The effect of three types of aquatic plants on water purification and removal of cadmium under different salinity conditions in northwestern Iran

Parameter

Description

Mn

Manganese

Fe

Iron

Zn

Zinc

N

Nitrogen

K

Potassium

Mn

Manganese

Cu

Copper

Ca

Calcium

Mg

Magnesium

Na

Sodium

P

Phosphorus

Cadmium (Cd) pollution in the environment has increased in recent years (Alloway 1995; Rahimi et al. 2021). Cadmium is one of the toxic heavy metals that negatively affect the environment, especially living organisms. It can enter the human food chain in various forms and endanger our health (Rahimi et al. 2021). According to the US Department of Health, there is ample evidence for the carcinogenicity of Cd and its compounds in humans. Cadmium can cause kidney, bone, liver, and blood cancer (Sari & Tuzen 2008; Jiang et al. 2021; Kiani et al. 2021).

It is costly to clean heavy metals from contaminated soil and water. Therefore, efforts have been made to develop practical and cost-effective technologies to rehabilitate degraded lands and polluted waters (Dodangeh et al. 2018; Ansari et al. 2020). Plants used for wastewater treatment and heavy metals absorption must resist salinity because effluents contain large amounts of soluble salts. The harmful effects of salinity on plant growth occur by reducing major processes such as photosynthesis, protein synthesis, and energy and lipid metabolism (Agastian et al. 2000). Water salinity can affect plant growth rate and metal uptake capacity (Parida & Das 2005).

Phytoremediation is a promising method for soil and water purification. In this method, plants absorb or extract contaminants from water and soil (Baker et al. 1994; Yan et al. 2020; Kamal et al. 2021). This method is less expensive than other conventional technologies and is environmentally friendly (Ali et al. 2013; Sharma & Pandey 2014). Kara & Kara (2005) used Duckweed (Lemna trisulca L.) to remove Cd from water. The researchers showed that Duckweed could remove 75% to 85% of Cd per 100 mL. The plant absorbs Cd at a high rate. The results of the Stêpniewska et al. (2005) study in Poland on Lead (Pb) and Cd uptake by Azolla Caroliniana showed Pb concentration reduction up to 90% and Cd concentration reduction up to 22% in contaminated water. However, Azolla Caroliniana's growth dropped between 22% and 47% compared to the control case. The effect of salinity and soil reaction on the biological accumulation of different Cd levels was investigated in Helianthus Annus. With increasing salinity, metal accumulation in roots and stems increased steadily (Bhargavi & Sudha 2013).

Due to the drought trend in many countries, remediation of water contaminated with Cd and other toxic elements is essential. The study of different plants in saline conditions is of particular importance for managing and treating contaminated water. Therefore, considering the importance of water purification, the purpose of this study was to investigate the Cd uptake by three plants, such as Azolla Caroliniana, Watercress (Nasturtium officinale), and Duckweed (Lemna minor L.), and changes in the concentration of some elements in these plants under different salinity stress conditions.

The study area was located in Zanjan province which is situated in northwestern Iran. Three plants, Azolla Caroliniana, Watercress, and Duckweed, were opted to perform this study. Plastic containers with a depth of 20 cm and a 15 cm diameter were used to grow plants. In this experiment, an Epestin nutrient solution with half concentration or ionic strength was used. Table 1 presents the composition of Epstein's nutrient solution.

The cadmium absorption potential of the opted plants was investigated from nutrient solutions with different salinities. The experiments were carried out factorially in a completely randomized design with three replications in the greenhouse. In these experiments, levels of Cd from the CdSO₄ source were 0, 5, 10, 20, 40, and 80 mg L⁻¹, and soluble salt concentrations from the NaCl source were 0, 10, 20, 40, and 80 mM prepared and added to Epstein's nutrient solution. Three aquatic plants Azolla, Watercress, and Duckweed, were grown in these prepared solutions (A total of 90 samples). After 30 days, the plants were removed from each container, washed with distilled water, and dried in an oven at 55 °C for 72 hours. Then, plant samples were milled, and after their digestion in the laboratory, their element contents were measured.

The content of heavy metals in plants was measured according to Figueroa et al. (2008). The amount of heavy metals such as Manganese (Mn), Iron (Fe), Zinc (Zn), Copper (Cu), Calcium (Ca), Magnesium (Mg), and Cd in the plants was measured using atomic absorption (spectrophotometer model Varian 220). Total Nitrogen (N) was measured using the Kjeldahl method (Sparks et al. 1996), Potassium (K) content was determined using the Flame photometer through digestion (Moradi 2002). Phosphorus (P) content was measured using the ammonium molybdate method (Cottenie 1980). The data analyses were performed using SAS 9¹ software, and Duncan's test at the 5% level was used to compare the data mean.

The results presented in Table 2 show that the highest concentration of Cd in the Duckweed plant was in Cd₅S₄ treatment with an average of 4,137.23 mg kg⁻¹ of its dried tissue and the lowest value was in the control treatment with an average concentration of 13.32 mg kg⁻¹. The interaction of salinity and Cd in nutrient solution increased the absorption of Cd in Duckweed. Increasing the salinity and Cd concentration of the nutrient solution has led to an increase in the Cd concentration in Azolla (Table 2). The highest concentration of Cd in Azolla was in Cd₄S₄ treatment with an average of 3,470.4 mg kg⁻¹. In Azolla, at concentrations above 40 mg Cd per liter of nutrient solution, Cd uptake decreased. Through comparing the means of interactions between salinity and soluble Cd, it was shown that the Cd concentration of the Watercress plant was highest in Cd₅S₄ and Cd₅S₃ treatments with 4,220.53 and 4,115.89 mg kg⁻¹, respectively. Many factors such as salinity, pH, redox potential, the concentration of metals in the growth medium affect the absorption of metals from the environment. Greger et al. (1995) stated that sodium (Na) ions could release Cd from sediment into the water and increase the Cd concentration. Smolder et al. (1998) reported that salinity is one of the significant factors influencing plant motility and Cd absorption. The results of this study are similar to the research conducted by Ozkutlu et al. (2007), in which they reported that Cd concentration in the plant increased as NaCl content increased. Mandakini et al. (2016) also show that Azolla is beneficial for Cd uptake and phytoremediation.

Table 3 presents the changes in the absorption of different elements in Azolla in various treatments. The highest N concentration, with an average of 2.5%, was related to the control treatment (Cd₀S₀) (Table 3). Increasing the salinity concentration and Cd content negatively affected the N concentration of Azolla. The lowest N concentration was measured in Cd₅S₄ treatment (Table 3). It can be inferred that both salinity and Cd reduced N concentrations in the plant. Shirazi et al. (2012) reported that Cd significantly reduced N content in seven rice cultivars. The significant drop in N concentration as salinity increases possibly results from Na and Cl ions interaction with NH₄ and NO₃ ions, respectively (Ben-Gal & Shani 2003). The highest concentration of K was observed in Azolla in the control treatment, which is 1.76%. It is also shown that Cd content and salinity adversely affected the K concentration in the plant. The lowest amount of plant K with a concentration of 0.145% is related to Cd₅S₄ treatment (Table 3). Replacement of K by Na in Azolla under saline conditions reduced K uptake (van Kempen et al. 2013). Nocito et al. (2002) stated that Cd reduced K uptake through the plant roots but did not affect P uptake.

Based on the mean comparison results, the highest Ca concentration was obtained from Cd5S0 treatment with an average of 5.42% (Table 3). Calcium concentration in the plant tissues increased with Cd but increasing the salinity prevented its absorption. The lowest Ca concentration with an average of 1.07% was related to Cd₀S₄ treatment. As mentioned above, Ca concentration increased with Cd, probably due to the relative content of Ca and K ions within the sample. The absorption potential of Ca increases with a decrease in the K concentration due to Cd elevation. By comparing the mean interactions of salinity and Cd levels (Table 3) on the plant's Mg concentration, it was found that the highest Mg concentration was obtained from the control treatment with an average of 0.77%. The lowest plant Mg concentration with a relative 54% reduction was related to Cd₅S₄ treatment with an average concentration of 0.36% (Table 3).

The interaction of different salinity levels and Cd on Fe concentration in Azolla was meaningful at a 5% probability level (Table 3). Fe concentration decreased in Azolla tissues under salinity and Cd stresses. The highest Fe concentration was obtained in the control plant with an average of 686.4 mg kg⁻¹ in dried tissues. Salinity and Cd treatments individually reduced Fe uptake, and their interaction further reduced the plant Fe concentration, which was expected. The lowest Fe concentration was related to Cd₅S₄ treatment with an average of 237.4 mg kg⁻¹ (Table 3). Based on the results of the analysis of the variance table, the interaction of salinity and Cd levels on Mn concentration in Azolla was meaningful at the level of 1% probability (Table 3). Increasing the concentration of Cd in the nutrient solution increased the Mn concentration in the plant tissues, while salinity decreased it. The highest and lowest Mn concentrations were from Cd₅S₀ and Cd₁S₄ treatments with averages of 266.4 mg kg⁻¹ and 165.9 mg kg⁻¹ of dried tissues, respectively. Increased Mn concentration in chickpea plants with increasing soil Cd concentration has been reported by Hernandez et al. (1996), probably due to the interaction of Fe and Mn ions. In addition, the plant's Fe concentration decreased with Cd concentration in the growing medium.

The results of data analysis showed that the interaction of different salinity and Cd levels on Zn concentration in Azolla was meaningful at a 5% probability (Table 3). The highest concentration of Zn with an average of 224.9 mg kg⁻¹ was obtained from the control treatment (Cd₀S₀). Increasing salinity and Cd concentration decreased Zn uptake, and the lowest Zn concentration was observed in Cd₅S₄ treatment with an average of 94.96 mg kg⁻¹. Abdel-Sabour et al. (1988) stated that the presence of Cd causes problems in the zinc and other trace elements transfer in the plant. The variance analysis showed that the interaction of salinity and Cd levels on Na concentration of Azolla was also meaningful at the level of 5% probability (Table 3). According to the comparison of the mean data, the highest Na concentration was obtained from Cd₅S₄ treatment. Increasing both salinity and Cd factors increased Na concentration within plant tissues. The lowest plant Na concentration was observed in Cd₀S₀ and Cd₁S₀ treatments with 229.8 and 257.8 mg kg⁻¹, respectively which did not differ significantly. Khellaf & Zerdaoui (2010) examined the growth response of blue lentils to the bioaccumulation of Copper and Nickel. They found that blue lentils were resistant to the presence of ≤0.3 mg L⁻¹ copper and ≤0.5 mg L⁻¹ nickel. When copper in the growing medium reached 0.45 mg L⁻¹ and nickel reached 0.75 mg L⁻¹, the plant growth decreased by 50%. Their results also showed that blue lentils accumulated much more copper in their tissues than nickel. Xue et al. (2012) investigated the bioaccumulation and speciation of arsenic in aquatic macrophytes Ceratophyllum Demersum L, and their results showed a significant accumulation of arsenic (862–963 μg g⁻¹) in plant branches when exposed to 10 mM of arsenate and arsenite, regardless of whether arsenate or arsenite was supplied to the plant. Arsenite was the predominant species in plant tissues.

The results showed that the interaction of salinity and Cd on the N concentration of Watercress was meaningful at the level of 5% probability (Table 4). Through comparing the means of interaction between salinity and Cd levels on plant N concentration (Table 4), it was found that Cd₀S₀ and Cd₁S₀ treatments with averages of 1.614% and 1.572% were the highest N plant concentrations. The N concentration in plant tissues decreased with increasing the Cd concentration and salinity in the nutrient solution. The lowest plant N concentrations were related to Cd₂S4 and Cd₅S₄ treatments with 1.482% and 1.48% averages, respectively.

The interaction of salinity and Cd levels on the K concentration of Watercress tissues was meaningful at a 5% probability level (Table 4). The highest K concentration of Watercress tissues was related to Cd0S0 treatment. With increasing Cd concentration and salinity in the nutrient solution, the K tissue concentration of plant tissues decreased. Its lowest value was observed at the highest salinity and Cd concentration (Cd₅S₄) (Table 4). According to the obtained results, it can be stated that salinity has intensified the adverse effect of Cd on plant K concentration. Subsequently, the interaction of salinity and Cd has further reduced the K concentration of the Watercress. Increasing the amount of Na in plant tissues may lead to changes in the osmotic pressure of cells. This factor causes plasmolysis and reduces the selective uptake in root cells (Pessarakli 1999).

The interaction of different salinity and Cd levels on the P concentration of Watercress was significant at the level of 5% probability (Table 4). The highest P concentration was obtained from Cd₀S₀ and Cd₀S₁ treatments with an average of 1.07% and 1.02%. Increasing the salinity and Cd concentration of the nutrient solution decreased the plant P uptake. The lowest plant P concentration with an average of 0.32% was assigned to Cd₅S₄ treatment. Each of the salinity and Cd treatments adversely affects the plant P concentration. Their interaction had a more severe effect on plant P concentration. Cadmium toxicity may cause P deficiency or problems in P transfer within the plant (Haghiri 1974).

The interaction of different salinity and Cd levels on the Ca concentration of Watercress was significant at a 5% probability level (Table 4). The maximum plant Ca concentration was obtained from Cd₀S₀ treatment with an average of 5.74%. Like their simple individual effects, the interaction of salinity and Cd reduced the Ca concentration in the plant. The minimum Ca concentration of the plant was observed from Cd₅S₄ treatment with an average concentration of 1.11% (Table 4). Hu & Schmidhalter (2005) attribute the lack of calcium in saline conditions to competition between Na and Ca elements and an increase in the Na/Ca ratio in the plant. According to the results of comparing the mean of the data (Table 4), the highest amount of plant Mg with an average of 0.86% was related to the control treatment. The lowest concentration of Mg with an average of 0.36% was observed in Cd₅S₄ treatment.

The interaction of different salinity and Cd levels on Mn concentration of Watercress was significant at the level of 1% probability (Table 4). Based on comparing the mean data obtained from the interaction of salinity and Cd on Mn concentration, the highest plant Mn concentration was observed in Cd₄S₀ and Cd₅S₀ treatments with mean concentrations of 267.6 and 268.2 mg kg⁻¹, respectively (Table 4). The Mn concentration increased with Cd of the nutrient solution but decreased as salinity increased. The lowest concentration of Mn with an average of 1.192 mg kg⁻¹ was related to Cd0S4 treatment. Based on the comparison of the mean data (Table 4), the highest Zn concentration was obtained from the Cd₀S₀ treatment with an average of 71.4 mg kg⁻¹. Cd₅S₄ treatment had the lowest Zn content (with an average of 16.7 mg kg⁻¹) with a 77% reduction compared to the control. Yildiz (2005) stated in a study that with increasing Cd levels, Zn concentration decreased in both tomato and corn. The decrease in Zn concentration following the increase in Cd concentration is probably due to the chemical similarity of these two elements and their antagonistic relationship in adsorption.

The interaction of different salinity levels and Cd on plant Cu concentration was meaningful at the level of 5% probability (Table 4). Cd₅S₀ treatment had the highest Cu concentration with an average of 40 mg kg⁻¹ of the plant tissues. Increasing salinity decreases the Cu concentration. The lowest Cu concentration of the plant was observed in Cd0S4 treatment, with an average of 12.77 mg kg⁻¹ (Table 4). Anjum (2008) reported that trace elements Fe, Zn, Cu, and Mn in citrus leaves and roots decreased with increasing salinity (80 mM). The highest Na concentrations in Cd₄S₃, Cd₅S₃, and Cd₅S₄ treatments were 3,759.8, 4,039.2, and 4,123 mg kg⁻¹, respectively. The lowest Na content was obtained from Cd₀S₀ and Cd₁S₀ treatments with averages of 483.3 and 575.4 mg kg⁻¹, respectively (Table 4).

The interaction of different salinity and Cd levels on N concentration in Duckweed was meaningful at a 5% probability level (Table 5). Comparison of the data means showed that the interaction of salinity and Cd levels reduced the N uptake. Maximum plant N concentration was observed in Cd₀S₀ treatment with an average of 0.875%. In Cd₅S₄ treatment, the lowest N value was obtained with an average of 0.146%. Cadmium disrupts N metabolism by inhibiting the activity of the enzymes glutamine synthetize, glutamate syntheses, nitrate reductase, and the nitrate reduction process (Wang et al. 2008).

Based on the comparison of the mean data, the control treatment with an average of 1.08% had the highest K concentration. With increasing salinity and Cd levels in the nutrient solution, K concentration decreased (Table 5). The lowest K concentrations were measured in three treatments of Cd₃S₄, Cd₄S₄, and Cd₅S₄ with averages of 0.24%, 0.23%, and 0.21%, respectively. Haouari et al. (2012) reported that the concentration of Cl and Na ions in the plant increased with salinity. In that condition, the amount of K decreased, and Cl and Na caused plant poisoning. Metabolic Na toxicity results from the ability of this ion to compete with K ions to attach to major sites for cell functions. More than 50 enzymes are activated by K, and Na cannot substitute these enzymes (Tester & Davemport 2003).

The interaction of different salinity and Cd levels on the Ca concentration of the Duckweed plant was meaningful at the level of 5% probability (Table 5). The highest Ca concentration was obtained from Cd₀S₀, Cd₀S₁, and Cd₁S₀ treatments with averages of 3.9, 3.7, and 3.7%, respectively, which were not significantly different. The interaction between Cd and salinity caused a sharp decrease in Ca concentration in this plant. The lowest Ca concentration was observed in the treatment containing the highest concentration of Cd and salinity (Cd₅S₄) (Table 5). Cadmium accumulation in many plants causes Fe, Mg, and Ca deficiency. It stops chlorophyll synthesis and drastically reduces growth rate and photosynthesis (Mobin & Khan 2007).

The analysis of variance showed that the interaction of different salinity and Cd levels on the Fe concentration of the Duckweed plant was significant at the level of 1% probability (Table 5). The highest plant Fe concentration was obtained in Cd₀S₀ treatment with an average of 566.16 mg kg⁻¹. The interaction of Cd and salinity levels reduced the Fe concentration so that the lowest Fe concentration was found in Cd₅S₄ treatment with an average of 223 mg kg⁻¹ (Table 5). The Fe concentration decreasing with increasing Cd content was due to antagonistic effects of these two elements and reported in Wong et al. (1984).

The interaction of different salinity and Cd levels on plant Mn concentrations was significant at the 5% probability level (Table 5). The highest concentration of plant Mn with an average of 311 mg kg⁻¹ was related to Cd₅S₀ treatment. The lowest concentration was observed in Cd₄S₄ treatment, with an average concentration of 203.2 mg kg⁻¹ (Table 5). Based on the results of data analysis (Table 5), the interaction of salinity and Cd on Cu concentration in Duckweed was significant at the level of 5% probability. The highest Cu concentration was obtained from Cd₀S₀ treatment with an average of 42.76 mg kg⁻¹. The lowest amount of Cu was observed in Cd₅S₄ treatment with an average of 8.33 mg kg⁻¹ (Table 5). Decreasing the concentration of trace elements in plants contaminated with heavy metals under saline conditions can be attributed to increased concentration of heavy elements and Na and their antagonistic relationship with trace elements. The highest Na concentration was obtained from Cd₀S₄ treatment with an average of 1,326.3 mg kg⁻¹. The lowest concentration of Na in the plant was obtained in Cd₅S₀ treatment with 134.1 mg kg⁻¹ of the plant tissues.

This study showed that Azolla Caroliniana, Watercress, and Duckweed plants absorbed high concentrations of Cd. Cadmium uptake increased with the salinity concentration, and consequently, its content was elevated in the tissues of Azolla Caroliniana, Watercress, and Duckweed. Also, increasing the concentration of Cd in the nutrient solution decreased the concentrations of N, K, P, Mg, Fe, and Zn and increased the concentrations of Ca, Mn, Cu, and Na in Azolla Caroliniana. The results showed that increasing the concentration of Cd in the nutrient solution decreased the concentrations of N, K, P, Ca, Mg, Fe, and Zn, increasing the concentrations of Mn, Cu, and Na in Watercress and Duckweed. It has also been shown that increasing the salinity concentration decreased N, K, P, Mg, Fe, Mn, Zn, and Cu and increased Na in Azolla Caroliniana, Watercress, and Duckweed. It can be concluded from this study that the three opted plants help purify Cd-contaminated water. In general, according to the obtained results, these plants can be recommended for phytoremediation and removal of heavy metals, especially Cd, in unsuitable aqueous systems in the presence of salinity. This approach can be used in future studies to alleviate the cadmium pollution in water resources.

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The subject of plagiarism has been considered by the authors and this article is without problem.

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