Phytoaccumulation of heavy metals (Pb, Zn, and Cd) by 10 wetland plant species under different hydrological regimes

Ecological Engineering 107 (2017) 56–64

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Phytoaccumulation of heavy metals (Pb, Zn, and Cd) by 10 wetland plant species under different hydrological regimes Junxing Yang a , Guodi Zheng a , Jun Yang a , Xiaoming Wan a,∗ , Bo Song b , Wen Cai a , Junmei Guo a a b

Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, PR China College of Environmental Science and Engineering, Guilin University of Technology, Guilin, Guangxi 541004, PR China

a r t i c l e

i n f o

Article history: Received 2 July 2015 Received in revised form 21 June 2017 Accepted 26 June 2017 Keywords: Phytoaccumulation Hydrological regimes Fe plaque Radial oxygen loss Wetland plant species Rhizosphere

a b s t r a c t Wetland plants have been widely used in constructed wetlands to remove metal contaminants from water and soil. This study aimed to investigate radial oxygen loss (ROL) rate, metal (Pb, Zn, and Cd) uptake, Fe plaque formation, and their relationships in a pot trial with 10 emergent wetland plant species grown in metal-contaminated soil under flooded and non-flooded conditions. The results showed that biomass, ROL rates, metal (Pb, Zn, and Cd) uptake, and Fe plaque formation on root surfaces and in the rhizospheres of the wetland plant species were remarkably higher under flooded conditions than under non-flooded conditions. Generally, flooding mainly increased metal accumulation in the roots and Fe plaque on the root surface of wetland plant species. The wetland plant species with higher ROL rates had higher biomass, Fe plaque formation and metal adsorption on the roots and in the rhizospheres under flooded conditions. These results suggest the wetland plant species with higher ROL rates, biomass and metal accumulation ability, e.g. C. alternifolius, has the potential for use in phytoremediation of metal-contaminated wetlands. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Wetland plants have been widely used to remove metal contaminants from water and soil (Ye et al., 2004; Lizama et al., 2011). Previous studies have evaluated metal tolerance, accumulation and translocation in wetland plant species (Ye et al., 1997a,b, 1998a; Deng et al., 2006) and found that some of these plants have higher metal tolerance, biomass production and metal uptake (Deng et al., 2006; Yang et al., 2014). Furthermore, deep-root system of wetland plants serves as a biological filter of waste water and soil (Sheoran and Sheoran, 2006). These studies indicated that wetland plants are excellent candidates for phytoremediation of both metal-contaminated water and soil. In order to adapt to an anoxic environment, wetland plants have developed aerenchyma tissues containing enlarged gas spaces, which can be expressed quantitatively as porosity (ratio of gas spaces to tissues volumes). Enlarged gas spaces can transport O2 from aerial parts to roots for respiration and any excess O2 may diffuse from roots into the rhizosphere zone, a process referred

∗ Corresponding author at: Center for Environmental Remediation, Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, 11A, Datun Road, Chaoyang District, Beijing, 100101, PR China. E-mail address: [email protected] (X. Wan). http://dx.doi.org/10.1016/j.ecoleng.2017.06.052 0925-8574/© 2017 Elsevier B.V. All rights reserved.

to as radial oxygen loss (ROL) (Armstrong, 1979). ROL from roots enables wetland plants to tolerate a flooded, anoxic environment and to detoxify phytotoxins, such as Fe2+ , Mn2+ , and H2 S through oxidation (Armstrong, 1979; Armstrong and Armstrong, 2005). The tolerance of wetland plants to flooding (Chabbi et al., 2000), salinity (Rogers et al., 2008), and toxic metals (e.g. As, Cd and Zn) (Li et al., 2011; Wang et al., 2011; Yang et al., 2014) is positively correlated with ROL. ROL also allows the precipitation of Fe and Mn oxides in the root apoplast, the so-called Fe plaque (Armstrong, 1967). Fe plaque formation is influenced by the Fe availability of soil and the oxidizing capacity of roots (Hansel et al., 2002). Given the high absorption capacity of Fe oxides, Fe plaque provides a reactive substrate for metal sequestration and translocation of metals such as Zn, Pb, Cu and As (Ye et al., 1998a; Zhang et al., 1998; Liu et al., 2013). ROL also induces oxidation of mobile Fe2+ in rhizosphere soils into insoluble ferric hydroxide (Ahmad and Nye, 1990). The beneficial effects of Fe oxidization in rhizosphere soils include the suppression of toxic products (e.g. Fe2+ ) of anaerobic metabolism, and the coprecipitation of heavy metals (e.g., Zn, Pb, and Cd) (Cheng et al., 2014; Yang et al., 2014). Several studies reported that wetland plants can be applied to phytoremediate metal-contaminated wastewaters under flooded conditions (Sheoran and Sheoran, 2006) and Pb/Zn mine tailings under non-flooded conditions (Ye et al., 2004). The Metal accumula-

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tion patterns of the same wetland plant species and its rhizosphere remarkably differ between flooded and non-flooded conditions (Ye et al., 1998b; Kissoon et al., 2010, 2011; Chen et al., 2012). The mobility and phytoavailability of heavy metals remarkably differ between flooded soils and non-flooded soils (Du Laing et al., 2007). Hydrological regime is an important factor controlling physical, chemical, and biological properties of soil; hence, this factor affects pH, redox potential (Eh), ROL, metal bioavailability, Fe oxidation, and metal sulfide precipitation (Armstrong and Armstrong, 2005; Du Laing et al., 2009). However, insufficient information is currently available on the relationships among metal uptake, ROL, and subsequent Fe plaque formation in different wetland plant species under flooded and non-flooded conditions. Therefore, the relationships between ROL, Fe plaque formation, toxic metal uptake and distribution for wetland plant species under flooded and non-flooded conditions require an investigation. The present study aimed to investigate variations and correlations in the rates of ROL, degrees of Fe plaque formation, uptake and distribution of metals (Pb, Zn, and Cd) in shoots, roots, Fe plaque on the root surface and the rhizospheres under flooded and nonflooded conditions.

The wetland plant species mentioned above were grown in flooded or non-flooded rhizobag pots, with three replicates per treatment. Soils for the non-flooded treatment were watered with soft tap water once per day to keep the moisture at approximately 70% water holding capacity. Substrates for the flooded treatment were flooded with an inundation depth of c. 3–4 cm. Two seedlings or tillers of each species were transplanted into sand and then grown under the same glasshouse conditions as mentioned above. The plants were transplanted into sand (hereafter referred to as “rhizosphere” material) at the beginning of the pot experiment. At the end of the study, the sand was completely permeated by the roots. The whole experiment lasted for 90 days after the transplant of seedlings or tillers. All pots were arranged in a randomized block design and maintained under natural light in the greenhouse. Plant cultivation was conducted in a glasshouse in a randomized block design. The glasshouse was illuminated with cool-white fluorescent tubes, supplying a photon flux density of 300 ␮mol m−2 s−1 , a relative humidity of 85% and a light/dark cycle of 14 h day/10 h night. The day/night temperature regime was between 28 ◦ C/22 ◦ C.

2. Materials and methods

At the end of the experiment, pH and Eh in the rhizosphere (upper layer) sands were measured by using a portable pH/Eh meter (pH/oxi 340i, WTW, Weilheim, Germany). Then, all plants were harvested by carefully moving the rhizobags out of the pots. Two plants of each pot were separated and washed thoroughly with deionized water. One plant was used for determining the ROL and the other for the dithionite–citrate–bicarbonate (DCB) extraction of Fe plaque on the root surface. The rhizosphere material was simultaneously collected and used for the extraction of Fe plaque.

2.1. Soil and plant preparation The soil used in the pot trial was collected from an abandoned paddy field (0–20 cm) in Chongyang (CY) Pb/Zn mine area located in Shaoguan City, Guangdong Province, China. The soil was thoroughly mixed, air dried, and then ground to <2 mm. The physical and chemical properties of the soil were analyzed, and the results were presented as: pH (2.5:1 distilled water:soil, v/w), 6.3; organic matter (K2 CrO7 -H2 SO4 ), 11.6 g kg−1 ; total N (semi-quantitative titration), 0.69 g kg−1 ; Olsen-P (0.5 M NaHCO3 ), 1.95 mg kg−1 ; available K (1.0 M NH4 OAc), 40.8 mg kg−1 ; total Pb, 312 mg kg−1 ; total Zn, 457 mg kg−1 ; total Cd, 3.12 mg kg−1 ; total Fe, 15.7 g kg−1 ; and total Mn, 1032 mg kg−1 . Ten emergent wetland plant species were collected from non-contaminated sites. Tillers of Grass-leaved sweetflag (Acorus tatarinowii), Chinese taro (Alocasia cucullata), Umbrella palm (Cyperus alternifolius), Amazon sword (Echinodorus amazonicus), Red Diamond (Echinodorus baothii), Pennywort (Hydrocotyle vulgaris), Triangular club-rush (Scirpus triqueter) and Thyme leaved speedwell (Veronica serpyllifolia) were grown from vegetative propagation, whereas Canada Spikesedge (Eleocharis geniculata) and Torpedograss (Panicum repens) were germinated from seeds. Due to the different growth rates of these species, the author selected the wetland plant species with similar shoot heights and root lengths for a pot trial. 2.2. Experimental design Sand is a common substrate used in constructed wetlands (Bubba et al., 2003). A cylindrical nylon bag (400-mesh, 4 cm diameter, and 10 cm height) was designed to separate rhizosphere from non-rhizosphere. The rhizobag was separated into two halves by a thin plastic card in the center and filled with 300 g of dry sand, which was then placed in the center of a PVC pot (about 0.8 L in volume) filled with 1 kg of CY soil. This design successfully prevented roots and even root hairs from entering the adjacent non-rhizosphere soil zone while permitting the transfer of microfauna and root exudates between the two compartments. In other words, although the soil was used to enclose the outside of the rhizobag, the rhizosphere was confined to the sand compartment and effectively separated from the non-rhizosphere soil compartment.

2.3. Harvesting and sampling

2.4. Measurements of ROL rates and extraction of Fe plaque ROL rate was determined in accordance with the Ti3+ –citrate method described by Mei et al. (2009) and Yang et al. (2014). Pb, Zn, Cd, Fe and Mn in Fe plaque on the root surfaces and in the rhizospheres were extracted using the DCB method (Otte et al., 1989). 2.5. Sample analysis After DCB extraction, oven-dried plant shoot or root samples were grounded by Retsch grinder (Type: 2 mm, Retsch Company, Germany). Then Pb, Zn, and Cd in plant tissues were extracted by digesting the sample with HNO3 and HClO4 (4:1, V/V). The concentrations of Pb and Zn in the plant tissues and Pb, Zn, Fe, and Mn in the DCB-extracts were determined via inductively coupled plasma-atomic emission spectrometry (Optima 2000DV, Perkin Elmer, USA). The concentration of Cd in the plant tissues and DCB extracts was determined through graphite furnace atomic absorption spectrometry. Blanks and standard plant materials [GBW-07603 (GSV-2) China Standard Materials Research Center, Beijing, P.R. China] were employed to ensure quality. The average recovery rates for all metals (Pb, Zn, Cd, Fe, and Mn) were within the range of 90% ± 10%. 2.6. Statistical analysis Metal (Pb, Zn, and Cd) contents in Fe plaque of the root surfaces (TDCB−metal ) or in the plant tissue (root and shoot) (Tplanttissue−metal ) were calculated by multiplying metal concentration in Fe plaque or plant tissue by the plant tissue dry weight. Therefore, the total metal content (Tmetal  ) of the whole plant was calculated as the sum of TDCB−metal and Tplanttissue−metal .

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J. Yang et al. / Ecological Engineering 107 (2017) 56–64

Table 1 pH and Eh in the rhizosphere sand of 10 wetland plant species grown in soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

pH

Eh (mv)

F

N

F

N

6.3 ± 0.06 6.4 ± 0.10 6.1 ± 0.21 6.2 ± 0.10 6.2 ± 0.15 6.5 ± 0.21 6.3 ± 0.25 6.1 ± 0.12 6.2 ± 0.15 6.2 ± 0.06

6.0 ± 0.15 6.3 ± 0.12 6.2 ± 0.21 6.0 ± 0.17 6.1 ± 0.10 6.4 ± 0.15 6.3 ± 0.12 6.1 ± 0.15 6.0 ± 0.10 6.1 ± 0.12

56 ± 2.65c* 35 ± 4.58de* 41 ± 3.61de* 89 ± 3.21a* 74 ± 6.03b* −55 ± 4.16g* −42 ± 2.08f* 34 ± 5.57e* 47 ± 4.16cd* 69 ± 2.65b*

225 ± 3.06b 187 ± 7.77c 272 ± 6.25a 279 ± 7.64a 222 ± 5.00b 165 ± 13 cd 143 ± 7.77d 217 ± 10.5b 234 ± 8.5b 223 ± 9.45b

Note: Different letters within pH or Eh indicate a significant difference among the different wetland plant species under the flooded (F) and non-flooded (N) conditions at P < 0.05. The effects of water treatments on the same wetland plant species were analyzed via t-test ANOVA at P < 0.05 (indicated by *) (the same below).

All results were presented as arithmetic means with standard errors and analyzed using SPSS 13.0 statistical package. Statistical comparisons of the means of soil pH, Eh, biomass, ROL rates and metal concentrations among species or between flooded and non-flooded treatments were analyzed through one-way ANOVA followed by the least significant difference test or t-test at the 5% level. Linear correlation between rates of ROL, concentrations of Fe, Mn, Pb, Zn, and Cd on the root surfaces and in the rhizosphere under flooded and non-flooded conditions was analyzed. 3. Results 3.1. Eh and pH of soil The rhizospheres under flooded and non-flooded conditions significantly differed in Eh (Table 1). Eh was remarkably lower under flooded conditions than under non-flooded conditions, indicating a reduced environment. Rhizosphere pH of all plants generally increased by 0.1–0.3 units under flooded conditions than under non-flooded conditions. However, rhizosphere pH of C. alternifolius slightly decreased by 0.1 unit. 3.2. Plant growth and ROL The flooded treatment effectively affected growth (shoot and root biomasses) and ROL of the roots in all of the species tested (Table 2). Shoot and root biomasses of the 10 species significantly (P < 0.05) increased under flooded conditions. Among the 10

species, C. alternifolius showed the highest shoot biomass and P. repens the highest root biomass under flooded conditions. The ROL rates of all species increased under flooded conditions than under non-flooded conditions. The enhancement (in terms of % under non-flooded conditions) significantly differed (P < 0.05) between the wetland plant species, ranging from 52.2% (S. triqueter) to 397% (P. repens). 3.3. Concentrations of Fe and Mn in DCB extracts of the root surfaces and in the rhizosphere Degree of Fe plaque formation on the root surfaces and in the rhizospheres significantly varied among the wetland plant species under flooded and non-flooded conditions. The concentration ranges of Fe and Mn were 2176–9596 and 769–14,363 mg kg−1 on the root surfaces, respectively, and 3805–18,855 and 1832–6738 mg kg−1 on the sand surfaces in the rhizosphere under flooded conditions; these values were significantly higher (P < 0.05) than those under non-flooded condition (Table 3). 3.4. Concentrations of Pb, Zn, and Cd in shoot and root tissues, DCB extracts and total Pb, Zn, and Cd amounts of whole wetland plant species The concentrations of Pb, Zn, and Cd in the shoot and root tissues and in DCB extracts on the root surfaces significantly varied among the wetland plant species under both water treatments (Tables 4–6). Five of the 10 species had higher Pb and Zn concentrations in the shoots under flooded conditions than them under non-flooded conditions. Meanwhile, wetland plant species generally had lower Cd concentrations in the shoots under flooded conditions than under non-flooded conditions (Tables 4–6). The concentrations of Pb, Zn, and Cd in the rhizospheres generally increased under flooded conditions (Tables 4–6). The enhancement (in terms of % under non-flooded conditions) significantly differed (P < 0.05) between the wetland plant species. The flooded treatment obviously influenced Pb accumulation in different parts of the wetland plant species (Table 4). Distribution of Pb in the Fe plaque under flooded conditions can be arranged as follows: root tissues > root surfaces > rhizosphere > shoot tissues. Meanwhile, distribution of Pb in the Fe plaque under non-flooded conditions followed the order: root surfaces > root tissues > rhizosphere > shoot. Distribution of Zn concentration in the plants followed the same order of root tissues > rhizosphere > shoot tissues > root surfaces (Table 5). Distribution of Cd concentration in the plants followed the same order of root tissues > shoot tissues > root surfaces > rhizospheres (Table 6).

Table 2 Shoot and root of biomass (g plant−1 ) and ROL rates (mmol O2 kg−1 root d.w. d−1 ) of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

Shoot DW

Root DW

ROL

F

N

F

N

F

N

2.17 ± 0.01b* 1.71 ± 0.19c* 3.40 ± 0.44a* 1.32 ± 0.25c* 1.26 ± 0.15c* 0.23 ± 0.01d* 0.37 ± 0.06d 2.29 ± 0.4b* 2.07 ± 0.09b* 1.73 ± 0.02bc*

1.30 ± 0.12a 1.14 ± 0.07ab 1.02 ± 0.11bc 0.29 ± 0.05ef 0.14 ± 0.02ef 0.07 ± 0.01f 0.35 ± 0.06e 0.63 ± 0.05d 0.58 ± 0.05d 0.86 ± 0.11c

0.29 ± 0.12d 0.66 ± 0.08ab* 0.63 ± 0.21abc 0.29 ± 0.08d 0.36 ± 0.12bcd 0.15 ± 0.02d* 0.32 ± 0.04 cd 0.80 ± 0.08a* 0.28 ± 0.04d 0.70 ± 0.12a

0.12 ± 0.01ef 0.28 ± 0.04b 0.22 ± 0.06Bcd 0.13 ± 0.02def 0.04 ± 0.01f 0.05 ± 0.01f 0.25 ± 0.06bc 0.06 ± 0.01f 0.14 ± 0.04def 0.41 ± 0.06a

24.11 ± 0.99d* 6.65 ± 0.27f* 25.71 ± 1.33cd* 66.58 ± 4.24a* 42.56 ± 2.72b* 12.33 ± 0.83ef* 15.92 ± 1.51e* 6.57 ± 0.60f* 30.89 ± 1.50c* 17.42 ± 1.19e*

13.12 ± 0.48c 4.32 ± 0.18ef 12.4 ± 0.76 cd 39.6 ± 0.81a 24.5 ± 0.71b 7.96 ± 0.13de 10.3 ± 0.59 cd 1.32 ± 0.05d 20.3 ± 0.68b 11.22 ± 0.37 cd

Note: Different letters within shoot or root biomass and within ROL among the different species indicate a significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05.

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Table 3 Fe and Mn concentrations (mg kg−1 d.wt) in the Plaqueroot and Plaquerhizo of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

DCB Fe

DCB Mn

Root surface

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

Rhizosphere

Root surface

Rhizosphere

F

N

F

N

F

N

F

N

6351 ± 518c 2176 ± 86e* 7566 ± 230b* 9167 ± 315a* 9596 ± 506a* 6135 ± 127c* 6205 ± 141c* 3509 ± 195d* 6244 ± 406c* 8052 ± 429b*

4325 ± 609c 1398 ± 31e 4645 ± 166c 13488 ± 741a 7320 ± 193b 3686 ± 343c 3706 ± 202c 1469 ± 217de 2506 ± 116d 3858 ± 256c

4650 ± 279fg* 5990 ± 340de 3805 ± 163g* 17280 ± 269b* 18855 ± 413a 6982 ± 454d* 4568 ± 298fg* 5167 ± 396ef* 4727 ± 272fg* 12488 ± 655c*

3567 ± 167d 12272 ± 1717b 2876 ± 258d 11467 ± 558b 16442 ± 1576a 3393 ± 268d 3052 ± 226d 3235 ± 205d 3228 ± 171d 8010 ± 463c

5645 ± 508de* 3262 ± 152g* 7287 ± 277cd* 14363 ± 1407a* 12692 ± 693b* 3715 ± 352fg* 4244 ± 295efg* 3470 ± 144fg* 5115 ± 159ef* 7697 ± 263c*

3073 ± 251 cd 1547 ± 283ef 3652 ± 189bc 8375 ± 349a 8028 ± 346a 2255 ± 215de 2357 ± 271de 991 ± 58f 2494 ± 209d 4135 ± 417b

1832 ± 199e* 4003 ± 289b* 2800 ± 94cd* 3933 ± 99b 6738 ± 243a* 1527 ± 652e 3567 ± 406ab 3592 ± 134ab 2373 ± 107de* 2888 ± 97cd*

695 ± 103f 1875 ± 133d 1863 ± 179d 3900 ± 121b 5613 ± 226a 1228 ± 43e 2427 ± 182c 2838 ± 284c 1222 ± 59e 1723 ± 36d

Note: Different letters within root surface or rhizosphere among the different species indicate a significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05. Table 4 Pb concentrations (mg kg−1 d.wt) in shoot tissues, root tissues, and plaque on the root surface (Plaqueroot ) and plaque in the rhizosphere (Plaquerhizo ) of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

Shoot Pb

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

Root Pb

DCB Pb on the root surface

DCB Pb in the rhizosphere

F

N

F

N

F

N

F

N

3.7 ± 0.4de 6 ± 0.7 cd 11 ± 1bc* 3.6 ± 0.4de* 35 ± 2a* 4.4 ± 0.3de 38 ± 3a* 4.0 ± 0.4de 2.1 ± 0.6e* 14 ± 1e*

4.5 ± 0.4de 7.7 ± 1.2bc 6.9 ± 0.9bcd 30 ± 1a 9.2 ± 0.5b 4.8 ± 1.1cde 4.6 ± 0.9cde 3.3 ± 0.8e 7.9 ± 1.3b 7.1 ± 0.9bcd

78 ± 6de* 50 ± 3ef* 46 ± 3f* 356 ± 7b* 407 ± 22a* 96 ± 4d* 51 ± 5ef 226 ± 13c* 365 ± 13b* 85 ± 5d*

16 ± 1fg 23 ± 4fg 82 ± 9c 117 ± 3b 134 ± 6a 11 ± 1g 60 ± 3d 38 ± 1e 84 ± 8c 27 ± 2ef

76 ± 8de* 81 ± 7de 101 ± 7cd* 283 ± 24a 232 ± 18b* 135 ± 17c* 50 ± 3e 62 ± 17de 70 ± 3de* 57 ± 6e*

39 ± 3c 93 ± 15b 42 ± 4c 340 ± 16a 348 ± 28a 100 ± 2b 37 ± 9c 25 ± 6c 47 ± 2c 27 ± 2c

59 ± 4ef* 62 ± 5def 77 ± 4d* 158 ± 5b 176 ± 7a* 93 ± 4c 58 ± 6ef* 47 ± 4f* 53 ± 8ef* 66 ± 6de*

24 ± 7d 57 ± 12c 26 ± 4d 147 ± 6a 136 ± 6a 103 ± 5b 23 ± 8d 15 ± 1d 29 ± 3d 17 ± 3d

Note: Different letters among the 10 species indicate significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05. Table 5 Zn concentrations (mg kg−1 d.wt) in shoot tissues, root tissues, and plaque on the root surface (Plaqueroot ) and plaque in the rhizosphere (Plaquerhizo ) of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

Shoot Zn

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

Root Zn

DCB Zn

Rhizosphere Zn

F

N

F

N

F

N

F

N

27 ± 3e* 37 ± 4f* 27 ± 2f* 102 ± 4e 253 ± 15c* 148 ± 12d* 526 ± 17a* 29 ± 3f* 37 ± 6f* 334 ± 23b*

49 ± 4f 86 ± 5d 36 ± 2f 95 ± 6 cd 112 ± 6c 46 ± 3f 67 ± 2e 125 ± 8b 128 ± 7b 172 ± 10a

197 ± 9d* 79 ± 4Fg* 55 ± 6g* 146 ± 7e* 192 ± 8d* 343 ± 23b* 616 ± 26a* 144 ± 5e 104 ± 7f* 288 ± 5c*

542 ± 27a 143 ± 4d 138 ± 8d 398 ± 18b 115 ± 10de 82 ± 9e 96 ± 5e 138 ± 7d 224 ± 14c 209 ± 12c

97 ± 5c 57 ± 10d* 87 ± 4c* 172 ± 13b* 203 ± 11a* 97 ± 6c* 90 ± 8c 98 ± 9c* 103 ± 16c 112 ± 7c

78 ± 7 cd 27 ± 3f 50 ± 3e 127 ± 10b 152 ± 10a 70 ± 4de 76 ± 5 cd 66 ± 5de 61 ± 9de 96 ± 4c

147 ± 6cd* 89 ± 9e* 135 ± 12d* 264 ± 12b* 332 ± 18a* 159 ± 6cd* 131 ± 7d 154 ± 7cd* 159 ± 8cd* 171 ± 3c*

106 ± 6d 57 ± 7f 69 ± 7ef 168 ± 10b 201 ± 8a 99 ± 11d 109 ± 6 cd 88 ± 6de 72 ± 9ef 130 ± 5c

Note: Different letters among the 10 wetland plant species indicates a significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05. Table 6 Cd concentrations (mg kg−1 d.wt) in shoot tissues, root tissues, and plaque on the root surface (Plaqueroot ) and plaque in the rhizosphere (Plaquerhizo ) of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

DCB Cd on the root surface

DCB Cd in the rhizosphere

F

Shoot Cd N

Root Cd F

N

F

N

F

N

0.46 ± 0.07a 0.29 ± 0.04c 0.15 ± 0.02d 0.27 ± 0.04bcd 0.24 ± 0.03cd* 0.18 ± 0.02 cd 0.26 ± 0.03bcd 0.51 ± 0.07A 0.43 ± 0.05a* 0.39 ± 0.03ab*

0.65 ± 0.04a 0.41 ± 0.06b 0.11 ± 0.01d 0.38 ± 0.04bc 0.64 ± 0.05a 0.13 ± 0.02d 0.36 ± 0.04bc 0.74 ± 0.12a 0.61 ± 0.04a 0.23 ± 0.03 cd

4.08 ± 0.07cd* 1.62 ± 0.09e* 4.42 ± 0.17c* 5.83 ± 0.17b* 6.94 ± 0.14a* 3.71 ± 0.26d* 3.65 ± 0.30d* 1.99 ± 0.14e* 3.92 ± 0.17cd* 5.33 ± 0.18b*

6.74 ± 0.28 cd 2.61 ± 0.24e 7.13 ± 0.13c 9.40 ± 0.42ab 10.2 ± 0.62a 5.97 ± 0.42d 5.88 ± 0.32d 3.21 ± 0.22e 6.32 ± 0.48 cd 8.60 ± 0.24b

0.32 ± 0.04bc* 0.12 ± 0.02e 0.34 ± 0.04bc* 0.45 ± 0.05ab* 0.53 ± 0.08a* 0.28 ± 0.05cd* 0.27 ± 0.04cd* 0.15 ± 0.03de 0.31 ± 0.04c* 0.32 ± 0.04bc*

0.14 ± 0.02abcde 0.079 ± 0.008e 0.15 ± 0.02abcd 0.18 ± 0.03ab 0.19 ± 0.04a 0.11 ± 0.01cde 0.12 ± 0.03bcde 0.09 ± 0.01de 0.13 ± 0.01abcde 0.17 ± 0.01abc

0.084 ± 0.007bc* 0.032 ± 0.006d 0.089 ± 0.01bc* 0.118 ± 0.013a* 0.139 ± 0.01a* 0.073 ± 0.013c 0.071 ± 0.009c* 0.039 ± 0.009d 0.082 ± 0.007bc* 0.111 ± 0.011ab*

0.039 ± 0.009bc 0.015 ± 0.003d 0.042 ± 0.006b 0.056 ± 0.004ab 0.066 ± 0.011a 0.035 ± 0.006bcd 0.034 ± 0.008bcd 0.018 ± 0.002 cd 0.039 ± 0.008bc 0.053 ± 0.007ab

Note: Different letters among the 10 wetland plant species indicates a significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05.

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Table 7 Metal (Pb, Zn, Cd) contents (␮g plant−1 ) of 10 wetland plant species grown in the soil collected from an abandoned paddy field in Chongyang Pb/Zn mine area for 3 months under flooded and non-flooded conditions (mean ± S.E., n = 3). Species

A. tatarinowii A. cucullata C. alternifolius E. amazonicus E. baothii E. geniculata H. vulgaris P. repens S. triqueter V. serpyllifolia

Pb

Zn

Cd

F

N

F

N

F

N

51 ± 16d* 97 ± 10cd* 131 ± 38bcd* 194 ± 53abc* 278 ± 89a* 36 ± 1d* 47 ± 9d* 245 ± 46bcd* 125 ± 15bcd* 124 ± 17bcd*

11 ± 1de 40 ± 5b 33 ± 4c 69 ± 5a 20 ± 4cde 6.2 ± 0.8e 27 ± 9bcd 5.8 ± 0.6e 22 ± 5 cd 28 ± 4bc

142 ± 37 cd 156 ± 35 cd 178 ± 35cd* 229 ± 10cd* 464 ± 92b* 102 ± 13d* 419 ± 53b* 266 ± 48c* 135 ± 24 cd 855 ± 13a*

135 ± 9bc 145 ± 10b 78 ± 15cde 98 ± 6bcd 27 ± 4ef 11 ± 1f 66 ± 13def 92 ± 9bcd 113 ± 18bcd 274 ± 50a

2.26 ± 0.34bcd 1.68 ± 0.32bcd 3.52 ± 1.02ab 2.21 ± 0.38bcd 2.93 ± 0.80abc* 0.66 ± 0.09d* 1.37 ± 0.24 cd 2.95 ± 0.65abc* 2.09 ± 0.27bcd 4.67 ± 0.68a

1.64 ± 0.16b 1.21 ± 0.07bcd 1.72 ± 0.46b 1.38 ± 0.15bc 0.51 ± 0.11de 0.33 ± 0.06e 1.57 ± 0.31b 0.66 ± 0.08cde 1.20 ± 0.26bcd 3.72 ± 0.43a

Note: Different letters within the same metal (Pb, Zn, or Cd) among the 10 wetland plant species indicates a significant difference under the flooded (F) and non-flooded (N) conditions at P < 0.05.

Furthermore, Pb, Zn, and Cd contents (␮g plant−1 ) of the wetland plant species were generally increased under flooded conditions (Table 7). The enhancement (in terms of % under nonflooded conditions) significantly differed (P < 0.05) between the wetland plant species. 3.5. Correlation analysis Interesting positive correlations were found between rates of ROL and concentrations of Pb, Zn, and Cd on the root surfaces under flooded and non-flooded conditions (Fig. 1). Obvious positive correlations were also found between the rates of ROL and concentrations of Pb, Zn, and Cd on the sand surfaces (plaque in the rhizosphere) in both water treatments (Fig. 2). Significant correlation was observed between the rates of ROL and Fe plaque formation on the root surfaces (plaque on the root surface) and sand surfaces (plaque in the rhizosphere) in both water treatments (Tables S1 and S2). Significant positive correlations were also found between DCBFe, DCB-Mn, DCB-Zn, and DCB-Pb on the root and sand surfaces in both water treatments (Tables S1 and S2). The DCB-Cd on the root surfaces positively correlated with Fe and Mn on the root surfaces under both water treatments and with Fe on the sand surfaces under flooded conditions. 4. Discussion 4.1. ROL under flooded and non-flooded conditions ROL induction by wetland soils is a well-known phenomenon observed in various wetland plant species (Armstrong, 1979). ROL from Taxodium distichum roots is reportedly higher in flooded plants than in non-flooded plants (Kludze et al., 1994). In the present study, ROL rates of the wetland plant species were remarkably higher under flooded conditions than under non-flooded conditions. The enhancement (in terms of % under non-flooded conditions) of ROL significantly (P < 0.05) differed between the wetland plant species, ranging from 52.2% (S. triqueter) to 397% (P. repens). These results suggest that ROL enhancement under flooded conditions is partly due to root porosity change, such as aerenchyma tissue induction under flooded conditions (Jackson and Armstrong, 1999). Tanaka et al. (2005) revealed that ROL shares a significantly positive relationship to aboveground biomass and leaf surface area in Phragmites australis. Liu et al. (2009) reported that biomass of the wetland plant species positively correlates with ROL rates. In the present study, shoot and root biomasses of the wetland plant species significantly (P < 0.05) increased under flooded conditions. Moreover, maintaining a large aboveground

biomass and leaf surface area is crucial to improve concentrations of photosynthetic pigments and efficiency of photosynthesis, and is an important source of oxygen for ROL of Typha orientalis (Sasikala et al., 2009). These results suggest that increment of biomass, particularly leaves, promotes photosynthesis and consequently increases ROL rates from the entire roots of all wetland plants grown in flooded soils.

4.2. Uptake, translocation, and distribution of Pb, Zn, and Cd in the wetland plant species as affected by ROL and Fe plaque under flooded and non-flooded conditions The wetland plant species studied accumulated significantly (P < 0.05) lower Pb, Zn, and Cd concentrations in the shoot tissues comparing to root tissues, irrespective of water treatments (Tables 4–6). Similar results have been reported in T. latifolia and P. australis (Taylor and Crowder, 1983; Ye et al., 1997a,b). The present results also showed that the plants widely differ in their capacity to accumulate Pb, Zn, and Cd (Tables 4–6). Among the wetland plant species, S. triqueter accumulated the lowest Pb (2.1 mg kg−1 ), C. alternifolius accumulated the lowest Zn (27 mg kg−1 ) and Cd (0.15 mg kg−1 ), H. vulgaris accumulated the highest Pb (38 mg kg−1 ) and Zn (526 mg kg−1 ) and P. repens accumulated the highest Cd (0.51 mg kg−1 ) in the shoot tissues under flooded conditions. In the present study, metal (Pb, Zn, and Cd) uptake expressed as content per plant in the wetland plant species significantly increased under flooded conditions (P < 0.05) than under nonflooded conditions. Moreover, the present results showed that concentrations of Fe, Mn, Pb, Zn, and Cd in the plaque on the root surfaces were generally higher under flooded conditions than under non-flooded conditions, which indicated that flooding mainly increased metal accumulation in the roots and Fe plaque on the root surface. Similar results have been reported in some wetland species (Folsom et al., 1988; Gambrell and Patrick, 1989; Vandecasteele et al., 2010). Ye et al. (1998b) indicated that Phragmites seedlings absorbed more amount metal (Pb, Zn, Cd, and Cu) under flooded conditions than under non-flooded conditions. Deng (2005) revealed that C. alternifolius absorbs more amount of Pb and Zn under flooded conditions. Similarly, Kissoon et al. (2010, 2011) and Chen et al. (2012) reported that flooded treatment of wetland plant species significantly increases metal (e.g. Cu, Fe, Mn) content in the roots. Therefore, these results indicate that capacity of wetland plant species to adsorb more mobile metal ions present in soil solution is mainly determined by the total quantity of these ions in the soil, the amount of roots and Fe plaque under flooded conditions (Colmer et al., 1998; Wild, 1988).

300

Flooded condition

200

100

20

40

60

400

300

200

100

0 0

20

40

60 -1

-1

Rate of ROL (mmol O2 kg root d.w. d )

0.6

R N P --------------------0.70 30 <0.01

Flooded condition

Total Zn conc. on root surface (mg kg-1)

50

-1

100

20

-1

40

-1

Rate of ROL (mmol O2 kg root d.w. d )

(mg kg )

150

Total Cd conc. on root surface (mg kg-1)

Total Zn conc. on root surface (mg kg-1)

200

Flooded condition

R N P --------------------0.77 30 <0.01

Non-flooded condition

R N P --------------------0.78 30 <0.01

Rate of ROL (mmol O2 kg-1 root d.w. d-1) 250

61

-1

N P R --------------------0.83 30 <0.01

Total Pb conc. on root surface (mg kg )

Total Pb conc. on root surface (mg kg-1

J. Yang et al. / Ecological Engineering 107 (2017) 56–64

150

Non-flooded condition

R N P --------------------0.70 30 <0.01

100

50

0

20

40

Rate of ROL (mmol O2 kg-1 root d.w. d-1) 0.30

0.25

R N P --------------------0.65 30 <0.01

Non-flooded condition

0.20

0.4 0.15

0.10

0.2

20

40

60

0.05

0

20

40

Fig. 1. Correlations between rates of radial oxygen loss (ROL) and total concentrations of Pb, Zn and Cd on root surfaces of 10 wetland plant species grown in CY soil under flooded (left panels) and non-flooded (right panels) conditions.

4.3. Correlation between rates of ROL, Fe plaque and metal adsorption in Fe plaque In the present data, significant positive correlations were detected between ROL rates and DCB extractable Pb, Zn, Cd, Fe, and Mn on the root surfaces under both flooded and non-flooded conditions. This result indicates that the wetland plant species with higher ROL possess more Fe plaques and metal deposition on the root surfaces. Fe plaque formation promotes the deposition of Zn, Pb, and As on the root surfaces of wetland plant species (Li et al., 2011; Yang et al., 2012; Liu et al., 2013). However, effects of Fe

plaque on metal uptake and translocation by wetland plant species remain unclear (Ye et al., 1998a; Liu et al., 2006; Cheng et al., 2014). Fe plaque formation reduces Pb, Cd, and As uptake and translocation in rice with high ROL rates (Mei et al., 2009; Cheng et al., 2014). By contrast, other studies showed that metal uptake by plants is promoted or unaffected by Fe plaque formation (Ye et al., 1998a; Liu et al., 2006). Fe plaque formation enhances Zn uptake by the roots but may act as a barrier when excessive amounts of Fe are deposited on the root surfaces (Otte et al., 1989; Jacob and Otte 2003).

-1

Flooded condition

R N P --------------------0.76 30 <0.01 150

100

50 20

40

60

Rate of ROL (mmol O2 kg-1 root d.w. d-1) 400

300

Flooded condition

N P R --------------------0.75 30 <0.05

200

100

20

40

60

Total Zn conc. in rhizosphere (mg kg-1)

Total Zn conc. in rhizosphere (mg kg-1)

200

Total Pb conc. in rhizosphere (mg kg )

J. Yang et al. / Ecological Engineering 107 (2017) 56–64

Total Pb conc. in rhizosphere (mg kg-1)

62

150

50

0

250

200

20

40

Rate of ROL (mmol O2 kg-1 root d.w. d-1)

R N P --------------------0.64 30 <0.05

Non-flooded condition

150

100

50

0

20

40

Rate of ROL (mmol O2 kg-1 root d.w. d-1) -1

(mg kg )

Total Cd conc. in rhizosphere (mg kg )

-1

0.15

Non-flooded condition

100

Rate of ROL (mmol O2 kg-1 root d.w. d-1) R N P --------------------0.69 30 <0.01

R N P --------------------0.65 30 <0.05

Flooded condition

0.08

R N P --------------------0.65 30 <0.01

Non-flooded condition

0.06

0.10

0.05

0.04

0.02

Fig. 2. Correlations between rates of radial oxygen loss (ROL) and total concentrations of Pb, Zn and Cd on sand surfaces (rhizosphere) of 10 wetland plant species grown in CY soil under flooded (left panels) and non-flooded (right panels) conditions.

The functions of Fe plaque on metal uptake may highly depend not only on amounts of Fe/Mn deposited on the root surfaces but also on metal bioavailability in the rhizospheres. Generally, metal bioavailability in the rhizospheres of wetland plant species is often controlled by Eh and associated pH in the rhizospheres (Gambrell, 1994). These two properties consequently are influenced by rates of ROL from the roots (Mei et al., 2012; Yang et al., 2012). In the present study, soil pH did not obviously influence metal bioavailability in the rhizospheres of the wetland plant species because overall range of pH was narrow (0.1–0.3). In addition, Eh values remarkably differed in the rhizospheres of the wetland plant species under flooded conditions. This result may be attributed to different rates of ROL and oxidation of Fe(II) in various plants (Davies, 1994). This differ-

ence may cause influx of metals that have an affinity for Fe plaque formation (Otte et al., 1995) in plant roots and subsequent metal accumulation in the rhizosphere (Jacob and Otte, 2003). Bravin et al. (2008) showed that Eh varies temporally and spatially in the rhizosphere of rice. It could alter Fe plaque formation, concurrent with Fe and Mn oxidation in the rhizosphere. Overall, the present and previous results suggest that ROL from the roots plays important roles in formation of Fe plaque on the root surfaces and in the rhizospheres, changes of pH and Eh, and mobility and bioavailability of Pb, Zn, and Cd in the rhizospheres (Cheng et al., 2014; Yang et al., 2014; Liu et al., 2016). In addition, in-depth studies on the roles of Fe plaque formation combined with

J. Yang et al. / Ecological Engineering 107 (2017) 56–64

different characteristics of rhizospheres (e.g. soil organic acids and soil water chemistry) are needed. 5. Conclusions The results clearly indicated that the wetland plant species has higher biomass, ROL rates, Fe plaque formation on the roots and in the rhizospheres, and metal (Pb, Zn, and Cd) contents under flooded conditions than under non-flooded conditions. Furthermore, wetland plant species with higher rates of ROL have more Fe plaques on the root surfaces and in the rhizospheres under flood conditions than under non-flooded conditions. These data indicate that ROL plays important roles in biomass production, Fe plaque formation, and heavy metal adsorption on the root surfaces and in the rhizospheres of wetland plant species under flooded conditions. Therefore, these results suggest the wetland plant species with higher ROL rates, biomass and metal accumulation ability, e.g. C. alternifolius, has the potential for use in phytoremediation of metal-contaminated wetlands. Acknowledgments This research was financially supported by the National Natural Science Foundation of China (Nos. 30570345, 41201312) and Special Funding for Guangxi ‘BaGui scholars’ Construction Projects. Appendix A. Supplementary data Supplementary data associated with cle can be found, in the online http://dx.doi.org/10.1016/j.ecoleng.2017.06.052.

this artiversion, at

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