Assessment of Heavy Metals in Greenhouse Cultivated Soils, Northern Jordan

Abstract

Jordan has recently observed a gradual shift in vegetable production from open-fields to greenhouses with mounting consumer concerns about food quality and safety. We investigated heavy metals in soil collected from greenhouse vegetable production area in northern Jordan. Sixty-one surface soil samples were collected, of which forty-seven from plastic-covered greenhouses and fourteen were sampled from the adjacent open-field land, with both designated for vegetable production. The average concentrations of Cr, Cu, Cd, Pb, Ni, Zn were 26.1, 26.8, 0.81, 53.0, 49.3, 139.1 mg/kg, and 19.1, 19.3, 0.66, 49.7, 46.7, 104.9 mg/kg for greenhouse and open-field soils, respectively. While the accumulation of heavy metals was consistently higher in greenhouse than in open-fields, both soils revealed a similar metal ranking with a few exceptions. Greenhouse soils revealed relatively lower pH values with higher variabilities. In greenhouse cultivated soils, CaCO3 content averaged 21.4% compared to 23% measured in open-field soils. Soil salinity showed greater values for greenhouse samples (averaging 1118.6 μs/cm) than those observed in open-field agricultural soils (a mean of 503.6 μs/cm). The soil organic matter (TOM) exhibited values in the range of 1.06-3.35% relative to 0.59-2.41% found in open-field area. The spatial distribution of heavy metal concentrations for greenhouse soils revealed higher levels in the northern soils, whereas the least was found in the southern sampling points. The Enrichment results showed 23.4% of sampling sites were moderately contaminated with Pb, and 38.3% were moderately contaminated with Cd, of which 8.5% indicating moderately severe contamination. The Igeo results indicate 25.5% of greenhouse soils were moderately contaminated with Pb and 38.3% were heavily polluted with Cd. The contamination factors showed 25.5% and 38.3% of greenhouse sampling soils were considerably contaminated with Pb and Cd, respectively. 2% indicate very high contamination for Cd and 2% showed considerable contamination for Zn. PLI indicates that only two sampling sites are polluted. The ecological risk assessment showed low Ei values for all heavy metals suggesting slight risks, except for Cd which indicate strong risk. Total potential ecological risks values showed low risk to the local environment. Cd accounts for most of the total risks (72.27-82.67%) followed by Pb (11.49-14.87%). Some greenhouse soils were non-compliant with soil quality standards especially for Ni, Cd, and Pb. The observed levels of heavy metals are attributable to agricultural activities including long-term application of pesticides, phosphatic and nitrogen fertilizers, sewage sludge, wastewater irrigation and chicken manure in addition to industrial dust and traffic related emissions.

Full text

Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Pol. J. Environ. Stud. Vol. 33, No. 1 (2024), 1-15
Original Research
Assessment of Heavy Metals in Greenhouse
Cultivated Soils, Northern Jordan
Abeer A. Al-Hamad1*, Ahmed A. Al-Taani1, 2, Habes Ghrefat1,
Mohammad Khawajah1, Abeer Zoubi1
1Department of Earth and Environmental Sciences, Faculty of Science, Yarmouk University,
P.O Box 566 ZipCode 21163, Irbid, Jordan
2Department of Life and Environmental Sciences, College of Natural and Health Sciences, Zayed University,
P.O. Box 144534, Abu Dhabi, United Arab Emirates
Received: 28 May 2023
Accepted: 25 August 2023
Abstract
Jordan has recently observed a gradual shift in vegetable production from open-elds to greenhouses
with mounting consumer concerns about food quality and safety. We investigated heavy metals in
soil collected from greenhouse vegetable production area in northern Jordan. Sixty-one surface soil
samples were collected, of which forty-seven from plastic-covered greenhouses and fourteen were
sampled from the adjacent open-eld land, with both designated for vegetable production. The average
concentrations of Cr, Cu, Cd, Pb, Ni, Zn were 26.1, 26.8, 0.81, 53.0, 49.3, 139.1 mg/kg, and 19.1, 19.3,
0.66, 49.7, 46.7, 104.9 mg/kg for greenhouse and open-eld soils, respectively. While the accumulation
of heavy metals was consistently higher in greenhouse than in open-elds, both soils revealed a similar
metal ranking with a few exceptions. Greenhouse soils revealed relatively lower pH values with higher
variabilities. In greenhouse cultivated soils, CaCO3 content averaged 21.4% compared to 23% measu red
in open-eld soils. Soil salinity showed greater values for greenhouse samples (averaging 1118.6 µs/cm)
than those observed in open-eld agricultural soils (a mean of 503.6 µs/cm). The soil organic matter
(TOM) exhibited values in the range of 1.06-3.35% relative to 0.59-2.41% found in open-eld area.
The spatial distribution of heavy metal concentrations for greenhouse soils revealed higher levels
in the northern soils, whereas the least was found in the southern sampling points. The Enrichment
results showed 23.4% of sampling sites were moderately contaminated with Pb, and 38.3% were
moderately contaminated with Cd, of which 8.5% indicating moderately severe contamination.
The Igeo results indicate 25.5% of greenhouse soils were moderately contaminated with Pb and 38.3%
were heavily polluted with Cd. The contamination factors showed 25.5% and 38.3% of greenhouse
sampling soils were considerably contaminated with Pb and Cd, respectively. 2% indicate ver y high
contamination for Cd and 2% showed considerable contamination for Zn. PLI indicates that only two
sampling sites are polluted. The ecological risk assessment showed low Ei values for all heavy metals
suggesting slight risks, except for Cd which indicate strong risk. Total potential ecological risks values
DOI: 10.15244/pjoes/171558 ONLINE PUBLICATION DATE:
*e-mail: abeer.h@yu.edu.jo

Al-Hamad A.A., et al.
2
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Introduction
Heavy metals are ubiquitous and persistent in the
soil environment [1]. Major sources of heavy metals in
soils are organic and inorganic fertilizers, pesticides, in
addition to sources such as industries, mining, irrigation
water and atmospheric deposition [2-4]. Agricultural soil
contamination has a negative effect on soil functions,
plants, environment, food quality, and human health
[5-10].
Greenhouse vegetable cultivation is widely applied
in off-seasons production in many countries around the
globe to meet the growing demands of vegetables while
improving yield and reducing environmental impact
and production cost [11, 12]. Relative to open-eld
cultivation, greenhouses are intensive, multi-cropping
way of food production which involve excessive use of
fertilizers, pesticides and irrigation water that may cause
soil salination and acidication, nutrient imbalance,
and heavy metal accumulation [13-16]. Acidication of
greenhouse soils affects the mobility of heavy metals
and accelerates their leaching to groundwater and
increases their uptake by crops [17]. Animal manure is
often used as organic fertilizers to increase soil organic
matter, nutrient availability, cation exchange capacity
and water holding capacity of soil [18], however, manure
application is an important source of heavy metals in
soil [19, 20]. Production of vegetables in greenhouses
requires different types of fertilizers including water-
soluble fertilizer, cattle manure, organic fertilizers,
compound fertilizers, chemical fertilizers, and bacterial
manure, leasing to variations in heavy metal pollution
[21]. Sewage sludge and fertilizer are important sources
of heavy metals [22-24].
In recent years, Jordan has observed a gradual
shift in vegetable production from open elds to
greenhouses. For example, the plastic-covered
vegetables greenhouse accounted for 17.9% of the total
vegetable cultivated lands in 2017 which has risen to
18.5% in 2018 and to about 19.2% in 2019 [25-27]. This
is primarily triggered by increasing demand for food
in response to the large population growth (especially
due to uxes of Syrian refugees) and higher net prot
margins. Greenhouses in Jordan are simple tunnels
covered with polyethylene plastic sheets, most of which
are constructed in Jordan Valley (southwest) and in the
northern highlands where the majority of fertile arable
elds are located.
Excessive use of agrochemicals (including fertilizers
and pesticides), animal manure and irrigation water
(often treated wastewater) are common practices in
greenhouse vegetable production in Jordan. These
unsafe farming practices are largely driven by a lack of
knowledge of health implications among farmers.
As such, consumer concerns are mounting in
recent years about food quality and safety. Previous
studies found eutrophicated greenhouse soils that are
also contaminated with heavy metals. Assessing the
potential ecological risk of heavy metals associated with
greenhouse cultivation in relation to soil properties is
necessary to develop sustainable greenhouses while
minimizing environmental impact [28]. There are
currently no published studies about heavy metal
contamination of soils in greenhouse vegetable growing
regions of Jordan. This study aims to measure the
concentration of heavy metals (Cd, Cr, Cu, Ni, Zn,
and Pb) in soils in an important greenhouse vegetable
production area in northern Jordan and identify soil
properties that may contribute to the observed heavy
metal levels. It also intends to assess the potential risk
and sources based on a variety of widely used pollution
and ecological risk indices.
The Study Area (Location, Geology, and Soil)
The study was performed in greenhouse vegetable
cultivation area (170 Km2) located in the fertile at
lands of Ramtha district, northern Jordan. The soil
sampling points were selected in the area between the
city of Ramtha and At-Turrah to the east, and the city
of Irbid, Huwwarah and Wadi shallala to the west with
Huwwarah highway bordering the area from the south
(Fig.1). The study area is dominated by mid-latitude
dry semiarid (Steppe) climate where evapotranspiration
exceeds precipitation. July is the warmest month, with
an average high temperature of 33ºC and the coldest is
January, with a mean high temperature of 14ºC. The
annual rate of precipitation is about 250 mm with the
largest amounts occur ring in December, January, and
February, peaking in January. The relative humidity is
highest in February (70%), and lowest in May (35%)
[29]. The geology of the study area shown in Fig. 1 is
characterized by sedimentary rocks deposited in warm
shallow marine environment. All formations belong to
Belqa group which is composed of (1) Muwaqqar chalk
showed low risk to the local environment. Cd accounts for most of the total risks (72.27-82.67%)
followed by Pb (11.49-14.87%). Some greenhouse soils were non-compliant with soil quality standards
especially for Ni, Cd, and Pb. The observed levels of heavy metals are attributable to agricultural
activities including long-term application of pesticides, phosphatic and nitrogen fertilizers, sewage
sludge, wastewater irrigation and chicken manure in addition to industrial dust and trafc related
emissions.
Keywords: heavy metals, greenhouse soils, pollution indices, Jordan

Assessment of Heavy Metals in Greenhouse... 3
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
marl formation, which consists of fossil rich rocks of
soft chalk, chalky limestone, and clayey marl with hard
limestone concretions, (2) Umm Rijam chert limestone
formation of chalky, marly and kerogen limestones in
addition to beds and concretions of chert, and (3) Wadi
Shallala chalk formation that is made up of massive
grey-white chalk found to the north of Wadi Shallala
and Shajara-Turrah area [30, 31]. Pleistocene-Recent
sediments are found as soil and Pleistocene gravel.
The study area is an agriculturally important region
containing wide ranges of soil types, reecting different
physical characteristics. Vertisols and Inseptisols of
Xerochrepts, Chromoxererts and Calcixerollic are the
major soil great groups, covering 4.31% of Jordan [32,
33] (Fig. 1). Soils of this region are mainly clay with high
cation exchange capacity and high carbonate content
and are considered as the most productive rainfed soils
in Jordan [34].
The study area is intensively cultivated with rainfed
agriculture as the main land use. It hosts a variety of
Fig. 1. Location map of the study area showing (A) the geological settings, (B) the soil types, and (C) the soil sampling points.

Al-Hamad A.A., et al.
4
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
industrial activities as well. According to the Irbid
Agricultural Directorate survey [29] the actual cultivated
land in Ramtha district is 137,242 donum (1 donum
= 1000 m2) out of a total arable land of 233,633 donum,
of which 42,550 donum are planted with olives and fruit
trees, 49,105 donum with summer and winter vegetables,
and 36,845 donum used to produce winter eld cereal
crops (wheat, barley, lentils, and broad beans). Fertile
plains occupy a large percentage of the study area. This
region has historically served as the nation’s breadbasket
but has been encroached by urbanization [35].
Due to the scarcity of freshwater resources in Jordan
and particularly in this region, agriculture relies mainly
on highly variable rainwater which affects production
and yields of the rainfed lands, livestock, and irrigated
crops in Ramtha area. The agricultural sector adopted
several strategies to control agricultural practices
in terms of irrigation methods through greenhouse
vegetable cultivation, which brought nancial
and economic security to farmers of this region.
The number of greenhouses in Ramtha is 11650, with a
total cultivated area of about 5825 donum.
Materials and Methods
Sixty-one composite top-soil samples (0-20 cm)
were obtained from the study area during the
vegetable cultivation season in October 2022 (Fig. 1),
of which forty-seven were collected from plastic-
covered greenhouse area and fourteen were sampled
from the adjacent open-eld land, with both are
designated for vegetable production. A GPS global
position system (GARMEN) was used to obtain the
coordinates of soil sampling points. During the time
of sample collection, the greenhouses were cultivated
with tomato, cucumber, green beans, bell paper, lettuce,
and strawberry. Each composite soil sample collected
represents a mixture of three samples (200 g each) from
greenhouse group cultivated with the same crop under
the same agricultural conditions.
The samples were air-dried, hand-crushed, well-
mixed, and sieved through a 2 mm sieve, and were
stored in polyethylene plastic bags for chemical
analyses. Heavy metal concentration (Cd, Cr, Cu, Zn,
Ni, Pb) was measured as follows: 1 g of sieved soil
fractions were digested with 4ml HNO3, 4 ml HCl
and 2 ml HF. After heating, the samples were ltered
through a Whatman lter paper (no. 42), and the digest
was diluted to 50 ml with deionized water and analyzed
using novAA 800 D-Flame- and Graphite Furnace
AAS. The instrument was calibrated using a multi-
element stack solution (1000 ppm) for the preparation of
standard solutions (0, 2, 4, 8, and 12 ppm). The accuracy
of the instrument was represented by a linear calibration
curve of R2˃0.99. Instrumental precision was veried
by testing the concentration of the standard solutions
after every ten samples. To ensure data quality triplicate
sample, deionized water, and blank sample analysis
were performed. Soil pH and electrical conductivity
(EC) was measured for a soil/water suspension (1w:5v)
using a digital calibrated pH and conductivity meters.
Soil organic matter was determined by oxidation
method according to Walkley and Black [36], Loring
and Rantala [37], using potassium dichromate (K2Cr2O7)
and sulfuric acid (H2SO4). The CaCO3 soil content was
determined using the calcimeter in which the volume of
CO2 released from the sample is measured relative to the
volume released from a similar weight of pure CaCO3
(standard). Microsoft Excel was used for statistical
calculations and performing Spearman’s correlation
coefcients. ArcGIS 10.3 software was used to generate
the location map.
The assessment of heavy metal concentrations was
performed by calculating the contamination levels and
degree of pollution using variable pollution indices, as
follows:
Enrichment factor (EF) is used to evaluate the
contamination level of heavy metals using the equation
[38]
EF = (M/Fe) sample/ (M/Fe) backgrou nd
Where (M/Fe)sample is the ratio of metal to Fe
concentrations in the sample and (M/Fe)background is the
ratio of metal to Fe concentrations in the background.
The background metal concentrations in the present
study are determined using the Turekian and Wedepohl
[39] crustal shale background concentrations.
Enrichment factor classication is listed in Table 1.
Geo-accumulation index (Ige o) is widely used for
the evaluation of contamination levels derived from
anthropogenic activities using the equation [40]:








=
B n
Cn
Log
Igeo 1.5
2
Where Cn represents metal contents in the soil, Bn the
geochemical background value in shale [39], and 1.5 is a
factor used for possible changes in the background data
due to lithological variations. The Igeo contamination
categories are represented in Table 1.
Contamination Factor (CF) was calculated using
the following equation [41]:
CF = Ci/Ci
n
Where (Ci) is the concentration of metal in the
studded soil and (Ci
n) is the crustal shale background
value of the metal. Categories of contamination factor
are listed in Table 1.
Pollution load index (PLI) was calculated using
the (CF) of each heavy metal according to the following
equation [42]:

Assessment of Heavy Metals in Greenhouse... 5
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Where (Ei) is the individual ecological risk factor,
(Ti) is the toxic-response factor for heavy metals
(Cd = 30, Cu = Pb = Ni = 5, Cr = 2, Zn = 1), (Ci) is
the metal concentration in the studied soil samples,
and (Bi) is the shale background metal concentration.
The categories of individual potential ecological risk
(Ei), and total ecological risk index (RI) are represented
in Table 1.
PLI = (CF1 × CF2 × . . . × CFn) 1/n
where (n) is the number of heavy metals measured in the
current study. The (PLI) contamination categories are
represented in Table 1.
Total potential ecological risk index (RI) is
calculated by using the equation [41]:
RI = ∑ Ei
Ei = Ti × (Ci/Bi)
Index Category Contamination level
Enrichment factors (EF)
<1 None
1-3 Minor
3-5 Moderate
5-10 Moderately severe
10-25 Severe
25-50 Very severe
>50 Extremely severe
Contamination factors (CF)
< 1 Low contamination
1-3 Moderate contamination
3-6 Considerable contamination
>6 Very high contamination
Pollution load Index (PLI)
<1 No pollution
= 1 Baseline level
>1 Elevated pollution
Geo-accumulation Index (Igeo)
Igeo≤0 Uncontaminated
0<Igeo<1 Uncontaminated / moderately contaminated
1<Igeo<2 Moderately contaminated
2<Igeo<3 Moderately / strongly contaminated
3<Igeo<4 Strongly contaminated
4<Igeo<5 Strongly / extremely contaminated
5<Igeo Extremely contaminated
Individual ecological risk factor (Ei)
Ei<30 slight risk
30≤Ei<60 Medium risk
60≤Ei<120 Strong risk
120≤Ei<240 Very strong risk
Ei ≥ 240 Extremely strong risk
Total potential ecological risk (RI)
RI<150 Low risk
150≤RI<300 Moderate risk
300≤RI<600 Severe risk
RI≥600 Serious risk
Table 1. Classication of soils based on different pollution indices.

Al-Hamad A.A., et al.
6
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Results and Discussion
Summary statistics of heavy metals and soil
properties for 47 greenhouse samples and 14 open-
eld agricultural land samples are tabulated in Table 2.
The concentrations of Cr, Cu, Cd, Pb, Ni and Zn
ranged from 7.4-59.5, 17.9-51.7, 0.0-2.2, 33.4-71.1,
32.2-69.23, 90.5-318.3 mg/kg for greenhouse soils and
from 5.7-40.6, 11.9-27.8, 0-2, 26.5-67.7, 30.7-69, 56.1-
151.2 for open-eld soils (Table 2). Based on heavy
metal abundance, both soils revealed a similar ranking
with few exceptions. The greenhouse soil showed the
descending order Zn>Pb>Ni>Cu>Cr>Cd and open-
eld soil follow the ranking Zn>Pb>Ni>Cr>Cu>Cd.
However, the accumulation of heavy metals was
consistently higher in greenhouse than in open-elds.
The average concentrations of Cr, Cu, Cd, Pb, Ni and
Zn were 26.1, 26.8, 0.81, 53.0, 49.3 and 139.1 mg/kg 19.1,
19.3, 0.66, 49.7, 46.7 and 104.9 for greenhouse and open-
eld soils, respectively (Table 2).
The pH values for greenhouse soil samples range
from moderately acidic (5.47) to moderately alkaline
(7.94) with an average of 6.86 indicating a generally
slightly acidic soil (with low coefcient of variation
(CV = 9.56)). Whereas open-eld soils demonstrated
pH levels that varied from 6.2-7.93 with a mean value of
7.26. Greenhouse soils revealed relatively lower average
pH value with higher variabilities. The pH is one of the
most important soil parameters controlling heavy metal
adsorption, availability, and uptake by plants [43-45].
While several studies have reported a signicant decline
in soil pH [46, 47], in this study minor decreases in pH
values were observed for greenhouse compared to open-
eld top-soils. This suggests that the intensive cultivation
practices probably have small impact on pH values and
consequently on the observed heavy metals contents.
While the variability of soil pH can be linked to
the use of agrochemicals (fertilizers and pesticides),
manure, organic fertilizers, a signicant contributor
to pH values is the geology of the study area with
abundance of carbonate rocks (Fig. 1). Both soils appear
to be of relatively higher buffering capacity, due to high
concentrations of CaCO3. In greenhouse cultivated soils,
CaCO3 content ranged from 15% to 39% with an average
amount of 21.4%, compared to 12.4-39% measured in
open-eld soils and a mean amount of 23% (Table 2).
Open-eld soils are highly exposed to atmospheric
deposition of mineral dust containing CaCO3, where
higher average has been observed.
The greenhouse cultivation in the study area is
limited to the summer season. The unsustainable
agricultural practices in greenhouses, of intensive use
of agrochemicals, manure, and irrigation water, where
treated wastewater is an important source of irrigation
water, may cause soil nutrient imbalances and heavy
metals accumulation [16]. By the end of the growing
season, plastics covering greenhouses are dismantled
and removed, where soils are exposed to the ambient
environment for the rest of year, especially windblown
dust containing CaCO3, salts and heavy metals, among
others [48, 49].
Soil salinity (EC) revealed relatively greater values
for greenhouse samples (averaging 1118.6 µs/cm) than
those observed in open-eld agricultural soils (with
a mean of 503.6 µs/cm). These average values indicate
non-saline soils. However, in some locations, greenhouse
soil salinity levels demonstrated weakly saline soils,
with a maximum value observed in greenhouse was
3170 µs/cm compared to 1261 µs/cm in open-eld soils
(Table 2). The highest EC value measured in site 2
(greenhouse) is largely attributed to the irrigation
treated wastewater where this site is close to Ramtha
wastewater treatment plant (Fig. 1). In addition to the
excessive use of fertilizers and pesticides are sources of
salinity to soils [50].
The soil organic matter (TOM) shows values in the
range of 1.06 to 3.35% with an average of 1.87% relative
to 0.59-2.41% found for open-eld area. About 50%
of the greenhouse soil samples are within the medium
organic matter category [51]. The TOM is linked
to decomposition of plant residues in greenhouses
and use of organic fertilizers. Soil organic matter has
Soil type pH
EC TOM CaCO3Cr Cu Cd Pb Ni Zn
µs/cm % mg/kg
Greenhouse soil
(47 samples)
Mean 6.86 1118.6 1.87 21.4 26.1 26.8 0.81 53.0 49.3 139.1
Min 5.47 405 1.06 15.1 7.4 17.9 0.0 33.4 32.2 90.5
Max 7.94 3170 3.35 39 59.5 51.7 2.2 71.1 69.23 318.3
SD 0.6 764.5 0.46 5.7 16.2 8.6 0.5 9.8 11.8 47
Open-eld
agricultural soil
(14 samples)
Mean 7.26 503.6 1.68 23.0 19.1 19.3 0.66 49.7 46.7 104.9
Min 6.2 138 0.59 12.4 5.7 11.9 0.00 26.5 30.7 56.1
Max 7.93 1261 2.41 39 40.6 27.8 2.0 67.7 69.0 151.2
SD 0.4 404.1 0.56 7.1 12.1 4.5 0.7 11.7 13.25 23.9
Table 2. Summary statistics of the chemical parameters and selected heavy metals of soil samples collected from greenhouses and open-
elds in the study area.

Assessment of Heavy Metals in Greenhouse... 7
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
been reported to affect the heavy metals mobility
and availability [52-54]. The increasing soil organic
matter may reduce availability of heavy metals within
the organic fraction of the soil and lower the risk of
adsorption by plants [55, 56]. Despite the relatively
higher content of TOM in greenhouse soils compared to
open-eld lands, this is generally lower than expected.
The relative low TOM content for greenhouse soils is
likely related to the use of chicken manure along with
plant residues [57]. Liu et al. [57] observed low soil
organic matter for greenhouse soils of about 1% in the
topsoil that raises nutrient leaching due to decreases in
the retention capacity of soil for nutrients.
For better characterization of heavy metals
distribution, the greenhouse soils were grouped into
3 clusters (Fig. 1). Data tabulated in Table 3 show the
average values of heavy metals for the three clusters,
where cluster 1 includes samples from the southern
area (1-25), cluster 2 contains samples from 26 to
35 located in central part of study area, and cluster 3 in
the northern area which encompasses samples 36-47.
The spatial distribution of heavy metal concentrations
for greenhouses soils revealed the following ranking of
metals for cluster 1 Zn˃Pb˃Ni˃Cu˃Cr˃Cd with average
concentrations of 127.30, 52.82, 39.36, 22.54, 13.26,
and 0.65 mg/kg respectively. The highest variability of
distribution was observed for Cd (0-2.2 mg/kg) with
a coefcient of variation exceeding 50% (57.88%).
Cluster 2 exhibited a slightly different descending
order Zn˃Ni˃Pb˃Cr˃ Cu˃Cd with the average values
of 149.03, 57.35, 54.30, 31.53, 28.34, and 0.71 mg/kg,
respectively. The highest variability of distribution
of heavy metal concentration in this cluster is also for
Cd (CV = 72.85%). For cluster 3, heavy metal contents
follow the ranking of Zn˃Ni˃Pb ˃Cu=Cr˃Cd with mean
amounts of 156.30, 60.83, 57.47, 33.09, 33.06, and 0.75
mg/kg and highest variability of distribution observed
for Cd (CV = 61.79%).
In all clusters, Zn was the most abundant heavy
metal in soils whereas Cd was consistently the least.
Cluster 3 showed the highest contents of heavy metals,
whereas cluster 1 had the lowest averages of metals. Cd
appeared to be the highest variable in greenhouse soils
for all clusters, while Ni showed the least variations.
Cluster 1 showed the lowest contents of heavy metals
with identically a similar order of metals to that of open-
eld soils (Table 2 and Table 3). Relatively lower Cr and
Ni values were observed for cluster 1 compared to open-
eld soils.
Spearman’s correlation coefcients were calculated
for the metals determined in the greenhouse soils
(Table 4). The results showed strong correlations
between the following pairs of metals Ni-Cr, Pb-
Cd and Zn-Cu (coefcient>0.5), positively moderate
correlations were also observed between Ni-Cu, and
low correlations were found between Pb-Ni, Pb-Cr
and Ni-Zn. Associations among Ni-Cr, Pb-Cd, Zn-Cu
and Ni-Cu suggest that they may have originated from
similar sources. It should be noted that soil heavy metal
concentrations did not correlate well with any of the
greenhouse soil parameters. The soil pH was negatively
and weakly correlated with all heavy metals. Similar
Soil type
Cr Cu Cd Pb Ni Zn
mg/kg
Greenhouse
soils
Cluster 1
Mean 13.26 22.54 0.65 52.82 39.36 127.30
Min 7.44 17.94 0 37.4 32.16 90.45
Max 24.09 37.67 2.2 71.1 50.56 196.6
STD 5.59 5.81 0.55 9.01 5.45 34.61
CV (%) 42.17 25.77 57.88 17.06 13.86 27.19
Cluster 2
Mean 31.5328.34 0.71 54.30 57.35 149.03
Min 26.11 273 0 33.4 43.71 100.6
Max 59.5 43.38 1.69 69.2 69.28 235.9
STD 12.78 7.17 0.54 12.53 8.71 40.52
CV (%) 27.47 25.31 72.85 22.26 15.18 27.19
Cluster 3
Mean 33.06 33.09 0.75 50.47 60.83 156.30
Min 16.62 20.89 0 35.1 49.4 91.41
Max 51.93 51.65 1.24 66.1 68.51 318.3
STD 10.72 10.11 0.35 9.36 5.08 69.18
CV (%) 32.42 30.55 61.79 18.54 8.36 44.26
Table 3. Heavy metal concentrations for collected soil samples from plastic greenhouse soils (cluster 1, cluster 2, cluster 3) in the study
area.

Al-Hamad A.A., et al.
8
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
observations were reported by Kim et al. [58] and Zhang
et al. [59] for Cu, Ni, Pb, and Zn availability.
Soil pollution indices are tabulated in Table 5. While
the average values of pollution indicators revealed
broadly uncontaminated-moderately contaminated
soils, the greenhouse exhibited slightly higher
contamination degrees relative to open-eld soils.
All EF averages showed values less than 3, indicating
a minor contamination of these metals. The EF results
showed that 23.4% sampling sites had EF values above 3
(moderate contamination) for Pb, and only 5.3% for Zn.
Whereas 38.3% of sampling points exceeded EF value
of 3 for Cd, of which 8.5% were above 5 indicating
moderately severe contamination. Greenhouse soils
exhibited considerable enrichment for Cd. A widespread
Cd pollution in greenhouse soils was reported in Wuwei
(China) and Çanakkale (Turkey) [16, 60].
Based on the average Igeo values, greenhouse
soils appear to be mostly unpolluted to moderately
polluted (Igeo values<1). Cr, Ni and Cu are categorized
as unpolluted, whereas the remaining heavy metals
indicate unpolluted-moderately polluted soils. Around
25.5% of greenhouse soils showed Igeo values above 1
for Pb, and 38.3% for Cd (with one sample exceeding 2),
and only one sample exceeded 1 for Zn. These results
indicate that some soil sampling points were moderately
(Pb and Zn) to heavily (Cd) polluted, where greenhouse
cultivation is more intensive in these points resulting in
increased Cd, Pb, and Zn accumulation.
The CF exhibited moderate contamination (Pb, Cd
and Zn) and low contamination (for Cr, Ni and Cu).
However, 25.5% of greenhouse sampling soils revealed
CF values above 3 (considerable contamination) for
Pb, 38.3% above 3 for Cd, of which 2% indicate very
high contamination (site 16) and only 2 % showed
considerable contamination for Zn. PLI indicates that
only two sampling sites (31 and 33) are polluted as the
PLI values are greater than 1. The remaining greenhouse
soils showed varying degrees of PLI values but below 1.
The ecological risk assessment showed low Ei
values for all heavy metals (below 30) indicating
slight risks, except for Cd (Table 5). Heavy metals
ranked in the following order: Cd>Pb>Ni>Cu>Zn>Cr.
The average Ei values for Cd indicate strong risk
(Ei = 80.79) (Table 5). Based on Ei values for Cd, about
29.8% of greenhouse soils are of medium risk for Cd,
34% with strong risk and 23.4% showed a very strong
risk for Cd. Cadmium has a higher ecological risk than
other heavy metals in greenhouse soils [61]. The results
suggest that greenhouse soils are at a greater risk of Cd
contamination than open eld soils, which are consistent
with others [60].
Total potential ecological risks values showed low
risk (100.82) to the local environment. About 17% of
soil sampling locations in greenhouse revealed very
strong risk with RI above 150. All clusters revealed
low ecological risks, in which cluster 1 showed the
highest potential ecological risk value and cluster 3 had
the lowest (77.3) (Table 5). The percent contribution
of individual heavy metal to overall RI is presented
in Fig. 2, which reveals that Cd accounts for most of
Table 4. Spearman correlation among heavy metals in greenhouse
soils of the study area.
Cu Cd Pb Ni Zn
Cr 0.000 -0.260 0.220 0.841 0.075
Cu -0.114 0.034 0.491 0.528
Cd 0.568 -0.073 -0.050
Pb 0.218 0.003
Ni 0.324
Fig. 2. The percentage of heavy metals individual ecological risk (Ei) to the total potential ecological risk (RI).

Assessment of Heavy Metals in Greenhouse... 9
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Pb Cd Zn Cr Ni Cu RI PLI
EF Igeo CF Ei EF Igeo CF Ei EF Igeo CF Ei EF Igeo CF Ei EF Igeo CF Ei EF Igeo CF Ei
Greenhouse
(all)
Mean 2.45 0.8 2.48 12.4 2.65 0.87 2.69 80.79 1.29 -0.1 1.28 1.28 0.22 -2.66 0.22 0.43 0.68 -1.09 0.68 3.39 0.51 -1.4 0.51 2.53 100.82 0.2
Min 0 0.15 0 0 0 -0.36 0 0 0 -0.66 0 0 0 -4.18 0 0 0 -1.67 0 0 0 -1.91 0 0 3.79 0
Max 3.89 1.25 3.56 17.78 7.23 2.29 7.33 220 3.59 1.16 3.35 3.35 0.82 -1.18 0.66 1.32 1.44 -0.56 1.02 5.09 1.57 -0.39 1.15 5.74 244.8 1.33
STD 0.83 0.28 0.81 4.05 1.75 0.71 1.74 52.07 0.77 0.42 0.68 0.68 0.21 0.97 0.2 0.4 0.29 0.35 0.25 1.23 0.32 0.42 0.28 1.39 54.71 0.31
Cluster 1
Mean 2.7 0.8 2.64 13.21 3.19 1.14 3.17 95.04 1.22 -0.21 1.18 1.18 0.1 -3.47 0.1 0.2 0.52 -1.39 0.51 2.55 0.41 -1.62 0.4 2 114.17 0.07
Min 1.94 0.32 1.87 9.35 0 -0.17 0 0 0 -0.66 0 0 0 -4.18 0 0 0 -1.67 0 0 0 -1.91 0 0 12.54 0
Max 3.89 1.25 3.56 17.78 7.23 2.29 7.33 220 2.18 0.46 2.07 2.07 0.28 -2.49 0.27 0.54 0.74 -1.01 0.74 3.72 0.88 -0.84 0.84 4.19 244.8 0.43
STD 0.51 0.25 0.45 2.25 1.83 0.64 1.83 55.01 0.62 0.37 0.56 0.56 0.09 0.6 0.09 0.17 0.21 0.2 0.21 1.03 0.25 0.33 0.23 1.17 57.31 0.11
Cluster 1
Mean 2.16 0.87 2.53 12.67 2.08 0.91 2.46 73.9 1.23 0.02 1.41 1.41 0.3 -1.59 0.36 0.72 0.73 -0.85 0.84 4.22 0.49 -1.29 0.57 2.83 95.75 0.49
Min 0 0.15 0 0 0 -0.03 0 0 0 -0.5 0 0 0 -2.37 0 0 0.64 -1.22 0.64 3.21 0 -1.7 0 0 3.79 0
Max 2.9 1.21 3.46 17.3 4.99 1.91 5.63 169 2.34 0.73 2.48 2.48 0.55 -1.18 0.66 1.32 0.84 -0.56 1.02 5.09 0.91 -0.64 0.96 4.82 194.29 1.33
STD 0.88 0.37 1.07 5.34 1.52 0.65 1.79 53.83 0.6 0.37 0.64 0.64 0.22 0.45 0.28 0.55 0.06 0.23 0.13 0.64 0.23 0.34 0.25 1.25 59.35 0.52
Cluster 1
Mean 2.16 0.68 1.99 9.97 2.07 0.34 1.92 57.45 1.51 0.03 1.35 1.35 0.39 -2.1 0.34 0.67 1 -0.76 0.89 4.45 0.76 -1.07 0.68 3.39 77.29 0.22
Min 0 0.23 0 0 0 -0.36 0 0 0 -0.64 0 0 0 -3.02 0 0 0.67 -1.05 0.73 3.63 0 -1.69 0 0 8.31 0
Max 3.82 1.07 3.15 15.75 5.88 1.46 4.13 124 3.59 1.16 3.35 3.35 0.82 -1.38 0.58 1.15 1.44 -0.57 1.01 5.04 1.57 -0.39 1.15 5.74 146.46 0.74
STD 1.24 0.24 1.05 5.25 1.53 0.67 1.23 36.77 1.19 0.57 0.96 0.96 0.25 0.5 0.16 0.33 0.31 0.13 0.08 0.39 0.41 0.44 0.32 1.58 39.68 0.24
Table 5. A variety of pollution indices and ecological risk calculations for greenhouse soils (and its clusters) collected from northern Jordan.

Al-Hamad A.A., et al.
10
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
the total risks (72.27-82.67%), followed by Pb which
is responsible for 11.49-14.87% of the risk. These
results indicate that the high ecological risk is mainly
posed by Cd and Pb, with minor contributions from
Ni>Cu>Zn>Cr.
The comparison of the observed concentrations of
heavy metals in greenhouse soils with the environmental
quality evaluation standard for farmland of greenhouse
vegetable production (EQESFGVP), and the Canadian
soil quality guidelines of environmental health (SQGEH)
(Table 6) revealed that Cr, Cu, and Zn in greenhouse
soils are within the reported limits of SQGEH and
EQESFGVP. The soil’s average Cd content is below
the threshold of SQGEH but in excess of EQESFGVP.
The average level of Ni in greenhouse soils is around
the upper limits of both SQGEH and EQESFGVP.
However, the concentration of Pb is slightly higher than
the limit set by EQESFGVP but within the Canadian
soil quality guidelines (SQGEH). Only Pb, Cd and Zn
contents in greenhouse soils exceeded their respective
concentrations in the crustal shale.
However, approximately 25.5% of greenhouse
samples had Pb concentrations ranging between 60 and
71 mg/kg and exceeding the EQESFGVP limit, of which
one is non-compliant with SQGEH. Additionally, 87.2%
of soil samples were found with Cd concentrations
of greater than 0.3 (in excess of EQESFGVP), 8 of
them showed values above 1.46 mg/kg for Cd (above
SQGEH standards for Cd). Zn levels in 3 locations
(6.4%) surpassed the SQGEH limit of 200 mg/kg, one
of which reported a value above 250 mg/kg (exceeding
EQESFGVP guideline for Zn). 20 samples (42.6%)
revealed Ni content above 50 mg/kg, that are higher
than the Ni limits set by both soil quality standards.
Nonetheless, no greenhouse soils exceeded any of the
soil quality guidelines for Cr nor Cu. Based on average
values, none of the open-eld soils exceeded the soil
quality standards for heavy metals, except for Cd which
is slightly in excess of EQESFGVP.
Possible Heavy Metal Pollution Sources
in the Study Area
The concentration of heavy metals in the study area
and their correlation indices reect their multiple sources.
Heavy metal concentrations in soil are increasing with
the growing industrial and agricultural activities and
inuenced by local contamination and long-range
transport of pollutants [2]. The long-term application
of pesticides (insecticides, herbicides, and fungicides),
phosphatic and nitrogen fertilizers in addition to chicken
manure contributes to the accumulation of Cd, Pb, Zn,
Cu, Ni and Cr in agricultural soils [64-70]. Our multiple
eld visits to the study area and through questioning the
local farmers, it was found that chicken manures are
widely used as organic fertilizer due to the abundance of
chicken farms in the region, where farmers placed these
chicken manures in ponds covered with plastic sheets
(for fermentation) and mixed with water before they
were pumped to greenhouses with irrigation water. Zn,
Pb and Cd (which are higher than the crustal background
shale (Table 6)), phosphatic fertilizers [71] and chicken
manure are important anthropogenic sources of these
metals in the study area. Cd, Pb, and Zn in greenhouse
soils are mainly derived from agricultural activities
[72]. Application of manure is thought to be the primary
source Cd, Zn, and Cu contamination in greenhouse
soils [12], where the availability of heavy metal in soil
is linked to the organic matter, cation exchange capacity,
salinity, and other factors [73-75]. Soil fertilized with
regular manure tends to have higher soluble Cu, Zn,
and Mn concentrations than soil fertilized with mineral
fertilizers due to higher contents of Cd, Cu, and Zn in
manure [72, 76]. Wierzbowska et al. [77] found that the
application of fertilizer and manure to soils increased
the levels of soluble forms of heavy metals such as Cu,
Ni, Pb, and Zn.
Another potential source of heavy metals in
greenhouse soils is the application of sewage sludge to
Table 6. Average heavy metals concentration in the study area (mg/kg) compared with average crustal background shale, the Canadian
agricultural soil quality guidelines of environmental health (SQGEH) and the environmental quality evaluation standard for farmland of
greenhouse vegetable production (EQESFGVP).
Current study
Greenhouse soil SQGEH (1) EQESFGVP (2) Crustal Shale (3)
Cr 26.1 64 200 90
Cu 26.8 63 100 45
Cd 0.81 1.4 0.3 0.3
Pb 53.0 70 50 20
Ni 49.3 50 50 68
Zn 139.1 200 250 95
(1) [62]: Canadian agricultural soil quality guidelines of environmental health.
(2) [63]: Environmental Quality Evaluation Standard for Farmland of Greenhouse Vegetable Production (6.5˂ soil pH˂ 7.5),
(HJ333- 2006).
(3) [39].

Assessment of Heavy Metals in Greenhouse... 11
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
the soil and wastewater irrigation obtained from Ramtha
wastewater treatment plant, located in the eastern side
of the study area (closer to cluster 2), as wastewater is an
important source of irrigation water, especially in arid
and semiarid regions [78]. Many studies have reported
that sewage sludge and fertilizers are important sources
of heavy metals [22-24]. Many recent studies observed
that the use of sewage sludge increases the soil levels
of Zn, Cu, Ni, Cr, Pb, Cd, and Hg [79-83]. Xu et al. [84]
reported that elevated levels of Cd were related to the
application of manures and fertilizers and that elevated
Cr concentrations were originated from wastewater
irrigation.
The study area is bordered by Huwwarah highway
from the southern side (Fig. 1) connecting the city of
Irbid and Ramtha with Al-Mafraq directorate in addition
to other secondary roads cutting through the study area
to facilitate transportation of goods and products and
mobility of people between small towns and villages.
Combustion of leaded gasoline on this network of roads
is a contributing source to Pb, Cd, and Zn, especially
in cluster 1 which is the closest to Huwwarah highway.
Other sources in relations to trafc related activities
including the corrosion of metal vehicle parts, tires,
batteries, pigments, and lubricants from motor vehicles
[1, 62, 85, 86].
Plastic materials used in constructing plastic
greenhouses, waterpipes for irrigation, sheets covering
the irrigation ponds, sheets covering the seedlings root
inside the greenhouses. In addition, they are used as
plastic packages to collect agricultural products to be
transported to the market. Plastic materials gradually
release pollutants to soil and the environment [87].
Besides, the plastics additives (usually contain heavy
metals such as Pb, Cd, Cr, Cu and Zn) are used as inert
llers, pigments, stabilizers, biocides, antimicrobial
agents, lubricants, and ame retardants [88, 89]. These
materials can be a source of heavy metals to greenhouse
soils when exposed to sunlight or because of tear and
wear.
Despite being a center for greenhouse vegetable
cultivation, the study area hosts factories for detergents,
concrete, and dairy products, along with Al-Hassan
Industrial City (mainly textile industries) located in
the eastern side of study area (Fig. 1). Many studies
conrmed the anthropogenic impact of these industries
on the concentration of heavy metals in soils as a point
source and by atmospheric deposition of transported
industrial dust and emissions [69, 90-94]. Cd and Pb in
greenhouse soils in the study area are likely originated
from industrial activities and are inuenced by intensive
agricultural practices, through livestock and poultry
manure, sludge, organic fertilizer, phosphatic fertilizer
and irrigation wastewater.
The heavy metals in greenhouse soils reported in this
study were compared to other studies conducted in other
regions (Table 7). Overall, the observed concentrations
of heavy metals from this study are comparable to
those measured in other countries. Zn is slightly
greater than those concentrations measured in all other
countries. Except for Spain, Cd observed in the current
study showed higher levels relative to other countries.
Similarly, Pb is higher than those found in greenhouse
soils in other regions, except for Spain. Ni average level
is the second highest after those reported from Turkey.
However, Cr and Cu contents exhibited relatively the
least among all other greenhouse soils.
Conclusions
This study provides valuable data and results of
heavy metal concentrations in greenhouse soils in one
of the most important vegetables cultivated area north
Jordan. The average concentration of heavy metals
is in the order Zn˃Pb˃Ni˃Cu˃Cr˃Cd. The analyzed
greenhouse soils are generally more impacted with
heavy metals than the soils collected from agricultural
open-eld soils. The greenhouse soils heavy metal
concentrations are higher than the crustal background
for Cd, Pb, and Zn and within the reported limits
of environmental quality evaluation standards for
farmland of greenhouse vegetable production (HJ333-
2006) except for Cd. Pollution indicators showed that
greenhouse soils are particularly contaminated with Pb
and Cd. The ecological risk assessment revealed low
risks, except for Cd.
Country Cr Cu Cd Pb Ni Zn Reference
Jordan 26.1 26.8 0.81 53.0 49.3 139.1 Current study
Turkey/Antalya - - 0.3 19.4 122 138 [95]
China/Hengshui - 41.91 0.17 13.25 28.12 112.85 [96]
East China 67.13 27.86 0.196 20.06 28.93 115.79 [97]
Spain/Almeria - - 0.4-0.8 2.5-89.9 16.1-30.7 - [98]
Spain 30.2 50.3 1.1 68.9 36 133 [99]
Table 7. Average concentration of heavy metals (mg/kg) in greenhouse soils in the current study compared with their respective contents
in other countries.

Al-Hamad A.A., et al.
12
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Acknowledgment
This study was nancially supported by the Dean
of Scientic Research and Graduate Studies, Yarmouk
University, Jordan (Project grant No.:15/2023, 20/2023,
and 23/2023).
Conict of Interest
The authors declare no conict of interest.
References
1. AL-TAANI A.A., NAZZAL N., HOWARI F. Assessment
of heavy metals in roadside dust along the Abu Dhabi–
Al Ain National Highway, UAE. Environmental Earth
Sciences, 78, 411, 2019. https://doi.org/10.1007/s12665-019-
8406-x.
2. AL-TAANI A.A., RASHDAN M., KHASHASHNEH S.
Atmospheric dry deposition of mineral dust to the Gulf of
Aqaba, Red Sea: Rate and trace elements. Marine Pollution
Bulletin, 92 (1-2), 252, 2015b. https://doi.org/10.1016/J.
MARPOLBUL.2014.11.047
3. EL-RADAIDEH N. AL-TAANI A.A. Geo-environmental
study of heavy metals of the agricultural highway soils,
NW Jordan. Arab. J. of Geosciences, 11, 787, 2018. doi.
org/10.1007/s12517-018-4099-9.
4. TIMOTHY N., TAGUI WILLIAMS E. Environmental
pollution by heavy metal: an overview. IJEC, 3, 72, 2019.
https://doi.org/10.11648/j.ijec.20190302.14.
5. WANG S., CAI L., WEN H., LUO J., WANG Q.,
LIU X. Spatial distribution and source apportionment
of heavy metals in soil from a typical county-level
city of Guangdong Province, China. Sci. Total
Environ, 655, 92, 2019. https://doi.org/ 10.1016/j.
scitotenv.2018.11.244.
6. CHEN Y., HUANG B., HU W., WEINDORF D., LIU
X., YANG L. Accumulation and ecological effects of soil
heavy metals in conventional and organic greenhouse
vegetable production systems in Nanjing, China. Environ.
Earth Sci. 71, 3605, 2014. https://doi.org/10.1007/s12665-
013-2752-x.
7. EDELSTEIN M., BEN-HUR M. Heavy metals and
metalloids: sources, risks and strategies to reduce their
accumulation in horticultural crops. Sci. Hortic, 234, 431,
2018. https://doi.org/10.1016/j.scienta.2017.12.039
8. VARDHAN K., KUMA, P., PANDA R. A review on heavy
metal pollution, toxicity and remedial measures: current
trends and future perspectives. J. Mol. Liq, 290, 111197,
2019. https://doi.org/10.1016/j.molliq.2019.111197
9. NAZZAL Y., BARBULESCU A., HOWARI F., AL-
TAANI A.A. Assessment of Metals Concentrations in
Soils of Abu Dhabi Emirate Using Pollution Indices and
Multivariate Statistics. Toxics, 9, 95, 2021.
10. GREFAT H., ZAMAN H., BATAYNEH A., WAHEIDI
M., QAYSI S., AL-TAANI A.A. Assessment of Heavy
Metal Contamination in the Soils of the Gulf of Aqaba
(Northwestern Saudi Arabia): Integration of Geochemical,
Remote Sensing, GIS, and Statistical Data. Journal of
Coastal Research, 37 (4), 864, 2021.
11. SERRA G., TOGNONI F., LEONI S. ISHS Acta
Horticulturae 361: International Symposium on New
Cultivation Systems in Greenhouse, Cagliari, Italy. ISBN
978-90-66051-66-9, ISSN 0567–7572. 1994.
12. YANG L., HUANG B., HU W., CHEN Y., MAO M.
Assessment and source identication of trace metals
in the soils of greenhouse vegetable production in
eastern China. Ecotoxicology and Environmental Safety,
97, 204, 2013. https://doi.org/10.1016/j.ecoenv.2013.08.002
13. LI W, Q., ZHANG M., VAN D.Z. Salt contents in soils
under plastic greenhouse gardening in China. Pedosphere,
11, 359, 2001.
14. YAO H.Y., JIAO X.D., WU F.Z. Effect of continuous
cucumber cropping and alter native rotations under
protected cultivation on soil microbial community
diversity. Plant Soil, 284, 195, 2006.
15. YU H.Y., LI T.X., ZHANG, X.Z. Nutrient budget and soil
nutrient status in greenhouse system. J Integr Agr, 9 (6),
871, 2010.
16. BAI L.Y., ZENG X.B., SU S.M., DUAN R.,
WANG Y.N., GAO X. Heavy metal accumulation and
source analysis in greenhouse soils of Wuwei District,
Gansu Province, China. Environ. Sci. Pollut. Res, 22, 5359,
2015.
17. KASHEM M., SINGH B. Metal availability in
contaminated soils: I. Effects of ooding and organic
matter on changes in Eh, pH and solubility of Cd, Ni and
Zn. Nutrient Cycling in Agroecosystems, 61, 247, 2001.
https://doi.org/10.1023/A:1013762204510
18. BOLAN N., ADRIANO D., MAHIMAIRAJA S.
Distribution and bioavailability of trace elements in
livestock and poultry manure by-products. Critical Reviews
in Environmental Science and Technology, 34 (3), 291,
2004.
19. CANG L., WANG Y., ZHOU D., DONG Y. Heavy metals
pollution in poultry and livestock feeds and manures under
intensive farming in Jiangsu Province, China. Journal of
Environmental Sciences, 16 (3), 371, 2004.
20. AL-TAANI A.A., BATAYNEH A., MOGREN S.,
NAZZAL N., GHREFAT H., ZAMAN H., ELAWADI
E. Groundwater Quality of Coastal Aquifer Systems
in the Eastern Coast of the Gulf of Aqaba, Saudi Arabia.
Journal of Applied Science and Agriculture, 8 (6), 768,
2013.
21. MENG M., YANG L., YU J., WEI B., LI H., CAO Z.,
CHEN Q., ZHANG G. Identication of spatial patterns
and sources of heavy metals in greenhouse soils using
geostatistical and positive matrix factorization (PMF)
methods. Land Degrad Dev, 32 (18), 5412, 2021.
22. FACCHINELLI A., SACCHI E., MALLEN L. Multivariate
statistical and GIS-based approach to identify heavy metal
sources in soils. Environmental Pollution, 114 (3), 313,
2001.
23. GUPTA S., SATPATI S., NAYEK S., GARAI D. Effect
of wastewater irrigation on vegetables in relation to
bioaccumulation of heavy metals and biochemical changes.
Environmental Monitoring and Assessment, 165 (1-4), 169,
2010.
24. NABULO G., BLACK C.R., YOUNG S.D. Trace metal
uptake by tropical vegetables grown on soil amended with
urban sewage sludge. Environmental Pollution, 159 (2),
368, 2011.
25. JDS (Jordan Department of Statistics). Agricultural
Statistics 2017. http://dosweb.dos.gov.jo/wp-content/
uploads/2017/08/Agr2017.pdf 2020.
26. JDS (Jordan Department of Statistics). Agricultural
Statistics 2018. http://dosweb.dos.gov.jo/wp-content/
uploads/2021/08/agr_strat2018.pdf 2020.

Assessment of Heavy Metals in Greenhouse... 13
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
27. JDS (Jordan Department of Statistics). Agricultural
Statistics 2019. http://dosweb.dos.gov.jo/DataBank/Agri/
Agr_2019.pdf (2020).
28. HU W.Y., CHEN Y., HUANG B., NIEDERMANN
S. Health risk assessment of heavymetals in soils and
vegetables from a typical green house vegetable production
system in China. Hum. Ecol. Risk Assess, 20, 1264, 2014.
29. IRBID AGRICULTURE DIRECTORATE, Ministry of
Agriculture, Jordan, 2021.
30. MO’HD B. Geological Map of Irbid (3155II). 1:50,000,
Natural Resources Authority, Amman, Jordan. 1997.
31. BANDEL K., SALAMEH E. Geologic Development
of Jordan-Evolution of Its Rocks and Life. Deposit No.
690/3/2013 of the National Library, Amman, 278, 2013.
32. MoE (Ministry of Environment, Jordan). National Action
Plan and Strategy to Combat Desertication. Amman,
Jordan, 2006.
33. USDA-SSS (United States Department of Agriculture,
Soil Survey Staff), Keys to Soil Taxonomy, 4th ed.; SMSS,
Technical monograph 19, Blacksburg, Virginia, 1990.
34. AL-SHEREIDEH S., WAHSHA M., EL-RADAIDEH
N., AL-TAANI A.A., ABDERAHMAN N., ODAT S.,
AL-MOMANI T., KHAWAJAH M. Geo-Environmental
Assessment of Al-Ramtha Soils, Jordan. Current World
Environment, 10 (2), 386, 2015.
35. OBEIDAT M., AWAWDEH M., LABABNEH A. (2019).
Assessment of land use/land cover change and its
environmental impacts using remote sensing and GIS
techniques, Yarmouk River Basin, north Jordan. Arab J
Geosci, 12, 685, 2019. https://doi.org/10.1007/s12517-019-
4905-z
36. WALKLEY A., BLACK I.A. An Examination of the
Degtjareff Method for Determining Soil Organic Matter
and a Proposed Modication of the Chromic Acid Titration
Method. Soil Science, 37, 29, 1934.
37. LORING H.D., RANTALA R. Manual for the
Geochemical Analyses of Marine Sediments and
Suspended Particulate Matter. Earth-Science Review, 32,
235, 1992. http://dx.doi.org/10.1016/0012-8252(92)90001-A
38. ZHANG J., LIU C.L. River in composition and estuarine
geochemistry of particulate metals in China-weathering
features, anthropogenic impact and chemical uxes.
Estuarine Coast Shelf Sci, 54, 1051, 2002.
39. TUREKIAN K., WEDEPOHL K. Distribution of the
elements in some major units of the earth’s crust. Geol.
Soc. Am. Bull, 72 (2), 175, 1961.
40. MüLLER G. Heavy metals in the sediments of the R hine
– changes since 1971. Umschau 79 (24), 778, 1979 [In
German].
41. HAKANSON L. An ecological risk index for aquatic
pollution control: A sedimentological approach. Water
Res, 14 (8), 975, 1980. https://doi.org/10.1016/0043-
1354(80)90143-8
42. TOMLINSON D.C., WILSON J.G., HARRIS C.R.,
JEFFREY D.W. Problems in the assessment of heavy-
metal levels in estuaries and the formation of a pollution
index. Helgol. Mar. Res., 33, 566, 1980.
43. NADIMI-GOKI M., WAHSHA M., BINI C., KATO Y.,
VIANELLO G. ANTISARI L.V. Assessment of total soil
and plant elements in rice-production systems in NE Italy.
Journal of Geochemical Exploration, 147, 200, 2014.
44. ADENIYI A.A., YUSUF K.A., OKEDEYI O.O.
Assessment of the exposure of two sh species to metals
pollution in the Ogun River catchments, Ketu, Lagos,
Nigeria. Environ Monit Assess, 137, 451, 2008. https://doi.
org/10.1007/s10661-007-9780-5
45. MUHAIDAT R., AL-QUDAH K., AL-TAANI A.A.,
ALJAMMAL S. Assessment of nitrate and nitrite levels in
treated wastewater, soil, and vegetable crops at the upper
reach of Zarqa River in Jordan. Environmental Monitoring
and Assessment, 191, 153, 2019. https://doi.org/10.1007/
s10661-019-7292-8
46. BAI X., GAO J., WANG S., CAI H., CHEN Z., ZHOU
J. Excessive nutrient balance surpluses in newly built
solar greenhouses over ve years leads to high nutrient
accumulations in soil. Agriculture, Ecosystems &
Environment, 288, 2020. https://doi.org/10.1016/j.
agee.2019.106717
47. LV H., ZHAO Y., WANG Y., WAN L., WANG J.,
BUTTERBACH-BAHL K., LIN, S. Conventional
ooding irrigation and over fertilization drives soil pH
decrease not only in the top- but also in subsoil layers
in solar greenhouse vegetable production systems.
Geoderma, 363, 114156, 2020. https://doi.org/10.1016/j.
geoderma.2019.114156.
48. AL-TAANI A.A., AL-QUDAH K., Investigation of Deser t
Subsoil Nitrate in Northeastern Badia of Jordan. Science
of the Total Environment, 442, 111, 2013.
49. EL-RADAIDEH N., AL-TAANI A.A., AL-MOMANI T.,
TARAWNEH K., BATAYNEH A., TAANI A. Evaluating
the Potential of Sediments in Ziqlab Reservoir (northwest
Jordan) for Soil Replacement and Amendment. Lake and
Reservoir Management, 30 (1), 32, 2014.
50. BATAYNEH A., ELAWADI E., ZAMAN H., AL-TAANI
A. A., NAZZAL Y., GHREFAT H. Environmental
assessment of the Gulf of Aqaba coastal surface waters,
Saudi Arabia. Journal of Coastal Research, 30 (2), 283,
2014.
51. TAN K.H. Soil Sampling, Preparation, and Analysis, 2nd ed.;
CRC Press, 2005. https://doi.org/10.1201/9781482274769
52. HOLM P. Correlation of cadmium distribution
coefcients to soil characteristics. J. Environ. Qual, 32, 8,
2003.
53. XU D., ZHOU P., ZHAN J., GAO Y., DOU C., SUN Q.
Assessment of trace metal bioavailability in garden soils
and health risks via consumption of vegetables in the
vicinity of Tongling mining area, China. Ecotoxicol.
Environ. Saf, 90, 103, 2013. https://doi.org/10.1016/j.
ecoenv.2012.12.018
54. AL-TAANI A.A., BATAYNEH A., EL-RADAIDEH
N., GHREFAT H., ZUMLOT T., AL-RAWABDEH A.,
AL-MOMANI T., TAANI A. Spatial distribution and
pollution assessment of trace metals in surface sediments
of Ziqlab Reservoir, Jordan. Environmental Assessment
and Monitoring, 187 (32), 1, 2015a
55. LI G. IOP Conf. Ser.: Mater. Sci. Eng. 394 052081, 2018.
56. LAIR G.J., GERZABEK M.H., HABERHAUER G.
Sorption of heavy metals on organic and inorganic soil
constituents. Environ Chem Lett, 5, 23, 2007. https://doi.
org/10.1007/s10311-006-0059-9
57. LI F., SHI W., JIN Z., WU H., SHENG G. Excessive
uptake of heavy metals by greenhouse vegetables. J.
Geochem. Explor, 173, 76, 2017. https://doi.org/10.1016/j.
gexplo.2016.12.002.
58. KIM R., YOON J., KIM T., YANG J., OWENS G., KIM
K. Bioavailability of heavy metals in soils: Denitions
and practical implementation – A critical review. Environ.
Geochem. Health, 37, 1041, 2015. doi: 10.1007/s10653-015-
9695-y
59. ZHANG J., LI H., ZHOU Y., DOU L., CAI L., MO L.,
YOU J. Bioavailability and soil-to-crop transfer of heavy
metals in farmland soils: A case study in the Pearl River

Al-Hamad A.A., et al.
14
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
Delta, South China. Environ. Pollut, 235, 710, 2018.
doi: 10.1016/j.envpol.2017.12.106
60. SUNGUR A., SOYLAK M., ÖZCAN H. Chemical
fractionation, mobility and environmental impacts of
heavy metals in greenhouse soils from Çanakkale, Turkey.
Environmental Earth Science, 75, 334, 2016. https://doi.
org/10.1007/s12665-016-5268-3
61. KONG X., CAO J., TANG R., ZHANG S., DONG F.
Pollution of intensively managed greenhouse soils by
nutrients and heavy metals in the Yellow River Irrigation
Region, Northwest China. Environmental Monitoring
and Assessment, 186, 7719, 2014. https://doi.org/10.1007/
s10661-014-3962-8
62. CANADIAN COUNCIL OF MINISTERS OF THE
ENVIRONMENT (CCME),Canadian sediments quality
guidelines for the protection of aquatic life: summary
tables: update in: Canadian Environmental Quality
Guidelines (1999) CCME, Winnipeg, 2007.
63. LIAO Z., CHEN Y., MA J., ISLAM M.S., WENG L., LI
Y. Cd, Cu, and Zn Accumulations Caused by Long-Term
Fertilization in Greenhouse Soils and Their Potential Risk
Assessment. Int J Environ Res Public Health, 16 (15),
2805, 2019. doi: 10.3390/ijerph16152805. PMID: 31390808;
PMCID: PMC6695759.
64. ROBERTS T.L. Cadmium and Phosphorous Fertilizers:
The Issues and the Science. Procedia Eng, 83, 52, 2014.
65. WANG F., WANG Z., KOU C., MA Z. ZHAO D.
Responses of Wheat Yield, Macro- and Micro-Nutrients,
and Heavy Metals in Soil and Wheat following the
Application of Manure Compost on the North China Plain.
PLOS ONE, 11 (1), e146453, 2016. https://doi. org/10.1371/
journal.pone.0146453
66. GHARAIBEH M.A., MARSCHNER B., HEINZE S.,
MOOS N. Spatial distribution of metals in soils under
agriculture in the Jordan Valley. Geoderma, 20, 2020.
67. ALENGEBAWY A., ABDELKHALEK S.T., QURESHI
S.R., WANG M.Q. Heavy Metals and Pesticides Toxicity in
Agricultural Soil and Plants: Ecological Risks and Human
Health Implications. Toxics, 9 (3), 42, 2021. doi: 10.3390/
toxics9030042. PMID: 33668829; PMCID: PMC7996329.
68. XIN X., SHENTU J., ZHANG T., YANG X., BALIGAR
V.C., HE Z. Sources, Indicators, and Assessment of Soil
Contamination by Potentially Toxic Metals. Sustainability,
14 (23), 15878, 2022. https://doi.org/10.3390/su142315878
69. ALAM M.N.E., HOSEN M.M., ULLAH A.K.M.A.
Pollution Characteristics, Source Identication, and Health
Risk of Heavy Metals in the Soil-Vegetable System in
Two Districts of Bangladesh. Biol Trace Elem Res, 2023.
https://doi.org/10.1007/s12011-023-03558-7.
70. AL-TAANI A.A., NAZZAL Y., HOWARI F., IQBAL
J., NASEEM M. Metal composition and Contamination
Assessment of Urban Roadway Dusts in Abu Dhabi-Liwa
Highway, UAE. Frontiers in Environmental Sciences, 11,
2023. https://doi.org/10.3389/fenvs.2023.1157101
71. AL-TAANI A.A., BATAYNEH A., NAZZAL Y.,
GHREFAT H., ELAWADI E., ZAMAN H. Status
of t race metals in surface seawater of the Gulf of Aqaba,
Saudi Arabia. Marine Pollution Bulletin, 86 (1-2), 582,
2014.
72. TIAN K., HU W., XING Z., HUANG B., JIA M., WAN
M. Determination and evaluation of heavy metals in soils
under t wo different greenhouse vegetable production
systems in eastern China. Chemosphere, 165, 55, 2016.
https://doi.org/10.1016/j.chemosphere.2016.09.012
73. ACOSTA J.A., JANSEN B., KALBITZ K., FAZ A.,
MARTíNEZ-MARTíNEZ S. Salinity increases mobility
of heavy metals in soils. Chemosphere, 85, 1318, 2011.
doi: 10.1016/j.chemosphere.2011.07.046
74. BATAYNEH A., GHREFAT H., ZUMLOT T., ELAWADI
E., MOGREN S., ZAMAN Z., AL-TAANI A.A.,
NAZZAL Y., ELWAHEIDI M. Assessing of Metals and
Metalloids in Surface Sediments along the Gulf of Aqaba
Coast, Northwestern Saudi Arabia. Journal of Coastal
Research. 31 (1), 163, 2015.
75. CAO X., WANG X., TONG W., GURAJALA H.K., LU
M., HAMID Y., FENG Y., HE Z., YANG X. Distribution,
availability and translocation of heavy metals in soil
oilseed rape (Brassica napus L.) system related to soil
properties. Environ. Pollut, 252, 733, 2019. doi: 10.1016/j.
envpol.2019.05.147
76. SIENKIEWICZ S., WOJNOWSKA T., KRZEBIETKE
S., WIERZBOWSKA J., ŻARCZYńSKI P. Content of
available forms of some micronutrients in soil after long-
term differentiated fertilization. J. Element, 14, 787, 2009.
doi: 10.5601/jelem.2009.14.4.787-794
77. WIERZBOWSKA J., KOVACIK P., SIENKIEWICZ S.,
KRZEBIETKE S., BOWSZYS T. Determination of heavy
metals and their availability to plants in soil fertilized with
different waste substances. Environ. Monit. Assess, 190,
567, 2018. doi: 10.1007/s10661-018-6941-7.
78. UZEN N. Use of Wastewater for Agricultural Irrigation
and Infectious Diseases. Diyarbakir Example.
Journal of Environmental Protection and Ecology, 17, 488,
2016.
79. BECKETT P.H.T., DAVIS R.D., BRINDLEY P., CHEM C.
The disposal of sewage sludge onto farmland: the scope of
the problem of toxic elements, Water Pollut. Control, 78,
419, 1979.
80. WHITE P.J., BROWN P.H. Plant nutrition for sustainable
development and global health. Ann Bot, 105 (7), 1073,
2010. doi: 10.1093/aob/mcq085. Epub 2010 Apr 29. PMID:
20430785; PMCID: PMC2887071.
81. PROSHAD R., KORMOKER T., ISLAM M.S., HANIF
M.A., CHANDRA K. Chronic exposure assessment of
toxic elements from agricultural soils around the industrial
areas of Tangail district, Bangladesh. Arch Agric Environ
Sci, 3, 317, 2018.
82. RODRíGUEZ-EUGENIO N., MCLAUGHLIN M.,
PENNOCK D. Soil Pollution: a hidden reality. Rome,
FAO. 142, 2018.
83. BARAKAT A., ENNAJI W., KRIMISSA S., BOUZAID
M. Heavy metal contamination and ecological-health risk
evaluation in peri-urban wastewater-irrigated soils of
Beni-Mellal city (Morocco). Int J Environ Health Res. 30
(4), 372, 2020. doi: 10.1080/09603123.2019.1595540. Epub
2019 Apr 12. PMID: 30977689
84. XU L., LU A.X., WANG J.H., MA Z.H., PAN L.G.,
FENG X.Y., LUAN Y.X. Accumulation status, sources
and phytoavailability of metals in greenhouse vegetable
production systems in Beijing, China. Ecotoxicol. Environ.
Saf, 122, 214, 2015.
85. HORNER J.M. Environmental health implications of
heavy metal pollution from car tires. Rev Environ Health,
11 (4), 175, 1996. doi: 10.1515/reveh.1996.11.4.175. PMID:
9085433.
86. WYSZKOWSKA J., BOROWIK A., KUCHARSKI M.,
KUCHARSKI J. Effect of cadmium, copper and zinc on
plants, soil microorganisms and soil enzymes. J. Elem, 18
(4), 769, 2013. DOI:10.5601/jelem.2013.18.4.455
87. ALAM O., YANG L., YANCHUN X. Determination of
the selected heavy metal and metalloid contents in various
types of plastic bags. J Environ Health Sci Eng, 17 (1), 161,

Assessment of Heavy Metals in Greenhouse... 15
Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy • Author Copy
2019. doi: 10.1007/s40201-019-00337-2. PMID: 31321044;
PMCID: PMC6582199.
88. LIU Y.B., LIU W.Q., HOU M.H. Metal dicarboxylates
as thermal stabilizers for PVC. Polym. Degrad. Stab, 92,
1565, 2007.
89. JANSSEN M.P.M., SPIJKER J., LIJZEN J.P.A.,
WESSELINK L.G. Plastics That Contain Hazardous
Substances: Recycle or Incinerate? Dutch National
Institute for Public Health and the Environment, RIVM,
Bilthoven, The Netherlands. 2016.
90. LIAO M., XIE X.M. Effect of heavy metals on substrate
utilization pattern, biomass, and activity microbial
communities in a reclaimed mining wasteland of red
soil area. Ecotoxicol. Environ. Saf, 66, 217, 2007.
DOI:10.1016/j.ecoenv.2005.12.013.
91. JUSTICE O.O., FREDERICK A.A., ISAAC L. Assessment
of spatial variability of heavy metals in soils under the
inuence of industrial soap and detergent wastewater
discharge. IJ RR AS, 9 (2), 322, 2011.
92. ACHTERNBOSCH M., BRäUTIGAM K. R., HARTLIEB
N., KUPSCH C., RICHERS U., STEMMERMANN P.,
GLEIS M. Heavy metals in cement and concrete resulting
from the co-incineration of wastes in cement kilns with
regard to the legitimacy of waste utilisation. Karlsruhe:
Forschungszentrum Karlsruhe GmbH. 2003.
93. OGUNKUNLE C.O., FATOBA P.O. Pollution Loads
and the Ecological Risk Assessment of Soil Heavy
Metals around a Mega Cement Factory in Southwest
Nigeria. Polish Journal of Environmental Studies, 22 (2),
2013.
94. AL-TAANI A.A., NAZZAL Y., HOWARI F.M., IQBAL
J., BOU ORM N., XAVIER C.M., BăRBULESCU
A., SHARMA M., DUMITRIU C.S. Contamination
Assessment of Heavy Metals in Agricultural Soil, in
the Liwa Area (UAE). Toxics, 9, 53, 2021. https://doi.
org/10.3390/toxics9030053
95. TOPÇUOĞLU B. Evaluation of heavy metal pollution
characteristics in greenhouse soils of Antalya (Turkey).
Tarım Bilimleri Araştırma Dergisi, 8 (1), 44, 2015.
96. WEI B., YU J., CAO Z., MENG M., YANG L., CHEN
Q. The availability and accumulation of heavy metals
in greenhouse soils associated with intensive fertilizer
application. International Journal of Environmental
Research and Public Health, 17 (15), 5359, 2020.
97. TIAN K., HU W., XING Z., HUANG B., JIA M., WAN
M. Determination and evaluation of heavy metals in soils
under t wo different greenhouse vegetable production
systems in easter n China. Chemosphere, 165, 555, 2016.
98. GIL C., BOLUDA R., RAMOS J. Determination and
evaluation of cadmium, lead and nickel in greenhouse
soils of Almerıa (Spain). Chemosphere, 55 (7), 1027, 2004.
https://doi.org/10.1016/j.chemosphere.2004.01.013
99. RODRíGUEZ MARTíN R J.A., RAMOS-MIRAS J.J.,
BOLUDA R., GIL C. Spatial relations of heavy metals
in arable and greenhouse soils of a Mediterranean
environment region (Spain). Geoderma, 200-201, 180,
2013. https://doi.org/10.1016/j.geoderma. 2013.02.014