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Effect of Intensive Greenhouse Vegetable Cultivation on Selenium Availability in Soil
Pedosphere 25(3): 343–350, 2015 ISSN 1002-0160/CN 32-1315/P c 2015 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press
Effect of Intensive Greenhouse Vegetable Cultivation on Selenium Availability in Soil FU Ming-Ming1,2 , HUANG Biao1,∗ , JIA Meng-Meng1,2 , HU Wen-You1 , SUN Wei-Xia1 , D. C. WEINDORF3 and CHANG Qing4 1 Key
Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008 (China) 2 University of Chinese Academy of Sciences, Beijing 100049 (China) 3 Department of Plant and Soil Science, Texas Tech University, Box 42122, Lubbock, TX 79409 (USA) 4 Geological Survey of Jiangsu, Nanjing 210018 (China) (Received September 3, 2014; revised November 19, 2014)
ABSTRACT Soil properties dramatically change after long-term greenhouse vegetable cultivation, which further affects soil selenium (Se) nutritional status and plant Se uptake. An evaluation of Se availability after long-term greenhouse vegetable cultivation (GVC) can help in better understanding its influential factors under GVC conditions and will also facilitate further regulation of soil Se nutrition in GVC systems. Two typical GVC bases were chosen: one with clayey and acidic soil in Nanjing, southern China, and the other with sandy alkaline soil in Shouguang, northern China. Twenty-seven surface soil samples at the Nanjing base and 61 surface soil samples at the Shouguang base were collected according to cultivation duration and cultivation intensity. Soil properties including soil available 3− Se (PO3− 4 -Se) and total Se (T-Se) were analyzed. The results showed that soil PO4 -Se was significantly and negatively correlated with soil Olsen-P, available K (A-K), and electrical conductivity (EC) at the Nanjing base. At the Shouguang base, however, no 3− significant correlation was found between soil PO3− 4 -Se and Olsen-P and EC, and soil PO4 -Se increased with increasing soil organic matter (OM). Intensively utilized greenhouse vegetable cultivation caused significant changes in soil properties and further affected soil Se availability. Due to different management practices, the dominant factors affecting Se availability varied between the two GVC bases. At the Nanjing base, the dominant influential factor on soil Se availability was soil nutritional status, especially Olsen-P and A-K status. At the Shouguang base, where organic fertilizers were applied at high rates, soil OM was the dominant influential factor. Key Words:
available Se, electrical conductivity, Olsen-P, soil organic matter, soil properties
Citation: Fu, M. M., Huang, B., Jia, M. M., Hu, W. Y., Sun, W. X., Weindorf, D. C. and Chang, Q. 2015. Effect of intensive greenhouse vegetable cultivation on selenium availability in soil. Pedosphere. 25(3): 343–350.
INTRODUCTION Selenium (Se), a trace element found in most soils, is an essential element for humans and other mammals (McKenzie et al., 1998; Rayman, 2000). Soil Se often occurs in low concentration in China. Due to the concern of Se deficiency, there is a need for evaluating the availability of Se and assessing influential soil factors (Yang et al., 1983, 1984; Tan et al., 2002). Availability is one of the most important factors that affect soil Se uptake by plants. Soils with similar total Se (T-Se) concentrations could present different available Se concentrations (Antanaitis et al., 2008). Regional studies have shown that factors affecting soil Se availability could be different among various locations. Take China as an example: in northeastern China, the key influential factor on soil Se availabi∗ Corresponding
author. E-mail: [email protected].
lity is soil organic matter (OM); while in the Huabei Plain, leaching is the primary factor (Wang and Gao, 2001). Selenium exists in soils in different forms, which also differ in availability. Thus, factors that affect soil Se existence in different forms also indirectly affect its availability. Studies have shown that soil OM, redox condition, pH, and competition ions are all factors that affect Se availability. Soil pH and redox conditions affect soil Se availability through combined effects on Se chemical forms (Fio et al., 1991; S´eby et al., 1998; Eich-Greatorex et al., 2007; Keskinen et al., 2011). Ions such as phosphate, sulfate, and carbonate and some organic acids could affect Se sorption-desorption processes through ion exchange mechanisms (Dhillon and Dhillon, 2000; Kaplan and Knox, 2004; Nakamaru and Sekine, 2008). Also, soil OM is shown to have a significant effect on Se sorption in soils (Johnsson, 1991; Gu-
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stafsson and Johnsson, 1992, 1994; Falk Øgaard et al., 2006). Greenhouse vegetable cultivation (GVC) is a special agriculture system that has attracted increased public attention due to its role in the supply of vegetables as well as environmental deterioration problems resulting from intensive management practices (Chen et al., 2004; Ju et al., 2006, 2007; Xu et al., 2007; Shi et al., 2009; Liang et al., 2013). To obtain higher economic profits from extra yields, farmers use large amounts of fertilizers and grow two or more crops each year (Zhu et al., 2005). Direct results of these practices include the intensive accumulation of macronutrients. For instance, soil Olsen-P and available K (A-K) contents in greenhouses could be up to 5.7 and 2.9 times higher than those in open fields (Xu et al., 2007; Cao et al., 2012). Significant increases in soil OM were also observed in GVC due to high organic fertilizer application rates (Ju et al., 2007; Qiu et al., 2010). Changes in soil properties may also affect the availability and uptake of other nutrients (Gustafsson and Johnsson, 1992, 1994; Ba˜ nuelos and Ajwa, 1999). Most of the studies on factors that affect Se availability in soils have been conducted under specific laboratory conditions, with only particular factors considered. There is little information on soil Se availability under intensive greenhouse cultivation conditions and studies on vegetable nutritional balance are needed as it relates to human health. In this study, the objective was to reveal the factors that affect soil Se availability under intensively cultivated conditions and provide basic information for further soil Se regulation in agriculture system. MATERIALS AND METHODS Study sites This research was conducted at two typical GVC bases: one was in Nanjing, Jiangsu Province in southern China, and the other in Shouguang, Shandong Province in northern China. The bases represented two typical greenhouse types in southern and northern China, respectively. Soil type difference was also considered when selecting the study sites. Soils at the Nanjing base were generally Stagnic Anthrosols developed from clayey Quaternary loess (Gong et al., 2003). Soils at the Shouguang base were generally Ustic Cambosols derived from loamy alluvium (Gong et al., 2003). The soils were acidic to neutral at the Nanjing base, and alkaline at the Shouguang base. Both of the bases are under typical monsoon climate, with average annual temperatures of 15.4 and 12.4 ◦ C, and annual pre-
cipitation of 1 100 and 593.8 mm for the Nanjing and Shouguang bases, respectively. The Nanjing base is located near the perimeter of Nanjing City, and is a major vegetable supplier for Nanjing City. This area has a long-term history of rice cultivation. However, in the most recent decade, greenhouses have began to flourish, and are mainly distributed in the east and northwest parts due to convenient traffic patterns and access to irrigation water (Fig. 1). In 2006, the base was constructed and operated as cooperative. As time progressed, the GVC area was further expanded. Hence, greenhouses distributed in the east and northwest parts have been under cultivation for longer periods of time and under higher cultivation intensities than the greenhouses in other parts of the Nanjing base. The Shouguang base is a well-known GVC base in China, operated as a small-family business. Vegetable greenhouses in the base feature different cultivation durations due to continuing expansion, some of which have gone on for more than 20 years. Farmers at the Shouguang base are local people, so they know the greenhouse cultivation durations precisely. Household survey A household survey was conducted to investigate fertilizer management practices at the two GVC bases. Large amounts of fertilizers were applied to increase vegetable output at both of the bases. The application rates of compound fertilizers, such as N-P2 O5 -K2 O (15-15-15) could be up to 3–4 t ha−1 year−1 . Potassium sulphate fertilizer was also used in some greenhouses to supply potassium. Higher rates of fermented chicken manure and other organic fertilizers were used at the Shouguang base (446 and 62 t ha−1 year−1 ) compared with the Nanjing base (15 and 4 t ha−1 year−1 ) (Yang et al., 2013). Soil sampling In order to evaluate the effect of cultivation intensity on soil Se availability, a series of topsoil samples were collected at the Nanjing and Shouguang bases in the fall of 2011 and the spring of 2012, respectively, based on cultivation duration information supplied by local farmers. At the Shouguang base, farmers are mostly local people, so the cultivation duration information was supplied precisely. At the Nanjing base, however, farmers are mostly from other provinces; thus, greenhouse cultivation duration information was not precisely available. As such, the cultivation intensity was based on both the cultivation duration information supplied by the farmers and the macronutrient
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Fig. 1 Environmental settings and spatial distribution of sampling sites at the Nanjing greenhouse vegetable cultivation base, southern China.
accumulation status in soils. This was based on a wellknown conclusion that soil macronutrients increase with increasing cultivation intensity in GVC (Cao et al., 2012). A total of 27 and 61 topsoil samples were collected using a stainless-steel auger from the 0–30 cm depth at the Shouguang base and the 0–20 cm depth at the Nanjing base, respectively. The difference in sampling depth reflected differences in root effective depths between the two areas. At the Nanjing base, cultivars were mainly leafy vegetables with short root lengths. By comparison, the Shouguang base featured mainly fruit vegetables with longer root lengths. Each soil sample was a composited mixture of five subsamples collected in polyethylene bags. All samples were air-dried at room temperature, ground, and screened through a 2.0-mm sieve. Part of the sieved sample was further ground and screened through a 0.15-mm sieve. The sample screened only through the 2.0-mm sieve was used for the determination of soil pH, electrical conductivity (EC), Olsen-P, A-K, and available Se, and that through the 0.15-mm sieve for the determination of soil OM, total N (T-N), and T-Se. Analytical methods Soil pH was measured using a 1:2.5 soil to wa-
ter ratio with a Model PHS-3C glass electrode pH meter (Shanghai Precision and Scientific Instrument Co. Ltd., Shanghai, China). Soil EC was measured using a 1:5 soil to water ratio with a DDS-307 conductivity meter (Shanghai Precision and Scientific Instrument Co. Ltd., Shanghai, China). Soil OM was determined with the Walkley-Black method, which is based on the oxidation of soil OM with K2 Cr2 O7 and H2 SO4 followed by titration with FeSO4 (Nelson and Sommers, 1982). Soil T-N was determined via the Kjeldahl method after digestion with H2 SO4 . The analysis of Olsen-P in soil was performed using the procedures developed by Olsen (1954). Soil A-K was extracted with 1 mol L−1 NH4 Ac and determined with an FP650 flame spectrometer (Shanghai Aopu Analytical Instruments Co. Ltd., Shanghai, China). Soil available Se (PO3− 4 -Se) was extracted with 0.1 mol L−1 KH2 PO4 -K2 HPO4 buffer solution at pH 7.0 by a modification of the method of Keskinen et al. (2009). In brief, 25 mL of phosphate buffer solution was added to 5.00 g of soil in a 100-mL centrifuge tube and was vibrated in a reciprocating shaker for 4 h. After vibration, the centrifuge tube was subjected to centrifugation for 10 min at 3 000 × g. The supernatant was filtered (Whatman) into a grass test tube for storage. An aliquot of the filtered extract was further tra-
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nsferred into a 50-mL beaker, digested with 5 mL of 14 mol L−1 HNO3 and 2 mL of 12 mol L−1 HClO4 on heat plate at 200 ◦ C. After the evolution of white fumes, 5 mL of 6 mol L−1 HCl was added to the beaker, covered with watch glass, and refluxed for 30 s. After cooling, the digested solution was transferred to a 25-mL volumetric flask and brought to volume with Milli-Q water for analysis. Soil T-Se was digested with concentrated HNO3 and HCl according to the National Environmental Protection Standards of China (HJ 680-2013). For Se analysis in soil solution, potassium borohydride stabilized with sodium hydroxide (2% (w/v) KBH4 in 0.1 mol L−1 NaOH) was used for hydride generation and was measured by an AFS-230 atomic fluorescence spectrometer (Beijing Haiguang Instruments Co. Ltd., Beijing, China). For quality assurance, each digestion batch of 20 samples contained 2 reagent blanks, 2 standard soil materials for total Se content (GSS-1 and GSS-3) and 2 in-house test soil samples for PO3− 4 -Se analysis. Three replicates for each soil sample were used in the analysis. Data for the quality assurance samples indicated that the analytical measurements are valid. Data and statistical analyses Raw data were analyzed with different software packages. Descriptive statistical analyses were performed using MS Excel 2013, SPSS software 16.0, and SigmaPlot 11.0. Spatial distribution maps were constructed with ordinary kriging interpolation using ArcGIS software (version 10.0). RESULTS AND DISCUSSION General soil properties Similar to other studies conducted in greenhouse fields, the soils at the Nanjing and Shouguang bases showed accumulation trends in macronutrients and OM. After > 10 years of cultivation, the concentrations of soil Olsen-P and A-K increased to more than twice the original values. At the Nanjing base, soil was acidic with pH ranging from 3.99 to 6.74 with an average of 5.06. Soil pH decreased under long-term greenhouse cultivation. Spatially, soil pH was lower in the center and southeast parts (< 4.7) than in the periphery (> 5.5) (Fig. 2). Average soil Olsen-P, A-K, T-N, EC, and OM were 111.7 mg kg−1 , 211 mg kg−1 , 1.50 g kg−1 , 265.1 µS cm−1 , and 26.37 g kg−1 , respectively. Spatially, these factors were higher in the east and northwest parts (Fig. 2). These results were in accordance with the cultivation duration information supplied by the farmers,
where the cultivation durations were longer in the east and northwest parts. To some extent, soil property status reflected the cultivation intensity in this area. At the Shouguang base, soil was alkaline with pH in the range from 7.78 to 8.48 with an average of 8.14. Soil pH was negatively correlated with cultivation duration (P < 0.05). Soil Olsen-P, A-K, EC, and OM showed a significant positive correlation with cultivation duration. These results were reflections of excessive fertilizer application rates. Soil Olsen-P, A-K, EC, and OM were only 46.6 mg kg−1 , 196.4 mg kg−1 , 204.2 µS cm−1 , and 15.83 g kg−1 at the newly built greenhouses, and increased to 68.8 mg kg−1 , 353.2 mg kg−1 , 255.9 µS cm−1 , and 21.03 g kg−1 , respectively, after > 10 years of continuous cultivation (Fig. 3). Status of soil Se Average soil PO3− 4 -Se concentrations were nearly the same at the two bases, being 0.031 and 0.029 mg kg−1 for the Nanjing and Shouguang bases, respectively. Variation was smaller at the Nanjing base within a range of 0.024–0.038 mg kg−1 compared with 0.016–0.044 mg kg−1 at the Shouguang base. Spatially, PO3− 4 -Se was higher in the center and southwest parts and lower toward the periphery (Fig. 2). Pearson’s correlation analysis showed significant negative correlations (P < 0.05) between soil PO3− 4 -Se and soil Olsen-P, A-K, and EC, which indicated a decrease in Se availability with cultivation intensity (Table I). At the Shouguang base, soil PO3− 4 -Se was significantly and positively correlated with cultivation duration, suggesting increased Se availability with increasing cultivation duration (Fig. 3). Soil T-Se averaged 0.362 and 0.288 mg kg−1 at the Nanjing and Shouguang bases, respectively, reflecting a moderate level within the worldwide context (Wang and Gao, 2001). The T-Se levels were higher in the northwest part and lower toward the periphery at the Nanjing base (Fig. 2). No relationship was found between T-Se and cultivation intensity or cultivation duration at both bases. In this study, the relationship between PO3− 4 Se and T-Se was investigated. According to the data obtained, PO3− 4 -Se was 5%–13% and 5%–16% of T-Se at the Nanjing and Shouguang bases, respectively, which supports the results of Keskinen et al. (2009). The correlation between PO3− 4 -Se and T-Se was weak at the Nanjing (R = 0.288) and Shouguang bases (R = 0.052), revealing no interdependence between them. Thus, it was possible to conclude that an increase in T-Se was not associated with an increase in PO3− 4 -Se. Other factors aside from T-Se likely played a much more important role in soil Se availability.
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Fig. 2 Spatial distribution patterns of soil Olsen-P, available K (A-K), total N (T-N), electrical conductivity (EC), pH, organic matter (OM), available Se (PO3− 4 -Se), and total Se (T-Se) at the Nanjing greenhouse vegetable cultivation base, southern China.
Factors influencing soil Se availability We also sought to work out the main factors that affect soil Se availability under greenhouse vegetable cultivation. Ion exchanges are common procedures in soil; factors that affect ion exchange equilibria in soil solution subsequently affect the availability of Se in soil (Fio et al., 1991). The composition of soil solution is complex, especially for GVC where excessive fertilizers
are used. Data showed that soil Olsen-P, A-K, and TN accumulated after long-term greenhouse vegetable cultivation (Figs. 2 and 3). These ions might compete with Se for adsorption sites due to differences in their characteristics, adsorption strength, and relative concentrations. At the Nanjing base, a significant negative correlation between soil PO3− 4 -Se and soil OlsenP, A-K, and EC revealed that soil samples with higher Olsen-P, A-K, and EC were lower in PO3− 4 -Se. Previ-
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Fig. 3 Relationships between cultivation duration and soil pH, organic matter (OM), electrical conductivity (EC), Olsen-P, available K (A-K) and available Se (PO3− 4 -Se) at the Shouguang greenhouse vegetable cultivation base, northern China. TABLE I Pearson’s correlation coefficients between some soil properties and soil Se at the Nanjing (southern China) and Shouguang (northern China) greenhouse vegetable cultivation (GVC) bases GVC base
Itema)
Nanjing
PO3− 4 -Se
Shouguang
T-Se pH OM Olsen-P A-K T-N EC PO3− 4 -Se T-Se pH OM Olsen-P A-K T-N EC
PO3− 4 -Se 1
1
T-Se
pH
OM
Olsen-P
A-K
T-N
EC
−0.660∗∗
−0.263 0.129 −0.671∗∗ 0.844∗∗ 0.610∗∗ 0.570∗∗ 1 0.227 −0.037 −0.472∗∗ 0.561∗∗ 0.273∗ 0.421∗∗ 1
−0.418∗ 0.131 −0.334 0.271 0.591∗∗ 0.589∗∗ 0.558∗∗ 1 0.079 0.285∗ −0.480∗∗ 0.465∗∗ 0.161 0.552∗∗ 0.323∗ 1
0.288 1
0.288 0.025 1
−0.001 0.148 −0.498∗∗ 1
−0.746∗∗ 0.014 −0.388∗ 0.355 1
−0.060 −0.596∗∗ 0.226 0.765∗∗ 1
0.052 1
−0.081 −0.125 1
0.384∗∗ 0.180 −0.615∗∗ 1
−0.181 −0.040 −0.444∗∗ 0.264∗ 1
0.341∗ 0.142 −0.563∗∗ 0.544∗∗ 0.264∗ 1
∗,∗∗ Significant a) PO3− -Se 4
at P < 0.05 and P < 0.01, respectively. = available Se; T-Se = total Se; OM = organic matter; A-K = available K; T-N = total N; EC = electrical conductivity.
ous research demonstrated that phosphate, sulfate, and carbonate could compete with Se sorbed onto soil particles through ion exchange mechanisms (Balistrieri and Chao, 1987; Dhillon and Dhillon, 2000; Kaplan and Knox, 2004; Nakamaru et al., 2006; Nakamaru and Sekine, 2008). The ions in soil could af-
fect soil surface chemical properties such as the surface charge and protonation, which will further affect sorption-desorption properties of other ions (Wijnja and Schulthess, 2000). Under intensively used GVC systems, sulfate and phosphate, together with other soil salts, have more chance to compete with Se for
GREENHOUSE CULTIVATION AND SOIL SELENIUM AVAILABILITY
sorption sites and desorb and dissolve Se in soil solution due to mass effects and strong adsorption strength. The negative correlation identified in our study is possibly because of the high uptake by plants stimulated by the higher nutritional status. The significant correlation between PO3− 4 -Se and A-K is presumed to be mainly because of the potassium sulfate fertilizer used. That notwithstanding, no correlation was found between soil Olsen-P and PO3− 4 -Se at the Shouguang base. Other factors instead of soil nutritional status might be the primary factors that affect Se availability. At the Shouguang base, soil PO3− 4 -Se was significantly and positively correlated with soil OM, which revealed that PO3− 4 -Se increased with increasing soil OM. Previous researches conducted to study the relationship between soil OM and Se availability obtained significantly different results due to the complexity of the soil OM pool. For example, Gustafsson and Johnsson (1992, 1994) and Qin et al. (2012) suggested that OM or OM-metal (Fe, Al, etc.) compounds could complex with soil Se through different mechanisms, and the solubility and availability of the complex depended on the type of OM as in Kamei-Ishikawa et al. (2008). Conversely, another research has shown a release of low-molecular-weight OM during the decomposition of organic manure (Baziramakenga and Simard, 1998), some of which might act as competing anions for adsorption sites. Furthermore, the decomposition of OM also released a certain amount of OM-bound Se, which may contribute to the soil available Se pool (Ba˜ nuelos and Ajwa, 1999). We attributed our results to the high organic fertilizer addition rates and the organic fertilizer types used. In GVC, organic fertilizer addition is a routine management practice in support of the maintenance of soil fertility (Xu et al., 2007; Cao et al., 2012), and large amounts of organic fertilizers are added to the soil. According to our survey, the organic fertilizers used at the Shouguang base could be as high as 500 t ha−1 year−1 , about 90% of which was fermented chicken manure. In spite of the large organic manure addition rate, soil OM was only 18.80 g kg−1 on average. The large gap between soil OM and organic fertilizer addition rates suggests a high decomposition rate, and large amounts of low-molecular-weight OM were subjected to release (Baziramakenga and Simard, 1998). The low-molecular-weight OM released could chelate with Se, and hence increase PO3− 4 -Se in soil. However, considering the complex composition of OM, other reactions between OM and Se are sure to exist, which may not reflect the major behavior in the greenhouse soils of the Shouguang base.
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CONCLUSIONS The concentrations of soil PO3− 4 -Se at the Nanjing and Shouguang GVC bases were in the range from 0.016 to 0.044 mg kg−1 and represented 5%–16% of soil T-Se. Soil T-Se had no significant effect on soil Se availability. Soil Se availability was related to soil OM, Olsen-P, and A-K, but the principal factors influencing soil Se availability varied between the two GVC bases. Soil PO3− 4 -Se decreased with increasing soil Olsen-P and A-K and interactions of Se with Olsen-P and AK prevailed at the Nanjing base. Inorganic competing ions, specifically Olsen-P and A-K, thus became the dominant influential factors on soil Se availability at the Nanjing base, where the organic fertilizer addition rate was low. At the Shouguang base, soil PO3− 4 -Se increased with increasing soil OM. Therefore, soil OM became the dominant factor affecting soil Se availability at the Shouguang base, where organic fertilizer was added in large amounts. ACKNOWLEDGEMENT This work was financially supported by the National Natural Science Foundation of China (No. 41473073) and the Special Research Foundation of the Public Natural Resource Management Department of the Ministry of Environmental Protection of China (No. 201409044). REFERENCES Antanaitis, A., Lubyte, J., Antanaitis, S., Staugaitis, G. and Viskelis, P. 2008. Selenium concentration dependence on soil properties. J. Food Agr. Environ. 6: 163–167. Balistrieri, L. S. and Chao, T. T. 1987. Selenium adsorption by goethite. Soil Sci. Soc. Am. J. 51: 1145–1151. Ba˜ nuelos, G. S. and Ajwa, H. A. 1999. Trace elements in soils and plants: An overview. J. Environ. Sci. Health. A. 34: 951–974. Baziramakenga, R. and Simard, R. R. 1998. Low molecular weight aliphatic acid contents of composted manures. J. Environ. Qual. 27: 557–561. Cao, Q. W., Zhang, W. H., Li, L. B., Sun, Y. L., Sun, X. L. and Ai, X. Z. 2012. Distribution and accumulation characteristics of nutrients in solar greenhouse soil in Jinan, Shandong Province of East China. Chinese J. Appl. Ecol. (in Chinese). 23: 115–124. Chen, Q., Zhang, X. S., Zhang, H. Y. Christie, P., Li, X. L., Horlacher, D. and Liebig, H. P. 2004. Evaluation of current fertilizer practice and soil fertility in vegetable production in the Beijing region. Nutr. Cycl. Agroecosys. 69: 51–58. Dhillon, S. K. and Dhillon, K. S. 2000. Selenium adsorption in soils as influenced by different anions. J. Plant Nutr. Soil Sci. 163: 577–582. Eich-Greatorex, S., Sogn, T. A., Falk Øgaard, A. and Aasen, I. 2007. Plant availability of inorganic and organic selenium fe-
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Effect of Intensive Greenhouse Vegetable Cultivation on Selenium Availability in Soil FU Ming-Ming1,2 , HUANG Biao1,∗ , JIA Meng-Meng1,2 , HU Wen-You1 , SUN Wei-Xia1 , D. C. WEINDORF3 and CHANG Qing4 1 Key
Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008 (China) 2 University of Chinese Academy of Sciences, Beijing 100049 (China) 3 Department of Plant and Soil Science, Texas Tech University, Box 42122, Lubbock, TX 79409 (USA) 4 Geological Survey of Jiangsu, Nanjing 210018 (China) (Received September 3, 2014; revised November 19, 2014)
ABSTRACT Soil properties dramatically change after long-term greenhouse vegetable cultivation, which further affects soil selenium (Se) nutritional status and plant Se uptake. An evaluation of Se availability after long-term greenhouse vegetable cultivation (GVC) can help in better understanding its influential factors under GVC conditions and will also facilitate further regulation of soil Se nutrition in GVC systems. Two typical GVC bases were chosen: one with clayey and acidic soil in Nanjing, southern China, and the other with sandy alkaline soil in Shouguang, northern China. Twenty-seven surface soil samples at the Nanjing base and 61 surface soil samples at the Shouguang base were collected according to cultivation duration and cultivation intensity. Soil properties including soil available 3− Se (PO3− 4 -Se) and total Se (T-Se) were analyzed. The results showed that soil PO4 -Se was significantly and negatively correlated with soil Olsen-P, available K (A-K), and electrical conductivity (EC) at the Nanjing base. At the Shouguang base, however, no 3− significant correlation was found between soil PO3− 4 -Se and Olsen-P and EC, and soil PO4 -Se increased with increasing soil organic matter (OM). Intensively utilized greenhouse vegetable cultivation caused significant changes in soil properties and further affected soil Se availability. Due to different management practices, the dominant factors affecting Se availability varied between the two GVC bases. At the Nanjing base, the dominant influential factor on soil Se availability was soil nutritional status, especially Olsen-P and A-K status. At the Shouguang base, where organic fertilizers were applied at high rates, soil OM was the dominant influential factor. Key Words:
available Se, electrical conductivity, Olsen-P, soil organic matter, soil properties
Citation: Fu, M. M., Huang, B., Jia, M. M., Hu, W. Y., Sun, W. X., Weindorf, D. C. and Chang, Q. 2015. Effect of intensive greenhouse vegetable cultivation on selenium availability in soil. Pedosphere. 25(3): 343–350.
INTRODUCTION Selenium (Se), a trace element found in most soils, is an essential element for humans and other mammals (McKenzie et al., 1998; Rayman, 2000). Soil Se often occurs in low concentration in China. Due to the concern of Se deficiency, there is a need for evaluating the availability of Se and assessing influential soil factors (Yang et al., 1983, 1984; Tan et al., 2002). Availability is one of the most important factors that affect soil Se uptake by plants. Soils with similar total Se (T-Se) concentrations could present different available Se concentrations (Antanaitis et al., 2008). Regional studies have shown that factors affecting soil Se availability could be different among various locations. Take China as an example: in northeastern China, the key influential factor on soil Se availabi∗ Corresponding
author. E-mail: [email protected].
lity is soil organic matter (OM); while in the Huabei Plain, leaching is the primary factor (Wang and Gao, 2001). Selenium exists in soils in different forms, which also differ in availability. Thus, factors that affect soil Se existence in different forms also indirectly affect its availability. Studies have shown that soil OM, redox condition, pH, and competition ions are all factors that affect Se availability. Soil pH and redox conditions affect soil Se availability through combined effects on Se chemical forms (Fio et al., 1991; S´eby et al., 1998; Eich-Greatorex et al., 2007; Keskinen et al., 2011). Ions such as phosphate, sulfate, and carbonate and some organic acids could affect Se sorption-desorption processes through ion exchange mechanisms (Dhillon and Dhillon, 2000; Kaplan and Knox, 2004; Nakamaru and Sekine, 2008). Also, soil OM is shown to have a significant effect on Se sorption in soils (Johnsson, 1991; Gu-
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stafsson and Johnsson, 1992, 1994; Falk Øgaard et al., 2006). Greenhouse vegetable cultivation (GVC) is a special agriculture system that has attracted increased public attention due to its role in the supply of vegetables as well as environmental deterioration problems resulting from intensive management practices (Chen et al., 2004; Ju et al., 2006, 2007; Xu et al., 2007; Shi et al., 2009; Liang et al., 2013). To obtain higher economic profits from extra yields, farmers use large amounts of fertilizers and grow two or more crops each year (Zhu et al., 2005). Direct results of these practices include the intensive accumulation of macronutrients. For instance, soil Olsen-P and available K (A-K) contents in greenhouses could be up to 5.7 and 2.9 times higher than those in open fields (Xu et al., 2007; Cao et al., 2012). Significant increases in soil OM were also observed in GVC due to high organic fertilizer application rates (Ju et al., 2007; Qiu et al., 2010). Changes in soil properties may also affect the availability and uptake of other nutrients (Gustafsson and Johnsson, 1992, 1994; Ba˜ nuelos and Ajwa, 1999). Most of the studies on factors that affect Se availability in soils have been conducted under specific laboratory conditions, with only particular factors considered. There is little information on soil Se availability under intensive greenhouse cultivation conditions and studies on vegetable nutritional balance are needed as it relates to human health. In this study, the objective was to reveal the factors that affect soil Se availability under intensively cultivated conditions and provide basic information for further soil Se regulation in agriculture system. MATERIALS AND METHODS Study sites This research was conducted at two typical GVC bases: one was in Nanjing, Jiangsu Province in southern China, and the other in Shouguang, Shandong Province in northern China. The bases represented two typical greenhouse types in southern and northern China, respectively. Soil type difference was also considered when selecting the study sites. Soils at the Nanjing base were generally Stagnic Anthrosols developed from clayey Quaternary loess (Gong et al., 2003). Soils at the Shouguang base were generally Ustic Cambosols derived from loamy alluvium (Gong et al., 2003). The soils were acidic to neutral at the Nanjing base, and alkaline at the Shouguang base. Both of the bases are under typical monsoon climate, with average annual temperatures of 15.4 and 12.4 ◦ C, and annual pre-
cipitation of 1 100 and 593.8 mm for the Nanjing and Shouguang bases, respectively. The Nanjing base is located near the perimeter of Nanjing City, and is a major vegetable supplier for Nanjing City. This area has a long-term history of rice cultivation. However, in the most recent decade, greenhouses have began to flourish, and are mainly distributed in the east and northwest parts due to convenient traffic patterns and access to irrigation water (Fig. 1). In 2006, the base was constructed and operated as cooperative. As time progressed, the GVC area was further expanded. Hence, greenhouses distributed in the east and northwest parts have been under cultivation for longer periods of time and under higher cultivation intensities than the greenhouses in other parts of the Nanjing base. The Shouguang base is a well-known GVC base in China, operated as a small-family business. Vegetable greenhouses in the base feature different cultivation durations due to continuing expansion, some of which have gone on for more than 20 years. Farmers at the Shouguang base are local people, so they know the greenhouse cultivation durations precisely. Household survey A household survey was conducted to investigate fertilizer management practices at the two GVC bases. Large amounts of fertilizers were applied to increase vegetable output at both of the bases. The application rates of compound fertilizers, such as N-P2 O5 -K2 O (15-15-15) could be up to 3–4 t ha−1 year−1 . Potassium sulphate fertilizer was also used in some greenhouses to supply potassium. Higher rates of fermented chicken manure and other organic fertilizers were used at the Shouguang base (446 and 62 t ha−1 year−1 ) compared with the Nanjing base (15 and 4 t ha−1 year−1 ) (Yang et al., 2013). Soil sampling In order to evaluate the effect of cultivation intensity on soil Se availability, a series of topsoil samples were collected at the Nanjing and Shouguang bases in the fall of 2011 and the spring of 2012, respectively, based on cultivation duration information supplied by local farmers. At the Shouguang base, farmers are mostly local people, so the cultivation duration information was supplied precisely. At the Nanjing base, however, farmers are mostly from other provinces; thus, greenhouse cultivation duration information was not precisely available. As such, the cultivation intensity was based on both the cultivation duration information supplied by the farmers and the macronutrient
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Fig. 1 Environmental settings and spatial distribution of sampling sites at the Nanjing greenhouse vegetable cultivation base, southern China.
accumulation status in soils. This was based on a wellknown conclusion that soil macronutrients increase with increasing cultivation intensity in GVC (Cao et al., 2012). A total of 27 and 61 topsoil samples were collected using a stainless-steel auger from the 0–30 cm depth at the Shouguang base and the 0–20 cm depth at the Nanjing base, respectively. The difference in sampling depth reflected differences in root effective depths between the two areas. At the Nanjing base, cultivars were mainly leafy vegetables with short root lengths. By comparison, the Shouguang base featured mainly fruit vegetables with longer root lengths. Each soil sample was a composited mixture of five subsamples collected in polyethylene bags. All samples were air-dried at room temperature, ground, and screened through a 2.0-mm sieve. Part of the sieved sample was further ground and screened through a 0.15-mm sieve. The sample screened only through the 2.0-mm sieve was used for the determination of soil pH, electrical conductivity (EC), Olsen-P, A-K, and available Se, and that through the 0.15-mm sieve for the determination of soil OM, total N (T-N), and T-Se. Analytical methods Soil pH was measured using a 1:2.5 soil to wa-
ter ratio with a Model PHS-3C glass electrode pH meter (Shanghai Precision and Scientific Instrument Co. Ltd., Shanghai, China). Soil EC was measured using a 1:5 soil to water ratio with a DDS-307 conductivity meter (Shanghai Precision and Scientific Instrument Co. Ltd., Shanghai, China). Soil OM was determined with the Walkley-Black method, which is based on the oxidation of soil OM with K2 Cr2 O7 and H2 SO4 followed by titration with FeSO4 (Nelson and Sommers, 1982). Soil T-N was determined via the Kjeldahl method after digestion with H2 SO4 . The analysis of Olsen-P in soil was performed using the procedures developed by Olsen (1954). Soil A-K was extracted with 1 mol L−1 NH4 Ac and determined with an FP650 flame spectrometer (Shanghai Aopu Analytical Instruments Co. Ltd., Shanghai, China). Soil available Se (PO3− 4 -Se) was extracted with 0.1 mol L−1 KH2 PO4 -K2 HPO4 buffer solution at pH 7.0 by a modification of the method of Keskinen et al. (2009). In brief, 25 mL of phosphate buffer solution was added to 5.00 g of soil in a 100-mL centrifuge tube and was vibrated in a reciprocating shaker for 4 h. After vibration, the centrifuge tube was subjected to centrifugation for 10 min at 3 000 × g. The supernatant was filtered (Whatman) into a grass test tube for storage. An aliquot of the filtered extract was further tra-
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nsferred into a 50-mL beaker, digested with 5 mL of 14 mol L−1 HNO3 and 2 mL of 12 mol L−1 HClO4 on heat plate at 200 ◦ C. After the evolution of white fumes, 5 mL of 6 mol L−1 HCl was added to the beaker, covered with watch glass, and refluxed for 30 s. After cooling, the digested solution was transferred to a 25-mL volumetric flask and brought to volume with Milli-Q water for analysis. Soil T-Se was digested with concentrated HNO3 and HCl according to the National Environmental Protection Standards of China (HJ 680-2013). For Se analysis in soil solution, potassium borohydride stabilized with sodium hydroxide (2% (w/v) KBH4 in 0.1 mol L−1 NaOH) was used for hydride generation and was measured by an AFS-230 atomic fluorescence spectrometer (Beijing Haiguang Instruments Co. Ltd., Beijing, China). For quality assurance, each digestion batch of 20 samples contained 2 reagent blanks, 2 standard soil materials for total Se content (GSS-1 and GSS-3) and 2 in-house test soil samples for PO3− 4 -Se analysis. Three replicates for each soil sample were used in the analysis. Data for the quality assurance samples indicated that the analytical measurements are valid. Data and statistical analyses Raw data were analyzed with different software packages. Descriptive statistical analyses were performed using MS Excel 2013, SPSS software 16.0, and SigmaPlot 11.0. Spatial distribution maps were constructed with ordinary kriging interpolation using ArcGIS software (version 10.0). RESULTS AND DISCUSSION General soil properties Similar to other studies conducted in greenhouse fields, the soils at the Nanjing and Shouguang bases showed accumulation trends in macronutrients and OM. After > 10 years of cultivation, the concentrations of soil Olsen-P and A-K increased to more than twice the original values. At the Nanjing base, soil was acidic with pH ranging from 3.99 to 6.74 with an average of 5.06. Soil pH decreased under long-term greenhouse cultivation. Spatially, soil pH was lower in the center and southeast parts (< 4.7) than in the periphery (> 5.5) (Fig. 2). Average soil Olsen-P, A-K, T-N, EC, and OM were 111.7 mg kg−1 , 211 mg kg−1 , 1.50 g kg−1 , 265.1 µS cm−1 , and 26.37 g kg−1 , respectively. Spatially, these factors were higher in the east and northwest parts (Fig. 2). These results were in accordance with the cultivation duration information supplied by the farmers,
where the cultivation durations were longer in the east and northwest parts. To some extent, soil property status reflected the cultivation intensity in this area. At the Shouguang base, soil was alkaline with pH in the range from 7.78 to 8.48 with an average of 8.14. Soil pH was negatively correlated with cultivation duration (P < 0.05). Soil Olsen-P, A-K, EC, and OM showed a significant positive correlation with cultivation duration. These results were reflections of excessive fertilizer application rates. Soil Olsen-P, A-K, EC, and OM were only 46.6 mg kg−1 , 196.4 mg kg−1 , 204.2 µS cm−1 , and 15.83 g kg−1 at the newly built greenhouses, and increased to 68.8 mg kg−1 , 353.2 mg kg−1 , 255.9 µS cm−1 , and 21.03 g kg−1 , respectively, after > 10 years of continuous cultivation (Fig. 3). Status of soil Se Average soil PO3− 4 -Se concentrations were nearly the same at the two bases, being 0.031 and 0.029 mg kg−1 for the Nanjing and Shouguang bases, respectively. Variation was smaller at the Nanjing base within a range of 0.024–0.038 mg kg−1 compared with 0.016–0.044 mg kg−1 at the Shouguang base. Spatially, PO3− 4 -Se was higher in the center and southwest parts and lower toward the periphery (Fig. 2). Pearson’s correlation analysis showed significant negative correlations (P < 0.05) between soil PO3− 4 -Se and soil Olsen-P, A-K, and EC, which indicated a decrease in Se availability with cultivation intensity (Table I). At the Shouguang base, soil PO3− 4 -Se was significantly and positively correlated with cultivation duration, suggesting increased Se availability with increasing cultivation duration (Fig. 3). Soil T-Se averaged 0.362 and 0.288 mg kg−1 at the Nanjing and Shouguang bases, respectively, reflecting a moderate level within the worldwide context (Wang and Gao, 2001). The T-Se levels were higher in the northwest part and lower toward the periphery at the Nanjing base (Fig. 2). No relationship was found between T-Se and cultivation intensity or cultivation duration at both bases. In this study, the relationship between PO3− 4 Se and T-Se was investigated. According to the data obtained, PO3− 4 -Se was 5%–13% and 5%–16% of T-Se at the Nanjing and Shouguang bases, respectively, which supports the results of Keskinen et al. (2009). The correlation between PO3− 4 -Se and T-Se was weak at the Nanjing (R = 0.288) and Shouguang bases (R = 0.052), revealing no interdependence between them. Thus, it was possible to conclude that an increase in T-Se was not associated with an increase in PO3− 4 -Se. Other factors aside from T-Se likely played a much more important role in soil Se availability.
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Fig. 2 Spatial distribution patterns of soil Olsen-P, available K (A-K), total N (T-N), electrical conductivity (EC), pH, organic matter (OM), available Se (PO3− 4 -Se), and total Se (T-Se) at the Nanjing greenhouse vegetable cultivation base, southern China.
Factors influencing soil Se availability We also sought to work out the main factors that affect soil Se availability under greenhouse vegetable cultivation. Ion exchanges are common procedures in soil; factors that affect ion exchange equilibria in soil solution subsequently affect the availability of Se in soil (Fio et al., 1991). The composition of soil solution is complex, especially for GVC where excessive fertilizers
are used. Data showed that soil Olsen-P, A-K, and TN accumulated after long-term greenhouse vegetable cultivation (Figs. 2 and 3). These ions might compete with Se for adsorption sites due to differences in their characteristics, adsorption strength, and relative concentrations. At the Nanjing base, a significant negative correlation between soil PO3− 4 -Se and soil OlsenP, A-K, and EC revealed that soil samples with higher Olsen-P, A-K, and EC were lower in PO3− 4 -Se. Previ-
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Fig. 3 Relationships between cultivation duration and soil pH, organic matter (OM), electrical conductivity (EC), Olsen-P, available K (A-K) and available Se (PO3− 4 -Se) at the Shouguang greenhouse vegetable cultivation base, northern China. TABLE I Pearson’s correlation coefficients between some soil properties and soil Se at the Nanjing (southern China) and Shouguang (northern China) greenhouse vegetable cultivation (GVC) bases GVC base
Itema)
Nanjing
PO3− 4 -Se
Shouguang
T-Se pH OM Olsen-P A-K T-N EC PO3− 4 -Se T-Se pH OM Olsen-P A-K T-N EC
PO3− 4 -Se 1
1
T-Se
pH
OM
Olsen-P
A-K
T-N
EC
−0.660∗∗
−0.263 0.129 −0.671∗∗ 0.844∗∗ 0.610∗∗ 0.570∗∗ 1 0.227 −0.037 −0.472∗∗ 0.561∗∗ 0.273∗ 0.421∗∗ 1
−0.418∗ 0.131 −0.334 0.271 0.591∗∗ 0.589∗∗ 0.558∗∗ 1 0.079 0.285∗ −0.480∗∗ 0.465∗∗ 0.161 0.552∗∗ 0.323∗ 1
0.288 1
0.288 0.025 1
−0.001 0.148 −0.498∗∗ 1
−0.746∗∗ 0.014 −0.388∗ 0.355 1
−0.060 −0.596∗∗ 0.226 0.765∗∗ 1
0.052 1
−0.081 −0.125 1
0.384∗∗ 0.180 −0.615∗∗ 1
−0.181 −0.040 −0.444∗∗ 0.264∗ 1
0.341∗ 0.142 −0.563∗∗ 0.544∗∗ 0.264∗ 1
∗,∗∗ Significant a) PO3− -Se 4
at P < 0.05 and P < 0.01, respectively. = available Se; T-Se = total Se; OM = organic matter; A-K = available K; T-N = total N; EC = electrical conductivity.
ous research demonstrated that phosphate, sulfate, and carbonate could compete with Se sorbed onto soil particles through ion exchange mechanisms (Balistrieri and Chao, 1987; Dhillon and Dhillon, 2000; Kaplan and Knox, 2004; Nakamaru et al., 2006; Nakamaru and Sekine, 2008). The ions in soil could af-
fect soil surface chemical properties such as the surface charge and protonation, which will further affect sorption-desorption properties of other ions (Wijnja and Schulthess, 2000). Under intensively used GVC systems, sulfate and phosphate, together with other soil salts, have more chance to compete with Se for
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sorption sites and desorb and dissolve Se in soil solution due to mass effects and strong adsorption strength. The negative correlation identified in our study is possibly because of the high uptake by plants stimulated by the higher nutritional status. The significant correlation between PO3− 4 -Se and A-K is presumed to be mainly because of the potassium sulfate fertilizer used. That notwithstanding, no correlation was found between soil Olsen-P and PO3− 4 -Se at the Shouguang base. Other factors instead of soil nutritional status might be the primary factors that affect Se availability. At the Shouguang base, soil PO3− 4 -Se was significantly and positively correlated with soil OM, which revealed that PO3− 4 -Se increased with increasing soil OM. Previous researches conducted to study the relationship between soil OM and Se availability obtained significantly different results due to the complexity of the soil OM pool. For example, Gustafsson and Johnsson (1992, 1994) and Qin et al. (2012) suggested that OM or OM-metal (Fe, Al, etc.) compounds could complex with soil Se through different mechanisms, and the solubility and availability of the complex depended on the type of OM as in Kamei-Ishikawa et al. (2008). Conversely, another research has shown a release of low-molecular-weight OM during the decomposition of organic manure (Baziramakenga and Simard, 1998), some of which might act as competing anions for adsorption sites. Furthermore, the decomposition of OM also released a certain amount of OM-bound Se, which may contribute to the soil available Se pool (Ba˜ nuelos and Ajwa, 1999). We attributed our results to the high organic fertilizer addition rates and the organic fertilizer types used. In GVC, organic fertilizer addition is a routine management practice in support of the maintenance of soil fertility (Xu et al., 2007; Cao et al., 2012), and large amounts of organic fertilizers are added to the soil. According to our survey, the organic fertilizers used at the Shouguang base could be as high as 500 t ha−1 year−1 , about 90% of which was fermented chicken manure. In spite of the large organic manure addition rate, soil OM was only 18.80 g kg−1 on average. The large gap between soil OM and organic fertilizer addition rates suggests a high decomposition rate, and large amounts of low-molecular-weight OM were subjected to release (Baziramakenga and Simard, 1998). The low-molecular-weight OM released could chelate with Se, and hence increase PO3− 4 -Se in soil. However, considering the complex composition of OM, other reactions between OM and Se are sure to exist, which may not reflect the major behavior in the greenhouse soils of the Shouguang base.
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CONCLUSIONS The concentrations of soil PO3− 4 -Se at the Nanjing and Shouguang GVC bases were in the range from 0.016 to 0.044 mg kg−1 and represented 5%–16% of soil T-Se. Soil T-Se had no significant effect on soil Se availability. Soil Se availability was related to soil OM, Olsen-P, and A-K, but the principal factors influencing soil Se availability varied between the two GVC bases. Soil PO3− 4 -Se decreased with increasing soil Olsen-P and A-K and interactions of Se with Olsen-P and AK prevailed at the Nanjing base. Inorganic competing ions, specifically Olsen-P and A-K, thus became the dominant influential factors on soil Se availability at the Nanjing base, where the organic fertilizer addition rate was low. At the Shouguang base, soil PO3− 4 -Se increased with increasing soil OM. Therefore, soil OM became the dominant factor affecting soil Se availability at the Shouguang base, where organic fertilizer was added in large amounts. ACKNOWLEDGEMENT This work was financially supported by the National Natural Science Foundation of China (No. 41473073) and the Special Research Foundation of the Public Natural Resource Management Department of the Ministry of Environmental Protection of China (No. 201409044). REFERENCES Antanaitis, A., Lubyte, J., Antanaitis, S., Staugaitis, G. and Viskelis, P. 2008. Selenium concentration dependence on soil properties. J. Food Agr. Environ. 6: 163–167. Balistrieri, L. S. and Chao, T. T. 1987. Selenium adsorption by goethite. Soil Sci. Soc. Am. J. 51: 1145–1151. Ba˜ nuelos, G. S. and Ajwa, H. A. 1999. Trace elements in soils and plants: An overview. J. Environ. Sci. Health. A. 34: 951–974. Baziramakenga, R. and Simard, R. R. 1998. Low molecular weight aliphatic acid contents of composted manures. J. Environ. Qual. 27: 557–561. Cao, Q. W., Zhang, W. H., Li, L. B., Sun, Y. L., Sun, X. L. and Ai, X. Z. 2012. Distribution and accumulation characteristics of nutrients in solar greenhouse soil in Jinan, Shandong Province of East China. Chinese J. Appl. Ecol. (in Chinese). 23: 115–124. Chen, Q., Zhang, X. S., Zhang, H. Y. Christie, P., Li, X. L., Horlacher, D. and Liebig, H. P. 2004. Evaluation of current fertilizer practice and soil fertility in vegetable production in the Beijing region. Nutr. Cycl. Agroecosys. 69: 51–58. Dhillon, S. K. and Dhillon, K. S. 2000. Selenium adsorption in soils as influenced by different anions. J. Plant Nutr. Soil Sci. 163: 577–582. Eich-Greatorex, S., Sogn, T. A., Falk Øgaard, A. and Aasen, I. 2007. Plant availability of inorganic and organic selenium fe-
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