A field study of the fate of biosolid-borne silver in the soil-crop system

Journal Pre-proof A field study of the fate of biosolid-borne silver in the soil-crop system Lu Yang, Simin Li, Longhua Wu, Yibing Ma, Peter Christie, Yongming Luo PII:

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https://doi.org/10.1016/j.envpol.2019.113834

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ENPO 113834

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Environmental Pollution

Received Date: 9 September 2019 Revised Date:

30 November 2019

Accepted Date: 15 December 2019

Please cite this article as: Yang, L., Li, S., Wu, L., Ma, Y., Christie, P., Luo, Y., A field study of the fate of biosolid-borne silver in the soil-crop system, Environmental Pollution (2020), doi: https://doi.org/10.1016/ j.envpol.2019.113834. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

TOC

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A field study of the fate of biosolid-borne silver in the soil-crop system

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Lu Yang a, b, Simin Li a, Longhua Wu a, *, Yibing Ma c, d, Peter Christie a, Yongming Luo a

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a

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Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China

b

State Environmental Protection Key Laboratory of Soil Environmental Management and

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Pollution Control, Nanjing Institute of Environmental Sciences, Ministry of Ecology and

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Environment, Nanjing 210042, China

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c

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Macau Environmental Research Institute, Macau University of Science and Technology, Macau 999078, China

d

Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China

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* Corresponding author, Tel.: +86 25 86881128, fax: +86 25 86881126, E-mail:

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[email protected]

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Abstract

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Land application of biosolids is a major route for the introduction of silver (Ag) into the

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terrestrial environment. Previous studies have focused on the risks from Ag to the human

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food chain but there is still a lack of quantitative information on the flow of biosolid-borne

23

Ag in the soil-crop system. Two long-term field experiments were selected to provide

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contrasting soil properties and tillage crops to investigate the fate of Ag from sequentially

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applied biosolids. Biosolid-borne Ag accumulated in the soil and ˂ 1‰ of applied Ag was

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26

taken up by the crops. The biosolid-borne Ag also migrated down and accumulated

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significantly (p < 0.05) in the soil profile to a depth of 60‒80 cm at an application rate of 72 t

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biosolids ha−1. Soil texture significantly affected the downward transport of biosolid-borne

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Ag and the migration of Ag appeared to be more pronounced in a soil profile with a low clay

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content. Moreover, loss of Ag by leaching may not be related to the biosolid application rate.

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Leaching losses of Ag may have continued for some time after biosolid amendment was

32

suspended. The results indicate that soil texture may be a key factor affecting the distribution

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of biosolid-borne Ag in the soil-crop system.

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Keywords: Biosolid application; Environmental risk; Silver; Soil; Transfer behaviour

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Capsule: Soil texture may be a key factor affecting the downward transport of biosolid-borne

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Ag but the amount of Ag leached may be unrelated to the biosolid application rate.

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Introduction

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Recent concerns over the environmental risks of silver (Ag) are partly due to the

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increasing use of Ag nanoparticles (Ag-NPs) for home products and furniture. Biosolids are

41

potential sources of engineered nanomaterials (Sun et al., 2014; Keller et al., 2013) and Ag

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can move into the terrestrial environment via the wastewater-sewage sludge-soil pathway.

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Silver can accumulate in the tissues of different crops in soils receiving biosolid

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applications with low bioconcentration factors ranging from 0.0007 to 0.023 (Hirsch, 1998).

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The Ag concentrations found in selected crop samples are generally ˂ 0.70 mg kg−1 in the

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edible tissues (Wang et al., 2018). There are also varietal differences in the tissue

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concentrations of Ag. The concentration of Ag increased to a maximum of 20.8 µg kg−1 in

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whole wheat grains but not in brown rice following repeated applications of biosolids (Wu et

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al., 2018). Silver concentrations were 2 to 15 times as high in wheat as in cowpea (Wang et

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al., 2015). In a pot experiment, 0.02 ± 0.015 % of total Ag accumulated in rape seedlings but

2

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0.21 ± 0.044 % accumulated in wheat shoots (Pradas del Real et al., 2016).

52

Indeed, the majority of biosolid-borne Ag found subsequently in soils in previous studies

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occurs in the form of Ag2S (Meier et al., 2016). Through a sequence of chemical species such

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as Ag, AgCl or AgNPs, most of the Ag in biosolids will be converted to Ag2S after sewage

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treatment (Potter et al., 2019; Schlich et al., 2018; Lombi et al., 2013; Kim et al., 2010).

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There are also no differences in the speciation of biosolid-borne Ag from different sources or

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production areas following weathering and aging (Donner et al., 2015). The bioavailability of

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Ag is related to its speciation rather than to the total concentration (Ratte, 1999), and Ag2S is

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considered to be very stable. Although Ag2S may still be the predominant species in amended

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soils (Pradas del Real et al., 2016), the insoluble Ag2S cannot readily be taken up by plants.

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The risk of silver transfer from soils to the human food chain following biosolid application

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has been therefore been considered to be low (Wang et al., 2018). This suggests that the great

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majority of biosolid-borne Ag will remain in the soil. However, very few studies have

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examined the movement of Ag in soil profiles based on long-term experiments.

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A number of studies report the vertical migration of biosolid-borne potentially toxic

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elements (PTEs) in the soil profile (Zeng et al., 2015; Baveye et al., 1999). Some studies find

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that PTEs are sparingly transported below the root zone (Dowdy and Volle, 1983). However,

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repeated application may accelerate the downward flow of biosolid-borne Ag. Cadmium, Cr,

69

Cu, Ni, Pb, and Zn concentrations have been found to increase significantly down the soil

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profile to a depth of 80 cm following biosolid application (Seo et al., 2019; Udom et al., 2004;

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Campbell and Beckett, 1988). The bulk < 2 µm clay fraction significantly influences the

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occurrence and vertical migration of metals in soil profiles (Proust et al., 2013). However,

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leaching-induced migration of Ag is rarely reported after repeated biosolid applications.

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There is therefore a lack of quantitative information on the dynamic flow of biosolid-borne

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Ag in the soil-crop system with repeated application.

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Here, soil and crop samples were collected from two long-term biosolid application field

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plot experiments which differed greatly in soil properties and crops and the Ag concentrations

78

were determined. The aims were to investigate the distribution of Ag in soils and crops with

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repeated biosolid application, to analyse the effects of crop variety and soil properties on the

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environmental fate of biosolid-borne Ag, and to assess the potential environmental risks from

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Ag derived from biosolid application. This information will help in elucidating the fate of

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biosolid-borne Ag in the soil-crop system and identifying the critical risks associated with

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repeated biosolid application.

84 85

Material and methods

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Site description and sample collection

87 88

Two field experimental stations were selected to provide contrasting soil properties and cropping systems with a randomized complete block design at both sites.

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The first was at the station of Suzhou Academy of Agricultural Sciences located at

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Suzhou city, Jiangsu province, east China (31° 27′ N, 120° 25′ E). The soil is a Typic

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Hapli-Stagnic Anthrosols with a pH (in H2O) of 6.05 and the cropping system is a rice-wheat

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rotation. The rice and wheat varieties selected, Suxiangjing 1 and Yangmai 19, respectively,

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are widely used in Jiangsu province. Seeds were provided each season by Suzhou Academy

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of Agricultural Sciences. The field experiment at Suzhou started in December 2009 with four

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replicate plots (each 1.4 m long × 1.2 m wide) of each treatment. Soil water content was

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maintained by irrigation during the wheat season but the water level was controlled to

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maintain flooded conditions during the rice season. Four treatments were selected, namely

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zero biosolid control (SZ_CK), soil amended with domestic biosolids (SZ_SS1), industrial

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biosolids (SZ_SS2) and commercial sludge fertilizer (SZ_SS3). The biosolids were mixed

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with soil twice a year before sowing. This field experiment was originally designed to

4

101

investigate the effects of Cd uptake by rice with repeated biosolid application, and selected

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biosolids were later found to contain different concentrations of Ag, i.e. 4.39, 7.33 and 10.4

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mg kg−1, respectively. The biosolid amendment rate of SZ_SS1 and SZ_SS2 was 21.9 kg per

104

plot and that of SZ_SS3 was 4.5 kg per plot.

105

The second site was at the field station of the Chinese Academy of Agricultural Sciences

106

located at Dezhou city, Shandong province, northeast China (37° 20′ N, 116° 38′ E) (Li et al.,

107

2012; Yang et al., 2018). The soil is a Calcaric Ochri-Aquic Cambosols with a pH (in H2O) of

108

8.90 and the cropping system is a maize-wheat rotation. The field experiment started in

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October 2006 with three replicate plots (each 4 m long × 5 m wide) of each treatment. Five

110

treatments were selected, namely a control (DZ_CK), a chicken manure treatment (DZ_1CM),

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and three biosolid treatments with different application rates (DZ_1SS, DZ_2SS and

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DZ_4SS). The biosolids/manure were applied once a year before the wheat was sown.

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Biosolid rates of DZ_1SS, DZ_2SS and DZ_4SS were 36, 72 and 144 kg per plot,

114

respectively. This field experiment was originally designed to investigate the effects of

115

nutrient effects of repeated biosolid application. Further details of the long-term experiment

116

have been provided by Li et al. (2012) and Yang et al. (2018). Selected physico-chemical

117

properties and Ag concentrations of the test soils and biosolid samples are shown in Table 1.

118

Five evenly-distributed soil cores from the top 15 cm of the soil profile were thoroughly

119

mixed to give a composite sample from each plot collected after the rice harvest (Suzhou) or

120

maize harvest (Dezhou) each year. In addition, soil profile samples were collected to observe

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the vertical migration of Ag in 2017. Specifically, one-meter-deep soil profile samples within

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each plot were collected and separated into 5 20-cm depth categories (P1, 0‒20 cm; P2, 20‒

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40 cm; P3, 40‒60 cm; P4, 60‒80 cm; and P5, 80‒100 cm). The soil samples were taken with

124

a stainless-steel soil auger. Soil samples were air-dried and sieved through a 0.15-mm nylon

125

mesh. Plant aboveground parts were collected when the grains were fully developed and

5

126

separated into grain and straw (comprising all materials other than the grain). Plant samples

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were dried in a constant temperature drying oven at 70 ℃ and sieved through a 0.175-mm

128

nylon mesh.

129 130

Determination of silver concentrations

131

The crop samples were oven dried at 70 °C before analysis. A sealed high-pressure

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digestion method (Zhou et al., 2016a) was used to digest the biosolid, soil and crop samples

133

for the determination of total metal concentrations. In brief, the dried samples were digested

134

with an HNO3+HF+H2O2 mixture (5 mL + 2 mL + 1 mL) in a sealed high-pressure reaction

135

vessel followed by dilution with Milli-Q water (18.2 MΩ cm, 25 °C). The protocol is shown

136

in detail in Table S1. All digests were filtered through a 0.45-µm filter before analysis.

137

The Ag concentrations in digest solutions were determined by ICP-MS (7700x, Agilent

138

Technologies, Santa Clara, CA). Certified reference materials GBW07405 and GBW10020

139

(National Geochemical Standard Materials, Institute of Geophysical and Geochemical

140

Exploration, Langfang, Hebei, China) were used for QA/QC of soil and plant digestions,

141

respectively. Digestion blanks were also included to eliminate matrix effects.

142 143 144 145

Dynamics of mass balance The dynamic mass balance for biosolid-borne Ag accumulated was calculated using the following equations.

146

Δ =  −   −  ,

(E 2.3.1)

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 =  ∗  ∗  ,

(E2.3.2)

148

  = ∑  ∗  ∗ ,

(E2.3.2)

149

where, Δ is the total increment of silver in soil;  is the silver input with biosolid

150

application;   is the uptake of silver by crops; and  is the loss of silver from the 6

151

farmland system;  is the application count;  in the concentration of Ag in biosolids;

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 is the application rate of biosolids;  is the concentration of Ag in crops;  is the

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biomass of crops; and  is the moisture content of the crop.

154 155

Statistical analysis

156

The data were subjected to one-way analysis of variance (ANOVA) using the SPSS

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version 20.0 software package (SPSS, Chicago, IL). Duncan’s multiple range test was used to

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compare significant differences between different treatment means at the 5 % level.

159 160

Results

161

Silver concentrations in soils and plants at Suzhou long-term experimental station

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Silver accumulated in soils with biosolids application in successive years. Soil total Ag

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concentrations followed the sequence SZ_SS3 > SZ_SS2> SZ_SS1> SZ_CK after

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amendment with different types of biosolids (Fig. 1-A). There were still no significant

165

differences (p > 0.05) among the treatments in 2013 but the treatment effects reached

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significance (p < 0.05) in 2017. In 2013, soil total Ag in treatments SZ_SS1, SZ_SS2 and

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SZ_SS3 increased by 0.010, 0.014 and 0.043 mg kg−1, respectively, and the Ag increments in

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soil were 0.063, 0.097 and 0.24 mg kg−1 from 2014 to 2017. The accumulation rate of Ag in

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amended soils therefore increased about six times within four years.

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As shown in Fig. 1-B, Ag decreased from P1 to P5. Clearly, Ag accumulated in the

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surface soil with top dressing of biosolids and there was less effect deeper in the soil profile.

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Silver no longer significantly accumulated with biosolid application at only P2.

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Silver concentrations were significantly greater with biosolid application compared to the

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zero control in both 2013 and 2017, while Ag concentrations in crops might also be affected

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by weather conditions during the growing period (Fig. 2). Across all treatments, for any one

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crop the Ag in the straw (inedible part) was higher than that in the grain (edible part). Silver

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accumulation differed in different species and might be specific to wheat and rice. More

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specifically, wheat was more likely to accumulate Ag than rice with biosolid application.

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Regarding the edible part, Ag was higher in the whole wheat grain than in the brown rice, as

180

was the translocation factor (TF, grain Ag concentration divided by straw Ag concentration)

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of wheat.

182 183

Silver concentrations in soils and plants at Dezhou long-term experimental station

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Repeated biosolid application also resulted in a substantial accumulation of Ag in the

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surface soil at Dezhou station (Fig. 3-A). The observation period was divided into two

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segments, years 2006‒2011 and years 2012‒2017. Soil Ag concentrations in treatments

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DZ_1SS, DZ_2SS and DZ_4SS increased by 0.13, 0.27 and 0.48 mg kg−1, respectively,

188

during the first stage. The increment of soil Ag in DZ_2SS treatment was double that in

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DZ_1SS soil, the multiple of which was approximately equal to that of the application rate.

190

However, Ag in DZ_4SS soil increased 3.6 times that in DZ_1SS, slightly less than the

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multiple of the application rate. Soil Ag in treatments DZ_1SS, DZ_2SS and DZ_4SS in the

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second stage increased by 0.10, 0.23 and 0.52 mg kg−1. Silver in DZ_2SS and DZ_4SS soil

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increased by 2.3 and 5.4 times that in treatment DZ_1SS.

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Biosolid-borne Ag appeared to migrate more readily at Dezhou station (Fig. 3-B).

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Biosolid application led to downward migration of Ag and significant accumulation (p < 0.05)

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in the soil profile down to 60‒80 cm depth. Furthermore, the higher the application rate the

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stronger the Ag migration behaviour in the soil profile. There were no significant differences

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in Ag concentration between 1SS_DZ and 2SS_DZ at P3, nor with the control at P4.

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However, the Ag concentration in treatment 4SS_DZ was always higher than in the control or

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the other treatments in the soil profile from P1 to P4. Considering the homogeneity of

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Calcaric Ochri-Aquic Cambosols, the total Ag concentration in the soil profile provides a

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basis for comparing biosolid-borne Ag accumulation between different application rates. The

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values in DZ_2SS and DZ_4SS soils increased 2.2 and 4.7 times over DZ_1SS, and both

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were higher than the application rate.

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Differences among crops were also found in the light of the observations at Dezhou

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long-term experiment (Fig. 4). Biosolid application significantly increased Ag concentrations

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in wheat without clear dosage response relationships or long-term effects. However, biosolid

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application did not result in significant Ag accumulation in maize. The maize straw Ag

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concentrations were 7.07 ± 0.66, 3.33 ± 0.34, 4.43 ± 0.16, 4.58 ± 0.17 and 6.64 ± 0.96,

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respectively, in CK_DZ, 1CM_DZ, 1SS_DZ, 1SS_DZ and 4SS_DZ in 2017. Assuming that

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treatment 1CM_DZ received biosolids free of Ag, the input of Ag well balanced (p < 0.05)

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the negative effects of biosolid application.

213 214

Dynamics of silver mass balance in the soils

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Based on the example of Dezhou long term experiment the dynamic mass balances of

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silver were calculated to explore the behaviours of biosolid-borne Ag in the soil-crop systems

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with repeated application. In the Calcaric Ochri-Aquic Cambosols the texture and colour at

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each soil depth are relatively uniform. Assigning 1.38 g cm−3 to unit weight (Li et al., 2012),

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the amount of Ag in each layer was calculated (Table S2).

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According to the formula E2.3.1,

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Δ_ =  −   _ − _ ,

(E3.3.1)

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Δ_ = 2 ∗  −   _ − _ ,

(E3.3.2)

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Δ_ = 4 ∗  −   _ − _ ,

(E3.3.3)

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Assuming that leaching loss of Ag would have a linear correlation with application, that

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of

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_ =  ∗  ∗  + ,

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Considering this is less than 1 ‰ of the applied amount ( ),   was ignored.

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(E3.3.4)

Taking the data in Table S2, it was calculated that

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â = 0, _ = ĉ ≈ 1.22 g.

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This suggests that leaching loss of Ag might be constant and independent of application

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rate.

232 233

Discussion

234

Effects of downward transport of Ag in soils with biosolid application

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Suzhou and Dezhou long-term experiments showed substantial differences with repeated

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biosolid application. Specifically, Ag accumulated in the surface soil with little migration

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down to 20‒40 cm depth at Suzhou, and Ag migrated down to at least 60 cm with biosolid

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application, and to 60‒80 cm depth in the 4SS biosolid application treatment at Dezhou

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station. Generally, Ag would be more available in slightly acid soils for release of H+ (Wu et

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al., 2018; Zhou et al., 2016b). However, Ag migrated down deeper at Dezhou long-term field

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experiment where the soil pH is slightly alkaline (pH 8.90). This suggests that some other soil

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properties may have a role in the downward transport of silver in such as summer rainfall.

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Typic Hapli-Stagnic Anthrosols are typically waterloggogenic paddy soils of which the

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soil parent material is loess lacustrine sediment (Jiangsu Province Soil Survey Office, 1996).

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The soil profile consists of a plough horizon (Aa)-plow pan (Ap)-percogenic horizon

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(P)-waterloggogenic horizon (W)-C horizon (C) sequence from top to bottom (Du et al.,

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2007). This type of soil is slightly acid due to leaching of basic cations. Soil micro-aggregates

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are mainly (about 50‒60%) made up of 0.05‒0.01 mm granularity. Reducing action plays a

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dominant role in the process of soil formation with the seasonal rise and fall of phreatic water

250

resulting in redox variation during the year. Calcaric Ochri-Aquic Cambosols are slightly

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calcareous and are fluvial deposit basic soils. There is no clay interlayer within one meter of

252

depth and the soils are homogeneous light loams throughout the depth range investigated here.

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The downward transport of Ag, by contrast, was impeded by the heavy clay soil at Suzhou

254

long-term experimental station. Thus, the soil texture will be an important factor affecting the

255

downward transport of biosolid-borne Ag.

256 257

Forms of silver transported downward in soils with biosolid application

258

Another important question is the speciation of Ag moving down to deeper layers of the

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soil profile. Firstly, we have found that the leaching of biosolid-borne Ag might be constant

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for a certain soil even with different amendment rates. It is generally known that

261

biosolid-borne Ag is predominantly Ag2S and is therefore non-labile (Kim et al., 2010). Ag2S

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remains stable in soils during long-term weathering and ageing (Donner et al., 2015). There is

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very little dissolved silver in soils to which biosolids are applied. Combined with mass

264

balance, there is much more Ag transported down the soil profile than in the dissolved

265

fraction.

266

Secondly, downward transport of biosolid-borne Ag seems to be affected by the size of

267

the soil pores physically retarding movement rather than by soil pH. In addition,

268

breakthrough curves of Ag nanoparticles and Ag+ have been used to compare their transport

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in different soil types, with much easier leaching of Ag-NPs in paddy soil than in Calcaric

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Ochri-Aquic Cambosols (Wang et al., 2014). Their results are very different from those at

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Dezhou field experiment where the charge of the zeta potential affected the leaching of Ag

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nanoparticles and Ag+. The evidence indicates that the biosolid-borne Ag might be

273

transported downward in the form of Ag2S particles but this needs to be confirmed by further

274

study.

275

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Differences in silver concentrations among crop types

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There were similar trends in biosolid application effects at both Suzhou and Dezhou

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long-term field experiments in different years and there were marked differences in Ag

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uptake among the different crop types. The capacity of wheat grains to accumulate Ag seems

280

to be higher than that of other crops such as rice or maize and may be related to physiological

281

and biochemical characteristics of the crop. For example, spring wheat genotypes Lutescens

282

574 and Eritrospermum 78 and winter wheat genotypes Navruz and Tacika exhibit Fe and Zn

283

accumulation in the grains due to the presence of sulphur-containing amino acids

284

(Morgounov et al., 2007).

285

Seasonal variation in soil properties might also contribute to the Ag uptake by crops. A

286

typical rice-wheat rotation system is grown at Suzhou experimental station. There is therefore

287

a clear dry-wet alternation between the different plant growing seasons and the soil will be in

288

a reduced state during the rice season under flooded conditions. The soil redox (Eh) is

289

negative and the pH may be slightly increased under flooded conditions, leading to a decrease

290

in the availability of Ag in the soil (Wu et al., 2018). Maize is grown in the rainy season at

291

Dezhou experimental station. Heavy rainfall will accelerate the leaching loss of bioavailable

292

Ag and may suppress accumulation of the metal by the crop. It may therefore be more

293

difficult for rice or maize to take up metals despite their high total soil concentrations.

294 295

Potential environmental risks from soil silver inputs

296

Consumers will be increasingly at risk of exposure to Ag via the food chain with the

297

release of Ag into the soil-crop system from repeated biosolid applications. It is generally

298

acknowledged that there are limited risks of Ag transfer to the food chain because Ag2S is

299

likely the main form of Ag present (Wang et al., 2018, Donner et al., 2015). A value of 100 µg

300

Ag kg−1 has been adopted as a food safety standard that may lead to adverse effects in

12

301

animals (NRC, 2005). However, the chronic toxic effect has not been considered. Not overall

302

toxicity has been recorded in mice orally exposed to 46 µg AgNP per kg pellets, but even so,

303

this dose may induce considerable microbial changes in the murine gut (van Den Brûle et al.,

304

2015). The ability of Ag to bind to metallothionein is greater than that of copper, cadmium,

305

mercury or zinc (Scheuhamme and Cherian, 1986). In addition, straw in soils receiving

306

repeated biosolid amendments may lead to transfer of Ag to the food web if the straw were

307

used to feed livestock or cultivate mushrooms (Xing et al., 2016).

308

Based on the observations at Dezhou station, leaching might be the main pathway of Ag

309

loss from the soil-crop system. Soil-water dynamics will be influenced by precipitation and

310

irrigation and recharge rates were found to be 65.9‒126.8 mm y−1 on the North China Plain

311

(Lin et al., 2013).

312

 =

 !"## $∗ ∗%

(E 4.3.1)

313

where the  is the leaching loss of Ag, around 1.22 g in the current study; & is the

314

precipitation (mm y−1); ' is the area of the plots, 20 m2 at Dezhou station; ( is the biosolid

315

applied years, 11 years in the present study.

316

According to formula E4.3.1 the Ag concentration in groundwater ( ) was calculated to

317

be 0.044‒0.084 mg L−1 which is close to the safe level of 0.05 mg L−1 (Ministry of Health of

318

the People's Republic of China, 2006). Ag2S dissolution may be increased by oxidation of

319

Fe3+ and the hydroxyl radical in the aquatic environment (Li et al., 2017; Li et al., 2015).

320

It seems that the amount of Ag leaching is unrelated to the biosolid application rate.

321

There may be two possible scenarios for leaching loss of biosolid-borne Ag with different

322

application rates (Fig. 6). One is loss at a geometric level (assumption 1) and the other is loss

323

at equivalent level (assumption 2). The labile pool of available Ag leaching in

324

biosolid-amended soils may be proportionally determined by the application rate. However,

325

the leaching loss of biosolid-borne Ag might be constant and unrelated to application rate. 13

326

This suggests that the amount leached might be limited by water recharge and by soil

327

properties, resulting in an actual content of Ag leached less than the labile pool capacity,

328

especially in high application rate treatments. In other words, there is much more residual Ag

329

having higher leaching potential. It may therefore be expected that leaching losses of Ag

330

might continue for some time even after suspending biosolid application. Therefore, both

331

food security and groundwater protection based soil risk assessment may be required.

332 333

Conclusions

334

The accumulation of biosolid-derived metals in soils reflects the influence of human

335

activities on the geochemical cycles of metals. Biosolid amendments may accelerate the

336

natural flow of inert metals. Silver will accumulate in soils with repeated biosolid application.

337

Consequently, the concentration of Ag in crops may increase and wheat is suspected to take

338

up more than others. However, crops take up ˂ 1‰ of the input of biosolid-borne Ag. Indeed,

339

biosolid-borne Ag might be lost from soils by leaching or run-off. Soil texture is an important

340

factor affecting the downward transport of biosolid-borne Ag. A low clay content may

341

facilitate the migration of Ag in the soil profile. Biosolid-borne Ag is suspected to be

342

transported downward in the form of Ag2S. Further studies may elucidate the speciation of

343

migrating Ag through the use of

344

present evidence that the leaching loss of Ag was unrelated to the biosolid application rate.

345

This suggests that Ag losses from soils may be restricted by groundwater recharge and soil

346

properties. However, even low rates of Ag loss may continue in the long term. When Ag2S

347

reaches the aquatic environment the bioactivity and toxicity of the Ag will change

348

accordingly. Thus, there are some subsequent risks from the dynamic behaviour of Ag that

349

merit further investigation.

110

Ag isotopic dilution (Donner et al., 2015). Here, we

350

14

351

Conflict of interest

352 353

The authors declare no conflicts of interest.

354 355

Acknowledgments

356 357

This study was funded by the National Natural Science Foundation of China (41325003).

358

The authors would also like to thank Changyu Tian, Changying Lu and all other staff who

359

have managed the long-term field experiments.

360 361

Appendix A. Supplementary data

362 363

The following are the supplementary data relating to this article:

364

Supporting Information.

365 366

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18

470

Table1 Selected properties of the test soils and biosolids Soil type or biosolid source

471

pH

Clay/silt/sand

OM (g kg−1)

TN (g kg−1)

TP (g kg−1)

SZa

6.05

44/41/15

30.7

1.74

0.80

7.58

0.12

DZb

8.90

18/18/64

12.0

0.80

1.00

3.00

0.14

SS1a

6.23

-

463

46.8

11.0

14.4

4.39

SS2

6.07

-

487

40.8

13.2

10.2

7.33

SS3a

6.85

-

458

33.7

24.5

15.8

10.4

SSb

7.50

-

355

27.0

38.0

15.0

5.23

CMb

-

-

208

24.0

20.0

2.00

-

a

from Wu et al. (2018); b from Li et al. (2012).

472

19

TK Ag −1 (g kg ) (mg kg−1)

473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494

Figure captions, Fig. 1. Effect of different biosolids on silver concentrations in the soil arable layer and translocation in the profile at Suzhou field experimental site. P1, 0‒20 cm; P2, 20‒40 cm; P3, 40‒60 cm; P4, 60‒80 cm; and P5, 80‒100 cm. Fig. 2. Concentrations of Ag in stems and grains of wheat and rice under different biosolid applications in 2013 and 2017 at Suzhou field experimental site. Fig. 3. Effect of different biosolids on silver concentrations in the soil arable layer and translocation in the profile at Dezhou field experimental site. P1, 0‒20 cm; P2, 20‒40 cm; P3, 40‒60 cm, P4, 60‒80 cm; and P5, 80‒100 cm. Fig. 4. Concentrations of Ag in stems and grains of wheat and rice under different biosolid applications in 2011 and 2017 at Dezhou field experimental site. Fig. 5. The biosolid-borne Ag flux in the agricultural system at Dezhou field experimental site (g). Fig. 6. Diagrammatic representation of the leaching loss of Ag with different application rates. Grey dots, biosolid-borne Ag; green dots, leaching Ag.

20

495 496 497

Fig. 1

21

498 499 500

Fig. 2

22

501 502 503

Fig. 3

23

504 505 506

Fig. 4

24

507 508 509

Fig. 5

25

510 511

Fig. 6

26

Dear editor, Sorry for our mistakes on the figure captions of article: Reference: ENPO 113834 ENVPOL_2019_4994: A field study of the fate of biosolid-borne silver in the soil-crop system. The figure labels have been checked and provided as shown below in Fig. 1 Fig. 2, Fig 3, and Fig. 4. And, in the MS the citation for Fig. 5 has been added, the words: “(Fig. 5)” need be added into the MS at line 217, it is “Based on the example of Dezhou long term experiment the dynamic mass balances of silver were calculated to explore the behaviours of biosolid-borne Ag in the soil-crop systems with repeated application (Fig. 5)”.

Figure captions, Fig. 1. Effect of different biosolids on silver concentrations in the soil arable layer (A) and translocation in the profile (B) at Suzhou field experimental site. P1, 0‒20 cm; P2, 20‒40 cm; P3, 40‒60 cm; P4, 60‒80 cm; and P5, 80‒100 cm. Fig. 2. Concentrations of Ag in stems and grains of wheat and rice under different biosolid applications in 2013 (A and B) and 2017 (C and D) at Suzhou field experimental site. Fig. 3. Effect of different biosolids on silver concentrations in the soil arable layer (A) and translocation in the profile (B) at Dezhou field experimental site. P1, 0‒20 cm; P2, 20‒40 cm; P3, 40‒60 cm, P4, 60‒80 cm; and P5, 80‒100 cm. Fig. 4. Concentrations of Ag in stems and grains of wheat and rice under different biosolid applications in 2011 (A and B) and 2017 (C and D) at Dezhou field experimental site.

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Sincerely yours, Longhua Wu 2019.12.18 Nanjing

Highlights




Soil texture is an important factor in biosolid-borne silver behaviour in soil-crop system;




Ag accumulated in the soil after biosolid application;




Leaching losses of Ag may not be related to the biosolid application rate.

Author statements A field study of the fate of biosolid-borne silver in the soil-crop system

All authors of this paper have read and approved the final version submitted. We state that the paper has not been published previously elsewhere in any language; it is not being considered by another journal in any language; and all authors have seen and agreed to the version submitted. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Author contributions: Longhua Wu, Yibing Ma and Lu Yang designed and performed the research; Lu Yang, Simin Li, Longhua Wu and Yibing Ma collected the soil and plant samples; Lu Yang determined the metal concentrations, analysed and interpreted the data; Lu Yang, Simin Li, Longhua Wu, Yibing Ma, Yongming Luo and Peter Christie involved in writing the manuscript; Peter Christie from United Kingdom also helped improving the English writing.

Conflict of interest

The authors declare no conflicts of interest.