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Co-planting can phytoextract similar amounts of cadmium and zinc to mono-cropping from contaminated soils
Ecological Engineering 36 (2010) 391–395
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Co-planting can phytoextract similar amounts of cadmium and zinc to mono-cropping from contaminated soils Cheng-ai Jiang a , Qi-Tang Wu a,∗ , Thibault Sterckeman b , Christophe Schwartz b , Catherine Sirguey b , Stéphanie Ouvrard b , Jérôme Perriguey b , Jean-Louis Morel b a College of Natural Resources and Environment, Key Laboratory of Ecological Agriculture and Rural Environment of Ministry of Agriculture and Guangdong Province, South China Agricultural University, 510642 Guangzhou, China b Laboratoire Sols et Environnement, Nancy Université – INRA, 54505 Vandoeuvre-Les-Nancy, France
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Article history: Received 19 December 2008 Received in revised form 24 August 2009 Accepted 9 November 2009
Keywords: Cd Zn Thlaspi caerulescens Ryegrass Co-planting Interface soil
a b s t r a c t Co-planting crops normally decreases the main crop yield due to the reduced soil surface area occupied by the main crop. However, in our previous experiments, co-planting Sedum alfredii, a shade-requiring, Cd and Zn-hyperaccumulating plant, with corn increased the biomass and metal phytoextraction of S. alfredii. This experiment was conducted to verify if co-planting another hyperaccumulator, Thlaspi caerulescens, with ryegrass (Lolium perenne) in a pot-trial could obtain a similar result. The soil was separated by two permeable nets with a 2 mm interface soil layer to obtain a shared rhizosphere zone. Soluble metal concentrations in the soil in different rooting zones were measured using 0.01 mol L−1 CaCl2 extraction. The results showed that the growth of T. caerulescens was significantly promoted by co-planting, with a growth increase of about 2-fold compared with monoculture growth. The total uptake of Cd and Zn by T. caerulescens was not decreased by co-planting, and resulted in similar phytoextraction rates for Cd (about 26.6% of the soil total Cd) and Zn (about 2.4% of the soil total Zn) when compared with monoculture, though the T. caerulescens population was decreased by 50% because of co-planting. Analysis of soil samples showed that T. caerulescens substantially reduced the concentrations of 0.01 mol L−1 CaCl2 extractable Cd and Zn throughout the soil, even in the interface area and the ryegrass rooting area. The ryegrass roots did not mobilize more metals for the co-planted T. caerulescens. Based on these results, existing grass on contaminated land could be partly left while planting metal hyperaccumulators for phytoremediation in order to reduce runoff from the contaminated soil. However a field scale trial would be required for these results to be verified. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Heavy metals and metalloids cannot be degraded. Therefore, they persist in soils and are subjected to transport by and into water, where they may become a threat to ecosystems, and enter the food chain and threaten human health (Eapen and D’Souza, 2005; Khan, 2005). Risk management may require remediation of contaminated soils, but current physicochemical technologies to remove metals from soil, such as chemical washing and thermal treatments, are costly and deeply alter soil biological functions
∗ Corresponding author at: Department of Environmental Science and Engineering, College of Natural Resources and Environment, South China Agricultural University, Wushan Street, 510642 Guangzhou, Guangdong, China. Tel.: +86 20 85288326; fax: +86 20 85288326. E-mail addresses: [email protected], [email protected] (Q.-T. Wu). 0925-8574/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2009.11.005
(Glass, 2000; Fellet et al., 2007). Phytoremediation of metal contaminated soils is an alternative to physicochemical techniques and has been studied for almost two decades (Baker et al., 1994; Chaney et al., 1997; McGrath et al., 2002). It has been gaining much attention as it is an in situ technique, can be cost effective, especially for large surfaces, does not disturb the soil structure and can obtain high public acceptance due to the aesthetics of a green vegetation cover (Ma et al., 2001; Susarla et al., 2002; Mitsch and Jorgensen, 2003). Thlaspi caerulescens is one of the most studied metal hyperaccumulator plants and has a high potential to extract Cd and Zn from polluted soils due to its striking accumulation capacity for Zn and Cd at concentrations >10,000 and >100 mg kg−1 shoot dry weight, respectively (Schwartz et al., 1999, 2003; Ozturk et al., 2003). However, this species has a slow growth rate of only 3–4 t ha−1 per 6 months (Wójcik et al., 2005). To improve the potential for heavy metal phytoextraction using this hyperaccumulator, suggestions have been made to optimize the healthy growth of T. caerulescens. These suggestions include: choosing a suitable T.
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Table 1 Main characteristics of the studied soil in the pot experiment. Particle size distribution (g kg−1 )
Clay
Silt
Sand
158
603
239
a
Organic carbon (g kg−1 )
Total P2 O5 (g kg−1 )
pH
C/N
CECa (cmol kg−1 )
Mg (cmol kg−1 )
Ca (cmol kg−1 )
Total Cd (mg kg−1 )
Total Zn (mg kg−1 )
18.6
0.202
8.0
14
13.4
0.496
13.1
19.9
1410
CEC: cation exchange capacity of the soil.
caerulescens population (Schwartz and Morel, 1998); application of appropriate fertilizers (Keller and Hammer, 2004; Ozturk et al., 2003); and applying metal chelators such as EDTA (Blaylock et al., 1997), EDDS (Tandy et al., 2004) or a mixture of chelators (Wu et al., 2006). However, most chelators present an environmental risk to groundwater (Wu et al., 2006). Intercropping, a widely accepted agronomical practice in China for 2000 years, can increase total crop yields through increased resource use efficiency (Zhang and Li, 2003). Roots of some plants grow widely in the top soil and the others may grow downward with strong geotropism. Consequently, plants with different root types may utilize nutrients in different layers of the soil. Cocropping has recently received much attention by entomologists and pathologists aiming at reducing pest numbers and disease transmission by increasing biological diversity (Zhu et al., 2000). Root exudates and rhizosphere microorganisms differ among species (Jones, 1998; Khan, 2005), which may facilitate nutrient and metal (e.g., Fe) uptake between the co-planted plants (Zhang and Li, 2003). Hence, co-cropping with a non-hyperaccumulating plant could enhance the growth of the hyperaccumulator and increase heavy metal uptake while avoiding the side effects to the environment usually observed in chelator enhanced phytoextraction. For example, Wu et al. (2007) showed that the growth and metal uptake of Sedum alfredii were enhanced in the presence of Zea mays, where the corn provided shade to S. alfredii, a shade-requiring plant. Another gramineous plant, ryegrass (Lolium perenne), showed an isotopically measured phytoavailable pool of Cd and Zn (as indicated by the L value which can serve as an indicator of the effect of the plant rhizosphere on metal mobilization), higher than that for other species including T. caerulescens (Sterckeman et al., 2005). However, it is unknown whether T. caerulescens will behave as S. alfredii, with increased metal uptake by T. caerulescens when coplanted with ryegrass. A co-planting pot experiment was carried out. In the experiment, the soil in the pots was separated by two permeable nets between the two plants, to obtain a 2 mm interface soil layer identified as the “shared rhizospheric soil” between the roots of the two plant species. This allows for better understanding of the metal mobility in different plant rooting zones.
separation), where TC was T. caerulescens J. & C. Presl., a hyperaccumulator of Cd and Zn sourced from Viviez (south of France) (Schwartz et al., 2003); RG is ryegrass (L. perenne, L., cv. York); TA is Thlaspi arvense, a closely related species to T. caerulescens but nonhyperaccumulator; “||” indicated that the two plants root systems were separated diagonally by two nylon meshes separated by 2 mm which acted as vertical barriers (Fig. 1). These nets have a 30 m porosity which does not allow plant roots, including main root hairs, to penetrate but allows soil solution, its solutes and microorganisms to pass through (Li et al., 1991). The space between the two meshes was filled with the same soil. Plants grew close to the meshes. There was no mesh in TC + RG treatment in order to check the mesh separation effect on plant growth and metal uptake. Each pot (12 × 12 cm2 and 9 × 9 cm2 at the top and bottom, respectively, with a height of 12 cm) contained 1.5 kg soil, fertilized at rate of 150 mg N, 70 mg P2 O5 , 150 mg K2 O and 30 mg Mg (magnesium) per kg soil with NH4 NO3 , Ca(H2 PO4 )2 , KCl and MgSO4 , respectively. Pots were arranged in random order in a growth chamber with a photoperiod of 16 h day−1 , diurnal temperature range of 18 ◦ C/22 ◦ C, relative humidity of 70%, and light intensity of 500 mol photons m−2 s−1 . Soil moisture was adjusted every day by weighing and maintained at 80% of the water holding capacity (WHC) with deionized water. About 30 seeds of each plant were sown to each half-pot. Ryegrass was sown two weeks later than T. caerulescens and T. arvense. After germination, the number of seedlings was reduced to eight individuals for T. caerulescens and T. arvense in each half-pot, but no ryegrass plants were removed. Shoots of T. caerulescens and T. arvense were harvested after 110
2. Materials and methods 2.1. Pot experiment Soil was sampled from the ploughed horizon of a redoxic Cambisol developed on loess and tertiary sediment colluviums in France, and contaminated with Cd, Pb and Zn, as a consequence of atmospheric fallout from two large lead and zinc smelters (Sterckeman et al., 2002). This soil has been cultivated with annual crops for about 15 years. Soil samples were ground, homogenized, passed through a 5 mm sieve and air-dried. The main physical and chemical characteristics and heavy metal concentrations of the soil are listed in Table 1. The experiment included seven treatments with four replicates each (28 pots in total), identified as TC||RG, TC + RG, TA||RG, TA||TA, RG||RG, TC||TC and a control (no plants but with a mesh
Fig. 1. Schematic diagram of the pot experiment for collecting the shared rhizosphere soil.
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Table 2 Dry biomass of and heavy metal uptake by Thlaspi caerulescens shoots in the different co-planting treatments.
a
TC||RG TC + RG TC||TC
Biomass (g half-pot−1 )
Cd content (mg kg−1 DW)
Cd uptake (mg half-pot−1 )
Zn content (mg kg−1 DW)
Zn uptake (mg half-pot−1 )
9.21 ± 0.35b 9.09 ± 0.52b 4.78 ± 0.12a
865 ± 17a 885 ± 42a 830 ± 25a
7.949 ± 0.190b 7.985 ± 0.180b 3.974 ± 0.198a
5500 ± 146a 5401 ± 262a 5456 ± 290a
50.69 ± 2.761b 48.88 ± 2.810b 26.07 ± 1.514a
b
TC: Thlaspi caerulescens; RG: ryegrass; ||: two nets separation between two plant roots systems. All values were average ± SE (n = 4). Averages followed by the same letter in each column were not significantly different according to one-way ANOVA with Duncan’s test (˛ = 0.05). a
b
days. Ryegrass was cut twice, at 40 and 95 days after sowing. Fresh shoots were washed with deionized water, dried with clean absorbent paper, and then weighed to determine fresh weight. Dry weight was determined after drying at 70 ◦ C for 48 h.
growth. The increased growth of this hyperaccumulator was also observed where it was co-cropped with T. arvense (Whiting et al., 2001). Our previous experiment showed that when co-cropped with Z. mays, the shoot biomass of S. alfredii was significantly increased (Liu et al., 2005; Wu et al., 2007). It appears that this phenomenon may be reasonably common for hyperaccumulators on heavy metal contaminated soils. For ryegrass, the average shoot biomass was 1.96 g DW per half-pot for TC||RG, 1.52 for TC + RG, 4.07 for RG||RG, and 4.89 for TA||RG (Table 3). Hence, co-cropping with T. caerulescens appeared to decrease ryegrass biomass, but co-cropping with T. arvense did not decrease the ryegrass biomass.
2.2. Plant digestion and determination for Cd and Zn Dry biomass was ground and digested in a micro-oven (350 psi) with a mixture of concentrated HNO3 and H2 O2 (Sterckeman et al., 2005). The Cd and Zn concentrations were determined using graphite furnace atomic absorption spectrometry (AAS), or inductively coupled plasma optical emission spectrometry (ICP-OES) depending on the concentration levels.
3.2. Metal uptake by plants 2.3. Extraction of Cd and Zn in soil samples Similar Cd concentrations in T. caerulescens shoots were observed for the treatments TC||RG, TC + RG and TC||TC, which varied from 830 to 885 mg kg−1 DW (Table 2), considerably higher than the hyperaccumulator criteria Cd concentration (100 mg kg−1 DW) (Chaney et al., 1997) which equates to a concentration factor (shoot concentration/soil concentration) of 42–44. The Cd uptake per halfpot by T. caerulescens co-planted with ryegrass was about double that of the mono-cropped T. caerulescens due to the higher biomass produced. On the basis of the whole pot, the phytoextraction rates of Cd, obtained by dividing the total Cd uptake by T. caerulescens (on average 7.96 mg/pot) (Table 2) by the total amount of Cd in the pot (1.5 kg soil/pot × 19.9 mg kg−1 ) (Table 1), were about 26.6% for all treatments where T. caerulescens was planted. The same trend was observed for Zn between the different treatments, but the phytoextraction rates of the total soil Zn were only about 2.4% ((50.57 mg/pot)/(1.5 kg/pot × 1410 mg kg−1 )). The average Cd concentration in ryegrass shoots was increased by co-cropped T. caerulescens but not increased by co-cropped T. arvense (Table 3). However, the total Cd uptake by ryegrass co-cropped with T. caerulescens was not higher than that of monocropped ryegrass or when co-cropped with T. arvense due to the lower biomass produced. For Zn, co-cropping with T. caerulescens tended to decrease the Zn concentration and total uptake by ryegrass compared with mono-cropping or co-cropping with T. arvense. These observations suggest that the hyperaccumulator competes for Zn against the co-planted plant. Similar observations were made when non-contaminated soil was dosed with insoluble metal compounds (Whiting et al., 2001), where the Zn concentration was not sufficient for the hyperaccumulator.
Soil samples were collected separately in the shared rhizosphere layer and in each side of the mesh nets, ground, homogenized, passed through a 1 mm sieve. Five grams of each sample was shaken for 30 min in 25 mL of 0.01 mol L−1 CaCl2 , centrifuged (20 min at 5000 rd min−1 ), and filtered through a 0.45 m membrane. Cd and Zn concentrations were determined by AAS and ICP-OES. This dilute salt extract measures the size of the directly available metal pools (Houba et al., 2000). All analyses were conducted according to French standard methods (AFNOR, 1995). 2.4. Statistical analysis Data were analyzed by one-way ANOVA with Duncan’s test (p < 0.05) using SPSS 13.0 for Windows (Apache Software Foundation). 3. Results and discussions 3.1. Plant growth Better growth of T. caerulescens was observed when co-cropped with ryegrass than without (Table 2). The average shoot biomass in grams per half-pot of T. caerulescens was 9.21 in the TC||RG treatment, 9.09 in TC + RG and only 4.78 in TC||TC. Co-planting with ryegrass significantly promoted the growth of T. caerulescens, by up to a 1.90-fold increase over monoculture planting. There was no significant difference between the treatment TC||RG and TC + RG, showing that separation of plant roots did not affect the plant Table 3 Dry biomass of and heavy metal in ryegrass shoots in different co-planting treatments. Biomass (g half-pot−1 ) a
TC||RG TC + RG RG||RG TA||RG
1.96 1.52 4.07 4.89
± ± ± ±
b
0.16a 0.07a 0.31b 0.24c
Cd content (mg kg−1 DW) 1.907 1.968 1.129 1.119
± ± ± ±
0.123b 0.312b .094a 0.085a
Cd uptake (g half-pot−1 ) 3.778 2.953 4.518 5.513
± ± ± ±
0.501ab 0.422a 0.206bc 0.631c
Zn content (mg kg−1 DW) 135 137 162 189
± ± ± ±
7.0a 17a 9.0ab 3.1b
Zn uptake (mg half-pot−1 ) 0.261 0.207 0.652 0.929
± ± ± ±
0.008a 0.022a 0.039b 0.055c
TC: Thlaspi caerulescens; RG: ryegrass; TA: Thlaspi arvense; ||: two nets separation between two plant roots. All the values were average ± SE (n = 4). Averages followed by the same letter were not significantly different according to one-way ANOVA with the Duncan’s test (˛ = 0.05). a
b
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Table 4 Dry biomass of and heavy metal uptake by Thlaspi arvense in co-planting treatments.
a
TA||RG TA||TA a b
Biomass (g half-pot−1 )
Cd content (mg kg−1 DW)
Cd uptake (g half-pot−1 )
Zn content (mg kg−1 DW)
Zn uptake (mg half-pot−1 )
3.15 ± 0.78b 4.71 ± 0.69a
10.58 ± 0.832a 11.73 ± 4.12a
41.07 ± 12.95a 56.33 ± 21.49a
162 ± 6.0a 158 ± 42a
0.569 ± 0.126a 0.753 ± 0.237a
b
TA: Thlaspi arvense; RG: ryegrass; ||: two nets separation between two plant roots. All the values were average ± SE (n = 4). Averages followed by the same letter were not significantly different according to one-way ANOVA test (˛ = 0.05).
Cd concentrations and Cd uptakes by T. arvense shoots were not significantly different between the TA||RG and TA||TA treatments (Table 4). Similar results were observed for Zn. This indicated that the enhanced metal uptake by an individual plant co-planted with ryegrass was only applicable for T. caerulescens and not for the nonhyperaccumulator T. arvense. 3.3. Phytoavailable Cd and Zn in the soil Soil Cd and Zn concentrations extractable by 0.01 mol L−1 CaCl2 at the end of the planting experiment varied from 32 to 238 g kg−1 and from 898 to 2586 g kg−1 soil, respectively (Table 5). Extractable Cd in the soils planted with T. caerulescens (TC||RG and TC||TC treatments) was significantly less than in soils without the hyperaccumulator (RG||RG, TA||RG, TA||TA and control treatments) and the original soil, in both the rooting soils and the shared interface soils. Moreover, soil in the ryegrass rooting side in the TC||RG treatment had a significantly lower Cd concentration (43.29 g kg−1 soil) than that in the RG||RG treatment (205.5 g kg−1 soil) (Table 5), meaning that Cd was transported to the other side of the pot and taken up by T. caerulescens. The Cd that was removed from the ryegrass side of the pot in the TC||RG treatment was not taken up by the ryegrass, as Cd levels in the ryegrass were not significantly different to that for the RG||RG treatment (Table 3). Neither roots nor root hairs of T. caerulescens could reach the ryegrass side of the pots and no reports show this hyperaccumulator associated with mycorrhiza (Vogel-Mikus et al., 2005). Cd uptake by ryegrass and T. arvense significantly reduced the extractable Cd, with the remaining Cd levels at 200.1 and 205.5 g kg−1 soil, compared with soil in the control treatment (219.4 g kg−1 soil). The shared interface soils for all the planted treatments showed a higher extractable Cd than the rooting soils, possibly due to the absence of plant roots.
CaCl2 extractable Zn showed a trend similar to that observed for Cd, but the difference was less pronounced. Extractable Zn remained higher in the interface soil shared with ryegrass (the treatment TC||RG) than that shared with its own species (TC||TC), though it was not statistically significant, suggesting that the interface soil could provide more available metal to the hyperaccumulator side. The obtained N, P, K and S nutrient data in the soil solutions did not give a viable explanation for the better growth of co-cropped T. caerulescens and the worse growth of ryegrass (data not presented), because they were not significantly different between corresponding treatments. There was also no significant difference in soil pH between the treatments which varied from 7.8 to 7.9 for all planted treatments. Xiao et al. (2004) indicated that in a faba bean and wheat co-cropping system, wheat was a stronger competitor for soil available N and benefited from cocropping with the N-fixing faba bean. From the present experiment, the superiority of the hyperaccumulator growth when co-cropped with ryegrass was not explained by major nutrients, but by more Zn available to individual T. caerulescens plants. However it is also possible that the volatile organic compounds (VOCs) excreted by plant shoots may play a role in the competition as suggested for plant allelopathy (Baldwin et al., 2006). The total phytoavailable metal in a pot was calculated by adding the metal taken up by the plants to that remaining in the soil and extracted by CaCl2 (Table 5). Results showed that co-planting with ryegrass did not mobilize more Cd and Zn than mono-cropped T. caerulescens, because the total phytoavailable metals for TC||RG and TC||TC treatments were very similar, even though a half-pot soil was colonized by the different plants. The hyperaccumulation of metals by T. caerulescens under the present experimental conditions seems only the result of metal solubilization and transport in the soil–root interface powered by low metal concentration on the root surface of the hyperaccumulator rather than from changes to
Table 5 Cd and Zn extracted by 0.01 mol L−1 CaCl2 in the soil samples after pot experiment with co-planting treatments where the two plant root systems were separated by two nets with a 2 mm interface soil layer. TA or TC side (g kg−1 soil) Cd TC||RGb TC||TC RG||RG TA||RG TA||TA No plants Original soil Zn TC||RG TC||TC RG||RG TA||RG TA||TA No plants Original soil
32.10ac 38.31a – 193.5c 200.1cd – – 941.1a 898.9a – 1372bc 1419bc – –
Interface (g kg−1 soil) 95.93b 81.92b 220.0f 215.82f 210.9ef 219.4f 218.5f 1443bc 1064ab 1995d 2203de 2586e 2301de 1821cd
Ryegrass side (g kg−1 soil) 43.29a – 205.5de 205.3de – – – 1017a – 1371bc 1355bc – – –
Total phytoavailablea (mg/pot) 8.024Ac 8.007A 0.322B 0.349B 0.413B 0.351B 0.350B 52.53A 53.26A 3.12BC 3.66B 4.14B 2.60C 2.06C
The capital letters indicate differences for the total phytoavailable metals, because the data in this column are not comparable with data in the other columns. a Total phytoavailable = total extracted by 0.01 M CaCl2 + total uptake by plants. b TC: Thlaspi caerulescens; RG: ryegrass; TA: Thlaspi arvense; ||: two nets separation between two plant root systems. c The averages (n = 4) of the same metal followed by a same letter were not significantly different according to one-way ANOVA with Duncan’s test (˛ = 0.05).
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the phytoavailable pool in the rhizosphere caused by root exudation. 4. Conclusions Using a separation device which allowed for different rooting zones in a pot experiment, this study identified the competitive relationships between hyperaccumulator and co-cropped common plants with respect to plant growth and heavy metals uptake. It indicated clearly that the co-planting stimulates the growth of the hyperaccumulator and increases the Cd and Zn uptake for an individual plant. The phenomenon is specific for the hyperaccumulator T. caerulescens on heavy metal contaminated soil and does not occur for T. arvense, a closely related species to T. caerulescens but not a hyperaccumulator. The ryegrass roots did not mobilize metals for the co-planted T. caerulescens but the metals in the ryegrass rooting zone could be transported to the hyperaccumulator. This study confirms that co-planting metal hyperaccumulators with other plants can get a similar or higher phytoextraction rate than monoplanting. It is possible that the existing grass on contaminated sites could be partly left while planting metal hyperaccumulators for phytoextraction of metals in order to reduce the runoff from the contaminated soil but this should be verified in a field experiment. Acknowledgments This research was financially supported by the French–Chinese Programme de Recherche Avancée (PRA E03-04), National Science Foundation of China (NSFC-40571141 and U0833004) and National High-tech R&D Program (863 Program: 2008AA10Z405 and 2007AA061001-3). The authors are grateful to Dr. Y. Ouyang in the Department of Water Resources, St. Johns River Water Management District, Florida, USA, for his help and suggestions in the modification of the manuscript. References AFNOR, 1995. Qualite du Sol. AFNOR, Paris. Baker, A.J.M., Reeves, R.D., Hajar, A.S.M., 1994. Heavy metal accumulation and tolerance in British populations of metallophyte Thlaspi caerulescens. New Phytol. 127, 61–68. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C., Preston, C.A., 2006. Volatile signaling in plant-plant interactions: “Talking trees” in the genomics era. Science 311, 812–815. Blaylock, M.J., Salt, D.E., Dushenkov, S., 1997. Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ. Sci. Technol. 31, 860–865. Chaney, R.L., Malik, K.M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S., 1997. Phytoremediation of soil metals. Curr. Opin. Biotechnol. 8, 279–284. Eapen, S., D’Souza, S.F., 2005. Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol. Adv. 23, 97–114. Fellet, G., Marchiol, L., Perosa, D., Zerbi, G., 2007. The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol. Eng. 31 (3), 207–214. Glass, D.J., 2000. Economical potential of phytoremediation. In: Raskin, I.Y., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals. John Wiley & Sons, Inc., New York, pp. 15–31. Houba, V.J.G., Temminghoff, E.J.M., Gaikhorst, G.A., Van Vark, W., 2000. Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Commun. Soil Sci. Plant Anal. 31, 1299–1396.
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Jones, D.L., 1998. Organic acids in the rhizosphere—a critical review. Plant Soil 205, 25–44. Khan, A.G., 2005. Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J. Trace Elem. Med. Biol. 18, 355–364. Keller, C., Hammer, D., 2004. Metal availability and soil toxicity after repeated croppings of Thlaspi caerulescens in metal contaminated soils. Environ. Pollut. 131, 243–254. Li, X.L., George, E., Marschner, H., 1991. Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA-mycorrhizal white clover fertilized with ammonium. New Phytol. 119, 397–404. Liu, X.M., Wu, Q.T., Banks, M.K., 2005. Effect of simultaneous establishment of Sedum alfredii and Zea mays on heavy metal accumulation in plants. Int. J. Phytoremediation 7, 43–53. Ma, L.Q., Komar, K.M.M., Tu, C., Zhang, W., Cai, Y., Kennelley, E.D., 2001. A fern that hyperaccumulates arsenic. Nature 409, 579. McGrath, S.P., Zhao, F.J., Lombi, E., 2002. Phytoremediation of metals, metalloids, and radionuclides. Adv. Agron. 75, 1–56. Mitsch, W.J., Jorgensen, S.E., 2003. Ecological engineering: a field whose time has come. Ecol. Eng. 20, 363–377. Ozturk, L., Karanlik, S., Ozkutlu, F., Cakmak, I., Kochian, L.V., 2003. Shoot biomass and zinc/cadmium uptake for hyperaccumulator and non-accumulator Thlaspi species in response to growth on a zinc deficient calcareous soil. Plant Sci. 164, 1095–1101. Schwartz, C., Morel, J.L., 1998. How can agronomical practices improve phytoremediation of heavy metal contaminated soils? In: Proceedings of the 6th International FZK/TNO Conference on Contaminated Soil, ConSoil’98, Thomas Telford, London, pp. 609–617. Schwartz, C., Morel, J.L., Saumier, S., Whiting, S.N., Baker, A., 1999. Root development of the zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208, 103–115. Schwartz, C., Echevarria, G., Morel, J.L., 2003. Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249, 27–35. Susarla, S., Medina, V.F., McCutcheon, S.C., 2002. Phytoremediation: an ecological solution to organic chemical contamination. Ecol. Eng. 18, 647–658. Sterckeman, T., Douay, F., Proix, N., Fourrier, H., Perdrix, E., 2002. Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the north of France. Water Air Soil Pollut. 135, 173–194. Sterckeman, T., Duquène, L., Perriguey, J., Morel, J.L., 2005. Quantifying the effect of rhizosphere processes on the availability of soil cadmium and zinc. Plant Soil 276, 335–345. Tandy, S., Bossart, K., Mueller, R., Ritschel, J., Hauser, L., Schulin, R., Nowack, B., 2004. Extraction of heavy metals from soils using biodegradable chelating agents. Environ. Sci. Technol. 38, 937–944. Vogel-Mikus, K., Drobne, D., Regvar, M., 2005. Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ. Pollut. 133, 233–242. Whiting, S., Leake, J., Mcgrath, S., Baker, A.M., 2001. Hyperaccumulation of Zn by Thlaspi caerulescens can ameliorate Zn toxicity in the rhizosphere of cocropped Thlaspi arvense. Environ. Sci. Technol. 35, 3237–3241. Wójcik, M., Vangronsveld, J., Tukiendorf, A., 2005. Cadmium tolerance in Thlaspi caerulescens. I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ. Exp. Bot. 53, 151–161. Wu, Q.T., Deng, J.C., Long, X.X., Morel, J.L., Schwartz, C., 2006. Selection of appropriate organic additives for enhancing Zn and Cd phytoextraction by hyperaccumulators. J. Environ. Sci.(China) 18, 1113–1118. Wu, Q.T., Wei, Z.B., Ouyang, Y., 2007. Phytoextraction of metal-contaminated soil by hyperaccumulator Sedum alfredii H: effects of chelator and co-planting. Water Air Soil Pollut. 180, 131–139. Xiao, Y.B., Li, L., Zhang, F.S., 2004. Effect of root contact on interspecific competition and N transfer between wheat and fababean using direct and indirect 15 N techniques. Plant Soil 262, 45–54. Zhang, F.S., Li, L., 2003. Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248, 305–312. Zhu, Y.Y., Chen, H.R., Fan, J.H., 2000. Genetic diversity and disease control in rice. Nature 406, 718–722.
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Co-planting can phytoextract similar amounts of cadmium and zinc to mono-cropping from contaminated soils Cheng-ai Jiang a , Qi-Tang Wu a,∗ , Thibault Sterckeman b , Christophe Schwartz b , Catherine Sirguey b , Stéphanie Ouvrard b , Jérôme Perriguey b , Jean-Louis Morel b a College of Natural Resources and Environment, Key Laboratory of Ecological Agriculture and Rural Environment of Ministry of Agriculture and Guangdong Province, South China Agricultural University, 510642 Guangzhou, China b Laboratoire Sols et Environnement, Nancy Université – INRA, 54505 Vandoeuvre-Les-Nancy, France
a r t i c l e
i n f o
Article history: Received 19 December 2008 Received in revised form 24 August 2009 Accepted 9 November 2009
Keywords: Cd Zn Thlaspi caerulescens Ryegrass Co-planting Interface soil
a b s t r a c t Co-planting crops normally decreases the main crop yield due to the reduced soil surface area occupied by the main crop. However, in our previous experiments, co-planting Sedum alfredii, a shade-requiring, Cd and Zn-hyperaccumulating plant, with corn increased the biomass and metal phytoextraction of S. alfredii. This experiment was conducted to verify if co-planting another hyperaccumulator, Thlaspi caerulescens, with ryegrass (Lolium perenne) in a pot-trial could obtain a similar result. The soil was separated by two permeable nets with a 2 mm interface soil layer to obtain a shared rhizosphere zone. Soluble metal concentrations in the soil in different rooting zones were measured using 0.01 mol L−1 CaCl2 extraction. The results showed that the growth of T. caerulescens was significantly promoted by co-planting, with a growth increase of about 2-fold compared with monoculture growth. The total uptake of Cd and Zn by T. caerulescens was not decreased by co-planting, and resulted in similar phytoextraction rates for Cd (about 26.6% of the soil total Cd) and Zn (about 2.4% of the soil total Zn) when compared with monoculture, though the T. caerulescens population was decreased by 50% because of co-planting. Analysis of soil samples showed that T. caerulescens substantially reduced the concentrations of 0.01 mol L−1 CaCl2 extractable Cd and Zn throughout the soil, even in the interface area and the ryegrass rooting area. The ryegrass roots did not mobilize more metals for the co-planted T. caerulescens. Based on these results, existing grass on contaminated land could be partly left while planting metal hyperaccumulators for phytoremediation in order to reduce runoff from the contaminated soil. However a field scale trial would be required for these results to be verified. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Heavy metals and metalloids cannot be degraded. Therefore, they persist in soils and are subjected to transport by and into water, where they may become a threat to ecosystems, and enter the food chain and threaten human health (Eapen and D’Souza, 2005; Khan, 2005). Risk management may require remediation of contaminated soils, but current physicochemical technologies to remove metals from soil, such as chemical washing and thermal treatments, are costly and deeply alter soil biological functions
∗ Corresponding author at: Department of Environmental Science and Engineering, College of Natural Resources and Environment, South China Agricultural University, Wushan Street, 510642 Guangzhou, Guangdong, China. Tel.: +86 20 85288326; fax: +86 20 85288326. E-mail addresses: [email protected], [email protected] (Q.-T. Wu). 0925-8574/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2009.11.005
(Glass, 2000; Fellet et al., 2007). Phytoremediation of metal contaminated soils is an alternative to physicochemical techniques and has been studied for almost two decades (Baker et al., 1994; Chaney et al., 1997; McGrath et al., 2002). It has been gaining much attention as it is an in situ technique, can be cost effective, especially for large surfaces, does not disturb the soil structure and can obtain high public acceptance due to the aesthetics of a green vegetation cover (Ma et al., 2001; Susarla et al., 2002; Mitsch and Jorgensen, 2003). Thlaspi caerulescens is one of the most studied metal hyperaccumulator plants and has a high potential to extract Cd and Zn from polluted soils due to its striking accumulation capacity for Zn and Cd at concentrations >10,000 and >100 mg kg−1 shoot dry weight, respectively (Schwartz et al., 1999, 2003; Ozturk et al., 2003). However, this species has a slow growth rate of only 3–4 t ha−1 per 6 months (Wójcik et al., 2005). To improve the potential for heavy metal phytoextraction using this hyperaccumulator, suggestions have been made to optimize the healthy growth of T. caerulescens. These suggestions include: choosing a suitable T.
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Table 1 Main characteristics of the studied soil in the pot experiment. Particle size distribution (g kg−1 )
Clay
Silt
Sand
158
603
239
a
Organic carbon (g kg−1 )
Total P2 O5 (g kg−1 )
pH
C/N
CECa (cmol kg−1 )
Mg (cmol kg−1 )
Ca (cmol kg−1 )
Total Cd (mg kg−1 )
Total Zn (mg kg−1 )
18.6
0.202
8.0
14
13.4
0.496
13.1
19.9
1410
CEC: cation exchange capacity of the soil.
caerulescens population (Schwartz and Morel, 1998); application of appropriate fertilizers (Keller and Hammer, 2004; Ozturk et al., 2003); and applying metal chelators such as EDTA (Blaylock et al., 1997), EDDS (Tandy et al., 2004) or a mixture of chelators (Wu et al., 2006). However, most chelators present an environmental risk to groundwater (Wu et al., 2006). Intercropping, a widely accepted agronomical practice in China for 2000 years, can increase total crop yields through increased resource use efficiency (Zhang and Li, 2003). Roots of some plants grow widely in the top soil and the others may grow downward with strong geotropism. Consequently, plants with different root types may utilize nutrients in different layers of the soil. Cocropping has recently received much attention by entomologists and pathologists aiming at reducing pest numbers and disease transmission by increasing biological diversity (Zhu et al., 2000). Root exudates and rhizosphere microorganisms differ among species (Jones, 1998; Khan, 2005), which may facilitate nutrient and metal (e.g., Fe) uptake between the co-planted plants (Zhang and Li, 2003). Hence, co-cropping with a non-hyperaccumulating plant could enhance the growth of the hyperaccumulator and increase heavy metal uptake while avoiding the side effects to the environment usually observed in chelator enhanced phytoextraction. For example, Wu et al. (2007) showed that the growth and metal uptake of Sedum alfredii were enhanced in the presence of Zea mays, where the corn provided shade to S. alfredii, a shade-requiring plant. Another gramineous plant, ryegrass (Lolium perenne), showed an isotopically measured phytoavailable pool of Cd and Zn (as indicated by the L value which can serve as an indicator of the effect of the plant rhizosphere on metal mobilization), higher than that for other species including T. caerulescens (Sterckeman et al., 2005). However, it is unknown whether T. caerulescens will behave as S. alfredii, with increased metal uptake by T. caerulescens when coplanted with ryegrass. A co-planting pot experiment was carried out. In the experiment, the soil in the pots was separated by two permeable nets between the two plants, to obtain a 2 mm interface soil layer identified as the “shared rhizospheric soil” between the roots of the two plant species. This allows for better understanding of the metal mobility in different plant rooting zones.
separation), where TC was T. caerulescens J. & C. Presl., a hyperaccumulator of Cd and Zn sourced from Viviez (south of France) (Schwartz et al., 2003); RG is ryegrass (L. perenne, L., cv. York); TA is Thlaspi arvense, a closely related species to T. caerulescens but nonhyperaccumulator; “||” indicated that the two plants root systems were separated diagonally by two nylon meshes separated by 2 mm which acted as vertical barriers (Fig. 1). These nets have a 30 m porosity which does not allow plant roots, including main root hairs, to penetrate but allows soil solution, its solutes and microorganisms to pass through (Li et al., 1991). The space between the two meshes was filled with the same soil. Plants grew close to the meshes. There was no mesh in TC + RG treatment in order to check the mesh separation effect on plant growth and metal uptake. Each pot (12 × 12 cm2 and 9 × 9 cm2 at the top and bottom, respectively, with a height of 12 cm) contained 1.5 kg soil, fertilized at rate of 150 mg N, 70 mg P2 O5 , 150 mg K2 O and 30 mg Mg (magnesium) per kg soil with NH4 NO3 , Ca(H2 PO4 )2 , KCl and MgSO4 , respectively. Pots were arranged in random order in a growth chamber with a photoperiod of 16 h day−1 , diurnal temperature range of 18 ◦ C/22 ◦ C, relative humidity of 70%, and light intensity of 500 mol photons m−2 s−1 . Soil moisture was adjusted every day by weighing and maintained at 80% of the water holding capacity (WHC) with deionized water. About 30 seeds of each plant were sown to each half-pot. Ryegrass was sown two weeks later than T. caerulescens and T. arvense. After germination, the number of seedlings was reduced to eight individuals for T. caerulescens and T. arvense in each half-pot, but no ryegrass plants were removed. Shoots of T. caerulescens and T. arvense were harvested after 110
2. Materials and methods 2.1. Pot experiment Soil was sampled from the ploughed horizon of a redoxic Cambisol developed on loess and tertiary sediment colluviums in France, and contaminated with Cd, Pb and Zn, as a consequence of atmospheric fallout from two large lead and zinc smelters (Sterckeman et al., 2002). This soil has been cultivated with annual crops for about 15 years. Soil samples were ground, homogenized, passed through a 5 mm sieve and air-dried. The main physical and chemical characteristics and heavy metal concentrations of the soil are listed in Table 1. The experiment included seven treatments with four replicates each (28 pots in total), identified as TC||RG, TC + RG, TA||RG, TA||TA, RG||RG, TC||TC and a control (no plants but with a mesh
Fig. 1. Schematic diagram of the pot experiment for collecting the shared rhizosphere soil.
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Table 2 Dry biomass of and heavy metal uptake by Thlaspi caerulescens shoots in the different co-planting treatments.
a
TC||RG TC + RG TC||TC
Biomass (g half-pot−1 )
Cd content (mg kg−1 DW)
Cd uptake (mg half-pot−1 )
Zn content (mg kg−1 DW)
Zn uptake (mg half-pot−1 )
9.21 ± 0.35b 9.09 ± 0.52b 4.78 ± 0.12a
865 ± 17a 885 ± 42a 830 ± 25a
7.949 ± 0.190b 7.985 ± 0.180b 3.974 ± 0.198a
5500 ± 146a 5401 ± 262a 5456 ± 290a
50.69 ± 2.761b 48.88 ± 2.810b 26.07 ± 1.514a
b
TC: Thlaspi caerulescens; RG: ryegrass; ||: two nets separation between two plant roots systems. All values were average ± SE (n = 4). Averages followed by the same letter in each column were not significantly different according to one-way ANOVA with Duncan’s test (˛ = 0.05). a
b
days. Ryegrass was cut twice, at 40 and 95 days after sowing. Fresh shoots were washed with deionized water, dried with clean absorbent paper, and then weighed to determine fresh weight. Dry weight was determined after drying at 70 ◦ C for 48 h.
growth. The increased growth of this hyperaccumulator was also observed where it was co-cropped with T. arvense (Whiting et al., 2001). Our previous experiment showed that when co-cropped with Z. mays, the shoot biomass of S. alfredii was significantly increased (Liu et al., 2005; Wu et al., 2007). It appears that this phenomenon may be reasonably common for hyperaccumulators on heavy metal contaminated soils. For ryegrass, the average shoot biomass was 1.96 g DW per half-pot for TC||RG, 1.52 for TC + RG, 4.07 for RG||RG, and 4.89 for TA||RG (Table 3). Hence, co-cropping with T. caerulescens appeared to decrease ryegrass biomass, but co-cropping with T. arvense did not decrease the ryegrass biomass.
2.2. Plant digestion and determination for Cd and Zn Dry biomass was ground and digested in a micro-oven (350 psi) with a mixture of concentrated HNO3 and H2 O2 (Sterckeman et al., 2005). The Cd and Zn concentrations were determined using graphite furnace atomic absorption spectrometry (AAS), or inductively coupled plasma optical emission spectrometry (ICP-OES) depending on the concentration levels.
3.2. Metal uptake by plants 2.3. Extraction of Cd and Zn in soil samples Similar Cd concentrations in T. caerulescens shoots were observed for the treatments TC||RG, TC + RG and TC||TC, which varied from 830 to 885 mg kg−1 DW (Table 2), considerably higher than the hyperaccumulator criteria Cd concentration (100 mg kg−1 DW) (Chaney et al., 1997) which equates to a concentration factor (shoot concentration/soil concentration) of 42–44. The Cd uptake per halfpot by T. caerulescens co-planted with ryegrass was about double that of the mono-cropped T. caerulescens due to the higher biomass produced. On the basis of the whole pot, the phytoextraction rates of Cd, obtained by dividing the total Cd uptake by T. caerulescens (on average 7.96 mg/pot) (Table 2) by the total amount of Cd in the pot (1.5 kg soil/pot × 19.9 mg kg−1 ) (Table 1), were about 26.6% for all treatments where T. caerulescens was planted. The same trend was observed for Zn between the different treatments, but the phytoextraction rates of the total soil Zn were only about 2.4% ((50.57 mg/pot)/(1.5 kg/pot × 1410 mg kg−1 )). The average Cd concentration in ryegrass shoots was increased by co-cropped T. caerulescens but not increased by co-cropped T. arvense (Table 3). However, the total Cd uptake by ryegrass co-cropped with T. caerulescens was not higher than that of monocropped ryegrass or when co-cropped with T. arvense due to the lower biomass produced. For Zn, co-cropping with T. caerulescens tended to decrease the Zn concentration and total uptake by ryegrass compared with mono-cropping or co-cropping with T. arvense. These observations suggest that the hyperaccumulator competes for Zn against the co-planted plant. Similar observations were made when non-contaminated soil was dosed with insoluble metal compounds (Whiting et al., 2001), where the Zn concentration was not sufficient for the hyperaccumulator.
Soil samples were collected separately in the shared rhizosphere layer and in each side of the mesh nets, ground, homogenized, passed through a 1 mm sieve. Five grams of each sample was shaken for 30 min in 25 mL of 0.01 mol L−1 CaCl2 , centrifuged (20 min at 5000 rd min−1 ), and filtered through a 0.45 m membrane. Cd and Zn concentrations were determined by AAS and ICP-OES. This dilute salt extract measures the size of the directly available metal pools (Houba et al., 2000). All analyses were conducted according to French standard methods (AFNOR, 1995). 2.4. Statistical analysis Data were analyzed by one-way ANOVA with Duncan’s test (p < 0.05) using SPSS 13.0 for Windows (Apache Software Foundation). 3. Results and discussions 3.1. Plant growth Better growth of T. caerulescens was observed when co-cropped with ryegrass than without (Table 2). The average shoot biomass in grams per half-pot of T. caerulescens was 9.21 in the TC||RG treatment, 9.09 in TC + RG and only 4.78 in TC||TC. Co-planting with ryegrass significantly promoted the growth of T. caerulescens, by up to a 1.90-fold increase over monoculture planting. There was no significant difference between the treatment TC||RG and TC + RG, showing that separation of plant roots did not affect the plant Table 3 Dry biomass of and heavy metal in ryegrass shoots in different co-planting treatments. Biomass (g half-pot−1 ) a
TC||RG TC + RG RG||RG TA||RG
1.96 1.52 4.07 4.89
± ± ± ±
b
0.16a 0.07a 0.31b 0.24c
Cd content (mg kg−1 DW) 1.907 1.968 1.129 1.119
± ± ± ±
0.123b 0.312b .094a 0.085a
Cd uptake (g half-pot−1 ) 3.778 2.953 4.518 5.513
± ± ± ±
0.501ab 0.422a 0.206bc 0.631c
Zn content (mg kg−1 DW) 135 137 162 189
± ± ± ±
7.0a 17a 9.0ab 3.1b
Zn uptake (mg half-pot−1 ) 0.261 0.207 0.652 0.929
± ± ± ±
0.008a 0.022a 0.039b 0.055c
TC: Thlaspi caerulescens; RG: ryegrass; TA: Thlaspi arvense; ||: two nets separation between two plant roots. All the values were average ± SE (n = 4). Averages followed by the same letter were not significantly different according to one-way ANOVA with the Duncan’s test (˛ = 0.05). a
b
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Table 4 Dry biomass of and heavy metal uptake by Thlaspi arvense in co-planting treatments.
a
TA||RG TA||TA a b
Biomass (g half-pot−1 )
Cd content (mg kg−1 DW)
Cd uptake (g half-pot−1 )
Zn content (mg kg−1 DW)
Zn uptake (mg half-pot−1 )
3.15 ± 0.78b 4.71 ± 0.69a
10.58 ± 0.832a 11.73 ± 4.12a
41.07 ± 12.95a 56.33 ± 21.49a
162 ± 6.0a 158 ± 42a
0.569 ± 0.126a 0.753 ± 0.237a
b
TA: Thlaspi arvense; RG: ryegrass; ||: two nets separation between two plant roots. All the values were average ± SE (n = 4). Averages followed by the same letter were not significantly different according to one-way ANOVA test (˛ = 0.05).
Cd concentrations and Cd uptakes by T. arvense shoots were not significantly different between the TA||RG and TA||TA treatments (Table 4). Similar results were observed for Zn. This indicated that the enhanced metal uptake by an individual plant co-planted with ryegrass was only applicable for T. caerulescens and not for the nonhyperaccumulator T. arvense. 3.3. Phytoavailable Cd and Zn in the soil Soil Cd and Zn concentrations extractable by 0.01 mol L−1 CaCl2 at the end of the planting experiment varied from 32 to 238 g kg−1 and from 898 to 2586 g kg−1 soil, respectively (Table 5). Extractable Cd in the soils planted with T. caerulescens (TC||RG and TC||TC treatments) was significantly less than in soils without the hyperaccumulator (RG||RG, TA||RG, TA||TA and control treatments) and the original soil, in both the rooting soils and the shared interface soils. Moreover, soil in the ryegrass rooting side in the TC||RG treatment had a significantly lower Cd concentration (43.29 g kg−1 soil) than that in the RG||RG treatment (205.5 g kg−1 soil) (Table 5), meaning that Cd was transported to the other side of the pot and taken up by T. caerulescens. The Cd that was removed from the ryegrass side of the pot in the TC||RG treatment was not taken up by the ryegrass, as Cd levels in the ryegrass were not significantly different to that for the RG||RG treatment (Table 3). Neither roots nor root hairs of T. caerulescens could reach the ryegrass side of the pots and no reports show this hyperaccumulator associated with mycorrhiza (Vogel-Mikus et al., 2005). Cd uptake by ryegrass and T. arvense significantly reduced the extractable Cd, with the remaining Cd levels at 200.1 and 205.5 g kg−1 soil, compared with soil in the control treatment (219.4 g kg−1 soil). The shared interface soils for all the planted treatments showed a higher extractable Cd than the rooting soils, possibly due to the absence of plant roots.
CaCl2 extractable Zn showed a trend similar to that observed for Cd, but the difference was less pronounced. Extractable Zn remained higher in the interface soil shared with ryegrass (the treatment TC||RG) than that shared with its own species (TC||TC), though it was not statistically significant, suggesting that the interface soil could provide more available metal to the hyperaccumulator side. The obtained N, P, K and S nutrient data in the soil solutions did not give a viable explanation for the better growth of co-cropped T. caerulescens and the worse growth of ryegrass (data not presented), because they were not significantly different between corresponding treatments. There was also no significant difference in soil pH between the treatments which varied from 7.8 to 7.9 for all planted treatments. Xiao et al. (2004) indicated that in a faba bean and wheat co-cropping system, wheat was a stronger competitor for soil available N and benefited from cocropping with the N-fixing faba bean. From the present experiment, the superiority of the hyperaccumulator growth when co-cropped with ryegrass was not explained by major nutrients, but by more Zn available to individual T. caerulescens plants. However it is also possible that the volatile organic compounds (VOCs) excreted by plant shoots may play a role in the competition as suggested for plant allelopathy (Baldwin et al., 2006). The total phytoavailable metal in a pot was calculated by adding the metal taken up by the plants to that remaining in the soil and extracted by CaCl2 (Table 5). Results showed that co-planting with ryegrass did not mobilize more Cd and Zn than mono-cropped T. caerulescens, because the total phytoavailable metals for TC||RG and TC||TC treatments were very similar, even though a half-pot soil was colonized by the different plants. The hyperaccumulation of metals by T. caerulescens under the present experimental conditions seems only the result of metal solubilization and transport in the soil–root interface powered by low metal concentration on the root surface of the hyperaccumulator rather than from changes to
Table 5 Cd and Zn extracted by 0.01 mol L−1 CaCl2 in the soil samples after pot experiment with co-planting treatments where the two plant root systems were separated by two nets with a 2 mm interface soil layer. TA or TC side (g kg−1 soil) Cd TC||RGb TC||TC RG||RG TA||RG TA||TA No plants Original soil Zn TC||RG TC||TC RG||RG TA||RG TA||TA No plants Original soil
32.10ac 38.31a – 193.5c 200.1cd – – 941.1a 898.9a – 1372bc 1419bc – –
Interface (g kg−1 soil) 95.93b 81.92b 220.0f 215.82f 210.9ef 219.4f 218.5f 1443bc 1064ab 1995d 2203de 2586e 2301de 1821cd
Ryegrass side (g kg−1 soil) 43.29a – 205.5de 205.3de – – – 1017a – 1371bc 1355bc – – –
Total phytoavailablea (mg/pot) 8.024Ac 8.007A 0.322B 0.349B 0.413B 0.351B 0.350B 52.53A 53.26A 3.12BC 3.66B 4.14B 2.60C 2.06C
The capital letters indicate differences for the total phytoavailable metals, because the data in this column are not comparable with data in the other columns. a Total phytoavailable = total extracted by 0.01 M CaCl2 + total uptake by plants. b TC: Thlaspi caerulescens; RG: ryegrass; TA: Thlaspi arvense; ||: two nets separation between two plant root systems. c The averages (n = 4) of the same metal followed by a same letter were not significantly different according to one-way ANOVA with Duncan’s test (˛ = 0.05).
C.-a. Jiang et al. / Ecological Engineering 36 (2010) 391–395
the phytoavailable pool in the rhizosphere caused by root exudation. 4. Conclusions Using a separation device which allowed for different rooting zones in a pot experiment, this study identified the competitive relationships between hyperaccumulator and co-cropped common plants with respect to plant growth and heavy metals uptake. It indicated clearly that the co-planting stimulates the growth of the hyperaccumulator and increases the Cd and Zn uptake for an individual plant. The phenomenon is specific for the hyperaccumulator T. caerulescens on heavy metal contaminated soil and does not occur for T. arvense, a closely related species to T. caerulescens but not a hyperaccumulator. The ryegrass roots did not mobilize metals for the co-planted T. caerulescens but the metals in the ryegrass rooting zone could be transported to the hyperaccumulator. This study confirms that co-planting metal hyperaccumulators with other plants can get a similar or higher phytoextraction rate than monoplanting. It is possible that the existing grass on contaminated sites could be partly left while planting metal hyperaccumulators for phytoextraction of metals in order to reduce the runoff from the contaminated soil but this should be verified in a field experiment. Acknowledgments This research was financially supported by the French–Chinese Programme de Recherche Avancée (PRA E03-04), National Science Foundation of China (NSFC-40571141 and U0833004) and National High-tech R&D Program (863 Program: 2008AA10Z405 and 2007AA061001-3). The authors are grateful to Dr. Y. Ouyang in the Department of Water Resources, St. Johns River Water Management District, Florida, USA, for his help and suggestions in the modification of the manuscript. References AFNOR, 1995. Qualite du Sol. AFNOR, Paris. Baker, A.J.M., Reeves, R.D., Hajar, A.S.M., 1994. Heavy metal accumulation and tolerance in British populations of metallophyte Thlaspi caerulescens. New Phytol. 127, 61–68. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C., Preston, C.A., 2006. Volatile signaling in plant-plant interactions: “Talking trees” in the genomics era. Science 311, 812–815. Blaylock, M.J., Salt, D.E., Dushenkov, S., 1997. Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ. Sci. Technol. 31, 860–865. Chaney, R.L., Malik, K.M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S., 1997. Phytoremediation of soil metals. Curr. Opin. Biotechnol. 8, 279–284. Eapen, S., D’Souza, S.F., 2005. Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol. Adv. 23, 97–114. Fellet, G., Marchiol, L., Perosa, D., Zerbi, G., 2007. The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol. Eng. 31 (3), 207–214. Glass, D.J., 2000. Economical potential of phytoremediation. In: Raskin, I.Y., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals. John Wiley & Sons, Inc., New York, pp. 15–31. Houba, V.J.G., Temminghoff, E.J.M., Gaikhorst, G.A., Van Vark, W., 2000. Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Commun. Soil Sci. Plant Anal. 31, 1299–1396.
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