very high enrichment for Cu, Zn, and Ni. Across all sites, 33.4% showed moderate Cr enrichment, while 66.6% fell under deficiency to minimal enrichment for Cr. The EF in the soil of the study area was generally very high, which indicates a significant contribution from anthropogenic sources, especially for Cd and Ni, such as from industrials spills [35,45].

3.2.2. Contamination Factor (CF) and Pollution Load Index (PLI)

The CF values were calculated from the concentration of HMs in the soil samples of the study area sites and the normal soil crust for metals introduced by Lindsay (1979) as a background concentration values. The CF can be used to evaluate the levels of contamination of HMs in the soils by comparing it with the background concentrations of metals in the earth’s crust [33].

The range of value of CF for Cd is 18.33–366.70, Cr: 0.01–0.34, Cu: 0.27–0.75, Fe: 0.02–0.17, Pb: 0.34–2.55, Zn: 0.23–0.85 and Ni: 0.54–1.82 (

Table 7. Mean of contamination factor (CF) and pollution load index (PLI) of the studied metals in sites (S1–S12).

Site ID	Contamination Factor (CF)							Pollution Load Index (PLI)
	Cd	Cr	Cu	Fe	Pb	Zn	Ni
S1	28.33	0.16	0.49	0.11	1.67	0.68	0.67	0.78
S2	366.67	0.21	0.37	0.14	2.55	0.65	0.54	1.19
S3	51.67	0.16	0.62	0.13	1.81	0.4	1.5	0.95
S4	266.67	0.01	0.42	0.02	0.51	0.46	1.82	0.52
S5	215	0.34	0.57	0.17	1.09	0.85	1.13	1.33
S6	91.67	0.17	0.75	0.04	1.08	0.4	1.22	0.83
S7	251.67	0.12	0.41	0.03	1.26	0.42	1.66	0.87
S8	98.33	0.05	0.6	0.16	2.26	0.29	0.97	0.83
S9	128.33	0.18	0.5	0.13	0.34	0.43	0.73	0.77
S10	18.33	0.06	0.75	0.05	1.63	0.23	0.86	0.54
S11	138.33	0.03	0.27	0.05	2.26	0.31	0.81	0.60
S12	60	0.02	0.31	0.08	2.55	0.33	1.62	0.62
Range	18.3–366.7	0.01–0.34	0.27–0.75	0.02–0.17	0.34–2.55	0.23–0.85	0.54–1.82	0.52–1.33

). The highest contamination factors are found in site S2 for Cd (CF, 366.7) and Pb (CF, 2.55). The average values of these metals are higher than one (Stevanović et al. 2018), indicating the contamination of soil by these metals. According to Muller (1969), all sites were very polluted in regard to Cd with (CF > 6). The very high values of Cd and Pb could be attributed to the influence of industrial activities taking place at the study area such as disposal of substances containing metals from vehicles batteries, the automotive parts industry, smelting, and so on [36].

The PLI calculated from CF values is given in Table 7. The PLI has been widely used to estimate the relative degree of the pollution level of heavy metals in soils [46,47,48]. It provides a simple comparative means of the level of HMs in the study area, which represents the number of times certain metal content in the soil exceeds the natural background concentration average. The PLI values in this study ranged from 0.52 to 1.33 with a mean value of 0.82 for soil samples collected from the 12 sites. The highest PLI value (1.33) was found in S5 followed by S2 (1.19), with medium contamination of soil by the investigated HMs. The rest of the sites are considered to have low levels of pollution by HMs. On the other hand, it is evident from the results that contamination factors for Cd and Pb were higher, giving rise to a higher PLI value in the study area. The PLI as presented provides a tool for comparison to evaluate site quality: a value of zero indicates perfection, a value equal to one indicates only baseline levels of pollutants are present, and values above one would represent progressive deterioration of the site as found in S5 and S2 [37]. This indicates contamination from the study area activities which include oil refineries, petrochemicals, batteries, and cement factories as well as heavy vehicle traffic.

3.2.3. Heavy Metal Concentration in Plants

The contents of HMs in native plant samples are summarized in

Table 8. Summary of heavy metal contents (mg·kg⁻¹) in native plants (n = 36).

Heavy Metals	Minimum (mg·kg−1)	Maximum (mg·kg−1)	Mean (mg·kg−1)
Zn	6.6	22.1	12.75
Pb	0.7	22.1	5.4
Ni	7.5	28	12.9
Fe	125.9	2308	544.8
Cu	4.0	63	27.6
Cr	1.2	7.8	4.271
Cd	0.2	2.4	1.12

and

Table 9. Mean and SD of heavy metals concentrations (mg·kg⁻¹) in native plants (n = 36).

Plant Species	Mean (SD a)
	Cd	Cr	Cu	Fe	Ni	Pb	Zn
Calotropis procera	1.2 (0.80)	5 (1.41)	n.d.	445.98 (43.17)	15.1 (0.22)	5.5 (0.62)	17.6 (1.61)
Citrullus colocynthis	1.9 (0.22)	4.9 (0.45)	13 (1.41)	629.73 (86.93)	9.7 (1.84)	9.6 (1.81)	10.7 (1.37)
Cassia italica	1.7 (0.22)	7.8 (1.23)	n.d.	578.07 (31.96)	11.8 (2.65)	1.1 (0.65)	6.9 (0.92)
Phragmite australis	0.97 (0.16)	1.2 (0.22)	9.4 (0.78)	379.47 (27.69)	8.7 (1.44)	0.7 (0.33)	12.8 (2.57)
Cyperus laevigatus	2.4 (0.22)	3.2 (0.75)	10.5 (1.22)	171.25 (10.15)	14.5 (1.31)	3 (0.82)	22.1 (1.56)
Argemone mexicana	0.7 (0.14)	5.8 (0.67)	5.8 (2.19)	156.47 (4.94)	13.3 (1.63)	2.3 (0.29)	15.2 (2.62)
Rhazya stricta	1.3 (0.29)	5.3 (0.16)	7.2 (0.11)	125.98 (4.02)	28 (1.08)	22.1 (0.43)	18.9 (0.29)
Conocarpus lancifolius	1.1 (0.22)	2.41 (0.13)	14.13 (0.29)	242.21 (917.18)	11.40 (0.45)	7.51 (1.63)	8.9 (0.29)
Zygophyllum simplex	0.3 (0.11)	3.0 (0.36)	4.76 (0.20)	412.46 (23.17)	7.46 (0.09)	2.71 (0.19)	12.1 (0.22)
Salsola imbricata	0.2 (0.01)	4.1 (0.16)	17.25 (0.33)	543.3 (16.7)	8.8 (0.26)	6.3 (0.28)	6.6 (0.15)
Malva parviflora	1.25 (0.20)	3.2 (0.21)	22.6 (0.49)	2308 (221.5)	12.92 (0.07)	3.3 (0.24)	11.1 (0.62)
Sisymbrium irio	0.46 (0.05)	1.4 (0.14)	14.2 (0.11)	936.8 (18.26)	6.7 (0.12)	5.2 (0.03)	10.1 (0.15)

^a Standard deviation. n.d. Not determined.

and Figure 2 and Figure 3. The concentrations of Cd ranged from 0.2 to 2.4 mg·kg⁻¹, Cr (1.2 to 7.8 mg·kg⁻¹), Cu (4.0 to 6.3 mg·kg⁻¹), Fe (125.9 to 230.0 mg·kg⁻¹), Ni (7.5 to 28.0 mg·kg⁻¹), Pb (0.7 to 22.1 mg·kg⁻¹), and Zn (6.6 to 12.75 mg·kg⁻¹). Plant species that showed the highest concentration of metals were Citrullus Colocynthis (Cu and Ni), Cassia Italica (Cr), Phragmite australis (Ni), Cyperus Laevigatus (Ni), Argemone mexicana, Rhazya stricta (Ni), Conocarpus Lancifolius (Cd), and Sisymbrium irio (Fe). Results showed that the values for Fe and Cu concentrations compared to other HMs were highest in all plant species. Contents of Cd in all plant species ranged from 0.2 to 2.4 mg·kg⁻¹ and the highest value was in Cyperus laevigatus and lowest in Alsola imbricata. Contents of Cd in plant species Calotropis Procera and Citrullus colocynthis were 1.2 and 1.9 mg·kg⁻¹, respectively. These results were similar to those reported by Alyemeni where the average concentrations of Cd were 1.4 and 2.0 mg·kg⁻¹ in Calotropis procera and Citrullus Colocynthis, respectively [15]. These values were higher than the data reported by Cardwell, who found 0.11 to 0.85 mg·kg⁻¹ for 13 plant species from contaminated urban streams from southeast Queensland, Australia [49]. However, the Cd values found were not in the phytotoxic range of 5–700 mg·kg⁻¹ reported by Chaney [50]. Cd contents in normal plants grown in uncontaminated soils usually range from 0.05 to 0.2 mg·kg⁻¹. When the Cd concentration is higher than 2 mg·kg⁻¹, it could cause toxicity to most plant species, adversely affecting the photosynthesis process and inhibiting plant growth and development, thus resulting in plant death. The concentration of Cr ranged from 1.2 to 7.8 mg·kg⁻¹ and was the highest in Cyperus laevigatus and the lowest in Phragmite australis. Cr can cause toxicity in plants when concentrations exceed 2 mg·kg⁻¹ [2,51,52]. Cr in all plants except Phragmite australis and Sisymbrium irio were above the safe limit and could be harmful to the local public as reported by Shah et al. and Lim et al. [53,54]. The concentrations of Pb ranged from 0.7 to 22.1 mg·kg⁻¹ with a maximum in Rhazya stricta and a minimum in Cassia italica. The concentration of Zn ranged from 6.6 to 22.1 mg·kg⁻¹ and was the highest in Cyperus laevigatus and the lowest in Salsola imbricata. Most plants accumulate less than 20 mg·kg⁻¹ of Zn, which is considered to be deficient [53,54,55]. As a result, most plant species in this study were found to be deficient in Zn contents. Considering the maximum acceptable limits of HMs in plants, this study found that native plants have accumulated higher concentrations of the Fe, Cu, Ni, and Pb. Across all sites of the statistical analyses, one-way ANOVA (Figure 3) revealed that accumulation of Cd, Pb, and Ni by Cyperus laevigatus and Cd and Pb accumulation by Citrullus colocynthis were significantly (p < 0.001) higher than other studied species. In addition, Cassia italica showed significant (p < 0.001) uptake for Cr and Cd and Rhazya stricta showed significant (p < 0.001) uptake for Ni, Cr, and Zn. Accumulation of Cu and Fe by Malva parviflora was significantly (p < 0.001) higher compared to other studied species.

3.2.4. Bioaccumulation Factor (BF)

The BF in

Table 10. Bioconcentration factor (BF) of HMs (mg·kg⁻¹) in plants (n = 36) in the study area.

Plant Species	Sites	Bioconcentration Factor (BF)
		Cd	Cr	Cu	Fe	Pb	Zn	Ni
Calotropis procera	S1	0.71	0.32	n.d.	0.11	0.33	0.52	0.57
Citrullus colocynthis	S2	0.09	0.24	1.17	0.12	0.38	0.33	0.45
Cassia italica	S3	0.55	0.5	n.d.	0.12	0.06	0.34	0.20
Phragmite australis	S4	0.06	0.96	0.75	0.58	0.14	0.56	0.12
Cyperus laevigatus	S5	0.19	0.09	0.62	0.03	0.28	0.52	0.32
Argemone mexicana	S6	0.13	0.35	0.26	0.09	0.21	0.76	0.27
Rhazya stricta	S7	0.09	0.45	0.58	0.10	0.60	0.89	0.42
Conocarpus lancifolius	S8	0.19	0.54	0.79	0.04	0.98	0.62	0.29
Zygophyllum simplex	S9	0.04	0.17	0.32	0.08	0.81	0.56	0.25
Salsola imbricata	S10	0.18	0.72	0.77	0.27	0.39	0.57	0.26
Malva parviflora	S11	0.15	1.16	2.76	1.26	0.15	0.73	0.40
Sisymbrium irio	S12	0.13	0.88	1.54	0.30	0.20	0.61	0.10
Range		0.04–0.71	0.09–1.16	0.26–2.76	0.03–1.26	0.06–0.98	0.33–0.89	0.1–0.57

n.d. Not determined.

can be used to estimate the ability of plants to accumulate metals from soils, which is defined as the ratio of metal concentration in plants to that in the soil [37]. The process of phytoextraction generally requires the translocation of HMs to the easily harvestable plant parts, i.e., shoots [56]. The BF values in the current study ranged from 0.04–2.76. Among the 12 native plant species, Malva parviflora growing at S11 had the highest BF value of 2.76 and 1.16 for Cu and Cr, respectively. Several plant species, including Malva parviflora, Sisymbrium irio and Citrullus colocynthis, showed highest BF values in S2, S11, and S12 as well as the highest Cr and Cu uptake, which could indicate the ability of these plant species to accumulate HMs compared to other identified species. In general, the BF for the native plants indicate that some species could be candidates for phytoextraction potential, such as Conocarpus lancifolius for Pb and Malva parviflora for Cu and Cr. Usually, BF values less than one are unsuitable for phytoextraction, and as a result, most of the studied plants were limited as phytoremediators for HMs in contaminated soil [57].

4. Practical Implications

The rapid growth of industrial activities in the major industrial cities of SA has caused an accumulation of pollutants, including HMs. The environments of these cities as well as nearby areas have been affected. There is a lack of active research in SA on the bioremediation of anthropogenically affected areas. It is an urgent need to find solutions for remediating such sites. There is also a lack of active research on finding an indigenous plant species that would be able to accumulate HMs and be applied in the phytoremediation of contaminated sites. Many native plants were found to tolerate and accumulate HMs, and we found that the most promising plant species for phytoextraction and remediation were annuals or perennials such as Malva parviflora, Sisymbrium irio, and Citrullus colocynthis, especially for Cr and Cu. This study suggests that these native plant species may be applied for phytoremediation in the area. This study provides guidance for determining the status of HMs in soils and native plants species in an industrial zone in the industrial city of Riyadh. Further research should be done in other industrial cities in the region with emphasis on identifying plant species that could be used for phytoremediation with the aim of preserving biodiversity.

5. Conclusions

This study was conducted to determine HM contents in soil and in the second industrial city zone in Riyadh city, SA as well as to assess the native plants growing in the area and their potential use for remediating sites contaminated by HMs in the region. Th Indices of metal pollution (EF and CF) used in study indicate that the investigated area was highly polluted by Cd and Pb as well as slightly polluted by Ni and Zn. This could be due to the contamination generated from manufacturing activities in the study area, which include smelting, metal, chemicals, electroplating, energy, fuel production, and cement factories and industries, in addition to heavy traffic flow, where the assessed sites are located in a dense industrial zone. The release of HMs by various industrial activities is a significant reason for soil pollution by HMs. As the study area has experienced quick development and industrialization over the past decades, the risk of pollution by HMs has also become gradually prominent. In order to decrease hazards of HMs to health of local inhabitants, phytoremediation can be adapted to clean up HM contamination sites. Using hyperaccumulator native plants will be essential for preventing pollution of the environment. This requires appropriate approaches to be used to protect the inhabitants and ecosystem that are in the vicinity of these contaminated sites in addition to implementation of an efficient remediation method to reduce contamination levels and minimize health and environmental risks. According to the results of the current study, the most promising species for phytoextraction and remediation were annuals or perennials such as Malva parviflora, Sisymbrium irio, and Citrullus colocynthis, especially for Cr and Cu. These native plant species can be used for phytoremediation of HM contaminated sites.