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The Availability and Accumulation of Heavy Metals in Greenhouse Soils Associated with Intensive Fertilizer Application International Journal of Environmental Research and Public Health Article The Availability and Accumulation of Heavy Metals in Greenhouse Soils Associated with Intensive Fertilizer Application Binggan Wei 1 , Jiangping Yu 1, Zhiqiang Cao 1,2, Min Meng 1,2, Linsheng Yang 1,2,* and Qing Chen 3 1 Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China; [email protected] (B.W.); [email protected] (J.Y.); [email protected] (Z.C.); [email protected] (M.M.) 2 College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100101, China 3 College of Resources and Environmental Sciences, China Agricultural University, Beijing 100083, China; [email protected] * Correspondence: [email protected]; Tel./Fax: +86-010-6485-6504 Received: 26 June 2020; Accepted: 21 July 2020; Published: 25 July 2020 Abstract: In China, greenhouse agriculture, which provides abundant vegetable products for human consumption, has been rapidly developed in recent decades. Heavy metal accumulation in greenhouse soil and products obtained have received increasing attention. Therefore, the availability and accumulation of cadmium (Cd), copper (Cu), nickel (Ni), lead (Pb), and zinc (Zn) and their association with soil pH, soil organic matter (SOM), inorganic nitrogen (IN), total nitrogen (TN), available phosphorus (AP), and planting year (PY) in greenhouse soils were analyzed. The results showed that the mean concentrations of available Cd, Cu, Ni, Pb, and Zn were 17.25 µg/kg, 2.89, 0.18, 0.36, and 5.33 mg/kg, respectively, while their suggested levels in China are 0.6, 100, 100, 120, and 250 mg/kg. Cd, Cu, and Zn might be mainly originated from fertilizer application. A lower soil pH significantly increased the available Cu, Ni, and Zn concentrations and reduced Cd, Cu, Ni, and Zn accumulation. A higher AP significantly increased the proportions of available Cu, Ni, and Zn and elevated Cd, Cu, and Zn accumulation. There was a strong positive correlation between Cd, Pb, and Zn availability and TN, while IN was negatively related to the availability and accumulation of Cu and Zn. It was concluded that chemical fertilizer application increased the availability of Cu, Ni, Pb, and Zn and the accumulation of Cd, Cu, and Zn. Manure application clearly elevated the accumulation and availability of Cd and Zn in greenhouse soil. Keywords: greenhouse soil; heavy metal; fertilizer application; soil pH; planting year 1. Introduction In China, agricultural soil has been extensively contaminated by heavy metals from anthropogenic activities, including fossil fuel combustion, mining, smelting, traffic, waste water irrigation, sewage sludge reuse, and fertilizer applications [1,2]. In recent decades, greenhouse agriculture (solar, plastic, and multi-span greenhouses) has been rapidly developed in China. The planting area of greenhouses was 2,082,880 ha in 2016 [3]. This provides an abundance of agricultural products, such as vegetables and fruits for human consumption. It has been reported that cadmium (Cd) contamination in greenhouse soil is more serious than that of the other metals. Approximately 41.5%, 54.5%, and 11.1% of soil samples from the respective southern, northern, and northwestern areas of China have higher Cd concentrations than the standard Int. J. Environ. Res. Public Health 2020, 17, 5359; doi:10.3390/ijerph17155359 www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2020, 17, 5359 2 of 13 value [3]. Greenhouse products can take up heavy metals from soil. The products may then pose a public health risk following their consumption [4]. Heavy metal accumulation in agricultural products is not only associated with the total metal concentrations in soil but is also strongly dependent on the uptake mechanisms, soil physicochemical properties, chemical speciation of metals, soil texture, nature and quantity of nutrients, climate, and other factors [5–8]. The availability of heavy metals (such as copper (Cu), nickel (Ni), and lead (Pb)) in soil is significantly related to crop uptake of metals [9]. Heavy metal transfer from soils to plants is directly correlated with the available metal concentration in soils [10]. Human health may be affected by heavy metals through the soil-plant-human pathway. Therefore, heavy metal availability plays an important role in the evaluation of phytoextraction. Heavy metal availability in soil may be influenced by various factors. Previous studies have suggested that a longer planting duration in greenhouses will increase the mobility of heavy metals in soil [11]. Soil pH is the main factor influencing heavy metal availability in soil. Soil pH is generally negatively correlated with Cu, Ni, Pb, and Zn availability [9,12]. Heavy metal availability is also associated with soil organic matter (SOM), soil cation exchange capacity, soil salinity, and other factors [13–15]. In soil fertilized with nitrogen/phosphorous/potassium (NPK) and manure, the soluble forms of heavy metals such as Cu, Ni, Pb, and Zn, are usually increased [16]. Soil fertilized with regular manure tends to have higher soluble Cu, Zn, and Mn concentrations than soil fertilized with mineral fertilizers due to higher contents of Cd, Cu, and Zn in manure [17,18]. Excessive fertilizer has usually been applied in greenhouse soil, and the availability and accumulation of heavy metals related to soil pH, SOM, and soil nutrients in greenhouse soil need to be further investigated. Therefore, the objective of this study was to determine total and available concentrations of Cd, Cu, Ni, Pb, and Zn in greenhouse soils to identify the main sources of the metals and to determine the correlations of soil pH, SOM, PY, inorganic nitrogen (IN), total nitrogen (TN), and available phosphorus (AP) with the availability and accumulation of heavy metals. 2. Materials and Methods 2.1. Study Area and Sample Collection The study area was Hengshui City in Hebei Province, which is located between the coordinates of 115◦100–116◦340 E and 37◦030–38◦230 N (Figure1). The distance from the study area to Beijing is about 250 km. The area is located within the continental monsoon climate zone, with an annual average precipitation of 640 mm. It is an important vegetable supply base for Beijing. The study area is dominated by moist soils. In 2018, the area of greenhouses, mainly solar and plastic greenhouses, was 24,800 ha. The yield of vegetables cultivated in greenhouses was 1.06 million tons in 2018, accounting for about 36.9% of the totalInt. J. vegetableEnviron. Res. yieldPublic Health in the 2020 area. 3 of 14 Figure 1. The study study area area and and sampling sampling site. site. 2.2. Sample Analysis The soil samples were air-dried at room temperature to a constant weight in the laboratory. Then, stones and plant residues in the samples were removed. The samples were ground with a wood grinder and filtered through a 2 mm nylon sieve for routine analysis. Soil pH was measured by potentiometry using a soil/water ratio of 1:2.5. Inorganic nitrogen was extracted by 0.01 mol/L CaCl2 and determined using a continuous flowing analyzer (TRAACS 2000, Mequon, WI, USA). Total nitrogen was directly determined by an elemental analyzer (Vario MAX, Germany). Available phosphorus was extracted by a 0.5 mol/L NaHCO3 extraction. Soil organic matter was determined by oxidation with potassium dichromate. The treated soil samples were passed through a nylon sieve of mesh size ≤0.149 mm. About 0.1 g of each soil sample was weighed and digested with a 5:4:1 mixture of HF-HNO3-HClO4. Finally, the digested solution was diluted to 50 mL with deionized water. The blank and reference samples were also treated using the same procedure. The total Cd, Cu, Ni, Pb, and Zn concentrations were determined by inductively coupled plasma mass spectroscopy (ICP-MS) (PerkinElmer, Waltham, MA, USA). The detection limit was 1 ng. The available forms of Cd, Cu, Ni, Pb, and Zn were extracted by diethylenetriamine-pentaacetic acid (DTPA)/CaCl2/triethanolamine. Finally, ICP-MS (PerkinElmer, Waltham, MA, USA) was used to determine the available heavy metal concentrations. 2.3. Quality Assurance and Quality Control Standard reference material (GBW07304) was obtained from the National Research Center for Certified Reference Materials (Beijing, China) and analyzed as part of the quality assurance and quality control procedure. The Cd, Cu, Ni, Pb, and Zn recoveries were 96–103%, 96–101%, 94–104%, 95–102%, and 98–105%, respectively. Duplicate samples were analyzed for the sample determination, and the standard deviations were within ± 5%. A blank sample was also analyzed to determine the potential contamination of samples. 2.4. Statistical and Geostatistical Analyses Correlation analysis was used to estimate the relationships between soil factors and total concentrations, available concentrations, and the proportion of the available concentration for specific metals. The proportions of available concentrations for the metals were calculated as follows: () () = × % (1) () where is the metal; () is the proportion of the available concentrations for ; () is the available concentration of ; and () is the total concentration of . Int. J. Environ. Res. Public Health 2020, 17, 5359 3 of 13 A total of 51 surface soil samples (0–20 cm) were collected from cultivated greenhouses in 2017. The sample sites are shown in Figure1. Each soil sample consisted of a mixture of three subsamples collected around the site. Approximately 1000 g of soil was collected with a wooden shovel at each site and stored in a clean self-sealing polyethylene bag. The locations of sampling sites were determined by a global position system (GPS) device. After collection, the samples were transported to the laboratory for further analysis. The planting year (PY) for each greenhouse at the sampling site was obtained from a questionnaire interview with the owner of the greenhouse.
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