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Article

Heavy Metal Content in Medicinal Plants Grown in Hydroponics and Forest Soil in the Central Part of Western Siberia

by
Maksim A. Mulyukin
1,*,
Oleg S. Sutormin
1,2,
Zoya A. Samoylenko
1,
Inessa V. Kravchenko
1,
Elena V. Bulatova
1,
Natalia M. Gulakova
1,
Denis A. Baranenko
1,3 and
Yuliya Yu. Petrova
1
1
Institute of Nature and Technical Sciences, Surgut State University, Surgut 628412, Russia
2
Department of Biophysics, School of Fundamental Biology and Biotechnology, Siberian Federal University, Krasnoyarsk 660041, Russia
3
Faculty of Biotechnologies, ITMO University, Saint-Petersburg 197101, Russia
*
Author to whom correspondence should be addressed.
Forests 2024, 15(9), 1606; https://doi.org/10.3390/f15091606
Submission received: 30 July 2024 / Revised: 5 September 2024 / Accepted: 7 September 2024 / Published: 11 September 2024
(This article belongs to the Section Forest Soil)

Abstract

:
The Khanty-Mansi Autonomous Okrug-Yugra, situated within Russia’s Far North, has undergone substantial industrialization and economic development. However, it is confronted with considerable environmental challenges, notably soil contamination. This study examines the presence of heavy metals (lead, cadmium, copper and zinc) in medicinal and berry plants from the forest ecosystem of this region. The following plant species were analyzed: Hypericum perforatum, Rubus arcticus, Origanum vulgare and Thymus vulgaris. The samples were taken from both open ground and hydroponic cultivation under artificial lighting. The findings indicate that the levels of lead present in all samples remain below the permissible limit of 10 mg/kg. Cadmium levels exhibited variability, with hydroponically grown plants containing 0.01 to 0.5 mg/kg and open ground Hypericum and Rubus perforatum containing up to 0.8 mg/kg. The combination of hydroponic cultivation and specific lighting conditions has been demonstrated to reduce lead and cadmium accumulation by a minimum of 1.6 times in comparison to open ground cultivation. The copper content of the samples ranged from 3 to 8 mg/kg, while the zinc content was 1.2–1.5 times higher in the plants grown in the open compared to those grown hydroponically. Notwithstanding these variations, the heavy metal content of all plant samples remains below the threshold values, thus rendering them safe for harvesting and utilization. This research serves to illustrate the environmental impact of industrial activities and to identify hydroponics as a potential strategy for their mitigation.

1. Introduction

Active industrial development of the North by Russia and other countries can result in a number of environmental problems connected with pollution, damage of natural ecosystems and climate change. At present, an increasing number of countries that have access to northern areas express their desire to start the development of these territories. However, there is hardly any heated discussion of the problems that can arise due to this industrial development. It is obvious that the construction of industrial buildings, roads and residential areas in the North can cause the destruction of forests, swamps and other natural habitats. Moreover, it can trigger the disappearance of certain plant and animal species and the disruption of environmental balance [1].
However, in Russia, there are a significant number of areas that belong to the regions of the Far North, and they are industrially developed and actively involved in the economy of the country, for example, the Khanty-Mansi Autonomous Okrug-Yugra (KMAO-Yugra), which can serve as a good illustration in terms of studying and solving possible environmental problems due to the industrial development of the Northern Hemisphere. For example, in KMAO-Yugra, there are severe problems of soil pollution, which have a negative impact on the environment, health of the local population and biodiversity of the region. One of the main causes of soil pollution is the oil industry, which is highly developed in KMAO-Yugra. As a result of the operation of oil extraction facilities, there occur discharges of oil products as well as oil spills, inducing severe pollution of the soil. Moreover, automobile transport, which is widely used in this area, makes a significant contribution to the pollution of soils by toxic substances, for example, by heavy metals. As is known, heavy metals can accumulate in soil and, subsequently, can enter food chains through plants and animals, and finally, they can penetrate into the human organism. The continuous impact of heavy metals on the soil can result in the degradation of its physical, chemical and biological properties to bring about reduced crop yields and the total decrease in the soil cover quality. Moreover, the residents of the polluted areas are subject to the risk of developing various diseases, such as cancer, neurological disorders and liver and kidney problems, as well as the total decrease in physical and mental health [2].
The simplest way to estimate the amount of environmental damage in the northern areas is to study the safety of plant raw materials from the northern ecosystems, especially in big industrial centers where various sources of pollution are located [3], including those polluting the environment with heavy metals. In addition, the forest ecosystems of the North are known to have a poor ability to recover [4]. Thus, data on the pollution of plants by toxic elements allow for one to predict and to timely neutralize the damaging impact of the pollution sources. The content of heavy metals in the soils in KMAO-Yugra was earlier shown to continuously increase [5] due to the growing human activity: emissions from transport, pollution from agricultural activities, industrial wastes and garbage [6,7,8,9,10,11]. This has resulted in the increased accumulation of heavy metals in plants, berries and mushrooms [6,7,8,9,10,11].
However, as a rule, in the case of anthropogenic pollution, the uncontrolled harvesting of plant raw materials can lead both to the depletion of natural supplies and possible penetration of dangerous pollutants into the human organism. Thus, of special importance are technologies of safe plant growth in closed systems, e.g., vertical hydroponic farms, including conditions of light culture. In such closed systems, plants can form commercial biomass during the entire year and be a source of biologically active substances that are indispensable for the population of northern areas to prevent diseases [12,13,14,15,16]. In short, hydroponic systems are an efficient way to grow plants without soil. They are based on the fact that plant roots are located in a special solution containing all the nutrients that are necessary for their growth and development. The application of hydroponic systems allows for one to avoid soil pollution and to create safe conditions for plant growth. Moreover, hydroponic systems can be installed in closed buildings, which prevents environmental pollution. This is of special importance in cities and industrial areas where soils can already be polluted by heavy metals, with the soil cover in the KMAO-Yugra region being characterized by such conditions. However, it is worth noting that growing plants in hydroponics, anyway, involves requirements for control and purification of the applied nutrient solutions from heavy metals and other harmful substances. In this connection, the above-mentioned advantages of using hydroponic systems as compared with the growth conditions in the open ground can raise questions.
Thus, this research was aimed at the comparative analysis of the content of heavy metals in plants, including those from the forest ecosystem (Origanum vulgare, Thymus vulgaris, Hypericum perforatum, Artemisia dracunculus, Rubus arcticus), grown under the conditions of hydroponics and open ground in the area of KMAO-Yugra.

2. Materials and Methods

2.1. Research Area

Soil samples were collected in September 2022 from the specially selected locations of the forest ecosystem of the city of Surgut in the Khanti-Mansi Autonomous Okrug-Yugra (the central part of Western Siberia, 61°14′ N, 73°26′ E). According to botanic-geographical zoning, this area belongs to the boreal (taiga) zone, middle-taiga sub-zone. The main source of moisture is atmospheric precipitation, which amounts to 600–700 mm per year. The soils of the experimental plot are soddy-podzolic, illuvial-iron and sandy.

2.2. Plant Samples

The research objects included plants, most of them growing in the northern regions of Western Siberia; these plants are used as food and spices or medicinal herbs: tarragon or estragon (Artemisia dracunculus L.) from the family Asteraceae, common oregano (Origanum vulgare L.) and common thyme (Thymus vulgaris L.) from the family Lamiaceae, common hypericum (Hypericum perforatum L.) from the family Hypericaceae and Arctic raspberry (Rubus arcticus L.) from the family Rosaceae. Tarragon has a large habitat in Russia; it is cultivated as a spicy and medicinal plant, though in many areas it falls out of cultivation. In Western Siberia, tarragon grows in steppe meadows, birch forest outliers, on edges of dry pine and small-leaved forests, in bushwood, along riverbanks and along roadbeds [17]. Thymus vulgaris L. is cultivated in the southern regions of Russia and Western Siberia. Thyme is rich in vitamins A, B2, B6, B9 and C as well as in β-carotene, potassium, calcium, magnesium, phosphorus, iron, manganese, copper and zinc [18]. Hypericum perforatum is widely spread in Eurasia, including Western Siberia, growing in thinned birch and pine forests and on grass meadows; it is included into an additional list of the Red Book of RMAO-Yugra as a species whose state in the natural environment requires special attention [19,20,21]. Common oregano (Origanum vulgare L.), as a wild species, is abundant in the European part of Russia, North Caucasus and Western Siberia and, as a non-native species, in the Far East. This species is typical for pine–birch forests, forest edges, logging areas, burnt sites and dry meadows [20,22]. Rubus arcticus L. is spread in the Arctic and forest zones of the Northern Hemisphere, including the north of Russia, Siberia and the Far East. It grows in forests, on wet meadows and in swamps, in bushwood, along riverbanks and in tundra [23].

2.3. Hydroponics

Plants were grown on a hydroponic installation in polypropylene pots with a diameter of 6 cm with holes; mineral wool (Speland, Ryazan, Russia) was used as a substrate. The plants were fed with a nutrient solution supplied to the root growth zone with the ebb and flow method. “Yara Ferticare Hydro” (Yara International, Oslo, Norway) complex fertilizer and “Yara Liva Calcinit” (Yara International, Norway) were used for the hydroponic system. The nutrient solution was supplied 5 times a day for 15 min. Optimal cultivation conditions were maintained: pH of the nutrient solution 5.5–6.5, electrical conductivity 1.6–2.0 mS/cm, solution temperature +22℃, indoor air temperature +20–24 ℃ and humidity 50%–60%. White Power STANDART LED lamps were used (luminous flux 8000 lm, color temperature 4000 K, PPF 165 µmol/s/m2 (Era, Suzhou, China)). The plants were grown under a 16 h light regime.
To determine the heavy metals, leaves and young shoots at the age of 50–70 days were used (tarragon, thyme being at the growth stage, oregano, hypericum and Arctic raspberry at the blooming stage).

2.4. Sampling and Soil Analysis

Soil samples were collected at a depth of 15–20 cm. The sampling procedure was carried out in accordance with the State Standard GOST 17.4.4.02-84 [24]. The sample pre-treatment included drying to the air-dry state at room temperature, with the samples being protected from contamination. The dried samples were cleaned from foreign inclusions, plant roots and coarse particles, and subsequently, they were ground in a porcelain mortar and sieved using a 1 mm sieve; the separation and grinding were performed in accordance with the State Standard GOST ISO 11,464 [25].
A weighted sample of the dried and ground soil (the weight being 1g) was placed into a porcelain crucible and mineralized by dry ashing in an EKPS-10 muffle furnace (Smolensk Special Design Bureau, SPU, Russia) at a temperature of 550 °C for 1.0–1.5 h. The crucibles with the formed ash were cooled in a desiccator for 1 h.
Micro- and macroelements were identified in the ash by the method of X-ray fluorescence analysis using a ShimadzuEDX-8000 analyzer (Shimadzu, Tokyo, Japan). The measurements were made in a vacuum in a boric acid tablet. The elemental content (wt.%) in the ash was calculated by the method of fundamental parameters.

2.5. Analysis of the Mineral Wool Substrate and Fertilizers

Micro- and macroelements in the mineral wool substrate (Speland, Ryazan, Russia) and in the fertilizers (“Yara Ferticare Hydro” and “Yara Liva Calcinit”, Yara International, Oslo, Norway) were determined by X-ray fluorescence analysis on a ShimadzuEDX-8000 analyzer in vacuum conditions (Shimadzu, Japan).

2.6. Collection of Plant Samples and Laboratory Analyses

Plant samples were collected at the end of August 2022; in the case of hypericum and oregano, the upper parts of the shoots with blossom trusses were cut, and in the case of tarragon and thyme, we cut the leaves and young shoots at the growth stage. The collected aboveground plant biomass was cleaned from soil particles, and the leaves were spread in a thin layer, dried to the air-dry condition in a dark room with good ventilation at room temperature (18 °C) and periodically stirred. The dry plant material was ground in an LZM-1M laboratory mill (Russia), weighed and stored in double paper bags [26]. A weighed sample of the dry and ground plant raw material with a weight of 1 g was mineralized in an EKPS-10 muffle furnace (Smolensk Special Design Bureau SPU, Russia) at 550 °C for 1.0–1.5 h. The ash was dissolved in a crucible upon heating in concentrated nitric acid, the solution was evaporated to wet salts, and the obtained precipitate was dissolved with 1% nitric acid and quantitatively transferred to a calibrated flask with a volume of 25 mL and made up to volume by the same acid. The given solution was used to determine lead, cadmium, copper and zinc by the method of atomic absorption [27].
Heavy metals were determined with an MGA-915 MD spectrometer (Lumex, Russia). Standard internal solutions GSO aqueous solution of lead (No. 7012-93), cadmium (No. 6690-93), copper (No. 7998-93) and zinc (No. 7837-2000) ions were employed for calibration.

2.7. Statistical Analysis

The statistical data were processed by the software Statistica (13.3.721), MSExcel (16.0.14332.20763) and OriginPro 2017 (b9.4.2.380). A single-factor ANOVA (analysis of variance) was performed to analyze the difference in heavy metal accumulation between groups of plants grown hydroponically and in open ground. Repeatability and reproducibility of the results were estimated by calculating the standard deviation and confidence interval of 3–4 data using a confidence level of 0.95.

3. Results

3.1. Chemical Composition of the Soil Sample and Hydroponic Material

The elemental composition of the studied samples of soil, mineral wool substrate and fertilizers was studied using the method of energy-dispersive X-ray fluorescence analysis (Table 1). The results refer to dry weight (d.w.). As is shown in Table 1, as compared to the substrate, the soil was rich in the following macroelements (mg/g): silicon (504.2), aluminum (97.4), phosphorus (2.5), potassium (30.7), sodium (6.9) and titanium (9.0). The substrate had a significantly higher content (mg/g) of calcium (234.2), iron (48.3) and magnesium (39.1). In terms of the microelements, the soil was found to contain (mg/g) chromium (0.2), manganese (0.5) and zinc (0.1). Other microelements, including heavy metals, were not detected, implying that their content in the soil was below the detection limits (Table 1).
In the mineral wool substrate, compared to the soil, a significantly larger amount of microelements was determined (mg/g): chromium (1.8), manganese (2.0), copper (0.4), vanadium (0.4), strontium (0.4) and nickel (0.1). The soil sample contained copper, vanadium, strontium, nickel, rubidium and lead below the respective detection limits (Table 1). The elemental composition of the mineral fertilizers considered in this study was different. Particularly, in the Yara Ferticare Hydro sample, as compared to the Yara Liva Calcinit sample, a higher content (mg/g) of iron (2.0), phosphorus (40.5), magnesium (12.7), potassium (329.1), sulfur (42.5), manganese (3.4), zinc (0.5) and rubidium (0.1) was found. On the contrary, the Yara Liva Calcinit sample contained more calcium (351.1), silicon (1.6) and strontium (10.1). Copper (0.8) was also detected (mg/g) in both fertilizer samples. In addition, they contained lead and cadmium at ultra-trace levels (below their detection limits).

3.2. Chemical Composition of the Plants Grown in the Soil and Hydroponic System

The results of the detection of heavy metals in the plants grown in hydroponics and open ground are shown in Figure 1. It is shown that the lead content in the plants cultivated under hydroponic conditions does not exceed 4 mg/kg, while in the open ground conditions, the values can reach up to 7 mg/kg. The controlled hydroponic growing conditions make it possible to reduce the content of lead as compared to its content in the open ground plants: by 2.3 times in thyme (p < 0.001), by 3.7 times in oregano (p < 0.001) and by 2.1 times in hypericum (p < 0.001) (Figure 1a).
The cadmium content (Figure 1b) varied from 0.01 to 0.5 mg/kg in the studied plants grown under the hydroponic conditions, while in the open ground conditions, they accumulated up to 0.8 mg/kg (in Hypericum perforatum, p = 0.005). Tarragon and Arctic raspberry accumulated significantly less cadmium (up to 0.1 mg/kg) in the open ground and hydroponic conditions.
The copper content (Figure 1c) in the plants cultivated under hydroponic conditions varied from 4 to 6.4 mg/kg, and for the open ground, it amounted from 4 to 7 mg/kg. Significant differences (p < 0.005) were observed only in the tarragon sample, with the open ground plants accumulating 1.5 times as much copper as those grown in hydroponic conditions. The active accumulation of copper by the plants from the substrate and nutrient solution under hydroponic conditions indicates the importance of this element in metabolic reactions.
The zinc content in the studied plants grown in open ground conditions varied in the range from 39 mg/kg in hypericum to 99 mg/kg in oregano, and it was 1.2–1.5 times higher than in the plants grown in hydroponics (p < 0.015 for hypericum and p < 0.031 for oregano). Among the plants cultivated under hydroponic conditions, the minimum content of zinc was found in the Arctic raspberry sample, namely 22.3 mg/kg.

4. Discussion

In the present paper, the content of heavy metals was studied in plants sampled in the forest ecosystem of the city of Surgut in the Khanty-Mansiysk Autonomous Okrug-Yugra region, which were grown in open ground and hydroponic conditions. The content of lead, cadmium and zinc was shown to be significantly lower (by 1.2–3.7 times) in the studied samples of plants cultivated in hydroponics as compared to the open ground plant samples. Thus, it is important to take into account the possibility of the accumulation of heavy metals in plants when using plants from natural ecosystems for medicinal or food purposes due to soil contamination with heavy metals caused by anthropogenic load in cities.
Food safety is a key issue both in Russia and in the world. In Russia, food safety legislation is regulated by the Federal Law ‘On the Quality and Safety of Food Products’. At the international level, food safety issues are regulated by the World Health Organization (WHO) and the Food and Agriculture Organization of the United Nations (FAO). These organizations develop international food safety standards and guidelines and work with national governments to strengthen control and monitoring systems for food quality and safety. In this work, the detected content of heavy metals in a number of medicinal plants of the forest ecosystem of Western Siberia was compared with the Russian and international standards presented in Table 2.
The lead content in the studied samples of plants grown both in open ground and hydroponically did not exceed the permissible level (10 mg/kg) according to the recommendations of the World Health Organization for assessing the quality of herbal medicines [34]. The results obtained in this work (Figure 1) are in good agreement with the literature data. In particular, the content of lead in the leaves of Hypericum under the conditions of the urban ecosystem of Rome can vary from 0.02 to 7 mg/kg [35], while for the region of the southern part of Western Siberia, the concentration of lead, even in regions with high anthropogenic load, does not exceed 0.33 mg/kg (Kemerovo city) [36]. The lead content in Thymus vulgaris in the wild flora of Slovenia amounts to 0.11 mg/kg [37], while in Jordan, its concentration in the aboveground part of the plant can reach 32 mg/kg in areas where motor transport is the leading factor in soil contamination with lead [38]. At the same time, in the wild species Thymus serpyllum grown in its natural habitat, the Pb content was low (1.26 mg/kg), which is significantly below the toxic level (10 mg/kg).
The cadmium content in the plants grown hydroponically varies from 0.01 to 0.50 mg/kg (Figure 1) and does not exceed the permissible values (Table 2) according to SanHS (Sanitary and Hygiene Standard) 2.3.2.1078-01 (1.10.7), Regulation (EC) 396/2005 and FAO/WHO 2016. Under open ground conditions, the cadmium content in the samples of thyme, oregano and Hypericum is increased 1.6–2.0 times as compared to those grown in hydroponics, varying from 0.10 to 0.79 mg/kg (Figure 1). At the same time, the maximum amount of cadmium is accumulated in Hypericum (0.79 ± 0.16 mg/kg), which exceeds some permissible values (Table 2). The authors [36,39,40] also note that Hypericum perforatum is capable of accumulating cadmium. According to Siromlya et al. [36], the cadmium content in H. perforatum, cultivated by plantation methods in various regions in the south of Western Siberia, exceeds the maximum permissible concentration (MPC) by 1.2–1.5 times, although its content (0.5 mg/kg) in the soil does not exceed the MPC (1 mg/kg) according to Sanitary and Hygienic Standard 2.1.7.2511-09. Therefore, H. perforatum can be considered a selective concentrator of cadmium, regardless of its content in the environment [41].
The copper content in the samples of thyme, oregano, hypericum, tarragon and Arctic raspberry grown both in hydroponics and open ground varies from 3 to 8 mg/kg (Figure 1), which does not exceed the threshold values for medicinal plants (Table 2) adopted in China and Russia [30,33]. At the same time, the maximum copper content is detected in the open ground tarragon sample (7 ± 1 mg/kg). The data obtained are in good agreement with the literature data on the accumulation of copper by plants. It is known that, in unpolluted areas, the copper content in plants varies from 1 to 30 mg/kg dry weight [42], and in the south of Siberia, the copper content in plants varies from 3 to 11.4 mg/kg [36]. In H. perforatum, the accumulation of copper depends on the geographical location, soil type and level of pollution: from 6.3 to 11.0 mg/kg in Slovenia [37], from 2.7 to 10.1 mg/kg in the Natural Park of Rome [35] and from 5.6 to 19.8 mg/kg in Romania [43,44]. With soils polluted in areas with a developed mining industry [45], a high content of copper was found in samples of Origanum vulgare and Thymus vulgaris in the wild flora of Romania, i.e., 222 and 169 mg/kg, respectively, 13.23 mg/kg of copper was detected in samples of Thymus vulgaris in Jordan in conditions of high pollution from motor vehicles [38], and 23.95 mg/kg was found in Origanum vulgare in southeastern Serbia [46].
The zinc content in the open ground plants in this study (Figure 1) varied in the range from 39 mg/kg for Hypericum perforatum to 99 mg/kg for Origanum vulgare, which is 1.2–1.5 times higher than in the plants grown under hydroponic conditions (22–67 mg/kg) but does not exceed the permissible level for zinc in food in China (Table 2, [30]). Zinc is one of the important microelements in plants; it is involved in the biosynthesis of enzymes and some proteins. The zinc content in plants can amount to 20–150 mg/kg [38]. At the same time, other authors [36] note that, under conditions of soil contamination with heavy metals, the zinc content in plant biomass can increase from 76 to 103 mg/kg.
The metal content of Rubus arcticus cultivated in a hydroponic system was determined. It was demonstrated that the accumulation of Cu and Zn in Rubus arcticus cultivated in hydroponic systems is 5.5 mg/kg and 22 mg/kg, respectively (Figure 1c,d). Given the dearth of empirical data concerning the accumulation of these metals in open soil systems within the context of ongoing research, a comparison of the potential risks to human health posed by metals in hydroponic conditions with those in open soil systems was conducted using previously published data for the latter. It has been documented that the accumulation of copper (Cu) and zinc (Zn) in Rubus plants cultivated in open systems ranges from 8.5 to 126.1 mg/kg and 85 mg/kg, respectively [47,48]. The significant metal accumulation by the plant in the open soil systems may be attributed to the evidence that the content of most metals in plants is affected by airborne pollution originating from industrial activities, which is a relevant issue in the Khanty-Mansiysk Autonomous Okrug-Yugra region [2]. Moreover, copper is the most prevalent element in all plant and soil samples grown in open soil systems that are impacted by air pollution. Thus, it appears reasonable to conclude that the controlled hydroponic cultivation of plants may offer enhanced benefits for human health, thereby eliminating any negative impact of the plants’ metal accumulation caused by environmental issues.
Furthermore, an additional evaluation of the risk to human health posed by metals is based on a comparison of their levels to the tolerable daily intake (TDI). The TDI levels provided by regulatory bodies were compared, and the following results were revealed. (a) The TDI for lead is 0.0036 mg/kg body weight per day [49]. Consequently, the detected Pb concentrations are below the limit and, under typical consumption patterns, are unlikely to pose a significant risk to human health. (b) For Cd, the established TDI value is the same as for Pb [49]. The findings indicate that the upper level of 0.8 mg/kg in open ground Hypericum perforatum and Rubus may be a cause for concern, particularly if these plants are consumed regularly. In light of the low TDI for cadmium, regular consumption of plants with cadmium at this level could potentially exceed safe intake levels, particularly for vulnerable populations, such as children and pregnant women. Long-term exposure may result in kidney damage and other adverse health effects. (c) For copper, the TDI level is 0.05 mg/kg body weight per day [50]. The copper levels identified in the tested plants are below the TDI. At these concentrations, the intake of copper through these plants is unlikely to pose a health risk, provided that overall dietary copper intake does not exceed the recommended limits. However, excessive copper intake could result in gastrointestinal disturbances and, in severe cases, liver damage [51]. (d) With regard to zinc, the TDI level is 0.3 mg/kg body weight per day [52]. The zinc levels found in oregano, at up to 99 mg/kg, are relatively high. Although zinc is an essential nutrient, excessive intake may result in adverse health effects, including nausea, vomiting and disruption of copper metabolism [53]. In light of the TDI for zinc, the concentrations identified in this plant could contribute considerably to daily intake, particularly if consumed in large quantities. Consequently, while the levels of Pb and Cu appear to be safe under typical consumption patterns, the Cd and Zn concentrations observed in certain plants, especially those cultivated in open ground, may pose a risk to human health, particularly with regular or high consumption. It would be advisable to limit the intake of plants with higher levels of Cd and Zn to avoid potential toxicity.
Excessive accumulation of heavy metals by plants is due to both their species characteristics and high metal content in the soil. In their life activity, plants come into contact only with available forms of heavy metals, whose amount, in turn, depends on the buffering and acidity of soils, their mechanical composition, moisture conditions and other factors [8,9]. The most dangerous heavy metals to the environment are lead, zinc, copper, cadmium and mercury. It should be noted that some heavy metals, being microelements in small quantities, are part of many plant enzymes; however, if their content in soils increases, they are actively accumulated in plants, becoming toxic to people. In this case, physical and chemical processes in the soil are disrupted, the qualitative composition of humus and the entire absorbent soil complex, including microbiological processes, changes, and toxic compounds accumulate, which ultimately leads to a decrease in soil fertility. Therefore, an important place in considering the influence of heavy metals on plants is occupied by the study of the processes of their accumulation both in terms of different species and different parts of plants. Plants are capable of absorbing almost all chemical elements from the environment in a larger or smaller amount. This study shows (Table 2) that, among the considered plants grown in open ground conditions, thyme and oregano are capable of accumulating lead from the soil (more than 5 mg/kg); thyme and hypericum accumulate cadmium (more than 0.5 mg/kg); thyme, oregano and tarragon accumulate copper (more than 5 mg/kg), and oregano accumulates zinc (more than 80 mg/kg). Tarragon and hypericum grown in hydroponics are capable of accumulating lead (approximately 4 mg/kg) and cadmium (approximately 0.5 mg/kg), respectively, from ultra-trace amounts of these toxic elements in the substrate and fertilizers. Thyme and oregano under hydroponic conditions accumulate 6–7 mg/kg of copper from the substrate and fertilizers (Table 1), and oregano and tarragon accumulate approximately 60 mg/kg of zinc.

5. Conclusions

A comparison of the content of heavy metals in plants grown in hydroponics and in open ground conditions in the city of Surgut was carried out. In terms of the content of all the studied heavy metals, namely Pb, Cd, Zn and Cu, hydroponic plant products were shown to be cleaner compared to open ground products. At the same time, the content of the studied heavy metals in the plants under the conditions of open ground cultivation does not exceed the established sanitary standards, both in Russia and other countries.
This study examines the ability of individual plant species in the forest ecosystem of the central part of Western Siberia to accumulate toxic elements in open ground and hydroponic conditions under artificial lighting. It is shown that, while thyme, oregano and hypericum accumulate lead and cadmium from the soil, in the hydroponic conditions under white and colored lamps, their ability to accumulate these heavy metals from the substrate and fertilizers decreases by 1.6 times and more, which confirms the safety of plants grown by the hydroponic method.
Despite the low copper content in the soil (<1.0 × 10–2 mg/kg) compared to the substrate and fertilizers used (0.4–0.8 mg/kg), all the studied plants, grown both in the open ground and in hydroponics, accumulate copper equally, indicating the high mobility of its forms in both natural and artificial systems. On the other hand, all the plants accumulate zinc from the soil slightly more than from the substrate and fertilizers in hydroponic conditions.
Yet, it is shown that the content of toxic elements in the samples of thyme, oregano, hypericum, tarragon and Arctic raspberry grown both hydroponically and in open ground does not exceed the threshold values (Table 2). Consequently, these plants of the forest ecosystem of Western Siberia can be recommended for collecting and harvesting plant materials.

Author Contributions

Conceptualization, Y.Y.P.; methodology, Y.Y.P.; validation, Y.Y.P. and Z.A.S.; formal analysis, M.A.M. and I.V.K.; investigation, Z.A.S. and N.M.G.; writing—original draft preparation, M.A.M., I.V.K., Z.A.S., O.S.S. and N.M.G.; writing—review and editing, Y.Y.P., D.A.B. and O.S.S.; visualization, E.V.B.; supervision, Y.Y.P. and D.A.B.; project administration, Y.Y.P. and O.S.S.; funding acquisition, Y.Y.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Science and Higher Education (Programm of the West Siberian Interregional Scientific and Educational Center, agreement number 4-CS 08.11.2023) and the Government of the Khanty-Mansiisk Avtonomous Okrug-Yugra, grant number 2023-227-28.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors are grateful to Natalya V. Mikhailenko from the Department of Foreign Languages, Federal Research Center ‘Krasnoyarsk Science Center, Siberian Branch of the Russian Academy of Sciences’, for participation in editing this paper.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Henry, L.A.; Douhovnikoff, V. Environmental Issues in Russia. Annu. Rev. Environ. Resour. 2008, 33, 437–460. [Google Scholar] [CrossRef]
  2. Revich, B.A. Assessment of the effect produced by the fuel and energy complex on the environment and health. Stud. Russ. Econ. Dev. 2010, 21, 403–410. [Google Scholar] [CrossRef]
  3. Evseev, A.V.; Dushkova, D.O.; Goretskaya, A.G. Biomonitoring of aerothechnogenic contamination of ecosystems in the North of Russia by heavy metals. Arct. Ecol. Econ. 2020, 3, 23–33. [Google Scholar] [CrossRef]
  4. Wen, T.; Fu, W.; Li, X. Analysis of Spatial and Temporal Dynamics of Finland’s Boreal Forests and Types over the Past Four Decades. Forests 2024, 15, 786. [Google Scholar] [CrossRef]
  5. Bashkin, V.N.; Galiulin, R.V.; Galiulina, R.A.; Arabsky, A.K. Risk of soil contamination by heavy metals through gas-dust emissions. Probl. Risk Anal. 2019, 16, 42–49. [Google Scholar] [CrossRef]
  6. Tchounwou, P.B.; Yedjou, C.G.; Patlolla, A.K.; Sutton, D.J. Heavy metal toxicity and the environment. Exp. Suppl. 2012, 101, 133–164. [Google Scholar] [CrossRef] [PubMed]
  7. Petkovšek, S.A.; Pokaorny, B. Lead and cadmium in mushrooms from the vicinity of two large emission sources in Slovenia. Sci. Total Environ. 2013, 443, 944–954. [Google Scholar] [CrossRef]
  8. Kalhok, S.B.; Klint, M.; Olsen, S.M.; Mahonen, O.; Friðriksdóttir, S.; Kroglund, M.; Bulgakov, V.; Tsaturov, Y.; Lundeberg, T.; Turesson, A.; et al. AMAP Assessment 2021: Human Health in the Arctic. Arctic Monitoring and Assessment Programme; AMAP: Tromso, Norway, 2021; 240p. [Google Scholar]
  9. Zeiner, M.; Juranović Cindrić, I. Harmful Elements (Al, Cd, Cr, Ni, and Pb) in Wild Berries and Fruits Collected in Croatia. Toxics 2018, 6, 31. [Google Scholar] [CrossRef] [PubMed]
  10. Nalbandyan-Schwarz, A.; Bondo Pedersen, K.; Evenset, A.; Heimstad, E.; Sandanger, T.M.; Myllynen, P.; Rautio, A. Combined Contaminant Levels from Local Harvested Food Items in the Norwegian–Finnish–Russian Border Region. Resources 2024, 13, 54. [Google Scholar] [CrossRef]
  11. Annan, K.; Dickson, R.A.; Amponsah, I.K.; Nooni, I.K. The heavy metal contents of some selected medicinal plants sampled from different geographical locations. Pharmacogn. Res. 2013, 5, 103–108. [Google Scholar] [CrossRef]
  12. Lee, H.S.; Choi, C.-I. Black Goji Berry (Lycium ruthenicum Murray): A Review of Its Pharmacological Activity. Nutrients 2023, 15, 4181. [Google Scholar] [CrossRef] [PubMed]
  13. Ahmadi, T.; Shabani, L.; Sabzalian, M.R. LED light sources improved the essential oil components and antioxidant activity of two genotypes of lemon balm (Melissa officinalis L.). Bot. Stud. 2021, 9, 62. [Google Scholar] [CrossRef]
  14. Bespal’ko, L.V.; Pinchuk, E.V.; Ushakova, I.T. Lemon balm (Melissa officinalis L.) is a valuable aromatic culture. Veg. Crops Russ. 2019, 3, 57–61. [Google Scholar] [CrossRef]
  15. Balashova, I.T.; Bespal’ko, L.V.; Molchanova, A.V.; Sirota, S.M.; Kharchenko, V.A.; Soldatenko, A.V. Biochemical composition of some aromatic and medicinal plants after cultivation on the multi circle hydroponic installations. Plant Biol. Hortic. Theory Innov. 2021, 4, 67–77. [Google Scholar] [CrossRef]
  16. Sachir, E.E.; Puscasu, C.G.; Caraiane, A.; Raftu, G.; Badea, F.C.; Mociu, M.; Albu, C.M.; Sachelarie, L.; Hurjui, L.L.; Bartok-Nicolae, C. Studies Regarding the Antibacterial Effect of Plant Extracts Obtained from Epilobium parviflorum Schreb. Appl. Sci. 2022, 12, 2751. [Google Scholar] [CrossRef]
  17. Krasnoborov, I.M.; Lomonosova, M.N.; Tupitsyna, N.N. Flora of Siberia. Asteraceae (Compositae); Krasnoborov, I.M., Lomonosova, M.N., Tupitsyna, N.N., Eds.; Nauka: Novosibirsk, Russia, 1997; Volume 13, 472p. [Google Scholar]
  18. Yarkova, N.N.; Fedorova, V.M. Seed Science of Agricultural Plants; IPC “Prokrost”: Perm, Russia, 2016; 116p. [Google Scholar]
  19. Pimenov, M.G.; Vlasova, N.V.; Zuev, V.V. Flora of Siberia. Geraniaceae–Cornaceae; Malyschev, L.I., Ed.; Nauka: Novosibirsk, Russia, 1996; Volume 10, 254p. [Google Scholar]
  20. Krasnoborov, I.M.; Shaulo, D.N.; Lomonosova, M.N.; Vibe, E.I.; Vasina, A.L.; Tupitsyna, N.N. Key to Plants of the Khanty-Mansiysk Autonomous Okrug; Krasnoborov, I.M., Ed.; Basko Publication: Novosibirsk, Russia; Yekaterinburg, Russia, 2006; 304p. [Google Scholar]
  21. Vasin, A.M.; Vasina, A.L. The Red Book of the Khanty-Mansiysk Autonomous Okrug-Yugra: Animals, Plants and Fungi, 2nd ed.; Basko Publication: Yekaterinburg, Russia, 2013; 460p. [Google Scholar]
  22. Doron’kin, V.M.; Kovtonyuk, N.K.; Zuev, V.V. Flora of Siberia. Pyrolaceae-Lamiaceae (Labiatae); Doron’kin, V.M., Kovtonyuk, N.K., Zuev, V.V., Eds.; Nauka: Novosibirsk, Russia, 1997; Volume 11, 296p. [Google Scholar]
  23. Vydrina, S.N.; Kurbatskiy, V.I.; Polozhiy, A.V. Flora of Siberia. Rosaceae; Vydrina, S.N., Kurbatskiy, V.I., Polozhiy, A.V., Eds.; Nauka: Novosibirsk, Russia, 1988; Volume 8, 200p. [Google Scholar]
  24. GOST 17.4.4.02-84; Nature Conservation. The Soil. Method of Sampling and Preparation of Samples for Chemical, Bacteriological, Helminthological Analysis. Standartinform: Moscow, Russia, 2008; 8p.
  25. GOST R ISO 11464:2006; Soil Quality. Preliminary Preparation of Samples for Physical and Chemical Analysis. Standartinform: Moscow, Russia, 2019; 11p.
  26. Tache, A.M.; Dinu, L.D.; Vamanu, E. Novel Insights on Plant Extracts to Prevent and Treat Recurrent Urinary Tract Infections. Appl. Sci. 2022, 12, 2635. [Google Scholar] [CrossRef]
  27. GOST 30178-96; Raw Materials and Food Products. Atomic Absorption Method for Determining Toxic Substances. Standartinform: Moscow, Russia, 2010; pp. 24–32.
  28. Joint FAO/WHO Food Standards Programme Codex Committee on Contaminants in Foods. Working Document for Information and Use in Discussions Related to Contaminants and Toxins in the GSCTFF. Rotterdam, The Netherlands, 4–8 April 2016; CF/10 INF/1, March 2016. [Google Scholar]
  29. GB 2762-2022; National Food Safety Standard-Maximum Levels of Contaminants in Foods. National Health Commission (NHC) and the State Administration of Market Regulation (SAMR): China, 2023; 21p.
  30. Khan, C.S.; Cao, Q.; Zheng, Y.M.; Huang, Y.Z.; Zhu, Y.G. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollution. 2008, 3, 686–692. [Google Scholar] [CrossRef]
  31. European Commission. Regulation (EC) No 396/2005 of the European Parliament and of the Council of 23 February 2005 on Maximum Residue Levels in or on Food and Feed of Plant and Animal Origin and Amending Council Directive 91/414/EEC; European Commission: Brussels, Belgium, 2005; pp. 1–16. [Google Scholar]
  32. Commission Regulation (EU) 2023/915—Publications Office. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32023R0915 (accessed on 9 September 2024).
  33. SanPiN 2.3.2.1078-01. (1.10.7) Hygienic Safety Requirements and Food Products (as Amended and Supplemented on 6 July 2011), Standartinform: Moscow, Russia, 2002; 269p.
  34. World Health Organization. WHO Guidelines for Assessing Quality of Herbal Medicines with Reference to Contaminants and Residues; World Health Organization: Geneva, Switzerland, 2007; 118p. [Google Scholar]
  35. Pietrelli, L.; Menegoni, P.; Papetti, P. Bioaccumulation of Heavy Metals by Herbaceous Species Grown in Urban and Rural Sites. Water Air Soil Pollut. 2022, 233, 19. [Google Scholar] [CrossRef]
  36. Siromlya, T.; Zagurskaya, Y. Bayandina, Irina The elemental composition of Hypericum perforatum plants sampled in environmentally different habitats by the example of West Siberia. Bot. Pacifica 2020, 9, 127–132. [Google Scholar] [CrossRef]
  37. Glavač, N.K.; Djogo, S.; Ražić, S.; Kreft, S.; Veber, M. Accumulation of Heavy Metals from Soil in Medicinal Plants. Arch. Ind. Hyg. Toxicol. 2017, 68, 236–244. [Google Scholar] [CrossRef]
  38. Abu-Darwish, M.S. Essential Oils Yield and Heavy Metals Content of Some Aromatic Medicinal Plants Grown in Ash-Shoubak Region, South of Jordan. Adv. Environ. Biol. 2009, 3, 296–301. [Google Scholar]
  39. Lovkova, M.Y.; Buzuk, G.N. Medicinal plants–concentrators and superconcentrators of microelements, perspectives for their use in medicine. Vopr. Biol. Med. I Farm. Him. 2013, 11, 43–49. [Google Scholar]
  40. Jurca, T.; Marian, E.; Vicas, L.; Gatea, D. Simultaneous determination of metals in Hypericum perforatum L. by ICP-OES. Rev. De Chim. 2011, 62, 1154–1156. [Google Scholar]
  41. Ufimtseva, M.D. The patterns in accumulation of chemical elements by higher plants and their responses in biogeochemical provinces. Geochem. Int. 2015, 53, 441–455. [Google Scholar] [CrossRef]
  42. Medvedev, I.F.; Derevyagin, S.S. Heavy Metals in Ecosystems; Racurs Publication: Saratov, Russia, 2017; 178p. [Google Scholar]
  43. Barbeş, L.; Bărbulescu, A.; Stanciu, G. Statistical Analysis of Mineral Elements Content in Different Melliferous Plants from the Dobrogea Region, România. Rom. Rep. Phys. 2020, 72, 705. [Google Scholar]
  44. Pavlova, D.; Karadjova, I.; Krasteva, I. Essential and Toxic Element Concentrations in Hypericum Perforatum. Aust. J. Bot. 2015, 63, 152–158. [Google Scholar] [CrossRef]
  45. Marinescu, E.; Elisei, A.M.; Aprotosoaie, A.N.A.C.; Cioancă, O.; Trifan, A.; Miron, A.; Robu, S.; Ifrim, C.; Hăncianu, M. Assessment of Heavy Metals Content in Some Medicinal Plants and Spices Commonly Used In Romania. Farmacia 2020, 68, 1099–1105. [Google Scholar] [CrossRef]
  46. Kostić, D.; Mitić, S.; Zarubica, A.; Mitić, M.; Veličković, J.; Randjelović, S. Content of Trace Metals in Medicinal Plants and Their Extracts. Hem. Ind. 2011, 65, 165–170. [Google Scholar] [CrossRef]
  47. Slađana, Č.A.; Snežana, B.T.; Mile, D.D.; Milan, M.A.; Maja, M.N. Assessment of the quality of polluted areas based on the content of heavy metals in different organs of the grapevine (Vitis vinifera) cv Tamjanika. Environ. Sci. Pollut. Res. 2015, 22, 7155–7175. [Google Scholar] [CrossRef]
  48. Kudrevatykh, I.Y.; Geraskina, A.P. Comparison of structure and chemical composition of ground cover and soils of fir-spruce forests in Pechora-Ilych state nature reserve, Northern Urals. Nat. Conserv. Res. 2021, 6, 80–92. [Google Scholar] [CrossRef]
  49. EFSA Panel on Contaminants in the Food Chain (CONTAM). Scientific opinion on lead in food. EFSA J. 2010, 8, 1570. [Google Scholar]
  50. EFSA Scientific Committee; More, S.J.; Bampidis, V.; Benford, D.; Bragard, C.; Halldorsson, T.I.; Hernández-Jerez, A.F.; Bennekou, S.H.; Koutsoumanis, K.; Lambré, C.; et al. Re-evaluation of the existing health-based guidance values for copper and exposure assessment from all sources. EFSA J. 2023, 21, e07728. [Google Scholar]
  51. Araya, M.; Olivares, M.; Pizarro, F. Copper in human health. Int. J. Environ. Health 2007, 1, 608–620. [Google Scholar] [CrossRef]
  52. World Health Organization. Safety Evaluation of Certain Food Additives and Contaminants/Prepared by The Sixty-First Meeting of The Joint FAO/WHO Expert Committee on Food Additives (JEFCA); WHO: Geneva, Switzerland, 1991; Voluem 776, p. 1. [Google Scholar]
  53. Plum, L.M.; Rink, L.; Haase, H. The essential toxin: Impact of zinc on human health. Int. J. Environ. Res. Public Health 2010, 7, 1342–1365. [Google Scholar] [CrossRef]
Figure 1. The heavy metal content in the plant samples: Pb (a), Cd (b), Cu (c) and Zn (d) calculated on to dry weight (d.w.). * Significant at p ≤ 0.05.
Figure 1. The heavy metal content in the plant samples: Pb (a), Cd (b), Cu (c) and Zn (d) calculated on to dry weight (d.w.). * Significant at p ≤ 0.05.
Forests 15 01606 g001
Table 1. The elemental composition of the soil, substrate and fertilizers calculated on to dry weight (d.w.).
Table 1. The elemental composition of the soil, substrate and fertilizers calculated on to dry weight (d.w.).
ElementContent, mg/gElementContent, mg/g
SoilSubstrateFertilizersSoilSubstrateFertilizers
Yara Ferticare HydroYara Liva CalcinitYara Ferticare HydroYara Liva Calcinit
Ca15.6234.2351.1Cr0.21.8<2.0 × 10−3
Si504.2175.51.6Mn0.52.03.4<1.0 × 10−2
Al97.459.7Cu<1.0 × 10−20.40.80.8
Fe28.648.32.0V<1.0 × 10−20.4<1.0 × 10−2
P2.540.5Sr<5.0 × 10−30.4<5.0 × 10−310.1
Mg6.439.112.71.9Zn0.10.10.5<5.0 × 10−3
K30.72.1329.11.6Ni<4.0 × 10−20.1<1.0 × 10−3
S1.71.642.52.0Rb<5.0 × 10−30.1<5.0 × 10−3
Na6.9Pb<1.5 × 10−2
Ti9.02.8Cd<8.0 × 10−3
Table 2. The permissible limits for heavy metals in food supplements and herbal medicines calculated on to dry weight (d.w.).
Table 2. The permissible limits for heavy metals in food supplements and herbal medicines calculated on to dry weight (d.w.).
ReferencePb (mg/kg)Cd (mg/kg)Zn (mg/kg)Cu (mg/kg)
FAO/WHO 2016 [28]0.05–1.50.05–4.0--
GB 2762-2022. China [29]50.2--
Khan C.S., 2008 [30] 90.210020
Regulation (EC) 396/2005 [31]3.01.0-
Commission Regulation (EU) 915/2023 (for dried spices and cereals) [32]0.9–2.00.05–0.2--
MPC SanHS 2.3.2.1078-01 (1.10.7) [33]61--
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Mulyukin, M.A.; Sutormin, O.S.; Samoylenko, Z.A.; Kravchenko, I.V.; Bulatova, E.V.; Gulakova, N.M.; Baranenko, D.A.; Petrova, Y.Y. Heavy Metal Content in Medicinal Plants Grown in Hydroponics and Forest Soil in the Central Part of Western Siberia. Forests 2024, 15, 1606. https://doi.org/10.3390/f15091606

AMA Style

Mulyukin MA, Sutormin OS, Samoylenko ZA, Kravchenko IV, Bulatova EV, Gulakova NM, Baranenko DA, Petrova YY. Heavy Metal Content in Medicinal Plants Grown in Hydroponics and Forest Soil in the Central Part of Western Siberia. Forests. 2024; 15(9):1606. https://doi.org/10.3390/f15091606

Chicago/Turabian Style

Mulyukin, Maksim A., Oleg S. Sutormin, Zoya A. Samoylenko, Inessa V. Kravchenko, Elena V. Bulatova, Natalia M. Gulakova, Denis A. Baranenko, and Yuliya Yu. Petrova. 2024. "Heavy Metal Content in Medicinal Plants Grown in Hydroponics and Forest Soil in the Central Part of Western Siberia" Forests 15, no. 9: 1606. https://doi.org/10.3390/f15091606

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