Distribution feature of heavy metals in the system of sediment-submerged plant-water in Xuanwu Lake

In recent years, as industrialization rapidly developed, the concentration of pollutants in water has risen rapidly (Liu et al. 2020a, 2020b; Sun et al. 2021). The heavy metals in the water can be absorbed by aquatic organisms, and gradually enriched upward via the food chain. Eventually they go into the human body, causing such hazards as abnormal reproductive function, destructed immune system, and overall declining physical fitness at all aspects and levels (Kumar et al. 2019; Zhang et al. 2022). Heavy metals are highly toxic in small amounts and are some of the most hazardous substances in aquatic ecosystem with the features of the high toxicity, stability, concealment and non-degradability (Liu et al. 2020c; Chen et al. 2022). Studies have shown that aquatic plants are sinks of heavy metals in water ecosystems (Xing et al. 2013; Wang et al. 2022a). The accumulation ability of heavy metals in different aquatic plants showed: Submerged plants > Floating plant > Floating-leaf plant > Emergent plant (Li et al. 2015). Submerged plants are featured by massive biomass, strong reproductive ability and wide distribution (Xiao et al. 2009; Yang et al. 2020). As they are between sediments and water, heavy metals can be absorbed by the ground parts and root systems, respectively, and water pollution can be remedied by inhibiting sediment re-suspensions (Rezaei et al. 2019; Xu et al. 2022). They play an important role in the chemistry cycle of pollution elements in the bio-earth of the water environment (Huang et al. 2002). At present, there are many studies on heavy metal pollution of sediments and water at home and abroad (Liu et al. 2012; Niu et al. 2015; Khellaf et al. 2022). However, little is known about the accumulation of heavy metal in submerged plants whereas most studies are constrained in the laboratory simulation stage (Wang et al. 2020), causing the unclear role of submerged plants in practical application.

The Xuanwu Lake is diamond shaped with an area of 3.78 km² and an average depth of 1.14 m. Adjacent to the Nanjing Railway Station and bus station and located on the urban traffic mainline, it is a typical urban lake surrounded by urban commercial and residential areas. With the growth of urban populations and the impact of human activities, heavy metal pollutants in the surrounding sewage have a negative impact on the lake ecosystem (Su et al. 2021). Prior to this, there were reports on the studies of distribution of heavy metals in Xuanwu Lake (Zou et al. 2008; Zhao et al. 2012; Ohore et al. 2020). However, most studies were focused on a single system (water or sediments) and no analysis was carried according to the lake area. It is necessary to study the distribution and pollution of heavy metals in the water system of different Xuanwu Lake areas because of its larger area, different heavy metal sources and pollution.

In addition in 2019 spring, a comprehensive desalting project was organized and submerged plants were planted to restore the ecology. However, the positive effect of sediment dredging on lake management has not been verified yet. In this paper, the four dominant submerged plants in Xuanwu Lake after dredging were taken as an object to study the variation in heavy metal content of surface water, sediments and submerged plants in different Xuanwu Lake areas, and deeply analyze the accumulation ability in heavy metals of submerged plants in order to define the pollution and distribution of heavy metals in the sediment-submerged plants-water system in Xuanwu Lake, which provides a theoretical basis for the application of submerged plants in the ecological treatment of polluted water in Xuanwu Lake.

The 10 ml water sample with the impurity filtered was placed in a 50 ml centrifuge tube to dissolve particulate heavy metals by adding 10 ml nitric acid, then was digested at 80 °C for 6 hours on an electric heating plate (DB-2AB, Shanghai Lichen Instrument Technology Co., Ltd, China). The sample was measured after cooling (Lin et al. 2021).

After freeze drying, the sediment sample was mixed evenly and put into a polythene plastic bag. It was placed in a drier for use. Next, 2 g freeze-dried sample was accurately weighed and transferred to the cleaned centrifuge tube; 15 mL hydrochloric acid (at a ratio of 1:1) and 5 ml nitric acid are added to the centrifuge tube with the centrifuge tube shaken slightly, so that the sample and the digestion are mixed evenly. The centrifuge tube containing the sample and the digestion solution was placed and absorbed in the heating plate at 80 °C for 6 hours, which was mixed well by continuous shaking. After the centrifuge tube was cooled, the solution was filtered and collected. The volume was set to 50 ml.

The plant samples were washed and rinsed three times with the ionic water. After placing for 30 minutes in the oven (DHG-9053A, Shanghai Yiheng Electric Bast Drying Oven, China) at 105 °C, the temperature dropped to 65 °C and then stayed for 24 hours. Samples were ground with a grinder after their removal. Next, 0.1 g ground powder was weighed and placed in a Teflon slump, adding 2 ml hydrochloric acid, 8 ml nitric acid, 2 ml perchloric acid and 2 ml hydrofluoric acid. This was heated with an electric heating plate to 350 °C. During this time, nitric acid was added until the cooking liquid in the polytetrafluoroethylene was clear with no more visible residue. The residual cooking liquor was washed with deionized water into a 50 ml volumetric flask through a filter paper, and volume was set. Finally, 10 ml of the filtered fluid was taken out and placed into a test tube.

Finally, the contents of heavy metals were determined by inductively coupled plasma mass spectrometry (iCAP Q, Thermo Fisher Scientific, USA). The contents of Cr, Mn, Ni, Cu, Zn, Cd and Pb in each sample were analyzed with a mixed standard solution to establish the standard curve (Liu et al. 2008). Each sample was tested three times and the contents of heavy metal elements were recorded.

Table 3 showed the measured contents of Cr, Mn, Ni, Cu, Zn, Cd and Pb in surface water and sediments in Xuanwu Lake. From the table, the average concentration of heavy metals in surface water in order is Cr > Mn > Zn > Ni > Cu > Cd > Pd, The average concentrations of Cr and Ni in surface water were 1.79 and 1.1 times the national Grade-II standard on the quality of surface water (GB3838-2002), all other heavy metals exceeded this standard. There was a difference between the order of the average heavy metal in sediments and surface water. The order was Mn > Pd > Zn > Cr > Cu > Ni > Cd. The contents of Cd and Pd were 3.31 and 1.17 times of background value in the Nanjing soil, respectively. The contents of other heavy metals were obviously lower than the background value of Nanjing soil.

As the organic links between water and sediment reservoirs in water ecosystem, the growth metabolism of submerged plants played an important role in the migration and release of pollutants. By comparing the contents of seven heavy metals in the four submerged plants in Xuanwu Lake (Table 4), the results showed that the contents of heavy metals in different submerged plants were different. The contents of Cr, Ni and Cu were ranked as Potamogeton crispus > Vallisneria natans > Ceratophyllum demersum > Hydrilla verticillata while Mn and Cd were ranked as Ceratophyllum demersum > Vallisneria natans > Hydrilla verticillata > Potamogeton crispus. The contents of Mn and Cd in Ceratophyllum demersum is significantly higher than in Potamogeton crispus (p < 0.05, the same as below), while Zn is significantly higher than Hydrilla verticillata; The contents of Cr and Cu in Potamogeton crispus were significantly higher than Hydrilla verticillata, which were 46.65% and 135.83% higher than Hydrilla verticillata, respectively. The content of only Pb in Hydrilla verticillata is higher, while Ni in all submerged plants was not significantly different.

According to the range of heavy metal content of four submerged plants in Xuanwu Lake and the normal levels of heavy metal content of the plant leaves as determined by Kabata et al. (Table 5), the highest contents of Mn, Ni and Zn in Vallisneria natans were 7136.0,71.1 and 164.3 mg·kg⁻¹, respectively, the highest content of Mn and Ni was 17.84 times and 14.22 times as much as that of the normal leaves. The highest contents of Cr, Cu in the Potamogeton crispus and Cd of Ceratophyllum demersum are 51.5, 58.7 and 4.6 mg·kg⁻¹, respectively, which is 6.13 times, 1.28 times and 1.53 times as much as that of the normal leaves. This shows that Vallisneria natans, Potamogeton crispus and Ceratophyllum demersum have a strong ability to enrich such heavy metals. According to super enrichment plants defined by Xing and colleagues, the highest percentage of Cr, Mn, Ni, Cu, Zn, Cd and Pd in the submerged plants is 0.0051%, 0.7136%,0.0071%,0.0059%,0.0164%, 0.0005% and 0.0023%. These did not exceed the corresponding hyperaccumulator threshold and did not form hyperaccumulators.

The correlation between heavy metals in the four submerged plants is shown in Table 6, in which Zn is negatively correlated with Pd (p < 0.01, the same as below); Mn is positively correlated with Ni, Cu, Zn and Cd, Ni is positively correlated with Cu, Zn and Cd, Cd is positively correlated with Cu and Zn, showing that the absorption of these heavy metals by submerged plants was homologous.

The correlation analysis on submerged plants between heavy metal contents in sediments and surface water (Table 7) was conducted, showing that Cr in submerged plants was positively correlated with Cr and Ni in surface water and the correlation coefficients were 0.463 and 0.512, respectively; Cd was also positively correlated with Cd and Pd in surface water, while Pd is positively correlated with Cu in surface water, the correlation coefficients of which were 0.181, 0.496 and 0.499, respectively. Besides, Cr, Cd and Pd in submerged plants were positively correlated with Cr, Mn and Pd in sediments, the correlation coefficients were 0.16, 0.115 and 0.068, respectively.

When heavy metal pollutants go into water, most of them can be quickly absorbed by floating particles and the bottom sediment of the water, and then be enriched (Quan et al. 2021). Under certain conditions, the heavy metals adsorbed in the sediments can be released into the water, causing the secondary pollution (Zhang et al. 2020). For the closed waters such as lakes, once the heavy metal pollutants go into it, it is more difficult to be discharged by the water washing, which may have a long-term impact on the lake ecosystem (Tair & Eduin 2018). In the early period of Xuanwu Lake, the water quality was still faced with the problem of heavy metal pollution. Zou et al. (2008) determined the mass fraction of Zn, Cd and Ni in the sediments of Xuanwu Lake and found that they were 1.08–2.91 times, 51.70–89.80 times and 1.33–4.11 times the background values of Nanjing soil, respectively. Among them, Cd pollution is serious. The heavy metal contents in the water and sediment of the lake have been significantly reduced after the dredging works of Xuanwu Lake in recent years, especially the comprehensive removal and pollution interception project in 2012 and 2019. Chen et al. (2013) analyzed the contents of As, Cd, Co, Cr, Cu, Ni, Pb and Zn in surface sediments from Xuanwu Lake. The pollution levels and potential ecological risks of heavy metals were evaluated by means of the Geo accumulation index, enrichment factor and Hakanson potential ecological risk index. The results showed that the level of Cd is at a moderate level, Zn was a slight accumulation at most sampling sites, Pb is ranging from the clean level to the slight level, and the levels of other heavy metals were clean. Ohore et al. (2020) analyzed Ni, Cu, Zn, Cr, Mn, As, Cd and Pb of sediments in Xuanwu Lake in 2020. No pollution of heavy metals other than Cd was found. In this study, the contents of Cd and Pd in sediments were 3.31 and 1.17 times higher than the background values of Nanjing soil, respectively. The contents of other heavy metals were obviously lower than the background value of Nanjing soil. The Cd in the sediments of each sampling area is slight pollution, the other heavy metals are at a clean level, which was basically consistent with research results by Ohore et al. (2020) in the recent study. The heavy metal contents between the current study was compared with Xuanwu Lake in the early phase, showing that reducing the level of pollutants in sediments by sediment dredging is a quick and effective measure to improve water quality (Ma et al. 2021; Wang et al. 2022b).

In addition, although the overall concentration of heavy metal pollutants in Xuanwu Lake has dropped significantly, the levels of Cd and Pb are still relatively high. Pb is mainly derived from coal combustion, industrial utility of lead ores, and the burning of crude oil and leaded gasoline (Duzgoren-Aydin 2007; Guo et al. 2021), while Xuanwu Lake is at the main crossroads. Though unleaded petrol has been promoted in Nanjing for many years, early lead pollution had a cumulative effect (Hou et al. 2021). The gasoline Pb and that in car tires turns into flying dust as the tire becomes worn and then goes into the lake with wet and dry deposition, and finally go into the lake sediments (Wang et al. 2010; Zhang et al. 2021). Cd pollution may be relevant to the discharge of industrial wastewater around Xuanwu Lake. Therefore, the relevant departments should further strengthen the management of peripheral industrial sewage discharge (Guan et al. 2021).

Compared with other aquatic plants, the submerged plants in the water have the large contact surface with heavy metals, without wax layers on the epidermal cells, the thinner cuticle makes it easier to absorb heavy metal pollutants (Zhang et al. 2019a, 2019b; Wang et al. 2021). It is generally believed that the higher the concentration of heavy metals in polluted water, the stronger will be the accumulation ability of heavy metal for submerged plants (Fan et al. 2020). However, different submerged plants have certain selectivity to the accumulation of heavy metals (Nyquist & Greger 2007; Najila & Anila 2022). Huang et al. (2002) determined the contents of heavy metals in aquatic plants in some lakes in the middle reaches of the Yangtze River and found that water plants such as Hydrilla verticillata and Ceratophyllum demersum had a strong ability to absorb and accumulate Zn, Cr, Pb, Cd, Ni and Cu, and the contents of heavy metals in the same plants in the different lakes were much different). Rezaei et al. (2019) also found that most submerged plants showed a stronger ability to accumulate heavy metals in eutrophic rivers. However, the absorption of different heavy metal pollutants for different plants was not consistent. In this paper, Potamogeton crispus had the stronger ability to accumulate Cr, Ni and Cu, whereas the accumulation of Mn and Zn for Ceratophyllum demersum was significantly higher than for other three submerged plants. Qiao et al. (2016) found that heavy metals adsorbed by different submerged plants were distributed in different parts, causing different responses and tolerance to heavy metals. Tolerance ability is an important index of heavy metal accumulation for submerged plants.

It has been found in some studies that heavy metal contents in submerged plants are correlated with those of water and sediments. However, some scholars believe that it is difficult to determine their correlation as influenced by environmental variables such as temperature, nutrient, pH and oxidation state (Ge et al. 2019; Fang et al. 2021; Dai et al. 2022). In this study, except for a few heavy metals, the correlation of heavy metals in most submerged plants is not significant with surface water and sediments. After the experiment, Chibuike & Obiora (2014) showed that the submerged plants with heavy metals accumulated would lower the growth rate and obstruct the further absorption of heavy metal pollutants. Zhou et al. (2008) found from research that the growth of submerged plants could counteract the accumulation effect of heavy metals and weaken the relationship between heavy metal contents in plant tissue and sediment and water.

After desilting in recent years, the contents of heavy metals in the surface water and sediments of Xuanwu Lake have dropped significantly. The heavy metal contents were at a clean level except that Cd was a slight pollant in sediments. The contents of Mn, Ni, Zn, Cd and Pd in the surface water of North Lake where human activities are concentrated and Cr, Ni, Zn, Cd and Pd in sediments are higher than other lake areas; The content of heavy metals in Southeast Lake around which plants are better is relatively lower. The contents of heavy metals in four submerged plants are different. The content of Cr, Ni and Cu ranked by size are Potamogeton crispus >Vallisneria natans > Ceratophyllum demersum > Hydrilla verticillata. The contents of Mn and Zn is Ceratophyllum demersum > Vallisneria natans > Hydrilla verticillata > Potamogeton crispus. The Cr in submerged plants is positively correlated with Cr and Ni in surface water, Cd is positively correlated with Cu in surface water and Pd is positively correlated with Cu in surface water; The Cr, Cd and Pd in the submerged plants are positively correlated with Cr, Mn and Pd in sediments, respectively. The contents of heavy metals in plant tissue are related to various factors such as the transformation and accumulation abilities.

This work was supported by Suqian Key Research and Development Project – Social Development (S202002); supported by ‘Qinglan Project’ Outstanding Young Backbone Teachers Training Project of Jiangsu Universities (Su Teacher [2021] No. 10); supported by Suqian Key Laboratory of Garden Plants and Ornamental Horticulture (M202001); 2022 Suqian Transportation Technology and Achievement Transformation Project; 2021 Suqian Guiding Science and Technology Project (Z2021135).

No data were used to support this study.

The authors declare that they have no competing interests.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.