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Phytoextraction of Risk Elements by Willow and Poplar Trees a
b
b
Lada Kacálková , Pavel Tlustoš & Jiřina Száková a
Department of Biology, Faculty of Science, University of Hradec Králové, Jana Koziny, Hradec Králové, Czech Republic b
Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká Praha Suchdol, Czech Republic Published online: 13 Dec 2014.
Click for updates To cite this article: Lada Kacálková, Pavel Tlustoš & Jiřina Száková (2015) Phytoextraction of Risk Elements by Willow and Poplar Trees, International Journal of Phytoremediation, 17:5, 414-421, DOI: 10.1080/15226514.2014.910171 To link to this article: http://dx.doi.org/10.1080/15226514.2014.910171
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International Journal of Phytoremediation, 17: 414–421, 2015 C Taylor & Francis Group, LLC Copyright ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2014.910171
Phytoextraction of Risk Elements by Willow and Poplar Trees ´ ´ 1, PAVEL TLUSTOSˇ 2, and JIRINA ˇ ´ ´2 LADA KACALKOV A SZAKOV A 1
Department of Biology, Faculty of Science, University of Hradec Kr´alov´e, Jana Koziny, Hradec Kr´alov´e, Czech Republic Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kam´yck´a Praha Suchdol, Czech Republic
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2
To characterize the phytoextraction efficiency of two clones of willow trees (Salix x smithiana Willd., Salix rubens) and two clones of poplar trees (Populus nigra x maximowiczii, Populus nigra Wolterson) were planted in contaminated soil (0.4–2.0 mg Cd.kg−1, 78–313 mg Zn.kg−1, 21.3–118 mg Cu.kg−1). Field experiment was carried out in Czech Republic. The study investigated their ability to accumulate heavy metals (Cd, Zn, and Cu) in harvestable plant parts. The poplars produced higher amount of biomass than willows. Both Salix clones accumulated higher amount of Cd, Zn and Cu in their biomass (maximum 6.8 mg Cd.kg−1, 909 mg Zn.kg−1, and 17.7 mg Cu.kg−1) compared to Populus clones (maximum 2.06 mg Cd.kg−1, 463 mg Zn.kg−1, and 11.8 mg Cu.kg−1). There were no significant differences between clones of individual species. BCs for Cd and Zn were greater than 1 (the highest in willow leaves). BCs values of Cu were very low. These results indicate that Salix is more suitable plant for phytoextraction of Cd and Zn than Populus. The Cu phytoextraction potential of Salix and Populus trees was not confirmed in this experiment due to low soil availability of this element. Keywords: willow, poplar, contaminated soil, phytoextraction, cadmium, zinc, copper
Introduction Environmental pollution with heavy metals is a global disaster mostly related to human activities such as mining, smelting, electroplating, energy and fuel production, intensive agriculture, sludge dumping, and melting operations (Igwe and Abia 2006). While several techniques are available for remediation of soils polluted by organic compounds, only few and poorly developed methods exist for cleaning of heavy metal polluted soils. Heavy metals are non-degradable and generally strongly retained in the soil (Lone et al. 2008). Traditional land remediation techniques are very expensive, and result in deterioration of soil quality. Thus, costeffective alternative techniques, such as phytoremediation have gained acceptance in recent years (Pilon-Smits 2005). Phytoextraction refers to the uptake of contaminants from soil or water by plant roots and their translocation into the shoot, or any other harvestable plant part, to remove contaminants and promote long-term cleanup of soil or wastewater
Address correspondence to Pavel Tlustoˇs, Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kam´yck´a 129, 165 21 Praha 6 – Suchdol, Czech Republic. E-mail: [email protected] Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bijp.
(Sas-Nowosielska et al. 2008). For successful and economically feasible phytoextraction, it is necessary to use plants having a metal bioconcentration factor of 20 and a biomass production of 10 tons per hectare (t.ha−1) or plants with a metal bioconcentration factor of 10 and a biomass production of 20 t.ha−1 (Peuke and Rennenberg 2005). Copper is an essential element that only becomes an ecological hazard when it accumulates to toxic concentrations in the soil following repeated use of Cu-containing pesticides or application of Cu contaminated composts (Owojori et al. 2009). Native zinc concentrations in soils are generally low, total concentration of around 50 mg Zn.kg−1 (Kiekens 1995). At these concentrations Zn is sufficiently taken by plants as essential element for plant metabolism and growth (Marschner 1995). Zinc is the most widespread heavy metal contaminant in wastes arising from industrialized communities (Boardman and McGuire 1990); mixed contamination with other metals is also very frequent (Mertens et al. 2004). Compared with the other heavy metals, cadmium is not an essential nutrient in higher plants (Benavides et al. 2005), and the exposure to relatively low concentrations results in high toxicity to animals (Nedjimi and Daoud 2009). Cadmium contamination is connected with various agricultural, mining and industrial activities and also from the road transportation (Mhatre and Pankhurst 1997). Suitable plants for phytoextraction should possess multiple traits like ability to grow outside their area of collection, fast growth, high biomass production, easy harvest and high
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Phytoextraction of Elements by Trees accumulation of a range of heavy metals in their harvestable parts (Jabeen et al. 2009). The early phytoremediation studies used hyperaccumulator species, which are plants able to accumulate unusually high levels of metal in their tissues (McGrath et al. 1997). The metal accumulation by plants is closely correlated with available than with total soil metal concentrations ´ et al. 2004). (Nolan et al. 2005; Madejon Industrially used energetic plants, e.g., poplar and willow have phytoextraction ability (Banuelos and Ajwa 1999). Willow is a fast growing, productive and deeply rooted tree, well adapted to temperate region climatic conditions, tolerated temporary water-logging (Greger and Landberg 1999). In comparison with hyperaccumulators, trees tend to take up relatively small amounts of heavy metals, but they provide economic return of contaminated land through the production of biomass (Perttu 1995). Recent research has shown that willow has considerable potential for the phytoremediation of heavy metal contaminated land and has the capacity to accumulate elevated levels of Cd and Zn in aboveground biomass compartments (Witters et al. 2009; Rosselli et al. 2003). However, metal concentrations in willows depend on clones, growth performance, root density, distribution within the soil profile and sampling period (Chehregani et al. 2009). Several clones of hybrid poplar have been acknowledged as a hardly, perennial, fast growing, easily propagated, highly tolerant, and widely adapted plants, which could be potentially used as phytoremediation tools in the cadmium contaminated soil (Wan et al. 2008). Comparative studies on metal accumulation and growth demonstrated that different clones respond differently to the exposure to the same industrial waste or contaminants (Sebastiani et al. 2004; Tognetti et al. 2004). The results of Wu et al. (2010) with Populus deltoids x Populus nigra grown in cadmium contaminated purple and alluvial soils partly demonstrated the hypothesis that fast growing plant had the higher remediation efficiency compared to the other slow-growing hyperaccumulators. The objective of the current study was focused on the investigation of the heavy metal (Cd, Zn and Cu) phytoextraction potentials by two willow and two poplar clones in precise field experiment. Clones used in this study were: Salix x smithiana Willd., Salix rubens, Populus nigra x maximowiczii, and Populus nigra Wolterson.
Materials and Methods Small Scale Field Experiment The area of former waste incineration plant in the suburb of Hradec Kralove (Czech Republic) was chosen for the investigation of selected plants. This area was described in Kac´alkov´a et al. (2009). Waste incineration plant functioned between 1993 and 2002. Hazardous wastes were burnt and stored without protection on the mentioned allotment there. Three plots (F3, F4, F5) with different scale and history of contamination were chosen out of the eleven sampling points on the allotment. Three plots with the area of 3 × 3 m were made in our experiment. Individual plot was split for four identical squares and at each squares five plants were planted
415 Table 1. Physico-chemical soil characteristics, total and available metal concentrations in the soils
pH (H2 O) pH (CaCl2 ) Cox (%) Available nutrients after Mehlich 3 (mg.kg−1) P K Mg Total metal concentrations (mg.kg−1) Cd Zn Cu Available metal concentrations 0.11M CH3 COOH (mg.kg−1) Cd Zn Cu Available metal fraction in soil (%) Cd Zn Cu
F3
F4
F5
8.23 7.41 1.9
8.21 7.45 1.6
6.66 6.09 7
133 219 375
118 189 435
1042 966 1416
0.53 96.1 24.4
0.91 124 51.6
1.3 174 80.8
0.17 29.8 0.45
0.21 33.9 0.54
0.19 60.5 0.59
32 31 1.8
23 27 1.05
15 35 0.73
in one row. Totally twenty plants were check for biomass yield and heavy metals content. The size of plot for five plants of one clone was 1 m2. Plants were ordinarily treated (watering, weeding) for two vegetation periods. Every autumn before senescence these plants were harvested. Roots were harvested after second vegetation year. For biomass assessment and risk elements concentration detection only the main massive roots were collected manually using the spade. Fresh plant biomass was weighed. The sampled plants were washed in tap water and deionized water in the order, than separated to leaves and twigs. The root samples (3–5 cm diameter) still having small amounts of adhering soil particles, were separated from the soil and cut in small pieces of approximately 1–2 cm length. Surface-bound mineral particles were removed from roots by three successive super-sonic baths (Millipore water, < 10 μs.cm−1). After drying at the temperature of 60◦ C to constant weight and milled into powder for analyses of heavy metal contents. The plant samples for analyses were prepared mixing five plants from one plot (area of 1 m2). The used soil was collected from the top layer (0–20 cm). The sampled soils were dried in an air-circulating room, than were sieved (4 mm) to remove plant materials and stones. Basic characteristic of soil parameters are summarized in Table 1. Uptake of elements from soil is evaluated by the ratio of element concentration in plants to element concentration in soils and is variously referred to as biological absorption coefficient (BAC), index of bioaccumulation (IBA), transfer factor (TF) and/or bioaccumulation factor (BC). In this discussion, the term bioaccumulation coefficient (BC) will be used. (BC) was calculated: BC = the heavy metal content in the plant’s part / the heavy metal content in the soil (Brooks 1998).
416 For phytoextraction rate the risk element removal by plants will be calculated. The removal is product of dry biomass amount (in terms of soil area 300 m2) and risk element content in plant biomass.
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Analytical Methods All the chemical analyses were provided in analytical laboratories of the Department of Agroenvironmental Chemistry and Plant Nutrition at Czech University of Life Sciences Prague in order to determine the total contents of risk elements. Total element concentrations in soil were determined in the digests obtained by two-step decomposition (Sz´akov´a et al. 1999): 0.5 g of sample was decomposed by dry ashing in a mixture of oxidizing gases (O2 +O3 +NOx ) in an Apion Dry Mode Mineralizer (Tessek, CZ) at 400◦ C for 10 h; the ash was then decomposed in a mixture of HNO3 + HF, evaporated to dryness at 160◦ C and dissolved in diluted Aqua Regia. Plant samples were decomposed using the dry ashing procedure as follows: An aliquot (∼1 g) of the dried and powdered aboveground biomass or roots were weighed to 1 mg into a borosilicate glass test-tube and decomposed in a mixture of oxidizing gases as mentioned above. The ash was dissolved in 20 ml of 1.5% HNO3 (Miholov´a et al. 1993). The total contents of Cd, Cu, and Zn in soil and plant digests were determined by inductively coupled plasma optical emission spectroscopy (ICP-OES) with axial plasma configuration (Varian, VistaPro, Australia). Exchangeable values of pH were measured in a 1:20 (w/v) 0.01 mol.l−1 CaCl2 soluble extract at 20 ± 1◦ C, and active pH values in water extract (ratio 1:3, v/w) at 20 ± 1◦ C. The used pH meter was WTW pH 340 i set.
L. Kac´alkov´a et al. uble with greater portion Cd, Zn and low Cu available content. The highest available amount of Cd, Zn and Cu was in plots F5 and F4 compared to F3.
Biomass Production For both willow and poplar clones performed normal growth and no visual symptoms of site toxicity were observed. Total dry weight production per willow and poplar clones (Table 2) was significantly lower in the first year (2 to 8.9 g per one willow and 0.7 to 13.9 g per one poplar) compared to the second year of this experiment (5 to 11.2 g per one willow and 4 to 35.6 g per one poplar). Average dry weight production per one plant was significantly lower in the F3 plot compared to the other two plots (F4 and F5). The reason of the different willows and poplars biomass production was not obvious from measured parameters. The lower productivity in F3 can not be due to nutritional deficiencies or due to toxic effects (lower observed mobility of risk elements in comparison to the other soils). Willow did achieve lower biomass productions than the poplar trees for all soils under investigation. Significant differences in produced biomass were observed between the Salix and Populus clones. Salix x smithiana Willd. produced higher amount of biomass compared to Salix rubens and Populus nigra Wolterson produced higher amount of biomass compared to P. nigra x maximowiczii. Willows and poplars produced higher amount of leaves compared to twigs in the first year of experiment. However the production of twigs was higher compared to leaves in the second year.
Plant Uptake of Heavy Metals Statistical Analysis Statistical analyses were performed using the software Statistica 10 (analysis of variance - ANOVA, followed by the Tukey HSD test – α = 0.05 for multiple comparisons) and Microsoft Office Excel 2007 (standard deviation).
Results and Discussion Soil Characteristics Table 1 presents the soil properties for three plots (F3, F4, F5) used in this experiment. Tested plots showed elevated total content of all three tested elements in the order F3 < F4 < F5 confirming site contamination by storage of waste materials. According to Regulation No 13/1994 Collection of Laws of Ministry of the Environment provides maximum admissible risk element contents in soil in Czech Republic as follows: 1 mg.kg−1 Cd, 200 mg.kg−1 Zn and 100 mg.kg−1 Cu, only Cd at plot F5 exceeded these limits. Also physico-chemical soil characteristics mainly pH and nutrient concentrations confirmed high heterogeneity. Table 1 also presents the 0.11M CH3 COOH extractable trace element concentration in soil. The extractable fraction presented from 15 till 32% for Cd, from 27 till 35% of Zn and only from 0.7 till 1.8% of Cu. These results indicate that contaminants were partly acid sol-
Table 3 presents Cd and Zn concentrations in leaves, twigs and roots of Salix and Populus trees. The highest average amount of Cd and Zn is in willow leaves (from 5.16 to 8.18 mg Cd.kg−1 and from 748 to 1050 mg Zn.kg−1). Similarly, Vyslouˇzilov´a et al. (2003) and Kac´alkov´a et al. (2009) found out higher Cd and Zn concentration in leaves of willow than in its annual shoots. Salix x smithiana Willd. accumulated 8.15 mg Cd.kg−1 and 1020 mg Zn.kg−1 in our experiment. Higher amount of Cd and Zn in leaves of S. smithiana demonstrated Wieshammer et al. (2007). They published 250 mg Cd.kg−1 and 3300 mg Zn.kg−1 in willow leaves but in case of much higher soil concentration – 13.4. mg Cd.kg−1 and 955 mg Zn.kg−1. Tlustoˇs et al. (2007) found out higher Cd and Zn concentrations in willow leaves (Salix x rubens) – maximum 89.3 mg Cd.kg−1 and 3059 mg Zn.kg−1. In our experiment leaves of Salix rubens contained 7.26 mg Cd.kg−1 and 1050 mg Zn.kg−1. There were no significant differences between Zn and Cd accumulation in Salix rubens and S. smithiana. The results were not significantly affected by cadmium and zinc levels in soil which corresponded with similar amount extracted by acetic acid at all sites. Cadmium and zinc concentrations in particular poplar parts decreased in the order: leaves > twigs > roots. Only copper was accumulated in higher concentration in twigs compared to leaves. Similarly, Brunner et al. (2008) described higher Zn and Cd concentrations in leaves of Populus
Phytoextraction of Elements by Trees
417
Table 2. Biomass production of willow and poplar clones (per one plant). Different letters correspond to significant differences (P < 0.05) between clones (a,b) Biomass (g DW) Site F3
Plant W1
P1
F4
W1
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P1
F5
W1
P1
twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots
Biomass (g DW)
1st year
2nd year
Plant
1.7 ± 0.87a 3.3 ± 1.18a — 3.6 ± 0.7a 10.2 ± 3b — 4.04 ± 0.3a 6 ± 0.1b — 12.6 ± 4b 22.1 ± 6.4c — 5.1 ± 4.2b 7.1 ± 4.9b — 2.9 ± 0.5a 6.7 ± 0.7b —
9.2 ± 6.2a 3.2 ± 0.9a 2.4 ± 0.15a 10.9 ± 0.9b 9.5 ± 1.3b 3.6 ± 1.5a 9.8 ± 2.9b 5.9 ± 2a 1.9 ± 0.3a 35.9 ± 19c 23.9 ± 12c 5.9 ± 1.9b 9.8 ± 6.1b 5.7 ± 3.9a 4 ± 1a 10.7 ± 0.05b 11.2 ± 0.65b 4.9 ± 1.4b
W2
P2
W2
P2
W2
P2
twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots
1st year
2nd year
4.03 ± 0.15a 6.2 ± 0.3b — 0.46 ± 0.4a 1.4 ± 0.1a — 15.1 ± 5b 14.7 ± 3.8b — 2.3 ± 1a 4.1 ± 1.5a — 10.6 ± 2.8b 13.7 ± 3b — 4.8 ± 1.2b 7.8 ± 0.5b —
25.5 ± 6.2c 12.7 ± 4.4b 2.5 ± 0.05a 3.9 ± 2.8a 4.1 ± 3.1a 2.4 ± 0.35a 7.2 ± 0.6a 3.5 ± 0.1a 6.4 ± 4b 24.2 ± 21c 16.9 ± 14b 2.2 ± 0.35a 16.2 ± 4.1b 9.8 ± 3.4b 2.3 ± 0.65a 23.5 ± 3.7c 19.4 ± 4.1c 2.2 ± 0.16a
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
tremula compared to wood. The privileged accumulation of heavy metals in harvesting organs (i.e. woody structures of stem and branches) rather than in leaves, which return metals to ground annually due to shedding, is an important selective criterion for a phytoremediation species. The highest amount of Zn and Cd accumulated leaves of Populus nigra x maximowiczii (3.03 mg Cd.kg−1 and 561 mg Zn.kg−1). Copper concentration in tested plants was significantly higher in willows than in poplars (maximum 17.7 mg Cu.kg−1 in twigs of Salix rubens). Cd concentration in tested plants was affected by available amount of this element (higher Cd accumulation in plot F3 compared to F5). This tendency was not confirmed in case of Zn a Cu plant accumulation. Lower Cd and Zn contents in aboveground biomass of poplars in comparison with willows are in agreement with results of Robinson et al. (2000). Our results are not in accordance with Fern`andez et al. (2012). They analyzed two poplar clones (Populus deltoides x maximowiczii and P. x canadiensis euramericana) and found out that zinc was mainly accumulated in roots (40 000 mg Zn.kg−1) and zinc concentration in the various organs increased with increasing Zn content. Also Sebastiani et al. (2004) tested these two poplar clones and they reported that Zn was actively transported and accumulated in leaves of both clones, while Cu was almost entirely confined to roots. Punshon and Dickinson (1997) reported for Salix clones the magnitude of Cu accumulation in decreasing order: roots, wood, new stem and leaves. Greger and Landberg (1999) noticed that Cu concentrations in roots of Salix viminalis L. clones were at least 30 times greater than in shoots, indicating poor translocation potentials. Also Chen et al. (2012) demonstrated significantly higher amount of Cu in roots of willows
(Salix jiangsuensis and S. babylonica) compared to stems and leaves. Our results are not in agreement with this and other studies, e.g. Punshon et al. (1995), Rosselli et al. (2003). We found that most of Cu was localized in twigs and Cu accumulation in Salix and Populus clones decreased in order: twigs, leaves and roots. Nevertheless, the metal accumulation in response to Cu are strictly dependent on species and clones (Punshon et al. 1995). The extraction capacity of a plant is typically expressed on the basis of total soil metal concentrations (Mertens et al. 2005). BCs for Cd and Zn were generally greater than 1 (Table 4). BCs for Cd were 13.7 and 15.4 and for Zn 10.9 and 10.6 in willow leaves. These results indicate that Salix clones are more suitable plant for phytoextraction of Cd and Zn than Populus clones and all tested trees are not suitable for phytoextraction of Cu maximum BC 0.72 for Salix rubens. Also Laidlaw et al. (2012) demonstrated that the willows are effective in extracting Cd and Zn, the most readily available metals in the soil and copper is extracted to a lesser degree in the harvested biomass. Higher bioaccumulation coefficient for Cd (BC = 7) in Salix smithiana leaves demonstrated Wieshammer et al. (2007). However for Zn was the bioaccumulation coefficient only 3 in their study. BCs for Cd, Zn, and Cu were not affected of total soil concentrations in our experiment. While lower BCs for Cd and Zn on polluted soils found for several willow clones Vandecasteele et al. (2004) and Meers et al. (2003). Trees differ in their ability to translocate heavy metals from the roots to the shoots. Trees have massive root systems, which help to bind the soil (Stomp et al. 1993). Heavy metals have different patterns of behavior and mobility within a tree. Lead,
418 1.74 ± 0.61aB 3.05 ± 1.21bB 5.32 ± 2.03cA 1.28 ± 0.28aA 4.16 ± 2.43bA 7.31 ± 3.45cB 0.63 ± 0.05aA 1.66 ± 1.21aA 1.85 ± 1.1aA 0.88 ± 0.01aA 1.44 ± 0.5aA 1.77 ± 0.83aA
0.65 ± 0.11aA 3.98 ± 0.96bB 7.26 ± 2.75cB 1.83 ± 0.99aA 3.65 ± 0.85bA 8.18 ± 2.99aB 0.42 ± 0.14aA 1.71 ± 0.7aA 3.03 ± 1.57bB 0.76 ± 0.13aA 1.39 ± 0.44aA 1.83 ± 0.91aA
roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves
W1
0.46 ± 0.11aA 2.47 ± 1.26bA 5.16 ± 2.36cA 3.17 ± 2.38cB 3.27 ± 1.41bA 5.23 ± 2.15cA 0.71 ± 0.11aA 1.69 ± 0.64aA 2.1 ± 1.01aA 0.69 ± 0.08aA 1.16 ± 0.16aA 1.38 ± 0.25aA
F5 55 ± 6.67aB 330 ± 59.8bA 1050 ± 300cB 51.9 ± 3.45aA 316 ± 74bA 1020 ± 266cB 45.6 ± 9.38aB 163 ± 56.5bA 561 ± 307cA 62 ± 7.72aA 199 ± 41.5bA 538 ± 215cA
F3 53.8 ± 8.19aB 212 ± 61.8bA 851 ± 221cA 67.7 ± 4.13aA 358 ± 131bA 794 ± 146cA 28.5 ± 1.57aA 149 ± 35.8bA 461 ± 264cA 53.2 ± 9.32aA 206 ± 41.6bA 445 ± 148cA
F4
Zn
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
P2
P1
W2
F4
F3
Soil →
Cd
Plants ↓
Risk elements
33.9 ± 11.6aA 262 ± 145bA 1012 ± 303cB 58.1 ± 3.68aA 319 ± 133bA 748 ± 206cA 43.4 ± 4.7aB 184 ± 33.4bA 524 ± 163cA 49.9 ± 0.2aA 194 ± 11.3bA 529 ± 154cA
F5
9 ± 2.2a A 17.7 ± 0.3bA 11 ± 1.1a 7 ± 0.5aA 11.7 ± 0.1aA 12.3 ± 0.7b 5.3 ± 0.4aA 8.63 ± 0.1aA 7.5 ± 0.5aA 5.5 ± 0.8aA 9.1 ± 1.2aA 8.2 ± 0.3aA
F3
9.1 ± 1.9a A 11.7 ± 2bA 8.9 ± 1.4a 9.4 ± 0.3aA 11 ± 1.1bA 9.7 ± 0.6 4.8 ± 0.3aA 9.4 ± 0.5bA 8.2 ± 0.1aA 6.4 ± 0.3aA 11 ± 0.1bA 6.8 ± 0.5aA
F4
Cu
8.9 ± 3.7bA 13.1 ± 2bA 12.2 ± 1.4b 8.1 ± 2.2aA 12.6 ± 2.6bA 10.5 ± 1.4b 5 ± 1.2aA 10.8 ± 1.5bA 6.6 ± 0.4aA 4.8 ± 0.3aA 11.8 ± 1.2bA 8.4 ± 1.5aA
F5
Table 3. Cd and Zn concentration in particular parts of willows and poplars (mg.kg−1). The values marked by the same letter did not significantly differ at α = 0.05 within individual columns where the capital letters indicate the differences among the individual locations and small letters indicate the differences in element contents within one plant
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419
Table 4. Bioaccumulation coefficients (BCs) of the willow and poplar clones
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F3
W1 Cd Zn Cu W2 Cd Zn Cu P1 Cd Zn Cu P2 Cd Zn Cu
F4
F5
roots
twigs
leaves
roots
twigs
leaves
roots
twigs
leaves
1.18 0.57 0.37
7.5 3.43 0.72
13.7 10.9 0.45
1.91 0.44 0.18
3.35 1.72 0.23
5.85 6.88 0.17
0.35 0.2 0.11
1.9 1,51 0.17
3.97 5.83 0.15
3.5 0.54 0.29
6.9 3.29 0.48
15.4 10.6 0.5
1.41 0.55 0.18
4.57 2.89 0.22
8.03 6.42 0.19
2.44 0.33 0.1
2.52 1.84 0.16
4.02 4.31 0.13
0.8 0.48 0.22
3.23 1.7 0.35
5.72 5.84 0.3
0.69 0.23 0.09
1.82 1.2 0.18
2.03 3.73 0.16
0.55 0.25 0.06
1.3 1.06 0.13
1.62 3.02 0.08
1.43 0.65 0.22
2.62 2.1 0.3
3.45 5.6 0.1
0.97 0.43 0.12
1.58 1.66 0.22
1.95 3.6 0.13
0.53 0.29 0.06
0.89 1.12 0.15
1.06 3.1 0.1
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
chromium, and copper tend to be immobilized and held primarily in the roots, whereas Cd, Ni, and Zn are more easily translocated to the aerial tissues (Pulford and Watson 2003). Several authors, for example Vacul´ık et al. (2012), mentioned higher accumulation of Cd and Zn in leaves compared to roots of Salix (strictly S. caprea in their research). Hu et al. (2013) demonstrated the greatest accumulation of Cd and Zn in the leaves of P. pyramidalis as well, while Cu and Pb were mainly accumulated in the roots. However our results of risk elements accumulation in willow and poplar trees grown on that polluted soils are opposed (higher Cd and Zn concentration in roots compared to leaves). The potential role of different type of used soil and contamination level, and used clones can be taken into account. Differential patterns among species and clones of Salicaceae in accumulating Cd within the root profile demonstrated also Cocozza et al. (2011) and higher average Cd concentrations (4.4–12.2 mg.kg−1) in roots compared to leaves (5.0–8.8 mg.kg−1) mentioned Meers et al. (2005) for Salix alba viminalis “Orm”. The Cd and Zn concentrations in the order of root > leaf > stem, regardless of the willows species described as well Han et al. (2013).
Fig. 1. Removal of cadmium by trees (in mg.m−2)
Risk Elements Removal by Trees Relative removal of cadmium, zinc and copper within two years at plot F5 (with the highest amount of these risk elements) and at plot F3 (with the lowest amount of these risk elements) are displayed in Figures 1–3. Metal removal is influenced by two factors – the content of the element in particular above ground plant parts and by the yield of aboveground dry biomass (Tlustoˇs et al. 2006). Among metals studied, Cd is considered the most crucial element because of high toxicity and leachability (Merrington and Alloway 1994). The highest cadmium removal was found by W2 (Salix smithiana). This willow clone accumulated 33.6 mg Cd.m−2 twice more than in W1 (Salix rubens). Majority of cadmium was removed by aboveground biomass of trees (82–97% of removed Cd). Several studies have shown that Salix spp. exhibit the capacity to accumulate high levels of Cd and Zn (e.g., Meers et al. 2003; Hammer et al. 2003). This corresponds well with our findings. Zinc and copper are essential trace elements for plant. Zinc removal by used trees was much higher compared to copper removal. Salix smithiana removed the highest amount of
Fig. 2. Removal of zinc by trees (in mg.m−2)
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Fig. 3. Removal of copper by trees (in mg.m−2) W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
Zn (maximum 3956 mg.m−2) and Cu (maximum 93 mg.m−2) again. Percentage Zn removal by aboveground biomass of trees was 92-99% of total Zn removed. The highest roots portion of removed risk elements was found only in case of copper (61% of removed Cu). No significant effect of Salix clones or soil concentrations for Cu uptake demonstrated also Vandecasteele et al. (2005) in a greenhouse pot experiment with Salix fragilis and Salix viminalis.
Conclusions In our experiment, Cd, Zn, and Cu removal by willows and poplars clones positively correlated with biomass production. However, as concluded also by Tlustoˇs et al. (2007), the differences in element accumulation among the clones were affected more by the properties of clones than by the soil properties. Removal of Cd and Zn was highest by Salix smithiana regardless of site, and mentioned clone is suitable for phytoextraction, Cu was firmly bound to soil and its plant accumulation was insufficient.
Funding This research was supported by the specific research No 2103/2013 project from the University of Hradec Kr´alov´e and by TACR project BROZEN No TA01020366.
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International Journal of Phytoremediation Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/bijp20
Phytoextraction of Risk Elements by Willow and Poplar Trees a
b
b
Lada Kacálková , Pavel Tlustoš & Jiřina Száková a
Department of Biology, Faculty of Science, University of Hradec Králové, Jana Koziny, Hradec Králové, Czech Republic b
Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká Praha Suchdol, Czech Republic Published online: 13 Dec 2014.
Click for updates To cite this article: Lada Kacálková, Pavel Tlustoš & Jiřina Száková (2015) Phytoextraction of Risk Elements by Willow and Poplar Trees, International Journal of Phytoremediation, 17:5, 414-421, DOI: 10.1080/15226514.2014.910171 To link to this article: http://dx.doi.org/10.1080/15226514.2014.910171
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International Journal of Phytoremediation, 17: 414–421, 2015 C Taylor & Francis Group, LLC Copyright ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2014.910171
Phytoextraction of Risk Elements by Willow and Poplar Trees ´ ´ 1, PAVEL TLUSTOSˇ 2, and JIRINA ˇ ´ ´2 LADA KACALKOV A SZAKOV A 1
Department of Biology, Faculty of Science, University of Hradec Kr´alov´e, Jana Koziny, Hradec Kr´alov´e, Czech Republic Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kam´yck´a Praha Suchdol, Czech Republic
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2
To characterize the phytoextraction efficiency of two clones of willow trees (Salix x smithiana Willd., Salix rubens) and two clones of poplar trees (Populus nigra x maximowiczii, Populus nigra Wolterson) were planted in contaminated soil (0.4–2.0 mg Cd.kg−1, 78–313 mg Zn.kg−1, 21.3–118 mg Cu.kg−1). Field experiment was carried out in Czech Republic. The study investigated their ability to accumulate heavy metals (Cd, Zn, and Cu) in harvestable plant parts. The poplars produced higher amount of biomass than willows. Both Salix clones accumulated higher amount of Cd, Zn and Cu in their biomass (maximum 6.8 mg Cd.kg−1, 909 mg Zn.kg−1, and 17.7 mg Cu.kg−1) compared to Populus clones (maximum 2.06 mg Cd.kg−1, 463 mg Zn.kg−1, and 11.8 mg Cu.kg−1). There were no significant differences between clones of individual species. BCs for Cd and Zn were greater than 1 (the highest in willow leaves). BCs values of Cu were very low. These results indicate that Salix is more suitable plant for phytoextraction of Cd and Zn than Populus. The Cu phytoextraction potential of Salix and Populus trees was not confirmed in this experiment due to low soil availability of this element. Keywords: willow, poplar, contaminated soil, phytoextraction, cadmium, zinc, copper
Introduction Environmental pollution with heavy metals is a global disaster mostly related to human activities such as mining, smelting, electroplating, energy and fuel production, intensive agriculture, sludge dumping, and melting operations (Igwe and Abia 2006). While several techniques are available for remediation of soils polluted by organic compounds, only few and poorly developed methods exist for cleaning of heavy metal polluted soils. Heavy metals are non-degradable and generally strongly retained in the soil (Lone et al. 2008). Traditional land remediation techniques are very expensive, and result in deterioration of soil quality. Thus, costeffective alternative techniques, such as phytoremediation have gained acceptance in recent years (Pilon-Smits 2005). Phytoextraction refers to the uptake of contaminants from soil or water by plant roots and their translocation into the shoot, or any other harvestable plant part, to remove contaminants and promote long-term cleanup of soil or wastewater
Address correspondence to Pavel Tlustoˇs, Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kam´yck´a 129, 165 21 Praha 6 – Suchdol, Czech Republic. E-mail: [email protected] Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bijp.
(Sas-Nowosielska et al. 2008). For successful and economically feasible phytoextraction, it is necessary to use plants having a metal bioconcentration factor of 20 and a biomass production of 10 tons per hectare (t.ha−1) or plants with a metal bioconcentration factor of 10 and a biomass production of 20 t.ha−1 (Peuke and Rennenberg 2005). Copper is an essential element that only becomes an ecological hazard when it accumulates to toxic concentrations in the soil following repeated use of Cu-containing pesticides or application of Cu contaminated composts (Owojori et al. 2009). Native zinc concentrations in soils are generally low, total concentration of around 50 mg Zn.kg−1 (Kiekens 1995). At these concentrations Zn is sufficiently taken by plants as essential element for plant metabolism and growth (Marschner 1995). Zinc is the most widespread heavy metal contaminant in wastes arising from industrialized communities (Boardman and McGuire 1990); mixed contamination with other metals is also very frequent (Mertens et al. 2004). Compared with the other heavy metals, cadmium is not an essential nutrient in higher plants (Benavides et al. 2005), and the exposure to relatively low concentrations results in high toxicity to animals (Nedjimi and Daoud 2009). Cadmium contamination is connected with various agricultural, mining and industrial activities and also from the road transportation (Mhatre and Pankhurst 1997). Suitable plants for phytoextraction should possess multiple traits like ability to grow outside their area of collection, fast growth, high biomass production, easy harvest and high
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Phytoextraction of Elements by Trees accumulation of a range of heavy metals in their harvestable parts (Jabeen et al. 2009). The early phytoremediation studies used hyperaccumulator species, which are plants able to accumulate unusually high levels of metal in their tissues (McGrath et al. 1997). The metal accumulation by plants is closely correlated with available than with total soil metal concentrations ´ et al. 2004). (Nolan et al. 2005; Madejon Industrially used energetic plants, e.g., poplar and willow have phytoextraction ability (Banuelos and Ajwa 1999). Willow is a fast growing, productive and deeply rooted tree, well adapted to temperate region climatic conditions, tolerated temporary water-logging (Greger and Landberg 1999). In comparison with hyperaccumulators, trees tend to take up relatively small amounts of heavy metals, but they provide economic return of contaminated land through the production of biomass (Perttu 1995). Recent research has shown that willow has considerable potential for the phytoremediation of heavy metal contaminated land and has the capacity to accumulate elevated levels of Cd and Zn in aboveground biomass compartments (Witters et al. 2009; Rosselli et al. 2003). However, metal concentrations in willows depend on clones, growth performance, root density, distribution within the soil profile and sampling period (Chehregani et al. 2009). Several clones of hybrid poplar have been acknowledged as a hardly, perennial, fast growing, easily propagated, highly tolerant, and widely adapted plants, which could be potentially used as phytoremediation tools in the cadmium contaminated soil (Wan et al. 2008). Comparative studies on metal accumulation and growth demonstrated that different clones respond differently to the exposure to the same industrial waste or contaminants (Sebastiani et al. 2004; Tognetti et al. 2004). The results of Wu et al. (2010) with Populus deltoids x Populus nigra grown in cadmium contaminated purple and alluvial soils partly demonstrated the hypothesis that fast growing plant had the higher remediation efficiency compared to the other slow-growing hyperaccumulators. The objective of the current study was focused on the investigation of the heavy metal (Cd, Zn and Cu) phytoextraction potentials by two willow and two poplar clones in precise field experiment. Clones used in this study were: Salix x smithiana Willd., Salix rubens, Populus nigra x maximowiczii, and Populus nigra Wolterson.
Materials and Methods Small Scale Field Experiment The area of former waste incineration plant in the suburb of Hradec Kralove (Czech Republic) was chosen for the investigation of selected plants. This area was described in Kac´alkov´a et al. (2009). Waste incineration plant functioned between 1993 and 2002. Hazardous wastes were burnt and stored without protection on the mentioned allotment there. Three plots (F3, F4, F5) with different scale and history of contamination were chosen out of the eleven sampling points on the allotment. Three plots with the area of 3 × 3 m were made in our experiment. Individual plot was split for four identical squares and at each squares five plants were planted
415 Table 1. Physico-chemical soil characteristics, total and available metal concentrations in the soils
pH (H2 O) pH (CaCl2 ) Cox (%) Available nutrients after Mehlich 3 (mg.kg−1) P K Mg Total metal concentrations (mg.kg−1) Cd Zn Cu Available metal concentrations 0.11M CH3 COOH (mg.kg−1) Cd Zn Cu Available metal fraction in soil (%) Cd Zn Cu
F3
F4
F5
8.23 7.41 1.9
8.21 7.45 1.6
6.66 6.09 7
133 219 375
118 189 435
1042 966 1416
0.53 96.1 24.4
0.91 124 51.6
1.3 174 80.8
0.17 29.8 0.45
0.21 33.9 0.54
0.19 60.5 0.59
32 31 1.8
23 27 1.05
15 35 0.73
in one row. Totally twenty plants were check for biomass yield and heavy metals content. The size of plot for five plants of one clone was 1 m2. Plants were ordinarily treated (watering, weeding) for two vegetation periods. Every autumn before senescence these plants were harvested. Roots were harvested after second vegetation year. For biomass assessment and risk elements concentration detection only the main massive roots were collected manually using the spade. Fresh plant biomass was weighed. The sampled plants were washed in tap water and deionized water in the order, than separated to leaves and twigs. The root samples (3–5 cm diameter) still having small amounts of adhering soil particles, were separated from the soil and cut in small pieces of approximately 1–2 cm length. Surface-bound mineral particles were removed from roots by three successive super-sonic baths (Millipore water, < 10 μs.cm−1). After drying at the temperature of 60◦ C to constant weight and milled into powder for analyses of heavy metal contents. The plant samples for analyses were prepared mixing five plants from one plot (area of 1 m2). The used soil was collected from the top layer (0–20 cm). The sampled soils were dried in an air-circulating room, than were sieved (4 mm) to remove plant materials and stones. Basic characteristic of soil parameters are summarized in Table 1. Uptake of elements from soil is evaluated by the ratio of element concentration in plants to element concentration in soils and is variously referred to as biological absorption coefficient (BAC), index of bioaccumulation (IBA), transfer factor (TF) and/or bioaccumulation factor (BC). In this discussion, the term bioaccumulation coefficient (BC) will be used. (BC) was calculated: BC = the heavy metal content in the plant’s part / the heavy metal content in the soil (Brooks 1998).
416 For phytoextraction rate the risk element removal by plants will be calculated. The removal is product of dry biomass amount (in terms of soil area 300 m2) and risk element content in plant biomass.
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Analytical Methods All the chemical analyses were provided in analytical laboratories of the Department of Agroenvironmental Chemistry and Plant Nutrition at Czech University of Life Sciences Prague in order to determine the total contents of risk elements. Total element concentrations in soil were determined in the digests obtained by two-step decomposition (Sz´akov´a et al. 1999): 0.5 g of sample was decomposed by dry ashing in a mixture of oxidizing gases (O2 +O3 +NOx ) in an Apion Dry Mode Mineralizer (Tessek, CZ) at 400◦ C for 10 h; the ash was then decomposed in a mixture of HNO3 + HF, evaporated to dryness at 160◦ C and dissolved in diluted Aqua Regia. Plant samples were decomposed using the dry ashing procedure as follows: An aliquot (∼1 g) of the dried and powdered aboveground biomass or roots were weighed to 1 mg into a borosilicate glass test-tube and decomposed in a mixture of oxidizing gases as mentioned above. The ash was dissolved in 20 ml of 1.5% HNO3 (Miholov´a et al. 1993). The total contents of Cd, Cu, and Zn in soil and plant digests were determined by inductively coupled plasma optical emission spectroscopy (ICP-OES) with axial plasma configuration (Varian, VistaPro, Australia). Exchangeable values of pH were measured in a 1:20 (w/v) 0.01 mol.l−1 CaCl2 soluble extract at 20 ± 1◦ C, and active pH values in water extract (ratio 1:3, v/w) at 20 ± 1◦ C. The used pH meter was WTW pH 340 i set.
L. Kac´alkov´a et al. uble with greater portion Cd, Zn and low Cu available content. The highest available amount of Cd, Zn and Cu was in plots F5 and F4 compared to F3.
Biomass Production For both willow and poplar clones performed normal growth and no visual symptoms of site toxicity were observed. Total dry weight production per willow and poplar clones (Table 2) was significantly lower in the first year (2 to 8.9 g per one willow and 0.7 to 13.9 g per one poplar) compared to the second year of this experiment (5 to 11.2 g per one willow and 4 to 35.6 g per one poplar). Average dry weight production per one plant was significantly lower in the F3 plot compared to the other two plots (F4 and F5). The reason of the different willows and poplars biomass production was not obvious from measured parameters. The lower productivity in F3 can not be due to nutritional deficiencies or due to toxic effects (lower observed mobility of risk elements in comparison to the other soils). Willow did achieve lower biomass productions than the poplar trees for all soils under investigation. Significant differences in produced biomass were observed between the Salix and Populus clones. Salix x smithiana Willd. produced higher amount of biomass compared to Salix rubens and Populus nigra Wolterson produced higher amount of biomass compared to P. nigra x maximowiczii. Willows and poplars produced higher amount of leaves compared to twigs in the first year of experiment. However the production of twigs was higher compared to leaves in the second year.
Plant Uptake of Heavy Metals Statistical Analysis Statistical analyses were performed using the software Statistica 10 (analysis of variance - ANOVA, followed by the Tukey HSD test – α = 0.05 for multiple comparisons) and Microsoft Office Excel 2007 (standard deviation).
Results and Discussion Soil Characteristics Table 1 presents the soil properties for three plots (F3, F4, F5) used in this experiment. Tested plots showed elevated total content of all three tested elements in the order F3 < F4 < F5 confirming site contamination by storage of waste materials. According to Regulation No 13/1994 Collection of Laws of Ministry of the Environment provides maximum admissible risk element contents in soil in Czech Republic as follows: 1 mg.kg−1 Cd, 200 mg.kg−1 Zn and 100 mg.kg−1 Cu, only Cd at plot F5 exceeded these limits. Also physico-chemical soil characteristics mainly pH and nutrient concentrations confirmed high heterogeneity. Table 1 also presents the 0.11M CH3 COOH extractable trace element concentration in soil. The extractable fraction presented from 15 till 32% for Cd, from 27 till 35% of Zn and only from 0.7 till 1.8% of Cu. These results indicate that contaminants were partly acid sol-
Table 3 presents Cd and Zn concentrations in leaves, twigs and roots of Salix and Populus trees. The highest average amount of Cd and Zn is in willow leaves (from 5.16 to 8.18 mg Cd.kg−1 and from 748 to 1050 mg Zn.kg−1). Similarly, Vyslouˇzilov´a et al. (2003) and Kac´alkov´a et al. (2009) found out higher Cd and Zn concentration in leaves of willow than in its annual shoots. Salix x smithiana Willd. accumulated 8.15 mg Cd.kg−1 and 1020 mg Zn.kg−1 in our experiment. Higher amount of Cd and Zn in leaves of S. smithiana demonstrated Wieshammer et al. (2007). They published 250 mg Cd.kg−1 and 3300 mg Zn.kg−1 in willow leaves but in case of much higher soil concentration – 13.4. mg Cd.kg−1 and 955 mg Zn.kg−1. Tlustoˇs et al. (2007) found out higher Cd and Zn concentrations in willow leaves (Salix x rubens) – maximum 89.3 mg Cd.kg−1 and 3059 mg Zn.kg−1. In our experiment leaves of Salix rubens contained 7.26 mg Cd.kg−1 and 1050 mg Zn.kg−1. There were no significant differences between Zn and Cd accumulation in Salix rubens and S. smithiana. The results were not significantly affected by cadmium and zinc levels in soil which corresponded with similar amount extracted by acetic acid at all sites. Cadmium and zinc concentrations in particular poplar parts decreased in the order: leaves > twigs > roots. Only copper was accumulated in higher concentration in twigs compared to leaves. Similarly, Brunner et al. (2008) described higher Zn and Cd concentrations in leaves of Populus
Phytoextraction of Elements by Trees
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Table 2. Biomass production of willow and poplar clones (per one plant). Different letters correspond to significant differences (P < 0.05) between clones (a,b) Biomass (g DW) Site F3
Plant W1
P1
F4
W1
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P1
F5
W1
P1
twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots
Biomass (g DW)
1st year
2nd year
Plant
1.7 ± 0.87a 3.3 ± 1.18a — 3.6 ± 0.7a 10.2 ± 3b — 4.04 ± 0.3a 6 ± 0.1b — 12.6 ± 4b 22.1 ± 6.4c — 5.1 ± 4.2b 7.1 ± 4.9b — 2.9 ± 0.5a 6.7 ± 0.7b —
9.2 ± 6.2a 3.2 ± 0.9a 2.4 ± 0.15a 10.9 ± 0.9b 9.5 ± 1.3b 3.6 ± 1.5a 9.8 ± 2.9b 5.9 ± 2a 1.9 ± 0.3a 35.9 ± 19c 23.9 ± 12c 5.9 ± 1.9b 9.8 ± 6.1b 5.7 ± 3.9a 4 ± 1a 10.7 ± 0.05b 11.2 ± 0.65b 4.9 ± 1.4b
W2
P2
W2
P2
W2
P2
twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves roots
1st year
2nd year
4.03 ± 0.15a 6.2 ± 0.3b — 0.46 ± 0.4a 1.4 ± 0.1a — 15.1 ± 5b 14.7 ± 3.8b — 2.3 ± 1a 4.1 ± 1.5a — 10.6 ± 2.8b 13.7 ± 3b — 4.8 ± 1.2b 7.8 ± 0.5b —
25.5 ± 6.2c 12.7 ± 4.4b 2.5 ± 0.05a 3.9 ± 2.8a 4.1 ± 3.1a 2.4 ± 0.35a 7.2 ± 0.6a 3.5 ± 0.1a 6.4 ± 4b 24.2 ± 21c 16.9 ± 14b 2.2 ± 0.35a 16.2 ± 4.1b 9.8 ± 3.4b 2.3 ± 0.65a 23.5 ± 3.7c 19.4 ± 4.1c 2.2 ± 0.16a
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
tremula compared to wood. The privileged accumulation of heavy metals in harvesting organs (i.e. woody structures of stem and branches) rather than in leaves, which return metals to ground annually due to shedding, is an important selective criterion for a phytoremediation species. The highest amount of Zn and Cd accumulated leaves of Populus nigra x maximowiczii (3.03 mg Cd.kg−1 and 561 mg Zn.kg−1). Copper concentration in tested plants was significantly higher in willows than in poplars (maximum 17.7 mg Cu.kg−1 in twigs of Salix rubens). Cd concentration in tested plants was affected by available amount of this element (higher Cd accumulation in plot F3 compared to F5). This tendency was not confirmed in case of Zn a Cu plant accumulation. Lower Cd and Zn contents in aboveground biomass of poplars in comparison with willows are in agreement with results of Robinson et al. (2000). Our results are not in accordance with Fern`andez et al. (2012). They analyzed two poplar clones (Populus deltoides x maximowiczii and P. x canadiensis euramericana) and found out that zinc was mainly accumulated in roots (40 000 mg Zn.kg−1) and zinc concentration in the various organs increased with increasing Zn content. Also Sebastiani et al. (2004) tested these two poplar clones and they reported that Zn was actively transported and accumulated in leaves of both clones, while Cu was almost entirely confined to roots. Punshon and Dickinson (1997) reported for Salix clones the magnitude of Cu accumulation in decreasing order: roots, wood, new stem and leaves. Greger and Landberg (1999) noticed that Cu concentrations in roots of Salix viminalis L. clones were at least 30 times greater than in shoots, indicating poor translocation potentials. Also Chen et al. (2012) demonstrated significantly higher amount of Cu in roots of willows
(Salix jiangsuensis and S. babylonica) compared to stems and leaves. Our results are not in agreement with this and other studies, e.g. Punshon et al. (1995), Rosselli et al. (2003). We found that most of Cu was localized in twigs and Cu accumulation in Salix and Populus clones decreased in order: twigs, leaves and roots. Nevertheless, the metal accumulation in response to Cu are strictly dependent on species and clones (Punshon et al. 1995). The extraction capacity of a plant is typically expressed on the basis of total soil metal concentrations (Mertens et al. 2005). BCs for Cd and Zn were generally greater than 1 (Table 4). BCs for Cd were 13.7 and 15.4 and for Zn 10.9 and 10.6 in willow leaves. These results indicate that Salix clones are more suitable plant for phytoextraction of Cd and Zn than Populus clones and all tested trees are not suitable for phytoextraction of Cu maximum BC 0.72 for Salix rubens. Also Laidlaw et al. (2012) demonstrated that the willows are effective in extracting Cd and Zn, the most readily available metals in the soil and copper is extracted to a lesser degree in the harvested biomass. Higher bioaccumulation coefficient for Cd (BC = 7) in Salix smithiana leaves demonstrated Wieshammer et al. (2007). However for Zn was the bioaccumulation coefficient only 3 in their study. BCs for Cd, Zn, and Cu were not affected of total soil concentrations in our experiment. While lower BCs for Cd and Zn on polluted soils found for several willow clones Vandecasteele et al. (2004) and Meers et al. (2003). Trees differ in their ability to translocate heavy metals from the roots to the shoots. Trees have massive root systems, which help to bind the soil (Stomp et al. 1993). Heavy metals have different patterns of behavior and mobility within a tree. Lead,
418 1.74 ± 0.61aB 3.05 ± 1.21bB 5.32 ± 2.03cA 1.28 ± 0.28aA 4.16 ± 2.43bA 7.31 ± 3.45cB 0.63 ± 0.05aA 1.66 ± 1.21aA 1.85 ± 1.1aA 0.88 ± 0.01aA 1.44 ± 0.5aA 1.77 ± 0.83aA
0.65 ± 0.11aA 3.98 ± 0.96bB 7.26 ± 2.75cB 1.83 ± 0.99aA 3.65 ± 0.85bA 8.18 ± 2.99aB 0.42 ± 0.14aA 1.71 ± 0.7aA 3.03 ± 1.57bB 0.76 ± 0.13aA 1.39 ± 0.44aA 1.83 ± 0.91aA
roots twigs leaves roots twigs leaves roots twigs leaves roots twigs leaves
W1
0.46 ± 0.11aA 2.47 ± 1.26bA 5.16 ± 2.36cA 3.17 ± 2.38cB 3.27 ± 1.41bA 5.23 ± 2.15cA 0.71 ± 0.11aA 1.69 ± 0.64aA 2.1 ± 1.01aA 0.69 ± 0.08aA 1.16 ± 0.16aA 1.38 ± 0.25aA
F5 55 ± 6.67aB 330 ± 59.8bA 1050 ± 300cB 51.9 ± 3.45aA 316 ± 74bA 1020 ± 266cB 45.6 ± 9.38aB 163 ± 56.5bA 561 ± 307cA 62 ± 7.72aA 199 ± 41.5bA 538 ± 215cA
F3 53.8 ± 8.19aB 212 ± 61.8bA 851 ± 221cA 67.7 ± 4.13aA 358 ± 131bA 794 ± 146cA 28.5 ± 1.57aA 149 ± 35.8bA 461 ± 264cA 53.2 ± 9.32aA 206 ± 41.6bA 445 ± 148cA
F4
Zn
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
P2
P1
W2
F4
F3
Soil →
Cd
Plants ↓
Risk elements
33.9 ± 11.6aA 262 ± 145bA 1012 ± 303cB 58.1 ± 3.68aA 319 ± 133bA 748 ± 206cA 43.4 ± 4.7aB 184 ± 33.4bA 524 ± 163cA 49.9 ± 0.2aA 194 ± 11.3bA 529 ± 154cA
F5
9 ± 2.2a A 17.7 ± 0.3bA 11 ± 1.1a 7 ± 0.5aA 11.7 ± 0.1aA 12.3 ± 0.7b 5.3 ± 0.4aA 8.63 ± 0.1aA 7.5 ± 0.5aA 5.5 ± 0.8aA 9.1 ± 1.2aA 8.2 ± 0.3aA
F3
9.1 ± 1.9a A 11.7 ± 2bA 8.9 ± 1.4a 9.4 ± 0.3aA 11 ± 1.1bA 9.7 ± 0.6 4.8 ± 0.3aA 9.4 ± 0.5bA 8.2 ± 0.1aA 6.4 ± 0.3aA 11 ± 0.1bA 6.8 ± 0.5aA
F4
Cu
8.9 ± 3.7bA 13.1 ± 2bA 12.2 ± 1.4b 8.1 ± 2.2aA 12.6 ± 2.6bA 10.5 ± 1.4b 5 ± 1.2aA 10.8 ± 1.5bA 6.6 ± 0.4aA 4.8 ± 0.3aA 11.8 ± 1.2bA 8.4 ± 1.5aA
F5
Table 3. Cd and Zn concentration in particular parts of willows and poplars (mg.kg−1). The values marked by the same letter did not significantly differ at α = 0.05 within individual columns where the capital letters indicate the differences among the individual locations and small letters indicate the differences in element contents within one plant
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Table 4. Bioaccumulation coefficients (BCs) of the willow and poplar clones
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F3
W1 Cd Zn Cu W2 Cd Zn Cu P1 Cd Zn Cu P2 Cd Zn Cu
F4
F5
roots
twigs
leaves
roots
twigs
leaves
roots
twigs
leaves
1.18 0.57 0.37
7.5 3.43 0.72
13.7 10.9 0.45
1.91 0.44 0.18
3.35 1.72 0.23
5.85 6.88 0.17
0.35 0.2 0.11
1.9 1,51 0.17
3.97 5.83 0.15
3.5 0.54 0.29
6.9 3.29 0.48
15.4 10.6 0.5
1.41 0.55 0.18
4.57 2.89 0.22
8.03 6.42 0.19
2.44 0.33 0.1
2.52 1.84 0.16
4.02 4.31 0.13
0.8 0.48 0.22
3.23 1.7 0.35
5.72 5.84 0.3
0.69 0.23 0.09
1.82 1.2 0.18
2.03 3.73 0.16
0.55 0.25 0.06
1.3 1.06 0.13
1.62 3.02 0.08
1.43 0.65 0.22
2.62 2.1 0.3
3.45 5.6 0.1
0.97 0.43 0.12
1.58 1.66 0.22
1.95 3.6 0.13
0.53 0.29 0.06
0.89 1.12 0.15
1.06 3.1 0.1
W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
chromium, and copper tend to be immobilized and held primarily in the roots, whereas Cd, Ni, and Zn are more easily translocated to the aerial tissues (Pulford and Watson 2003). Several authors, for example Vacul´ık et al. (2012), mentioned higher accumulation of Cd and Zn in leaves compared to roots of Salix (strictly S. caprea in their research). Hu et al. (2013) demonstrated the greatest accumulation of Cd and Zn in the leaves of P. pyramidalis as well, while Cu and Pb were mainly accumulated in the roots. However our results of risk elements accumulation in willow and poplar trees grown on that polluted soils are opposed (higher Cd and Zn concentration in roots compared to leaves). The potential role of different type of used soil and contamination level, and used clones can be taken into account. Differential patterns among species and clones of Salicaceae in accumulating Cd within the root profile demonstrated also Cocozza et al. (2011) and higher average Cd concentrations (4.4–12.2 mg.kg−1) in roots compared to leaves (5.0–8.8 mg.kg−1) mentioned Meers et al. (2005) for Salix alba viminalis “Orm”. The Cd and Zn concentrations in the order of root > leaf > stem, regardless of the willows species described as well Han et al. (2013).
Fig. 1. Removal of cadmium by trees (in mg.m−2)
Risk Elements Removal by Trees Relative removal of cadmium, zinc and copper within two years at plot F5 (with the highest amount of these risk elements) and at plot F3 (with the lowest amount of these risk elements) are displayed in Figures 1–3. Metal removal is influenced by two factors – the content of the element in particular above ground plant parts and by the yield of aboveground dry biomass (Tlustoˇs et al. 2006). Among metals studied, Cd is considered the most crucial element because of high toxicity and leachability (Merrington and Alloway 1994). The highest cadmium removal was found by W2 (Salix smithiana). This willow clone accumulated 33.6 mg Cd.m−2 twice more than in W1 (Salix rubens). Majority of cadmium was removed by aboveground biomass of trees (82–97% of removed Cd). Several studies have shown that Salix spp. exhibit the capacity to accumulate high levels of Cd and Zn (e.g., Meers et al. 2003; Hammer et al. 2003). This corresponds well with our findings. Zinc and copper are essential trace elements for plant. Zinc removal by used trees was much higher compared to copper removal. Salix smithiana removed the highest amount of
Fig. 2. Removal of zinc by trees (in mg.m−2)
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Fig. 3. Removal of copper by trees (in mg.m−2) W1 – Salix rubens, W2 – Salix x smithiana Willd., P1 – Populus nigra x maximowiczii, P2 – Populus nigra Wolterson
Zn (maximum 3956 mg.m−2) and Cu (maximum 93 mg.m−2) again. Percentage Zn removal by aboveground biomass of trees was 92-99% of total Zn removed. The highest roots portion of removed risk elements was found only in case of copper (61% of removed Cu). No significant effect of Salix clones or soil concentrations for Cu uptake demonstrated also Vandecasteele et al. (2005) in a greenhouse pot experiment with Salix fragilis and Salix viminalis.
Conclusions In our experiment, Cd, Zn, and Cu removal by willows and poplars clones positively correlated with biomass production. However, as concluded also by Tlustoˇs et al. (2007), the differences in element accumulation among the clones were affected more by the properties of clones than by the soil properties. Removal of Cd and Zn was highest by Salix smithiana regardless of site, and mentioned clone is suitable for phytoextraction, Cu was firmly bound to soil and its plant accumulation was insufficient.
Funding This research was supported by the specific research No 2103/2013 project from the University of Hradec Kr´alov´e and by TACR project BROZEN No TA01020366.
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