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Article

Effect of Treated Wastewater Irrigation on the Accumulation and Transfer of Heavy Metals in Lemon Trees Cultivated in Arid Environment

by
Randa N. Albdaiwi
1,
Jehad S. Al-Hawadi
2,
Ziad B. Al-Rawashdeh
2,
Khaled A. Al-Habahbeh
2,
Jamal Y. Ayad
3,* and
Rabea S. Al-Sayaydeh
2,*
1
Department of Land, Water and Environment, School of Agriculture, The University of Jordan, Amman 11942, Jordan
2
Department of Agriculture Sciences, Faculty of Shoubak College, Al-Balqa Applied University, Al-Salt 19117, Jordan
3
Department of Horticulture and Crop Science, School of Agriculture, The University of Jordan, Amman 11942, Jordan
*
Authors to whom correspondence should be addressed.
Horticulturae 2022, 8(6), 514; https://doi.org/10.3390/horticulturae8060514
Submission received: 18 May 2022 / Revised: 9 June 2022 / Accepted: 10 June 2022 / Published: 12 June 2022
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Abstract

:
The Middle East is considered as one of the driest regions of the world and the use of municipal-treated wastewater (TWW) for agricultural purposes is needed. The aim of this study was to evaluate the effect of continuous irrigation of TWW in lemon orchards on the accumulation of heavy metals (HMs) in the soil, as well as their uptake and translocation to aerial parts of the trees. For this purpose, two lemon orchards were selected to be irrigated from two different water sources: TWW from a tertiary treatment plant and freshwater (SW) from Moses springs in Jordan. Continuous irrigation with TWW resulted in higher concentrations of nutrients and HM accumulation in the soil as compared to SW. However, HM accumulation in the soil was found to be within the acceptable range according to the standards of the WHO. On the contrary, the continuous irrigation with TWW resulted in the accumulation of HMs in plant parts when compared to SW irrigation; the fruits were clearly affected by the accumulation of high levels of Cd and Pb that exceed the maximum limits for the presence of HMs in plant tissues. The irrigation of lemon trees with TWW had a significant effect on the bioaccumulation factor and translocation factors (TF) of HMs into different lemon tree parts. Heavy metal accumulation coincided with high translocation rates to different tree parts, and this is considered to be a main challenge for long-term irrigation with TWW in arid environments.

1. Introduction

Water scarcity and climate change associated with high evapotranspiration rates in dry areas will increase the water demand for growing cultivated plants [1]. In the Mediterranean region, the lack of safe and renewable water resources is causing a regional crisis, particularly in the arid and semi-arid areas, which are expected to reach a permanent water scarcity status and water quality deterioration by 2025 [2,3]. Future scenarios predict that the Mediterranean region will be greatly affected by climate change and its associated conditions, in particular rising temperatures and decreased precipitation amounts [4].
Jordan, a country located in the eastern part of the Mediterranean basin, is characterized by its dry-hot summers and mild-wet winters with extreme variability in rainfall amounts within and between years [5]. Most of its arable land is considered arid and agricultural production is considered unstable since it depends on water availability and rainfall distribution over the growing season [6]. Moreover, the annual per capita water availability is less than 145 m3, making the country among the poorest countries in the world in terms of water scarcity [7].
In dry areas, water shortage is considered one of the main challenges affecting plant growth and productivity [8]. Municipal wastewater produced worldwide is expected to increase with global population growth and urbanization [9]. Therefore, the use of treated wastewater (TWW) for irrigation purposes is nowadays considered essential to meet the needs of humans and agriculture [2]. The use of TWW as a supplementary source of irrigation provides valuable solutions to meet the challenges of limited access and scarcity of water resources [10]. Using TWW at reasonable rates will add high concentrations of mineral nutrients to the rhizosphere zone, such as nitrogen (N), phosphorus (P), potassium (K), magnesium (Mg), iron (Fe), manganese (Mn), copper (Cu), and calcium (Ca), that can improve plant growth and production without the need to add chemical fertilizers [11]. However, using TWW is also associated with a high risk of heavy metal (HM) accumulation in the soil strata and phytotoxicity due to their accumulation in plant tissues [12]. In addition, these harmful metalloids may enter the food chain of humans or animals, which is considered a major challenge for using TWW in agriculture [10,13]. Heavy metal contamination has been reported in soils irrigated with TWW, regardless of their low content in the effluents [12,14].
Citrus fruit trees are widely cultivated all over the world, including the Mediterranean region. In Mediterranean-type climates, which are characterized by their mild winters, the production of high-quality lemon (Citrus limon L.) fruits is common compared to more humid environments where there are more pests and disease infections occur frequently [15,16]. Still, in such areas, lemon as an evergreen tree is considered sensitive to different forms of abiotic stresses that include salinity, heat, chilling, and drought [17]. For instance, the simultaneous exposure of lemon trees to high temperatures and drought stress will induce oxidative damage to photosystems that are associated with reduced carbon assimilation [15]. Salinity reduces growth parameters, such as tree height, stem diameter, and leaf area, accompanied by plant physiological disorders [18,19].
The HM content in soils of tree orchards irrigated with TWW has been studied in several locations across Jordan [14,20,21]. However, less information is available about the impact of TWW irrigation on lemon tree orchards in dry regions. Furthermore, the fate of HMs in the soil, as well as their absorption, bioaccumulation, and translocation to areal parts in response to long-term irrigation with TWW effluents for lemon trees, has not been studied before in dry environments. Therefore, the present study aimed to explore the effects of long-term irrigation with TWW on the accumulation of HMs in soils, and on their uptake, partitioning, and accumulation in lemon trees cultivated in arid environments.

2. Materials and Methods

2.1. Study Area

Two sites were selected to study the effect of TWW irrigation on lemon trees: the first site was near Wadi-Musa Wastewater Treatment Plant (WMTP), which is located 9 km to the northeast of the historic city of Petra (30°22′27.6″ N; 35°26′58.7″ E) [14], where lemon trees were irrigated with TWW from the plant; The second site was close to Moses springs (Ain Mousa (AM)), which is located 3 km to the east of the historic city of Petra (30°19′30.4″ N 35°29′49.4″ E), where the lemon trees were irrigated from an aquifer water source (spring water (SW)) and served as a control site.
Wastewater flows from adjacent communities of Wadi-Musa and Tibah villages were collected at the treatment plant and treated through a multi-stage wastewater cleaning process (tertiary water treatment). The study site of the WMTP consisted of an area of seven hectares cultivated with different types of trees and crops, including lemon. On the other hand, the control site (AM) consisted of an area of three hectares cultivated with different types of fruit trees, including lemons.
The study area climate is considered arid and is characterized by its mild winters and hot summers. The monthly averages of maximum and minimum temperatures and average precipitation for the last ten years at WMTP were reported previously [14]. This area is characterized by its hot and dry summers with the hottest maximum temperatures exceeding 30 °C during August and its low precipitation (170 mm annually), which mostly occurs during the winter months.

2.2. Soil and Water Analysis

Soil pH was measured using saturated soil pastes extracts, and electrical conductivity (EC) was measured in aqueous soil extract (5:1) as described in [22]. Soil calcium carbonate (CaCO3) analysis was performed by using gas chromatography method as described by [23]. Organic matter (OM) content was analyzed following [24] and calculated by using the conversion equation (Organic matter = 1.721 × organic carbon) [24] after analyzing organic carbon by using a carbon combustion furnace (Leco SC832, St. Joseph, MI, USA). Soil grain size was analyzed by laser diffraction (Mastersizer 3000, Malvern Panalytical, Malvern, UK) and the soil texture at both sites was classified as a sandy loam (Table 1). For the WMTP site, the soil pH and EC values were 7.6 and 2.1 dS·m−1, respectively, while the OM was 12.1 g·kg−1, whereas CaCO3 concentration was 13.12 g·kg−1. For the AM site, the soil pH and EC values were 7.8 and 1.85 dS·m−1, respectively, and the OM was approximately 3.4 g·kg−1, whereas CaCO3 concentration was 15.92 g·kg−1 (Table 1). The HM concentrations in soil samples were analyzed as described previously [25].
For water, analysis was performed at four intervals every three months to check for chemical and biological characteristics of water sources in both sites as described previously [14]. In brief, 100 mL of water samples (n = 4 from both sites) were filtered using a vacuum system through a 0.45 µm nitrate–cellulose filter and acidified with concentrated HNO3 (70%). The pH of irrigation water was measured with a pH meter, while EC and total dissolved salts (TDS) were measured with an inoLab Cond 720 (WTW, Weilheim, Germany). Chemical oxidation demand (COD), biochemical oxidation demand (BOD), and sodium adsorption ratio (SAR) were determined following (Pedrero and Alarcón, 2009) [26] through WMTP Service Laboratory. Coliforms were determined as described previously [26]. Table 2 summarizes the characteristics of TWW and SW during 2021. The obtained chemical and biological (bacterial load) analysis results were found to comply with the standards of safe use of TWW established by the Jordan Standards and Metrology Organization (JISM, 2013) [27], as well as with those of the World Health Organization (WHO, 2006) [28]. The filtrated samples were analyzed for HM concentrations according to [25].

2.3. Plant Material

Ten-year-old lemon trees from the study area were selected. The lemon trees at both sites were irrigated continuously once a week during December, January, February, and March, and twice a week for the rest of the year. The average monthly irrigation water for both sites ranged between 70 and 140 mm per month. No organic or chemical fertilizers were applied to the tree orchards at both sites. For each tree, the chlorophyll content index was measured for four fully mature leaves facing the sun per tree using an SPAD meter (CCM-200 plus; Opti-Sciences; Hudson, NH, USA).
Four lemon trees from each site were selected randomly and sampled for their roots, stem bark, leaves, and fruits in June 2021. For root samples, fine roots from the upper rooting zone of each tree were sampled (n = 4) using a soil corer of 10 cm diameter at a depth of about 25 cm that was taken 50 cm away from the trunks around the circumference of each tree. The fine roots with diameters of ~2–3 mm were sieved and then washed with distilled water and finally dried for 24 h at 80 °C. For bark, four samples were obtained from the outer bark of each selected lemon tree at a height of 1.0 m above the ground using a 10 mm increment borer. For leaf samples, four mature leaves (~100 g DW) were collected randomly from each tree from the middle of the current year twigs all around the tree periphery. For fruits, four samples of fully ripened fruit (5–6 cm in diameter) were collected from the outer side at the center of the tree canopy. The bark, leaves, and fruit samples of each tree were washed thoroughly with distilled water before drying for 24 h at a temperature of 80 °C in a dry oven. For each plant part, the four samples from each tree were mixed together and used as a composite study sample for further analysis. The dried samples were grounded into a fine powder and homogeneous samples of each lemon tree dried tissues (roots, bark, leaves, and fruit) were prepared for the analysis of various macronutrients, micronutrients, and HMs as described in [25].

2.4. Heavy Metals Analysis

The collected samples of soil, water, and tree parts (root, bark, leaf, and fruit samples) were analyzed for their HM content as described previously [25]. In brief, 0.5 g of dried samples were digested in a mixture of four ml of 70% HNO3 and one ml of 62% HClO4 using a high-pressure microwave apparatus (Milestone, MLS, Ultraclave, Sorisole, Italy), and the digested samples were filtered through a 45 µm filter. The final leachates were filled in a 25 mL volumetric flask with a 1% (v/v) HNO3 solution. The following elements (Fe, Cu, Mn, Zn, Cd, Cr, Pb, and Ni) were measured for all samples by using an atomic absorption spectrophotometer (Analyst 200, PerkinElmer, Waltham, MA, USA).

2.5. Bioconcentration and Translocation Factors

The bioconcentration (BCF) and translocation factors (TF) were analyzed to study the relationship between various HM contents in the soils and tree tissues. For this purpose, the BCF, which is defined as the ratio of the concentration of a mineral in the plant tissues to that in the soil, was used to determine the ability of lemon trees to accumulate minerals from the soil to their tissue. However, the TF was used to estimate the ability of lemon trees to translocate metals from their roots to the areal parts. The BCFs and TFs were calculated as described by Mellem [29] using the following equations:
BCF = concentration   of   metal   in   plant   tissue concentration   of   metal   in   soil
TF = BCF   of   the   bark   or   the   leaf BCF   of   root

2.6. Data Analysis

The data were expressed as the means of four replicates, which were arranged in a factorial design. The nutrients and HMs concentrations, BCFs, and TFs of different plant parts were subjected to analysis of variance (ANOVA) and the Least Significant Difference (LSD at p ≤ 0.05) was used for mean comparisons using the Statistical Analysis System (SAS; Version 9.3 for Windows; SAS Institute, Cary, NC, USA).

3. Results and Discussion

3.1. Chemical Analysis of Water and Soil

The concentrations of nutrients and HMs in TWW, as well as SW, used to irrigate lemon trees in both sites are shown in Table 3. Large quantities of macronutrients and micronutrients were detected in TWW compared to SW. In addition, the amounts of plant nutrients were within the standard limits as specified by JISM [27] and WHO [28], except for Fe and Zn, which exceed the standard limits (Table 3). Furthermore, the concentrations of Na and Cl ions were higher in the TWW compared to SW by 173% and 215%, respectively (Table 3); however, both ions were within the permitted limits of JISM [27] and the WHO [28]. These results are in general agreement with previous studies in which high concentrations of plant nutrients in TWW from WMTP were identified [14,30]. The obtained results of high macronutrient concentrations in TWW are in general agreement with previous studies as these elements were found at high concentrations in treated municipal water effluents [31,32].
Significant high levels of HMs were detected in TWW used for irrigation purposes when compared to SW. For instance, Cr, Cd, Ni, Pb, and Zn concentrations exceeded JISM and WHO standard limits with concentrations of 0.64 mg·L−1, 0.83 mg·L−1, 1.15 mg·L−1, 9.0 mg·L−1, and 22 mg·L−1, respectively (Table 3). This is in general agreement with Al-Habahba et al. [14], who identified high levels of several HMs in TWW from WMTP. On the other hand, low levels were detected for Cu, Mg, and Mn in TWW that were within the limits of JISM and WHO standards (Table 3). Moderate concentrations of Fe were found in TWW used for irrigation with an increase of ~28 times when compared to SW. Variability in the elemental composition of TWW was reported previously in Jordan and was found to depend on the sources of municipal or industrial water effluents. For instance, maximum values of Fe and Cu were recorded with values exceeding 200 and 85 mg·L−1, respectively [21,33], while Manasreh and Alzaydien [34] found high concentrations of Zn, Pb, Cd, and Cr with values of 90, 21, 2.1, and 2 mg·L−1, respectively.
For soil chemical analysis, higher concentrations of nutrients and HMs (except for Cu) were found in soil irrigated for a long time with TWW as compared to SW (Table 4). Soil samples irrigated with TWW were found to contain considerably high levels of N, P, K, and Mg with increases of 4.3, 2.8, 1.2, and 3 times, respectively, in concentrations compared to soil samples irrigated with SW (Table 4). It is well known that TWW contains high concentrations of nitrates, phosphates, and other ions [35,36]. Furthermore, this increase in soil ion content irrigated with TWW is attributed to the high content of OM accumulated over time [37,38]. Furthermore, such increases in the concentrations of essential nutrients suggest a fertilizing effect of TWW that usually enhances the growth of plants [36].
High levels of Na (394.1 mg·kg−1) and Cl (584.1 mg·kg−1) were detected in TWW irrigated soil, which indicates high salt loading in the rhizosphere zone of the lemon trees. Irrigation with TWW is usually accompanied by an increase in the concentrations of various ions, which can have a harmful effect on plants, especially high levels of sodium and chlorine [31]. However, in this study, no toxicity symptoms or physiological disorders were found on the leaves of the studied lemon trees irrigated with TWW (data not shown).
In this study, the HM analysis in the soil showed comparatively low levels of Cu, Cd, Cr, and Ni and their amounts were within the standard limits as specified by FAO/the WHO [39,40] (Table 4), which might suggest the possibility of a higher uptake of these elements by lemon trees. On the other hand, a significant increase in Pb, Fe, and Mn levels was found in soil samples irrigated with TWW when compared to SW samples with average concentrations of 2.44 mg·kg−1, 27.14 mg·kg−1, and 21.55 mg·kg−1, respectively (Table 4).

3.2. Effects of Irrigation with TWW on Nutrients and Heavy Metals Content in Lemon Trees

For nutrient analysis in different parts (leaves, roots, stem bark, and fruits) collected from the lemon trees at both sites, the majority of results showed no significant differences in nutrient concentrations within each part in response to continuous irrigation with TWW or SW (Table 5). The irrigation with TWW resulted in a significant accumulation of Mg in the leaves and roots of the lemon trees with mean values of 5.98 g·kg−1 and 5.78 g·kg−1, respectively, when compared with leaves and roots of the lemon trees irrigated with SW. For N and K concentrations, no significant differences were observed between each plant part at both experimental sites. For leaf Ca concentration, only the leaves of lemon trees irrigated with SW had a significantly higher concentration (17.88 g·kg−1) compared to the leaves of lemon trees irrigated with TWW (11.29 g·kg−1). Previous studies showed that there was no significant increase in macronutrients concentrations in fruits after irrigating citrus orchards with TWW [41], which is consistent with the results of the current study (Table 5).
For HM contents in the lemon tree parts, significant differences were observed among and within different tree parts in both sites (Table 5). For example, the highest concentration of Cu (31.89 mg·kg−1) was observed in the leaves of lemon trees irrigated with TWW, which was significantly different compared to the leaves of lemon trees irrigated with SW (21.10 mg·kg−1). However, Cu concentrations in the bark were not significantly different in trees from both sites. Lead (Pb), Cr, and Fe concentrations were significantly high in the roots of trees irrigated with TWW when compared to trees irrigated with SW or in comparison with their levels in other parts of trees from both sites, except for Cr levels in the bark of TWW irrigated trees (Table 5). The Cd content was found to have the highest mean value in the bark of lemon trees irrigated with TWW; however, no significant differences were observed in the bark of lemon trees irrigated with SW and the leaves of lemon trees irrigated with TWW (Table 5). For Ni and Cr, high concentrations were observed in all parts of lemon trees irrigated with TWW, with clear significant differences compared to trees irrigated with fresh water. The highest concentrations of Ni were also observed in the fruits and leaves of lemon trees irrigated with TWW, which were significantly different when compared to the bark and roots within the same trees (Table 5). On the contrary, Cr concentrations were significantly higher in the roots and bark of lemon trees irrigated with TWW when compared to the leaves and the fruits within the same trees. For Zn, the highest concentration was found in the roots of lemon trees irrigated with SW and it was significantly different compared to other trees’ parts from both sites (Table 5). The fruits of lemon trees irrigated with TWW were also found to have significantly higher concentrations of Cr, Ni, Cd, Pb, Fe, Zn, Cu, and Mn compared to the fruits of lemon trees irrigated with SW (Table 5). In addition, Pb, Cd, and Cr levels in the fruits of lemon trees irrigated with TWW were found to exceed the standard limits as specified by FAO/the WHO [39,40] (Table 5).
The presence of HMs in TWW effluents tends to accumulate in the rhizosphere zone and they become more readily available for uptake by plants. The accumulation of high levels of HMs in lemon fruit tissue observed in this study could be explained by the ability of the root system to remove substantial amounts of HMs from adjacent soil layers causing a depletion zone (Table 4), and then their transportation toward sink tissues, such as fruits [42]. In water-limited environments, the irrigation of lemon trees with TWW is considered a good option to overcome the shortage of irrigation water; however, excessive HM content can be accumulated in the lemon fruits, which is considered harmful to humans [26]. Although the concentrations of HMs in the water and the soil were found to be within the local and international limits (Table 3 and Table 4), significant accumulations of HMs were recorded in different parts of lemon trees after long-term irrigation with TWW (Table 5). High levels of HMs recorded in this study are consistent with previous studies that reported increased levels of Pb, Cd, and Cr contents of TWW-irrigated lemon trees [26,43]. However, in contrast to these studies, moderate concentrations of Cu, Mn, Ni, and Zn were detected in this study.
In spite of the high levels of HMs in response to irrigation with TWW, no clear toxicity symptoms were observed on the leaves of the selected trees, and the macro-nutrient and micro-nutrient concentrations were always found to be within the standard limits [44,45]. The leaf greenness of lemon trees was measured by using an SPAD instrument and trees irrigated with TWW were found to have significantly higher chlorophyll content with a mean value of 42.875, whereas lemon trees irrigated had a significantly lower mean value (31.975). Therefore, the irrigation with TWW might increase the photosynthetic capacity of plants that is associated with higher leaf nitrogen levels [46] and this is in general agreement with the results of this study (Table 5). Hence, using TWW for citrus irrigation is considered a good alternative to help farmers in dry areas to face challenges of water scarcity and poor soil nutrition [36,47].

3.3. Effects of Irrigation with TWW on Bioconcentration Factor of Heavy Metals in Lemon Trees

Bioconcentration factor (BCF) mean values of different metalloids have been used to evaluate the bioaccumulation behavior of HMs in various lemon trees parts as compared to their concentrations in the soil. If the BCF values exceeded one (BCF > 1), this reveals a high accumulation capacity for a metalloid as compared to its concentration in the soil [48]. As shown in Figure 1, the BCF values of HMs that exceeded one were found for all metalloids in all studied lemon tree parts in both sites, except for Mn in lemon fruits and for Cr in the leaves and fruits of lemon trees irrigated with SW (Figure 1). The BCF values of the Fe and Zn for the roots from trees irrigated with SW were significantly higher when compared to BCF values of the roots irrigated with TWW (Figure 1). For the bark, the BCF values for Zn, Fe, Ni, Cd, and Mn were not significantly different for both sites, while the BCF values for Cr and Pb were significantly higher for trees irrigated with TWW. The BCF values showed higher abilities of leaves and fruits of lemon trees irrigated with TWW to accumulate more quantities of metalloids when compared to SW-irrigated trees (Figure 1). For instance, Pb, Cr, and Ni BCF values of lemon tree leaf irrigated with TWW were significantly higher than SW-irrigated trees, with BCF mean values of about 11, 13, and 108, respectively, while the highest BCF value for Mn was recorded for SW irrigated trees. The leaves’ BCF values for Zn, Fe, Cu, and Cd were not significantly different for both sites (Figure 1). Lemon fruits were found to accumulate Fe, Mn, Cu, Ni, Cr, and Cd at various levels in response to the irrigation with TWW (Figure 1). The order of the BCF values of HMs for all parts of lemon tree irrigated with SW ranked as follows: Ni > Fe > Cu > Cd > Zn > Mn > Pb > Cr. However, the order of BCF values for TWW-irrigated trees exhibited the following ascending trend: Ni > Cu > Fe > Cd > Zn > Pb > Cr > Mn.
The BCF values are commonly used to evaluate the accumulation ability of plant parts for a specific metalloid from the soil of the rhizosphere zone [49]. Heavy metals with higher BCF values indicate a greater opportunity for their translocation to the aboveground parts [50]. Therefore, the BCF could be used for health risk assessments related to the accumulation of HMs in the food chain [51]. The results of this study are in general agreement with [52], who found that the lemon bark and leaves accumulated high concentrations of Cu, Pb, and Cd. In addition, leaves were found to accumulate more Mn and Cu than other tissues, whereas roots accumulated more Fe and Zn [14]. Similar responses were also observed in other studies for lemons and other species indicating a high potential for accumulating metalloids, such as Ni, Cd, Cd, Zn, and Pb, from soil to different tree parts [14,53,54]. High BCF values for Ni, Cd, Cr, and Pb were reported for many plant products irrigated with TWW, which present potential risks to humans [50,55].

3.4. Effects of Irrigation with TWW on Translocation Factor of Heavy Metals in Lemon Trees

Translocation factors (TF) were measured to evaluate the effect of irrigation with TWW on the transfer levels of HMs from the roots to other organs in lemon trees. From this perspective, any plant part is considered an accumulator for a HM once its TF values are >1 [48]. In this study, the TF values of all tested HMs in different lemon tree parts in both sites exhibited the following descending trends: Leaf > bark > fruit, with clearly higher TF means values for lemon trees irrigated with TWW compared to SW (Figure 2). Therefore, the ability of lemon trees to translocate HMs to their areal parts was considerably higher in response to continuous irrigation with TWW. Low Fe and Pb translocation rates for all areal trees parts were observed in both sites with mean values <1 (Figure 2). For Mn and Cu, they were the most actively translocated HMs in lemon tree leaves irrigated with SW with TF with mean values of 3.87 and 2.31, respectively. The TF values of Ni and Cr were the highest for stem bark for the same site (Figure 2). On the other hand, the highest translocation rates for Zn (1.69) were observed in the leaves of trees irrigated with TWW, while Cd translocation rate was the highest for lemon tree bark irrigated with TWW with TF mean values of 6.0 (Figure 2). The irrigation of lemon trees with TWW resulted in higher translocation rates for Zn, Mn, Cu, Cd, and Pb in the leaves compared to stem bark and fruits with TF values of 1.05. 0.07, 1.47, 4.31, and 0.65, respectively. In addition, the effect of continuous TWW irrigation obviously increased translocation rates of Cd, Ni, and Zn towards lemon fruits with TF values of 1.32, 1.32, and 1.05, respectively (Figure 2). On the other hand, low translocation rates of Fe, Mn, and Pb toward the fruits were observed in lemon trees irrigated with TWW with TF averages of 0.09, 0.07, and 0.27, respectively. Although the TF mean values of Cr and Cu in the fruits were <1 after TWW irrigation, they increased at a noticeable rate with mean values that reached 0.52 and 0.80, respectively (Figure 2). Plant parts featuring TF values <1 are considered metal excluders and they can prevent metal accumulation inside plant tissues and restrict root-to-shoot translocation of HMs [51]. The TF values of >1 for Cd, Ni, and Zn toward lemon fruits suggest a hazardous potential of lemon trees to translocate HM elements. Previous studies recommended a wise use of TWW to irrigate crops to avoid high levels of HM accumulation in edible parts [47,56]. Although TWW contains reasonable amounts of nutrients, the continuous use of TWW without combining it with freshwater may cause the transfer of harmful heavy metals toward the fruit, especially in perineal trees [26,36,57].

4. Conclusions

This study investigated the influence of continuous and long-term use of TWW for irrigating lemon orchards in arid environments. The use of available plant nutrients from TWW, as well as the uptake translocation and partitioning of heavy metals (HMs) in lemon trees, was analyzed. The irrigation of lemon trees with TWW provided the plants with valuable amounts of primary macronutrients (N, P, K), which would reduce reliance on chemical fertilizers. However, the long-term use of TWW in lemon orchards requires a scheduled irrigation regime, as this source of water contains high concentrations of HMs as compared to SW. The results of this study indicate that continuous irrigation using TWW resulted in the accumulation of HMs at various quantities in different aerial parts of the lemon trees. This was obviously clear for Cd and Pb, whose concentrations in fruit tissues exceeded the permissible levels, highlighting the urgent need to reduce their levels in TWW used for irrigation and the need to identify the direct sources for water contamination. Moreover, the uptake and partitioning of various HMs by different plant parts were correlated to their concentrations in treated wastewater and the soil. In conclusion, one of the biggest constraints for the use TWW in irrigation is that lemons seem to have the potential to be accumulators for some harmful metalloids, such as Cd and Ni, and therefore caution should be considered. Therefore, there is an urgent need to improve the process of wastewater treatment to reduce Cd and Ni accumulation as well as to identify sources of HM contamination and take suitable measurements to avoid their deposition in surrounding environments. Finally, it is necessary to assess the possibility of integrating TWW and SW within irrigation programs to reduce the transfer of such harmful elements to the fruits and therefore to the human diet.

Author Contributions

R.N.A. and R.S.A.-S. conceived and designed the experiments, analyzed the data and wrote the manuscript. J.S.A.-H., K.A.A.-H. and Z.B.A.-R. helped in chemical analysis of soil, water and plant samples. J.Y.A. helped in data and statistical analysis and manuscript preparation. All authors edited and provided a critical review of the initial draft of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded partially by the Genome Seeds LLC Company.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data sets supporting the results of this article will be freely available upon request to the corresponding author.

Acknowledgments

We sincerely acknowledged Ayed Al Abdallat for his scientific advice and Mohammed Nael Omar (the Genome Seeds LLC manager) for his continuous support of scientific research.

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 08 00514 g001 550
Figure 1. Bioconcentration factors (BCF) of different heavy metals in different parts of lemon trees irrigated with spring water (SW) and treated wastewater (TWW) at the Wadi-Musa region. Bars represent mean ± SD (n = 4). Different letters indicate significant differences according to LSD (p < 0.05).
Figure 1. Bioconcentration factors (BCF) of different heavy metals in different parts of lemon trees irrigated with spring water (SW) and treated wastewater (TWW) at the Wadi-Musa region. Bars represent mean ± SD (n = 4). Different letters indicate significant differences according to LSD (p < 0.05).
Horticulturae 08 00514 g001
Horticulturae 08 00514 g002 550
Figure 2. Translocation factors (TF) of different heavy metals in different parts of lemon trees irrigated with treated wastewater (TWW) and spring water (SW) in the Wadi-Musa region. Bars represent mean ± SD (n = 4). Different letters indicate significant differences according to LSD (p < 0.05).
Figure 2. Translocation factors (TF) of different heavy metals in different parts of lemon trees irrigated with treated wastewater (TWW) and spring water (SW) in the Wadi-Musa region. Bars represent mean ± SD (n = 4). Different letters indicate significant differences according to LSD (p < 0.05).
Horticulturae 08 00514 g002
Table
Table 1. Soil physicochemical properties at both Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) experimental sites. The data are averages ± SD (n = 4).
Table 1. Soil physicochemical properties at both Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) experimental sites. The data are averages ± SD (n = 4).
ParameterUnitWMTPAM
Sand20–200 µm, (% weight)71.21 ± 1.4573.67 ± 1.62
Silt2–20 µm, (% weight)18.81 ± 1.5416.42 ± 1.05
Clay<20 µm, (% weight)9.99 ± 1.169.91 ± 1.37
ECdS·m−12.10 ± 0.261.85 ± 0.91
pHpH unit7.60 ± 0.797.80 ± 0.85
OMg·kg−112.10 ± 1.283.40 ± 0.52
CaCO3g·kg−113.12 ± 1.2215.92 ± 1.73
Table
Table 2. Chemical and biological properties of irrigation water from Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) sites during 2021. The data are averages ± SD (n = 4).
Table 2. Chemical and biological properties of irrigation water from Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) sites during 2021. The data are averages ± SD (n = 4).
ParameterWMTPAMJISM 1WHO 2
pH7.57 ± 0.697.86 ± 0.546.0–9.06.5–8.0
EC (dS·m−1)2.68 ± 0.401.45 ± 0.221.0–3.00.7–3.0
BOD (mg·L−1)16.73 ± 1.50060300
COD (mg·L−1)34.13 ± 2.530120500
TDS (mg·L−1)629.05 ± 35.4240.38 ± 3.12<2000450–2000
SAR (ratio)8.38 ± 0.931.56 ± 0.579<13
Total Coliforms (MPN/100 mL)1.85 ± 0.060<10<9
1 JISM: Jordan Institution for Standard and Measurements standards. 2 WHO: World Health Organization standards.
Table
Table 3. Chemical analysis of irrigation waters from both Treated wastewater (TWW) and spring water (SW) sources compared with allowable Jordanian (JISM) and WHO standard limits for irrigation water. The data are averages ± SD (n = 4).
Table 3. Chemical analysis of irrigation waters from both Treated wastewater (TWW) and spring water (SW) sources compared with allowable Jordanian (JISM) and WHO standard limits for irrigation water. The data are averages ± SD (n = 4).
ElementTWWSWJISM 1WHO 2
PO4 (mg·L−1)15.67 ± 1.691.27 ± 0.0230.0030.00
NO3− (mg·L−1)20.81 ± 3.991.4 ± 0.5045.0050.00
N (mg·L−1)13.23 ± 1.620.7 ± 0.0650.005.00–50.00
K (mg·L−1)27.84 ± 2.037.92 ± 1.0080.0080.00
Ca (mg·L−1)91.05 ± 7.11112.2 ± 12.1400.00230.00
Na (mg·L−1)92.18 ± 5.8753.16 ± 4.15230.0069.00–207.00
Cl (mg·L−1)118.25 ± 9.0454.94 ± 5.38400.00140.00–350.00
Mg (mg·L−1)16.27 ± 1.4327.50 ± 3.4060.0060.00
Fe (mg·L−1)4.55 ± 0.510.16 ± 0.015.000.10–1.50
Zn (mg·L−1)22.00 ± 0.1328.00 ± 0.362.00<2.00
Mn (mg·L−1)0.02 ± 0.010.02 ± 0.001-0.20
Cu (mg·L−1)0.01 ± 0.0010.02 ± 0.002-0.20
Cr (mg·L−1)0.64 ± 0.340.01 ± 0.001-0.02
Ni (mg·L−1)1.15 ± 0.100.05 ± 0.02-0.20
Cd (mg·L−1)0.83 ± 0.300.01 ± 0.0020.01<0.01
Pb (mg·L−1)9.00 ± 1.210.03 ± 0.0025.00<5.00
1 JISM: Jordan Institution for Standard and Measurements standards. 2 WHO: World Health Organization standards.
Table
Table 4. Soil chemical analysis of various ions at both Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) experimental sites. The data are averages ± SD (n = 4).
Table 4. Soil chemical analysis of various ions at both Wadi-Musa Wastewater Treatment Plant (WMTP) and Ain Mousa (AM) experimental sites. The data are averages ± SD (n = 4).
ElementWWTPAMFAO/WHO 2
N total (g·kg−1)13.90 ± 1.103.20 ± 0.27-
K (mg·kg−1)684.20 ± 25.00245.10 ± 16.4-
P (mg·kg−1)94.80 ± 5.0376.80 ± 23.5-
Na (mg·kg−1)394.10 ± 17.80110.00 ± 6.14-
Cl (mg·kg−1)584.10 ± 20.2058.00 ± 4.81-
Mg (mg·kg−1)140.00 ± 6.04047.20 ± 3.27-
Fe (mg·kg−1)21.60 ± 3.038.43 ± 1.5050,000
Zn (mg·kg−1)11.30 ± 1.527.56 ± 4.6360
Mn (mg·kg−1)27.10 ± 2.5515.20 ± 1.032000
Cu (mg·kg−1)3.30 ± 0.213.60 ± 0.25100
Cr (mg·kg−1)0.09 ± 0.010.03 ± 0.01100
Ni (mg·kg−1)0.08 ± 0.01N.D. 150
Cd (mg·kg−1)0.03 ± 0.010.004 ± 0.0013.0
Pb (mg·kg−1)2.44 ± 0.230.004 ± 0.001100
1 N.D.: Not detected. 2 Maximum limits for the presence of HMs in the soil as defined by FAO and WHO [39,40].
Table
Table 5. Concentration of nutrients and heavy metals in the roots, stem bark, leaves, and fruits of lemon trees irrigated continuously with treated wastewater (TWW) and spring water (SW) at both experimental sites.
Table 5. Concentration of nutrients and heavy metals in the roots, stem bark, leaves, and fruits of lemon trees irrigated continuously with treated wastewater (TWW) and spring water (SW) at both experimental sites.
N (g·kg−1)K (g·kg−1)Ca (g·kg−1)Mg (g·kg−1)
PartSWTWWSWTWWSWTWWSWTWW
Root7.32b 18.53b21.34ab24.27a11.82bc11.29bc3.88b5.78a
Bark3.58c4.19c14.09d16.15cd10.28c9.82c1.49d2.57c
Leaf13.13a15.35a17.08c18.91b17.88a11.85b3.95b5.98a
Fruit2.19d5.12c13.16d14.61d0.81d0.74d0.38e0.46e
Fe (mg·kg−1)Zn (mg·kg−1)Mn (mg·kg−1)Cu (mg·kg−1)
PartSWTWWSWTWWSWTWWSWTWW
Root294.50b431.63a69.44a19.83c9.63d12.54cd9.63d25.15b
Bark138.56f182.18d13.81d12.56de13.19c23.15b17.44bc16.00c
Leaf160.38e212.69c27.25b33.18b36.19a31.89ab21.10bc35.81a
Fruit 29.26h38.65g10.50e20.61c0.12f0.84e0.40e17.25bc
Cr (mg·kg−1)Ni (mg·kg−1)Cd (mg·kg−1)Pb (mg·kg−1)
PartSWTWWSWTWWSWTWWSWTWW
Root0.29d2.81a0.70d3.93bc1.30b0.40d3.20d27.20a
Bark0.43d2.70ab0.70d2.95c1.58ab1.98a1.46e16.46b
Leaf0.04f2.11bc0.41e4.60ab0.78c1.58ab1.00e16.86b
Fruit0.15e1.46c0.40e5.15a0.05e0.46d1.27e7.46c
1 Different letters indicate significant differences according to LSD (p < 0.05). 2 Maximum limits for the presence of HMs in the plant tissue as defined by FAO and the WHO [39,40] are as follows: Fe (425 mg·kg−1), Zn (100 mg·kg−1), Mn (500 mg·kg−1), Cu (73 mg·kg−1), Cr (1.3 mg·kg−1), Ni (67 mg·kg−1), Cd (0.10 mg·kg−1), Pb (0.30 mg·kg−1).
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Albdaiwi, R.N.; Al-Hawadi, J.S.; Al-Rawashdeh, Z.B.; Al-Habahbeh, K.A.; Ayad, J.Y.; Al-Sayaydeh, R.S. Effect of Treated Wastewater Irrigation on the Accumulation and Transfer of Heavy Metals in Lemon Trees Cultivated in Arid Environment. Horticulturae 2022, 8, 514. https://doi.org/10.3390/horticulturae8060514

AMA Style

Albdaiwi RN, Al-Hawadi JS, Al-Rawashdeh ZB, Al-Habahbeh KA, Ayad JY, Al-Sayaydeh RS. Effect of Treated Wastewater Irrigation on the Accumulation and Transfer of Heavy Metals in Lemon Trees Cultivated in Arid Environment. Horticulturae. 2022; 8(6):514. https://doi.org/10.3390/horticulturae8060514

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Albdaiwi, Randa N., Jehad S. Al-Hawadi, Ziad B. Al-Rawashdeh, Khaled A. Al-Habahbeh, Jamal Y. Ayad, and Rabea S. Al-Sayaydeh. 2022. "Effect of Treated Wastewater Irrigation on the Accumulation and Transfer of Heavy Metals in Lemon Trees Cultivated in Arid Environment" Horticulturae 8, no. 6: 514. https://doi.org/10.3390/horticulturae8060514

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