Contrasting Effects of Cattle Manure Applications and Root-Induced

Apr 3, 2017 - To characterize the dynamic mobilization of heavy metals (HM) in a crop–soil system affected by cattle manure (CM) application, soybea...
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Contrasting Effects of Cattle Manure Applications and Root-Induced Changes on Heavy Metal Dynamics in the Rhizosphere of Soybean in an Acidic Haplic Fluvisol: A Chronological Pot Experiment Qingnan Chu,† Zhimin Sha,‡ Mitsuru Osaki,† and Toshihiro Watanabe*,† †

Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan School of Agriculture and Biology, Shanghai Jiaotong University, 200240 Shanghai, China

‡

S Supporting Information *

ABSTRACT: To characterize the dynamic mobilization of heavy metals (HM) in a crop−soil system affected by cattle manure (CM) application, soybean [Glycine max L. Merr. cv. Toyoharuka] crops were exposed in a chronological pot experiment to three CM application rates and sampled at two vegetative stages and two reproductive stages. A sequential extraction procedure for metal fractionation, soil pH, microbial activity, and plant HM uptake was determined. In non-rhizopshere soil, with CM application a liming effect was detected, and increased microbial activity was detected at the reproductive stage. CM application shifted Cd from available state to oxide-bound pool in non-rhizosphere soil; however, shifts in Cd from an oxide-bound pool to the available state were observed in rhizosphere soil. CM application stabilized the available Zn and Pb to oxide-bound Zn and organic-bound Pb in both non-rhizosphere and rhizosphere soils, and the stabilizing degree increased with higher CM application rates. The promoted Zn immobilization in the rhizosphere was due to the liming effects induced by added CM that counteracted the root-induced acidification. On the basis of a stepwise multiple regression analysis, the shift of Cd and Pb fractionation was mainly related to microbial activity. Adding manure inhibited Zn and Pb uptake but promoted Cd uptake by soybean, and a greater influence was detected at the reproductive stage, at which CM application increased the root Cd-absorbing power but did not significantly affect the Zn- and Pb-absorbing powers. In an agricultural context, long-term CM application, even at the recommended rate of 10.13 Mg ha−1, may cause a soybean Zn deficiency and high Pb accumulation in Haplic Fluvisols, although CM is often considered as an environmentally friendly fertilizer. KEYWORDS: acidic soil, cattle manure, heavy metal, metal fractionation, rhizosphere, soybean

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INTRODUCTION Farmyard livestock manure application has dual influence on altering soil heavy metal (HM) availability. On the one hand, it might reduce metal availability by promoting soil organic matter and phosphorus that immobilize metals by complexation or precipitation.1−4 On the other hand, the addition of animal manure has been shown to enhance the solubility of HMs in soils by adding a high amount of dissolved organic compounds, such as organic acids.5−7 Long-term and frequent animal manure application results in HM enrichment in soils8,9 that is toxic to plants and animals and also facilitates the entry of toxic metals into the human food chain.10 The rhizosphere is a microenvironment that is influenced by root secretions and associated soil microorganisms, and the physicochemical conditions may be drastically different in many respects from those in the non-rhizosphere soil (NRS).11 Therefore, root-induced changes in the rhizosphere soil (RS) have a considerable effect on HM speciation and phytoavailability. In particular, root-induced changes in pH via proton and organic acid release are recognized as a critical mechanism that influences HM solubility in the rhizosphere.12−14 In addition, root growth could promote microbial biological activity, and this interaction between roots and soil microbes can enhance metal bioavailability in the RS.15−17 Consequently, a dynamic analysis of HM mobilization in RS and NRS is vital to evaluate their potential risks. © 2017 American Chemical Society

The impact of organic amendments on the fate of HMs in the rhizosphere of a given soil and vegetation type is specific to a metal, even the metal state. This is likely due to the different capacities of metal sorption and desorption caused by different ionic structures and electronegativities. For instance, an Egyptian Entisol that developed on lacustrine and fluvial deposits showed a higher affinity for Zn, whereas a Histosol that developed on lacustrine deposits showed a higher affinity for Cd and a low affinity for Zn.18 Moreover, with the same soil and vegetation, a high deficiency of total Zn and a high accumulation of total Cd in agricultural calcareous soils after a long-term cattle manure (CM) application have also been reported.4 In acidic soil, a manure application generally increases the soil pH and causes differential effects on the bioavailability of different metals.9,19,20 Haplic Fluvisols were used in this study. They are widely distributed in the alluvial plain of coastal areas, alluvial fans, and lowlands and in regions with a favorable drainage performance in Japan. They are often intensively cultivated due to their good natural fertility and attractive dwelling on higher elevation in marine landscapes.21 They are the main acidic farmland soil Received: Revised: Accepted: Published: 3085

December 29, 2016 March 28, 2017 April 3, 2017 April 3, 2017 DOI: 10.1021/acs.jafc.6b05813 J. Agric. Food Chem. 2017, 65, 3085−3095

Article

Journal of Agricultural and Food Chemistry Table 1. Chemical Properties and Mineral Elements Content of the Soil Used in the Chronological Pot Experiments g kg−1 total N 5.30

total P

mg kg−1

total K

total Ca

total Mg

10.29

9.32

1.03 7.08 exchangeable cations (cmol kg−1)

total Na 912.05 mg kg−1

total Zn

total Cd

total Pb

72.34

0.90

34.39

K

Na

Ca

Mg

CEC

Truog-P

NO3−-N

NH4+-N

pH

organic matter (g kg−1)

6.43

1.12

16.82

4.36

37.48

83.15

13.4

4.05

5.30

65.08

Table 2. Chemical Properties and Mineral Element Contents of the Cattle Manure Used in the Chronological Pot Experiments g kg−1 total N

total P

mg kg−1

total K

total Ca

total Mg

total Na

total Zn

total Cd

total Pb

17.55

10.85

5700 mg kg−1

124.77

0.19

14.26

11.24 7.72 25.87 water extract (1:10, mg kg−1 dry wt) K

Na

Ca

Mg

EC (mS cm−1)

Truog-P

NO3−-N

NH4+-N

pH

organic matter (g kg−1)

2.43

83.85

18.31

8.84

4.08

5.16

0.72

0.13

7.18

414.5

Table 3. Extraction Methods for Sequential Extraction and Nominal Phasesa phase

abbreviation

water-soluble easily exchaneable bound to carbonate occluded to iron and manganese oxides or hydroxides bound to organic matter

CARB OXI

residual

RES

a

ORG

reagent 20 20 20 20

mL mL mL mL

of of of of

Milli-Q water 1 M NH4Ac at pH 7 1 M NH4Ac/HAc at pH 5 0.04 M NH2OH·HCl in 25% HAc at pH 2

15 mL of 30% H2O2 in 1 M HNO3 at pH 2; after cooling, followed by 5 mL of 3.2 M NH4Ac in 20% HNO3 20 mL of 7 M HNO3

heating time

6 h at 60 °C by water bath 6 h at 80 °C by water bath

shaking time 1 h at 25 °C 1 h at 25 °C 5 h at 25 °C 0.5 h at 25 °C 0.5 h at 25 °C microwave digestion

The sum of water-soluble and exchangeable fractions was considered as the available fraction. concentrations in the agricultural soil of Japan.26 The higher metal content in the soil may derive from the long-term fertilization with P in the form of superphosphate. Phosphate rock often contains heavy metals.23 Air-dried soils were sieved to pass through a 2 mm mesh, and then 2 kg of soil was filled in a free-draining plastic pot (2 L). This experiment comprised four treatments with different CM application rates: 0 (control, CM0), 9 (CM1), 18 (CM2), and 36 (CM3) g, which are equivalent to field application rates of 0, 10.13, 15.18, and 20.25 Mg ha−1, respectively. The selection of CM1 was based on the recommended application rate in the Hokkaido fields. The chemical properties and ion concentrations of CM are shown in Table 2. Each treatment was performed in triplicate. After the manure had been mixed with soil, the pots were incubated for 2 weeks in a greenhouse under moderately moist conditions (60% of field water-holding capacity). In the greenhouse, there is a 14 h photoperiod and day/ night temperatures of 25−28 and 18−22 °C, respectively, with natural light. Soybean (Glycine max L. Merr. cv. Toyoharuka) seeds were sterilized with 10% (v/v) of an H2O2 solution for 1 min and then rinsed with Milli-Q water. Ten seeds were then sown in each pot and thinned to two seedlings with similar growth 1 week after sowing. During the culture period, deionized water was added daily to maintain the water-holding capacity at 60%. Soil and Plant Sampling. Four groups of pot experiments were conducted at the same time, and soil and plant samples were collected 3, 4, 5, and 6 weeks after sowing, respectively. The four sampling times corresponded to two vegetative stages and two reproductive stages: second trifoliolate (V2), fourth trifoliolate (V4), beginning bloom (R1), and full pod (R4). The plant samples were separated into shoots (aboveground plant parts) and roots. The separated fresh samples were frozen immediately in liquid nitrogen, stored at −80 °C, and then lyophilized. The dry weight (DW) was measured, and then the plants were finely crushed before the HM concentrations were analyzed.

(pH 30 cmol kg−1).22,23 Acidified soils can decrease the adsorptive capacity of the soils and consequently increase HM phytoavailability;8 however, a high soil CEC can reduce the bioavailable fraction in soils.24 In our previous study, we have found that CM application promoted soybean Cd uptake by increasing the soil Cd availability.7,19 However, the exact mechanism in the rhizosphere of soybeans remains unknown. Considering Cd ions have been demonstrated more weakly adsorbed than other HMs across different soils,18 even in soils with an increased pH by an organic amendment,3,25 we hypothesized that the CM application would cause (1) high Cd availability in soil and plant Cd uptake; (2) lower Zn uptake with increasing Cd:Zn ratio in the soil; and (3) more Pb accumulation in the soil due to its high absorption capacity with soil minerals. In this study, we designed a time course pot system to elucidate the chronological variation of HM fractions in RS and NRS and further HM uptake under CM application.

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MATERIALS AND METHODS

Experimental Setup. One chronological pot trial was conducted in a greenhouse at Hokkaido University, Japan. Soil for the experiments was collected from the upper horizon (0−25 cm layer) of agricultural fields at Hokkaido University. It was classified as a Haplic Fluvisol according to the U.S. Soil Taxonomy Classification, developed from a sulfate sandy loam formation representative of the marine alluvia deposited in the brown lowland. Crops grown on the collected soil in the previous two years were maize (Zea mays L.) and cucumber (Cucumis sativus L.). The initial soil properties before the experiment began are shown in Table 1. Soil pH was determined by a soil/Milli-Q water ratio of 1:2.5 (w/v). CEC was assessed by leaching the soil with 1 M KCl. The soil total Cd, Zn, and Pb concentrations were 2.73, 1.11, and 2.43 times higher, respectively, than the mean 3086

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Journal of Agricultural and Food Chemistry Table 4. Effects of CM Treatments on pH, CEC, and Microbial Activity (AWCD) in RS and NRSa CM0-NRS V2 V4 R1 R4

5.33cA 5.37cdA 5.38bA 5.35cA

CM0-RS

CM1-NRS

5.23cA 5.16 dB 5.10cC 5.08dC

5.75bC 5.94bB 5.96abB 6.12bA

V2 V4 R1 R4

45.32dA 51.19dA 50.20dA 54.41dA

77.97bA 67.05cB 66.79cB 61.04cdC

55.74cC 61.52cdB 65.31cAB 73.55cA

V2 V4 R1 R4

0.54cA 0.57bA 0.61dA 0.54eA

0.88bA 0.61bB 0.54 dB 0.68 dB

0.57cA 0.62bA 0.61dA 0.64dA

CM1-RS

CM2-NRS

pH 5.71bA 5.81abC 5.52cAB 6.03bB 5.36bB 6.10abAB 5.35cB 6.17bA CEC (cmol kg−1) 76.15bB 56.35cC 79.56bAB 60.91cdC 80.27bAB 66.49cB 84.99bA 76.62cA AWCD 0.90bA 0.53cA 0.65bB 0.54bA 0.74cAB 0.65dA 0.86cA 0.67dA

CM2-RS

CM3-NRS

5.72bA 5.55cB 5.44bB 5.38cB

5.92aC 6.22aB 6.27aB 6.45aA

83.26abB 88.94bA 86.22bAB 90.12bA

60.22cC 61.70cdC 70.29cB 82.55bcA

1.00aA 0.71bB 0.87bB 1.06bA

0.61cB 0.66bB 0.77cA 0.82cA

CM3-RS 5.80abA 5.71bcA 5.58bB 5.46cB 97.16aB 100.30aB 109.34aA 102.06aB 1.07aAB 0.91aB 1.05aAB 1.24aA

a Different letters show significant difference among treatments (P < 0.05, n = 3): for each element, concentrations at different growth stages within one treatment denoted with the same letter (A−C) and concentrations at the same stage affected by different treatments denoted with the same letter (a−e). CM, cattle manure; RS, rhizopshere soil; NRS, non-rhizosphere soil; CEC, cation-exchangeable capacity; AWCD, microbial activity.

kinetics was carried out, as described by Cornu et al.29 The kinetics of metal influx by plant roots is given by

The root with adhering soil was dug up as carefully as possible to prevent fine root fracture. The soil that remained in the pot was considered to be the NRS. Soil 5 mm away from the roots was carefully removed with a brush and tweezers and then thrown away. Soil adjacent to the root segment, at 1−5 mm from the root surface, was shaken off and defined as RS, which was more affected by root behavior. RS and NRS samples were passed through a 2 mm mesh immediately upon collection. Soil sampling was completed in sterile plastic bags placed in an ice box and transported to the laboratory. Each sample was divided into three subsamples: one portion was airdried for the analysis of pH and CEC; some fresh soil samples were stored at 4 °C for a Biolog Ecoplate analysis; and the remaining were frozen rapidly with liquid nitrogen, stored at −80 °C, and then lyophilized before analysis of metal fractionation and organic acids. Plant and Soil Biochemical Analyses. Plant materials (0.05 g) were digested with 2 mL of 61% HNO3 and 0.5 mL of H2O2. Cd, Zn, and Pb concentrations were determined by an inductively coupled plasma mass spectrometer (ICP-MS) (Elan, DRC-e; Perklin-Elmer, Waltham, MA, USA).19 Soil pH and CEC were analyzed as described above. A sequential extraction technique was used to analyze the soil metal fractionation. The metals were separated into five operationally defined fractions as suggested by Kabala and Singh.27 Two gram soil samples were weighed and placed in a 15 mL polycarbonate centrifuge tube. The extracting methods were performed sequentially and are summarized in Table 3. After each extraction step, the supernatant liquid was separated from the solid phase by centrifugation at 4000g at 4 °C for 15 min. It was then filtered through filter paper (no. 5C) into a 50 mL metal-free polycarbonate centrifuge tube. The remaining residue was washed with 10 mL of Milli-Q water, and the water used for washings was discarded after centrifugation. The samples were analyzed for Cd, Zn, and Pb using ICP-MS as described in our previous study.19 The sum of the water-soluble and exchangeable fractions was considered as the available fraction. Soil microbial activity was determined using Biolog Ecoplates (Biolog Inc., Hayward, CA, USA), as described in our previous study.28 The reading at 96 h of incubation was collected by the plate reader. Normalization was performed against the blank well (control) for each replicate, and the average well color development (AWCD) was determined by calculating the mean of each well’s absorbance value (Abs) at 595 nm for the 96 carbon source-containing wells at every reading time. The AWCD was considered to reflect the microbial activity. Estimation of the Root HM-Absorbing Power (α). To estimate the mean root absorbing power for heavy metals (α) and to check whether they changed as a plant grew or were affected by different application amounts of CM, a calculation on Michaelis−Menten

dQ metal dt

= α × Cs × W (t )

(1)

where Qmetal is the quantity of metal cations absorbed (μg), t is the thermal time expressed in growing day degrees (GDD), α is the root metal-absorbing power (L g −1 GDD−1), Cs is the available concentration of metal cations in the soil (μg kg−1), and W is the root dry weight (g). Assuming an exponential growth of roots over thermal time

W (t ) = W0 × exp(root RGR × t )

(2)

Equation 1 gives

Q metal =

α × Cs × W (t ) + β root RGR

(3) −1

where root RGR is the relative growth rate of roots (GDD ) and W0 is the initial root biomass (g). Root biomass data were first fitted to the experimental growth model (eq 2) to estimate root RGR. The variables Qmetal × root RGR/Cs were then plotted against root dry weight [W(t)]; the slopes allowed an estimation of the root metal cation-absorbing power α. Data Analysis. All experimental data were statistically analyzed using SPSS version 18.0 (SPSS Inc., Chicago, IL, USA). Analysis of variance (ANOVA) followed by Tukey’s HSD test was used to detect significant differences among treatments at a P < 0.05 probability level. Analyses of covariance (ANCOVA) were used to test the effect of different CM application rates on the linear relationships relative to plant HM uptake, and a conservative P limit value of 0.01 was used. The correlation between variables was calculated using Pearson’s nonparametric test. To determine the key factor(s) affecting soil available HMs and the quantitative relationships between them, a stepwise multiple regression analysis was applied using the criteria of probability of P < 0.05 to accept and P > 0.05 to remove a variable from the analysis.

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RESULTS AND DISCUSSION pH, CEC, and Microbial Activity in RS and NRS. In the NRS, the CM application showed a significant liming effect as the pH rose from 5.33 to 5.80 (at V2) (Table 4), probably due to the dissolution of metal oxides, hydroxides, and carbonates with the organic compounds released from manure. Similar results were found in many other studies.4,9,20,28,30 As soybeans 3087

DOI: 10.1021/acs.jafc.6b05813 J. Agric. Food Chem. 2017, 65, 3085−3095

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Journal of Agricultural and Food Chemistry

Figure 1. Fractionation of Cd, Zn, and Pb in the NRS and RS of soybean in CM0, CM1, CM2, and CM3 treatments at different growth stages (Available, sum of water-soluble and exchangeable; OXI, bound to iron and manganese oxides; ORG, bound to organic matter). Only those fractions showing significant difference (P < 0.05) among treatments, according to ANOVA, are presented. Other fractions showing insignificant difference are shown in Table S1. Values are the average (n = 3) ± standard deviations. For each fraction at each growth stage, columns with the same letter do not differ significantly at the 5% level according to Tukey’s multiple-comparison test. CM, cattle manure; V2, second trifoliolate; V4, fourth trifoliolate; R1, beginning bloom; R4, full pod; OXI, metals bound to iron or manganese oxides or hydroxides; ORG, metals bound to organic matter.

grew and developed from V2 to R4, such a liming effect significantly increased under CM1, CM2, and CM3 treatments, which may have been due to the slow release of alkaline groups such as COO− from the manure. However, despite a pH increase in both RS and NRS with CM application, the pH in RS was significantly lower than that in NRS, irrespective of treatments and growth stages. This may have been due to the protons released by roots to compensate for a charge imbalance due to unequal uptakes of cations and anions.31 Soybean may promote the release of more protons into the rhizosphere and thus lower the soil pH because the ammonium synthesized from biological nitrogen fixation by rhizobium-colonizing soybean roots is a physiologically acidic form.

The CEC in RS or NRS was significantly improved with CM application from V4 to R4. At R4, the rhizosphere CEC under CM1, CM2, and CM3 treatments was 1.39, 1.48, and 1.67 times higher, respectively, than that under a CM0 treatment. This increase may have been due to the introduction of basic cations from CM, such as K+, Ca2+, and Na+, which was consistent with the results reported by a previous study with CM application.3,9 In this study, the total Na concentration in the CM was as high as 5.7 g kg−1 (data not shown), which may be a driver for an increased CEC. Moreover, as soybeans grew and developed, the CEC in the CM0 treatment became gradually lower, but under CM1, CM2, and CM3 treatments became higher, which was consistent with that observed by our 3088

DOI: 10.1021/acs.jafc.6b05813 J. Agric. Food Chem. 2017, 65, 3085−3095

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Journal of Agricultural and Food Chemistry previous study.19 This result may be due to the slow release of exchangeable cations from the CM, and more root exudates were released to increase the exchangeable cations as plants developed.32 In NRS, higher CM application rates did not cause a significant AWCD change at V2 and V4; however, a CM3 treatment caused a significantly higher AWCD at R1 and R4. In RS, the difference between CM0, CM1, and CM2 was not significant at the vegetative stages; however, after soybean bloomed, a significant difference among treatments followed a distinct order: CM0 < CM1 < CM2 < CM3. These results suggest that with or without the involvement of a root system, the effect of manure incubation on microbial activity was quite slow. In addition, these results suggest that during the vegetative stage of soybean, the CM application was not able to alter the rhizosphere microbial activity, which was consistent with the result in a previous study,33 which demonstrated that short-term changes (30 days) in bacterial community composition were not detected after a manure application. Nevertheless, the improvement of manure fertilization on soil microbial activity over the long-term has been widely reported,16,17,28,32,34 which may be attributed to the buildup of a larger microbial biomass, enhanced proteolysis, or the release of greater amounts of root exudates. In addition, the microbial activity in NRS was often significantly lower than that in RS irrespective of treatments or growth stages. For instance, at R4 the AWCD in RS affected by CM3 was 1.75, 1.38, 1.36, and 1.51 times higher than that in NRS. These results indicate that plant roots exert significant effects on the soil microbial activity in the rhizosphere by modifying soil conditions to be favorable for microbial growth. Root exudates such as polysaccharides and amino acids are released into the soil and stimulate microbial growth.17 Similar results were found in some rhizobox studies with the manure application.28,35 Effects of CM Application on HM Fractionation in NRS. The fractionation of Cd, Zn, and Pb in soil was assessed using a sequential extraction procedure.27 The significant difference of HM fractionation affected by CM applications is shown in Figure 1, and other insignificant differences are shown in Table S1. Results of the chemical fractionation of HMs in the NRS show that the CM application increased Cd availability, whereas it decreased Cd in the OXI pool (Figure 1); the CM application decreased the available Zn and Pb and increased Zn in the OXI pool and Pb in the ORG pool. In addition, a significant difference in HM shifts between fractions was mainly reflected during reproductive stages. The shift of Zn from the available state to the OXI fraction induced by CM application was most likely the result of the increase in soil pH, which promoted the precipitation of Zn with iron and manganese oxides or hydroxides.9,30 Notably, Cd showed a contrasting variation with Zn: the shift of Cd from the OXI fraction to the available state with higher rates of CM application. This result was totally inconsistent with the results of Zhao et al.,4 who reported that a long-term CM application caused a higher accumulation of Cd and a deficiency of Zn in the soil. The opposite result may be due to the different soil type used; Zhao et al. used an alkaline Aquic Cambosol (pH >8) in their experiment.4 Zn free ions could readily be transformed to zinc oxides or hydroxides under an alkaline soil with an increase of soil pH caused by CM application, thus decreasing Zn availability.24 However, because we used an acidic Haplic Fluvisols in our study with a pH range of 5−6, the significantly increased OXI-bound Zn was detected with the

gradually increasing pH that was induced by higher application rates of CM. In an acidic or slightly acidic soil, the Zn fractions associated with the iron and manganese oxides are likely to be the most available to plants.36,37 This result authenticated our first hypothesis. The contrasting effects of Zn and Cd mobilization in cultivated soil with manure application have been often reported.3,4,8,9,33 An important reason for this result may be because of the difference in sorption power and ion competition between Cd and Zn. Zn may have a higher replacing power than Cd, and it can be selectively fixed to the adsorbing sites, for example, in iron and manganese oxides. Shaheen et al. reported that in Fluvisols, Zn affinity for the carbonate and oxides surface was much higher than that of Cd.18 However, Pb showed a different shift in fractionation with Cd or Zn in NRS. The CM application decreased the available amount of Pb, whereas it increased that in the ORG pool, and at all growth stages (except V2). The inhibition of organic amendment on Pb availability has often been reported and used for amendment purposes in the contaminated regions.2,30,38,39 This result also authenticated our third hypothesis. It was also reported that the ORG-bound Pb inhibited the available Pb.31,38 In acidic and slightly acidic soils, the absorption capacity of HMs generally follows the order Pb > Zn > Cd.3,26,40 Effects of Root-Induced Changes on HM Factionation. In control or CM-treated soils, the growth of soybean significantly increased the available Cd and Zn at all growth stages (Figure 1). The difference with or without soybean growth became more obvious with higher application rates of CM. For instance, at R4 the growth of soybean increased the available Cd 1.34, 3.47, 4.14, and 4.57 times under CM0, CM1, CM2, and CM3 treatments, respectively. The higher soluble concentrations of Zn and Cd in RS compared to NRS have been found scientifically and may be related to the formation of soluble complexes between elements and organic compounds that are exuded from growing roots.41,42 Also, rhizosphere acidification (Table 4), which may derive from proton release from biological nitrogen fixation, may be an important reason for increased Cd and Zn availability in RS in comparison to NRS.13,19,22 The increased CEC in RS (Table 4) could also promote the shift of HM from the stabilized state to the available state. However, CM application shifted the available Zn to OXI-bound Zn in both NRS and RS (Figure 1), which suggests that root-induced changes in the rhizosphere, including RS acidification, may be counteracted by CM incubation. The depletion of Cd in the OXI pool may have been due to microbial activity and CEC; the increase of Zn in the OXI pool may have been due to the liming effect of added CM, according to the stepwise regression that showed which variables were significantly correlated with the available HMs in RS at different growth stages (Table 5). At V2, the significant variables affecting the available Cd and Zn were not detected. At V4, CEC positively affected Cd availability but negatively affected Zn availability. The CEC defines the amount of ions needed to occupy all adsorption sites per unit of mass, and the affinity of cations for adsorption sites is closely related to ionic potential. Moreover, the OXI-bound Cd negatively affected Cd availability, and with the decrease of OXI-bound Cd the available Cd was significantly and gradually increased under CM1, CM2, and CM3 treatments. At R1 and R4, Cd 3089

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Journal of Agricultural and Food Chemistry

For Pb, the available Pb in RS was higher than that in NRS from V4 to R4, irrespective of CM application rates (Figure 1), which suggests that the soybean root activity induced the solubility of stabilized Pb. Arshad et al. also reported that rootinduced changes were responsible for the modification of Pb of organic species into available Pb, and these changes mainly derived from the acidification, which is also detected in the present study, and increased dissolved organic carbon in the rhizosphere.44 However, similar to Zn, CM application shifted the available Pb to ORG-bound Pb but with or without effects on soybean growth. This result suggests that root-induced impacts on Pb stabilization may be weaker than the CM incubation. However, with higher application rates of CM, a significant declining trend was observed for available Pb, and an ascending trend was observed for Pb in the ORG pool (Figure 1). These results suggest that contrary to Cd, the root activity of soybean did not bring about a stronger impact on Pb solubility in comparison to CM application; however, the increase in Pb stabilization was more affected by CM incubation. This is different from some previous reports that related the effects of a biochar amendment and root growth to Pb mobilization. For instance, Houben and Sonnet reported that the growth of Agrostis capillaris or Lupinus albus significantly increased the exchangeable Pb in comparison to bulk soil under a biochar treatment.13 The inhibition of organic amendment on Pb has often been reported and is used in the amendment of contaminated regions.2,30,38,39 On the basis of stepwise regression analysis, the available Pb was negatively correlated with ORG-bound Pb at R1 and negatively correlated with microbial activity and ORG-bound Pb at R4 (Table 5). This result suggests that microbial activity may be involved in the immobilization of Pb to the ORG pool. Some prokaryotic organisms, for example, Bacillus megaterium and Acinetobacter spp., that can produce or excrete extracellular polymeric substances may play an important role in Pb adsorption and reduction.45 Effects of CM and Root-Induced Changes on HM Uptake by Plants. The effects of different CM application levels on the dry weight production of soybean shoots and roots are shown in Figure 2. The CM3 treatment substantially decreased the shoot dry weight at all growth stages except V2 and the root dry weight at all growth stages. At R4, the CM0, CM1, and CM2 treatments yielded 1.90, 2.14, and 1.97 times higher shoot biomass and 1.90, 181, and 1.64 times higher root

Table 5. Variables Detected by Stepwise Regression Analysis To Be Significantly Correlated with Available HM in the RS Affected by Different CM Teatmentsa dependent

stage

available Cd

V2 V4 R1

R4

available Zn

V2 V4 R1 R4

available Pb

V2 V4 R1 R4

variables related

R2

ND CEC OXI Cd AWCD CEC AWCD OXI Cd

ND 0.927*** −0.746* 0.909*** 0.938*** 0.839** −0.760**

ND CEC pH pH OXI Zn pH

ND −0.819** −0.647* −0.866** −0.729* −0.733**

CARB Pb CEC ORG Pb ORG Pb AWCD

0.843** −0.907*** −0.811** −0.870** −0.720**

a

OXI,bound to iron or manganese oxides or hydroxides; ORG, bound to organic matter; CEC, cation-exchangeable activity; AWCD, microbial activity; ND, not determined. *, **, ***, significant at P < 0.05, 0.01, and 0.001, respectively.

availability was positively affected by microbial activity but negatively affected by OXI-bound Cd, which suggests that some reducing bacteria may be involved in the release of free Cd ions out of the iron and manganese oxides. Different from Cd, the increase of OXI-bound Zn both with and without root-induced impacts indicated that liming effects caused by CM application exerted a stronger effect of Zn mobilization than root-induced acidification. Furthermore, it caused more free Zn ions to occlude in the OXI pool, as mirrored by the negative correlation between pH, OXI-bound Zn, and available Zn at R1 and R4 (Table 5). Although rhizosphere acidification promoting Zn availability has been widely reported, even in acidic soils,13,22,43 in this study we found that the liming effects of CM application counteracted the acidifying effects of root activity.

Figure 2. Effect of different CM application rates on the dry matter of shoots and roots at different growth stages. CM, cattle manure; V2, second trifoliolate; V4, fourth trifoliolate; R1, beginning bloom; R4, full pod. 3090

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Figure 3. Effect of different CM application rates on Cd, Zn, and Pb accumulation in soybean roots and shoots at different growth stages. Error bars indicate SE. Different letters show significant difference among treatments in individual growth stages (P < 0.05, n = 3).

Significant positive correlations were detected among CM0, CM1, and CM2 treatments for Cd at all growth stages, for Zn at V2, R1, and R4, and for Pb at R1 and R4 (Table 6). This result indicates that plant HM uptake was dependent on soil soluble and exchangeable HMs, in accordance with previous studies with respect to the impacts of a manure application on HM variation.3,7,8 Moreover, this dependence became more evident when plants developed to maturity. The significant increase of Cd in shoots and roots indicated that Cd in CM was more available to soybean in the acidic Haplic Fluvisol soils. Root-induced acidification hindered the formation of cadmium oxides or hydroxides in the rhizosphere and thus counteracted the immobilization effect in the NRS. However, due to a different ionic potential and adsorption capacity, Zn availability in the root−soil interface was contrary to Cd. The liming effect of CM exerted a stronger effect on Zn immobilization. This

biomass than the CM3 treatment, respectively. It is worth noting that a rapid exponential increase of soybean biomass was detected under CM0, CM1, and CM2 treatments, which agrees with a previous study with respect to the dynamic biomass change of radish and Chinese cabbage.46 However, the CM3 treatment (20.25 Mg ha −1 ) greatly inhibited biomass production. This growth inhibition may be derived from an oversupply of nutrients, especially nitrogen and phosphorus.47 The impacts of different CM application rates on the variation of plant HM uptake were almost consistent with rhizosphere HM availability (Figure 3), except that the variation by CM3 was not always consistent due to the inhibited growth. The CM1 and CM2 treatments inhibited Zn and Pb uptake and promoted Cd uptake, and the differences between CM0 and CM1 and CM2 were more obvious at the reproductive stages than at the vegetative stages. 3091

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increased uptake mainly occurred at R4, and most of the Pb was accumulated in the roots. This is because Pb is often stored to a considerable degree in root cell walls, and this characteristic prevents the upper translocation of risk elements to the vegetative organs.23,28,48 Figure 5 shows the relationship between Qmetal × root RGR/ Cs and root dry weight. According to eq 3, this plot tests whether the root-absorbing power for HMs (slope α) varied with the age of the plant and with the level of HM exposure. The slope α, which reflected the root-absorbing power of different HMs, was calculated and is shown in Table 7. By calculating and analyzing the α, the root absorbing power could be evaluated whether varied or not in response to different HM levels (in different CM rates). With the higher available Cd in the growth medium caused by higher CM application rates, the root Cd-absorbing power was significantly increased (Table 4; Figure 5), which suggests that Cd exposure at 0.08−0.11 mg kg−1 could trigger a regulatory mechanism to promote a Cd influx into the root symplast or an enhanced exudation of organic acids to increase availability.48 Interestingly, root Znand Pb-absorbing powers were very close among treatments. These results suggest that the altered available Zn and Pb did not trigger regulatory mechanisms to limit the Zn and Pb influx into the roots. This result may also be related to the contrast impacts of soybean growth on Cd, Zn, and Pb. Zn and Pb immobilization in RS was detected, and this immobilization was mainly derived from the CM incubation; however, the root activity promoted a shift of OXI-bound Cd to available Cd. Additionally, by increasing the available concentration in the growth medium, such as in soil spiked with active HMs, the linear relationship could be detected between the HM influx into roots and the HM concentration in the growth medium.49 Effects of Plant Age on the Dynamic State of HMs in Soil and Plants. According to the dynamic variation of HM fractions in RS and NRS affected by different CM application rates (Figure 1; Table S1), we found that the effect on HM fractionation at the reproductive stage was more marked than that at the vegetative stage. Notably, the dynamic variation of AWCD in RS from V2 to R4 was a parabola going upward, with the highest level of microbial activity at V2 and R4, irrespective of treatments. This result was different from some previous investigations of different crops, which observed a linear increase of AWCD as sugar beet developed to maturity.15 The seasonal shift of rhizosphere microbial activity of soybean may be related to biological nitrogen fixation and the slow-release property of manure. After flowering, the nodule began to senesce and the rhizobium activity declined,50 and at R4 with more nutrients released from CM and a rapid expansion of root mass, stabilized oxidizing and reducing bacteria and fungi began to activate. Therefore, it could be speculated that at the reproductive stages, soybean stores carbohydrate reserves in the taproot that coincides with a rapid expansion of the root mass, again increasing root exudation and enriching a specialized microbial community that affects HM fractionation. The most obvious difference of rhizosphere-available Cd among treatments was detected at R4 and available Zn at R1. At R4, 53.16, 49.19, and 46.53% of available Cd were increased, and at R1 28.30, 23.64, and 24.77% of available Zn were decreased by CM1, CM2, and CM3 treatments, respectively. In a field study of the dynamic uptake of HMs in soil and plants by Ai et al.,46 they also reported that HM uptake was higher at the reproductive stage. In our previous study, we also found that CM application promoted more nonessential element avail-

Table 6. Pearson Correlation Analyses for the Relationship between Availability of HM in the Rhizosphere of Soybean and Plant HM Uptake at Different Growth Stagesa V2 RS Cd availability RS Zn availability RS Pb availability

V4

Plant Cd Uptake 0.826** 0.853** Plant Zn Uptake 0.624 0.809** Plant Pb Uptake 0.654 0.652

R1

R4

0.724*

0.947***

0.909***

0.842**

0.817**

0.862**

*, **, and ***, significant at P < 0.05, 0.01, and 0.001, respectively. RS, rhizosphere soil. a

contrasting effect of an animal manure application on Zn and Cd mobilization in a soil−plant system was consistent with previous studies.3,4,22 Although Cd−Zn interactions have been commonly observed, findings are contradictory because both depressing and enhancing effects of each metal have been reported. Cd can be taken up by plant roots via a ZRT- and IRT-like protein and Nramp families of Zn.46 In this study, the results illustrated an increasingly available Cd:Zn ratio in the rhizosphere that caused an antagonistic effect between Cd and Zn and inhibited root Zn uptake. The contrasting accumulation of Zn and Cd in shoots with a higher Cd availability in the growth medium was consistent with the findings of Júnior et al. and Zhang et al.,3,48 but was inconsistent with those of Cornu et al.,29 which may have been due to the synergetic uptake between Zn and Cd that was observed as a sequence of the hormetic effect of Cd (20 nM). Moreover, in this study, the significant negative correlation between plant Cd and Zn uptake was detected among CM0, CM1, and CM2 treatments irrespective of growth stages (Figure 4), which authenticated our second hypotheses. The increased uptake of Pb was mainly due to an increase in Pb availability induced by CM incubation rather than by rootinduced effects. The reduced Pb accumulation in plants caused by Pb immobilization induced by added manure agrees with some previous studies of organic amendment.12,38 The

Figure 4. Relationship between plant Cd and Zn uptake among CM0, CM1, and CM2 treatments (n = 9). The solid line represents the best linear fit obtained between the plant Cd and Zn uptake. The correlation coefficients were calculated from the Pearson correlation analysis (∗, P < 0.05; ∗∗, P < 0.01). 3092

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Figure 5. Relationship between the variable Qmetal × root RGR/Cs and root dry weight in soybean affected by different application rates of CM. Qmetal stands for the plant uptake of metals, root RGR for the relative growth rate of roots (calculated from Figure 1), and Cs for the available concentrations of metals (sum of water-soluble and exchangeable concentrations). The solid lines of different colors represent the best linear fit obtained between the two variables at different application rates of cattle manure. The slope of the solid lines stands for the root metal absorbing power as shown in Table 7.

mobilization was more affected by CM incubation and showed a contrasting trend with Cd. The alteration in plant HM uptake was mainly reflected in the roots. Although the increased Cd in the soil and plant did not exceed the toxic threshold, the increasingly available Cd:Zn ratio may be an important factor to inhibit Zn uptake. Also, a significant negative correlation between plant Cd and Zn uptake was detected at all of the growth stages. Specifically, at R4 the decreased Zn uptake in shoots was most obvious, and this meant that the Zn accumulation in the edible part (seed) of soybean may be lowered. On the basis of the results of this study, if CM is applied to agricultural Haplic Fluvisols over the long-term, a Zn deficiency in the food can be predicted with further effects on human health, even if applying CM at the recommendation rate of 10.13 Mg ha−1 (CM1). Moreover, even though there would appear to be a low risk of crop contamination with Pb uptake following high application rates of CM, there may be a problem of Pb accumulation in the soil after repeated CM applications in the long term. In this study, when soybean developed to a full pod (R4), the plant removal of Pb was 0.022 Mg ha−1, but the addition of Pb in the manure resulted in a level 12.31 times higher than the plant removal under the recommended application rates (calculated from Tables 1 and 2 and Figure 3). Therefore, care needs to be taken regarding Pb pollutants when CM is applied. This study emphasized that ORG-bound Pb and microbial activity dominantly affected Pb availability. In future research, a metagenomic analysis of soil microbial communities in Haplic Fluvisols may be useful for detecting the exact bacterium or fungi type involved in oxidizing and reducing Pb. In conclusion, this study provides the chemical mechanism of heavy metals variation in acidic soil affected by CM application. Although CM is often considered to be an environmentally friendly fertilizer, its long-term and frequent use in Haplic Fluvisols may inhibit Zn biofortification and cause soil Pb pollution.

Table 7. Analysis of Covariance (ANCOVA) for the Slope of the Linear Relationship between the Two Variables from Figure 4 for Cd, Zn, and Pba slope treatment

Cd

Zn

Pb

CM0 CM1 CM2 CM3

0.0671c 0.0882b 0.1026a 0.1125a

0.5419a 0.5916a 0.5581a 0.6244a

0.1344a 0.1331a 0.1287a 0.0938b

a

Different letters show significant difference among treatments in individual growth stages (P < 0.01, n = 3).

ability in the root−soil surface at the reproductive stage.28 This variation between vegetative and reproductive stages may have been due to the slow release of mineral elements from the manure, rapid expansion of the root mass, and increasing root exudation.15 In addition, Tian et al. reported that short-term significant changes of available and total HMs in soil were not detected after a pig manure application.33 For HM uptake by soybean, the marked difference of shoot HM uptake between CM1, CM2, and CM3 was hard to detect before R4. Even at R4, a significant difference in shoot Pb uptake was not detected between CM1, CM2, and CM3 treatments (data not shown). However, the evident difference of HM accumulation in roots could be observed. These results illustrate that within the application rate range of CM1, CM2, and CM3 (10.13−20.25 Mg ha−1), increasing the CM application rate will not cause a significant variation of HM accumulation in the shoot. The root has a strong retention effect on HMs and prevents them from being transported to the upper organs, which coincides with some previous studies.13,29,38,46 Implications for the Management of CM Application on the Agricultural Haplic Fluvisols. The results of this work show that CM application increased the rhizosphere Cd availability and soybean Cd uptake and decreased Zn and Pb availability and uptake at different growth points. The greater influence of the plant developmental stage was reflected in the reproductive stage. Root-induced changes were mainly reflected by Cd fractionation. Even in the rhizosphere, Pb and Zn

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.6b05813. 3093

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Fractionation of Cd, Zn, and Pb in the NRS and RS of soybean in CM0, CM1, CM2, and CM3 treatments at different growth stages (PDF)

AUTHOR INFORMATION

Corresponding Author

*(T.W.) Phone: +81 11 706 2498. Fax: +81 11 706 2498. Email: [email protected]. ORCID

Qingnan Chu: 0000-0003-0020-812X Funding

This study was financially supported by a Grant-in-Aid for Scientific Research (No. 24580088) from the Japan Society for the Promotion of Science (T.W.). Notes

The authors declare no competing financial interest.

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