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Influence of increasing nickel content in soil on Miscanthus × giganteus Greef and Deu. Yielding and on the content of nickel in above-ground biomass / Wpływ wzrastającej zawartości niklu w glebie na plonowanie Miscanthus x giganteus Greef i Deu. i zawartość niklu w nadziemnej biomasie

Influence of increasing nickel content in soil on Miscanthus × giganteus Greef and Deu. Yielding... The aim of the research conducted in a 2-year pot experiment in an unheated plastic tunnel was to determine suitability of Miscanthus × giganteus for phytoextraction of nickel from soil as well as to assess tolerance of this species on increasing concentrations of this metal in soil. Pots were filled with mineral soil (sand) and a mixture of soil with high-moor peat and three levels of nickel were introduced, i.e. 75 mg dm-3, 150 mg dm-3 and 600 mg dm-3 and the control combinations used substrates without the addition of nickel. Nickel was introduced only in the first year of the experiment in the form of nickel sulfate (NiSO4 · 6H2O). Miscanthus × giganteus accumulated a considerable amount of nickel in biomass. Miscanthus × giganteus growing in contaminated mineral soil turned out to be a species tolerant to high nickel concentrations. Introduction Continuous phytoextraction is a cheap and cost-effective method used in the removal of heavy metals from soil (Ros et al. 1992, Boyajian and Sumner 1997, McGrath and Zhao 2003, Nadgórska-Socha and Ciepal 2009). Effectiveness of continuous phytoextraction depends on the selection of an appropriate plant species (urek and Majtkowski 2009, Bosiacki and Zieleziski 2011, Bosiacki and Wojciechowska 2012). Plants used in this method have to accumulate considerable amounts of heavy metals in their aboveground parts. They should produce high yields of biomass within a short period of time, be easy to harvest, have a deep root system (collecting heavy metals not only from a depth of 0­20 cm) and exhibit resistance to diseases and adverse environmental conditions (tolerance to high heavy metal concentrations). Renewable energy sources play an increasingly important role in energy policy of European countries. These sources are divided into annual (e.g. cereals, rape) and perennial (e.g. willow, poplar and Miscanthus × giganteus) (Lewandowski et al. 2000). The most significant parameters of these plants include high annual increment of biomass and its high calorific value (Pulford and Watson 2003, Szempliski and Dubis 2011). Hadde et al. (2013) conducted research aiming to assess the impact of Miscanthus × giganteus biomass crop on invertebrate communities in contaminated agricultural soils. A stimulus for the development of energy crop plantations, including Miscanthus, may be connected with phytoextraction of chemically contaminated soils. Miscanthus × giganteus Greef and Deu. is grown mainly in western Europe. In Poland it is still not a popular crop. In the nearest future interest in this plant cultivation in Poland will be increasing. Miscanthus × giganteus is a triploid species belonging to the Poaceae family (Greef and Deuter 1993). Plants of this species grow to a height of 3­4 m, they do not produce seeds and are propagated vegetatively. From 1 hectare of crop the annual yield may reach as much as 20 up to 35 tons of dry matter (Pyter et al. 2009). Miscanthus × giganteus exhibits resistance to drought and very high temperatures. Success of its cultivation results from its low environmental requirements, possibility to mechanize field operations both when establishing plantations and at harvest, as well as the plant resistance to diseases and pests. Species of energy crops, with a high yielding potential, are particularly recommended to be grown in areas exposed to erosion and in contaminated areas for phytoremediation purposes. The aim of the conducted studies was to determine the effect of increasing doses of nickel introduced to mineral soil (sand) and to mineral soil with an addition of high-moor peat (at a 1:1 ratio, v/v), on the yield of Miscanthus × giganteus and to estimate what amounts of nickel are transported to above-ground parts of this plant. Material and methods The vegetation experiment was conducted in an unheated plastic tunnel with suspended sides of 6 × 30 m in size, at the Marcelin Experimental Station of the Poznan University of Life Sciences. Seedlings of Miscanthus × giganteus were produced at a tissue culture laboratory of Vitroflora. Plants were planted at the beginning of May in pots filled with previously prepared substrate. The experiment comprised 8 combinations (in each year of the study) and each combination consisted of six replications. A replication comprised one plant growing in a drainless container of 7 dm3. Phytoremediation of nickel by Miscanthus × giganteus was investigated in two years of growth with the plants grown in two substrates, at four levels of metal contents. Since light soils with low contents of organic matter predominate in Poland, such soil was selected for the experiment. Another substrate was a mixture of this mineral soil with high-moor peat. High-moor peat was added to increase the amount of organic matter in the mineral soil. 1. Substrates a. Mineral soil (sand) b. Mineral soil with high-moor peat (1:1 v/v). 2. Doses of nickel: control (nickel contents in analyzed substrates after liming amounted to: in mineral soil 2.88 mg dm-3 and mineral soil with high-moor peat 1.12 mg dm-3), 75, 150 and 600 mg dm-3) Prior to the establishment of the experiment, Corg content in mineral soil was determined according to the Tiurin method (Golcz and Bosiacki 2011). In the substrate composed of a mixture of mineral soil with high-moor peat (1:1 v/v) the percentage of organic substance was determined by loss on ignition of the substrate by the direct method at high temperature in the presence of oxygen, under the influence of which organic substance is decomposed (carbon is released in the form of CO2, hydrogen in the form of H2O and nitrogen as N2, while the other elements remain in ash). The content of organic carbon in sand (the Tiurin method) was 0.55% (0.95% humus), while the percentage of organic matter in the mixture of sand and high-moor peat (from loss on ignition) was 10.05%. In mineral soil the method of Mocek and Drzymala (2010) was used to determine bulk density (1.62 g cm-3). Total porosity of mineral soil was 38.9%. Moreover, grain size distribution of mineral soil was determined by the areometric method according to Prószyski (Mocek and Drzymala 2010). On the basis of the percentage of fractions the grain size class of soil was identified as sand, according to the guidelines of the Polish Society of Soil Science and United States Department of Agriculture standard (PTG 2009). Experiments were conducted using high-moor peat produced by Hartmann (sphagnum, ground, fractional peat), with acidity of pH 4.50. This peat has a high water capacity, at the same time retaining its elastic structure. The weight of 1 dm3 of peat was 490 grams. In order to obtain an appropriate pH for growing of Miscanthus × giganteus a neutralization curve was plotted for the analyzed substrates. On its basis the dose of CaCO3 required for the maintenance of pH within the range of 6.5­7.0 was established. The reaction of the substrate (mineral soil + high-moor peat) was regulated using 3 g dm-3 CaCO3 (chemically pure reagent). The substrate composed of mineral soil did not need any pH regulation. Despite that fact 1 g dm-3 CaCO3 was applied in order to maintain pH at 6.5­7.0. An adequate amount of calcium carbonate was introduced to each experimental container with the substrate. Two weeks after liming, nutrients and nickel were introduced to the substrate. Nickel was introduced only in the first year of the experiment in the form of chemically pure reagents (C.P.): nickel sulfate (NiSO4*6H2O). Pre-vegetation fertilization (in the first year) with macro- and micronutrients was determined taking into consideration initial nutrient contents in substrates, after liming reaching the following levels (in mg dm-3): N 200, P 120, K 250, Mg 100, Fe 50, Mn 20, B 1.5 and Mo 1.5. All macro- and micronutrients were introduced in the form of solutions using chemically pure reagents (potassium mono-phosphate, potassium nitrate, ammonium nitrate, magnesium saltpeter, magnesium sulfate, iron sulfate, copper sulfate, zinc sulfate, manganese sulfate, ammonium molybdate, borax). In the second year of the experiment, an identical experimental design was used as in the first year. After plant cutting in the first year of the experiment the containers with polluted substrates were stored in an unheated tunnel to the next vegetation year (the second year of the study). In the second year of the study, in March, prior to the beginning of vegetation substrate samples were collected and chemical analyses were performed to determine nutrient contents. On this basis nutrient fertilization was established (leading to nutrient contents at the same levels, which were applied in the first year of the experiment). Nutrients in substrates were determined using the "Universal" method (Kozik and Golcz 2011) in CH3COOH extraction solution at a concentration of 0.03 mol dm-3, pH in water was determined by the potentiometric method (the substrate to water ratio of 1:2), while the conductivity method was applied to determine EC (mS cm-1), (the substrate to water ratio of 1:2) (Golcz 2011). The following nutrient determination techniques were applied: N ­ NH4 and N ­ NO3 by micro-distillation (Bremner modified by Starck), P by colorimetry using the vanadiummolybdenum method, K, Ca and Na by flame photometry, Mg by atomic absorption (AAS), Cl and S ­ SO4 by nephelometry (Kozik and Golcz 2011). In October in each year of the studies prior to harvest, plant height was measured. Dry weight of plants was recorded and samples of plant material were collected for analyses. Harvested plant material (entire aboveground mass) was dried in an extraction drier at a temperature of 105ºC for 48 h. Next the material was ground and at the amount of 2.5 g taken from each sample it was digested in a mixture of concentrated HNO3 (ultra pure) and HClO4 (analytically pure) at a 3:1 ratio (Bosiacki and Roszyk 2010). Content of nickel in the plant material was determined by flame atomic absorption spectrophotometry (FAAS), using AAS-3 spectrophotometer by Zeiss. Moreover, the content of nickel in the reference material (Pseudevernia furfuracea BCR®-482/2009, certified by the Institute for Reference Materials and Measurements in Belgium), was determined as well (Table 1). Table 1. Contents of nickel in reference materials Pseudevernia furfuracea (mg kg-1 dry weight) Reference material certified content mg kg-1 Ni 2.47 +/0.07 mg kg-1 2.37 recovery (%) 95.95 Digestion difference (mgkg-1) -0.10 difference (%) -4.05 Metal In the first and second year of the studies samples of the substrate were collected after harvest. Nickel was extracted from them using modified Lindsay's solution containing 5 g EDTA (ethylenediaminetetraacetic acid), 9 cm3 25% NH4OH solution, 4 g citric acid and 2 g Ca(CH3COO)2 2H2O in 1 dm3 (Nowosielski 1988). The ratio of the soil to the extraction solution was 1:4 (50 cm3 : 200 cm3). Next this metal was determined by flame atomic absorption spectrophotometry (FAAS) in AAS-3 spectrophotometer by Zeiss. Results of the nickel content in substrates and aboveground parts of Miscanthus × giganteus and results of plant dry weight, and height were elaborated statistically in the Statobl program applying a one-way analysis of variance for orthogonal factorial experiments, with differences between means determined at a significance level p < 0.05. Results and discussion Nickel is characterized by high mobility in ecosystems and it is generally readily absorbed by plants, typically in proportion to its content in soil (Kabata-Pendias and Pendias 1999). According to Antoniewicz and Jasiewicz (2002) the translocation of nickel to aboveground parts is limited, while Drkiewicz (1994) claimed that this metal penetrating to the soil as an industrial or agricultural pollutant is readily absorbed by the root system and transported to stems and leaves with xylem sap. In the opinion of Drkiewicz (1994), nickel in plants is found in complexes with organic compounds, while at excess Ni+2 it may be found in plants in the cation form (Knypl 1980) inhibiting plants growth (Reeves and Baker 2000, Nadgórska-Socha and Ciepal (2009), as well as their metabolism (Sheoran et al. 1990, Van Assche and Clijsters 1990). In the conducted investigations mineral soil polluted with increasing doses of nickel did not have a significant effect on plant dry weight in the first year of growth (Table 2). In mineral soil with an addition of peat, the lowest weight was found at a nickel dose of 600 mg dm-3, while it was highest at the 150 mg dm-3 dose of nickel, which did not differ significantly from the weight obtained in the control substrate (with no Ni added). In the first year of growth, in the mineral soil, the lowest plants were reported at a nickel dose of 150 mg dm-3, while doses of 75 and 600 mg Ni dm-3 did not have a significant effect on plant growth in comparison to plants growing in the soil, to which no nickel was introduced (Table 2). In a mixture of soil with peat, nickel introduced at 600 mg dm-3 caused the production of the lowest plants, which did not differ significantly from those growing in this substrate contaminated with 75 mg Ni dm-3. In the second year of growth, in mineral soil, a dose of 600 mg Ni dm-3 had a significant effect on the production of the greatest dry matter in plants, while in a mixture of soil with peat, both the lowest dry matter content and the lowest plants were obtained at this dose (Table 3). No effect of increasing nickel doses introduced to mineral soil was found on plant height in the second year of growth (Table 3). Table 2. Dry weight of above-ground parts of Miscanthus × giganteus (g plant-1) and height of plants (cm) in the first year of growth Dose of Ni mg dm-3 control Dry weight Mean control Height 75 150 600 Mean 44­48 35­54 23­49 44­48 4 19 26 4 44.2 a 75 150 600 Substrates Mineral soil min.-max. range 69­89 39­85 67­80 69­89 Range R 20 46 13 20 73.5 a 1.4 7.3 9.6 1.6 45.7 b 49.5 bc 35.5 a 46.3 b 60­66 54­65 60­66 47­72 6 11 6 25 60.2 b Standard deviation 7.0 15.2 5.3 7.8 Mean 77.0 a 65.2 a 72.8 a 79.0 a min. max. range 125­175 105­145 125­175 60­90 Mineral soil + high-moor peat Range R 50 40 50 30 125.7 b 2.3 3.5 2.2 9.2 63.2 e 59.2 de 62.7 e 55.7 cd Standard deviation 16.5 16.6 16.4 12.1 Mean 148.8 c 126.8 b 149.0 c 78.3 a Irrespective of nickel doses, both in the first and second year of growth of Miscanthus × giganteus a greater dry matter and plant height were recorded in a mixture of the soil with peat. The effect of nickel on the growth of ornamental plants was investigated by many researchers. Adhikari (2012) observed a growth inhibition in Ricinus communis only at a dose of 250 mg Ni dm-3. In turn, Ahmad et al. (2011) recorded a toxic effect of nickel on Helianthus annuus already at 10, 20, 30 and 40 mg Ni dm-3. Bosiacki and Wojciechowska (2012) obtained a lower total yield of above-ground parts in Tagetes erecta at all the applied nickel doses (from 25 to 300 mg dm-3). The same authors observed a stimulatory effect of nickel on the total yield of above-ground parts in Amaranthus caudatus, recorded in a substrate to which 150 mg Ni dm-3 were introduced. Phytoextraction assumes the use of the so-called hyperaccumulators, i.e. plants, which are genetically and physiologically capable of accumulating considerable amounts of heavy metals with no symptoms of their toxicity (Boyd and Martens 1994, Boyd 1998). The term hyper-accumulator of Ni was devised by many authors (Jaffré et al. 1976, Reeves 1992, Baker et al. 2000, Reeves and Baker 2000, McGrath and Zhao 2003). They claimed that a hyper-accumulator of Ni is a plant in which a Ni concentration of at least 1 000 g·g-1 (1 000 mg·kg-1) has been recorded in the dry matter of any above-ground tissue in at least one specimen growing in its natural habitat. According to Van der Ent et al. (2013) only plant leaves (or fronds) are to be considered in establishing hyper-accumulator status. Miscanthus sp. is a plant having the ability to accumulate large amounts of heavy metals in contaminated soil (Pogrzeba et al. 2011). Higher content of Cd, Pb and Ni in triploid than diploid Miscanthus biomass was found (Kalembasa and Malinowska 2009a). Kalembasa and Malinowska (2009a) also claimed that mineral fertilization (NPK) influences cadmium content in biomass of diploid genotypes and nickel in biomass of diploid and triploid genotypes, while the contents of Cd, Pb and Ni were dependent on a harvest date. The highest nickel concentration was recorded in Miscanthus biomass at the beginning of July. In the conducted investigations, the highest content of nickel was observed in the second year of growth, in plants growing in mineral soil contaminated with the highest levels of this metal (Table 4). When comparing the content of nickel in above-ground parts of plants in the first and second year of growth, significant differences in Ni contents were recorded only in plants growing in substrates with the highest nickel content (600 mg dm-3). In the above-ground parts of Miscanthus × giganteus growing in mineral soil contaminated with 600 mg Ni dm-3 a significantly higher content of nickel was detected in the second year of growth. The same dependence was found for nickel contents in above-ground parts of Miscanthus × giganteus growing in a mixture of soil and peat. Both in the first and second year of Miscanthus × giganteus growth higher nickel contents were observed in plants growing in the mineral soil. In the conducted analyses the nickel concentration index was calculated for above-ground parts of Miscanthus × giganteus. The metal concentration index was caluclated from the formula C=a:b a ­ content in a plant growing in a polluted substrate b ­ content in a plant growing in an unpolluted substrate (Bosiacki and Wojciechowska 2012). Nickel concentration index in the above-ground parts of Miscanthus × giganteus of over 100 was recorded both in the first and second year of plant growth in mineral soil and in a mixture of soil with peat which was contaminated with nickel at 600 mg dm-3 (Table 5). According to Kalembasa (2006) in ash of Miscanthus sinensis Thumb. the content of individual heavy metals ranks in the following decreasing levels: Zn>Cd>Pb>Ni>Cu>Cr. Miscanthus × giganteus is a more tolerant species to the total contamination of soil with Zn and Pb than mallow and Table 3. Dry weight of above-ground parts of Miscanthus × giganteus (g plant-1) and height of plants (cm) in the second year of growth Dose of Ni mg dm-3 control Dry weight Mean control Height 75 150 600 Mean 51­68 54­69 38­63 54­82 17 15 25 28 59.9 a 75 150 600 Substrates Mineral soil min.-max. range 50­92 72­114 60­111 117­135 Range R 42 42 51 18 97.9 a 6.8 6.6 9.0 9.6 59.8 a 61.5 a 55.0 a 63.3 a 67­90 63­120 60­96 48­58 23 57 36 10 72.2 b Standard deviation 15.5 15.5 21.4 7.4 Mean 80.5 b 100.0 b 86.7 b 124.5 c min.-max. range 122­180 116­147 115­170 21­83 Mineral soil + high-moor peat Range R 58 31 55 62 121.7 b 7.7 19.9 12.0 3.7 76.5 b 82.0 b 76.5 b 53.8 a Standard deviation 19.2 11.9 19.9 20.2 Mean 149.3 d 138.0 cd 143.0 cd 56.3 a greater amounts of macronutrients and lower amounts of heavy metals (Kalembasa and Malinowska 2009a, Kalembasa and Malinowska 2009b). Some researchers showed an effect of fertilization on changes in individual heavy metal content in the successive years of growth. In comparison to osier, Miscanthus is characterized by lower tolerance to high concentrations of heavy metals and as it is reported by Kabala et al. (2010), they need to be further tested in terms of phytoremediation capacity of individual cultivars of Miscanthus. phytoextraction of Zn and Pb from the soils contaminated with these metals are much higher for Miscanthus than for Virginia mallow (Koco and Matyka 2012). As reported by Kabala et al. (2010). Miscanthus may be grown on soils weakly contaminated with heavy metals on condition they are provided with adequate abundance of nutrients and water. In turn, on soils with medium and strong heavy metal contamination selected clones of osier are recommended. In comparison to osier, wood straw of Miscanthus grown on uncontaminated soils contains Table 4. Contents of Ni (mg kg-1 dry weight) in above-ground parts of Miscanthus × giganteus growing in substrates polluted with nickel Year of cultivation Substrate Dose of metal (mg dm-3) Control Mineral soil Ni 75 Ni 150 Ni 600 Mineral soil + high-moor peat Control Ni 75 Ni 150 Ni 600 1st year min.-max. range 3.2­4.0 24.9­49.3 198.3­269.1 389.2­467.3 3.3­4.1 22.1­28.2 212.3­280.6 333.3­403.7 range R 0.8 24.4 70.8 78.1 0.8 6.1 68.3 70.4 SD 0.3 9.5 26.8 27.9 0.3 2.1 26.7 27.0 mean 3.5 a 42.9 bc 244.8 d 426.0 f 3.7 a 25.7 ab 265.9 d 375.5 e min.-max. range 3.3­4.8 45.6­52.5 241.8­272.0 423.6­494.2 3.8­4.2 19.3­29.4 198.8­301.3 378.8­471.2 2nd year range R 1.5 6.9 30.2 70.6 0.4 10.1 102.5 92.4 SD 0.6 2.7 10.9 26.8 0.1 3.4 35.2 35.8 mean 4.0 a 50.9 c 261.5 d 476.0 g 4.00a 23.8 ab 265.2 d 446.5 f *homogeneous groups were identified using the Duncan test, p < 0.05 (values denoted with identical letters do not differ significantly) Table 5. Metal concentration indexes in above-ground parts of Miscanthus × giganteus Substrates Metal Dose of metal (mg dm-3) 75 Ni 150 600 Mineral soil The first year of growth 12.3 69.9 121.7 The second year of growth 12.7 65.4 119.0 Mineral soil + high-moor peat The first year of growth 6.9 71.9 101.5 The second year of growth 5.9 66.3 111.6 Table 6. Contents of nickel (extracted with Lindsay solution) in substrates (in mg dm-3) after the completion of plant growth in the first and the second years of analyses Type of pollution Control (native content of Ni mg dm-3) Weak pollution (Ni 75 mg dm-3) Medium pollution (Ni 150 mg dm-3) Strong pollution (Ni 600 mg dm-3) Substrate mineral soil soil + peat mineral soil soil + peat mineral soil soil + peat mineral soil soil + peat Year of growth 1st year 2.4 c 0.7 a 44.3 d 25.6 b 87.3 c 56.5 b 269.6 c 193.4 ab 2nd year 1.5 b 0.6 a 29.8 c 20.7 a 64.6 b 37.5 a 211.7 b 161.3 a Both in soil and in a mixture of soil with peat a lower nickel content was found after the second year of growth (Table 6). In all experimental combinations a lower nickel content was detected in the substrate being a mixture of soil and peat in comparison to that found in mineral soil. A lower content of soluble forms of nickel in that substrate results from the uptake of greater amounts of this metal in the biomass yield produced in that substrate. Moreover, as it was reported by Bosiacki and Tyksiski (2006) an addition of organic substance to soil results in a reduced availability of soluble heavy metal forms. Conclusions 1. Miscanthus × giganteus growing in contaminated mineral soil turned out to be a species tolerant to high nickel concentrations. 2. Miscanthus × giganteus accumulated a considerable amount of nickel in biomass. 3. Miscanthus × giganteus needs to be further tested in terms of nickel phytoextraction capacity from contaminated soil in natural habitat. Acknowledgments The study was financed from funds for science in the years 2008­2011 as a research project no. N N305 085535. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Environmental Protection de Gruyter

Influence of increasing nickel content in soil on Miscanthus × giganteus Greef and Deu. Yielding and on the content of nickel in above-ground biomass / Wpływ wzrastającej zawartości niklu w glebie na plonowanie Miscanthus x giganteus Greef i Deu. i zawartość niklu w nadziemnej biomasie

Bosiacki, Maciej
Archives of Environmental Protection , Volume 41 (1) – Mar 1, 2015
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Abstract

The aim of the research conducted in a 2-year pot experiment in an unheated plastic tunnel was to determine suitability of Miscanthus × giganteus for phytoextraction of nickel from soil as well as to assess tolerance of this species on increasing concentrations of this metal in soil. Pots were filled with mineral soil (sand) and a mixture of soil with high-moor peat and three levels of nickel were introduced, i.e. 75 mg dm-3, 150 mg dm-3 and 600 mg dm-3 and the control combinations used substrates without the addition of nickel. Nickel was introduced only in the first year of the experiment in the form of nickel sulfate (NiSO4 · 6H2O). Miscanthus × giganteus accumulated a considerable amount of nickel in biomass. Miscanthus × giganteus growing in contaminated mineral soil turned out to be a species tolerant to high nickel concentrations. Introduction Continuous phytoextraction is a cheap and cost-effective method used in the removal of heavy metals from soil (Ros et al. 1992, Boyajian and Sumner 1997, McGrath and Zhao 2003, Nadgórska-Socha and Ciepal 2009). Effectiveness of continuous phytoextraction depends on the selection of an appropriate plant species (urek and Majtkowski 2009, Bosiacki and Zieleziski 2011, Bosiacki and Wojciechowska 2012). Plants used in this method have to accumulate considerable amounts of heavy metals in their aboveground parts. They should produce high yields of biomass within a short period of time, be easy to harvest, have a deep root system (collecting heavy metals not only from a depth of 0­20 cm) and exhibit resistance to diseases and adverse environmental conditions (tolerance to high heavy metal concentrations). Renewable energy sources play an increasingly important role in energy policy of European countries. These sources are divided into annual (e.g. cereals, rape) and perennial (e.g. willow, poplar and Miscanthus × giganteus) (Lewandowski et al. 2000). The most significant parameters of these plants include high annual increment of biomass and its high calorific value (Pulford and Watson 2003, Szempliski and Dubis 2011). Hadde et al. (2013) conducted research aiming to assess the impact of Miscanthus × giganteus biomass crop on invertebrate communities in contaminated agricultural soils. A stimulus for the development of energy crop plantations, including Miscanthus, may be connected with phytoextraction of chemically contaminated soils. Miscanthus × giganteus Greef and Deu. is grown mainly in western Europe. In Poland it is still not a popular crop. In the nearest future interest in this plant cultivation in Poland will be increasing. Miscanthus × giganteus is a triploid species belonging to the Poaceae family (Greef and Deuter 1993). Plants of this species grow to a height of 3­4 m, they do not produce seeds and are propagated vegetatively. From 1 hectare of crop the annual yield may reach as much as 20 up to 35 tons of dry matter (Pyter et al. 2009). Miscanthus × giganteus exhibits resistance to drought and very high temperatures. Success of its cultivation results from its low environmental requirements, possibility to mechanize field operations both when establishing plantations and at harvest, as well as the plant resistance to diseases and pests. Species of energy crops, with a high yielding potential, are particularly recommended to be grown in areas exposed to erosion and in contaminated areas for phytoremediation purposes. The aim of the conducted studies was to determine the effect of increasing doses of nickel introduced to mineral soil (sand) and to mineral soil with an addition of high-moor peat (at a 1:1 ratio, v/v), on the yield of Miscanthus × giganteus and to estimate what amounts of nickel are transported to above-ground parts of this plant. Material and methods The vegetation experiment was conducted in an unheated plastic tunnel with suspended sides of 6 × 30 m in size, at the Marcelin Experimental Station of the Poznan University of Life Sciences. Seedlings of Miscanthus × giganteus were produced at a tissue culture laboratory of Vitroflora. Plants were planted at the beginning of May in pots filled with previously prepared substrate. The experiment comprised 8 combinations (in each year of the study) and each combination consisted of six replications. A replication comprised one plant growing in a drainless container of 7 dm3. Phytoremediation of nickel by Miscanthus × giganteus was investigated in two years of growth with the plants grown in two substrates, at four levels of metal contents. Since light soils with low contents of organic matter predominate in Poland, such soil was selected for the experiment. Another substrate was a mixture of this mineral soil with high-moor peat. High-moor peat was added to increase the amount of organic matter in the mineral soil. 1. Substrates a. Mineral soil (sand) b. Mineral soil with high-moor peat (1:1 v/v). 2. Doses of nickel: control (nickel contents in analyzed substrates after liming amounted to: in mineral soil 2.88 mg dm-3 and mineral soil with high-moor peat 1.12 mg dm-3), 75, 150 and 600 mg dm-3) Prior to the establishment of the experiment, Corg content in mineral soil was determined according to the Tiurin method (Golcz and Bosiacki 2011). In the substrate composed of a mixture of mineral soil with high-moor peat (1:1 v/v) the percentage of organic substance was determined by loss on ignition of the substrate by the direct method at high temperature in the presence of oxygen, under the influence of which organic substance is decomposed (carbon is released in the form of CO2, hydrogen in the form of H2O and nitrogen as N2, while the other elements remain in ash). The content of organic carbon in sand (the Tiurin method) was 0.55% (0.95% humus), while the percentage of organic matter in the mixture of sand and high-moor peat (from loss on ignition) was 10.05%. In mineral soil the method of Mocek and Drzymala (2010) was used to determine bulk density (1.62 g cm-3). Total porosity of mineral soil was 38.9%. Moreover, grain size distribution of mineral soil was determined by the areometric method according to Prószyski (Mocek and Drzymala 2010). On the basis of the percentage of fractions the grain size class of soil was identified as sand, according to the guidelines of the Polish Society of Soil Science and United States Department of Agriculture standard (PTG 2009). Experiments were conducted using high-moor peat produced by Hartmann (sphagnum, ground, fractional peat), with acidity of pH 4.50. This peat has a high water capacity, at the same time retaining its elastic structure. The weight of 1 dm3 of peat was 490 grams. In order to obtain an appropriate pH for growing of Miscanthus × giganteus a neutralization curve was plotted for the analyzed substrates. On its basis the dose of CaCO3 required for the maintenance of pH within the range of 6.5­7.0 was established. The reaction of the substrate (mineral soil + high-moor peat) was regulated using 3 g dm-3 CaCO3 (chemically pure reagent). The substrate composed of mineral soil did not need any pH regulation. Despite that fact 1 g dm-3 CaCO3 was applied in order to maintain pH at 6.5­7.0. An adequate amount of calcium carbonate was introduced to each experimental container with the substrate. Two weeks after liming, nutrients and nickel were introduced to the substrate. Nickel was introduced only in the first year of the experiment in the form of chemically pure reagents (C.P.): nickel sulfate (NiSO4*6H2O). Pre-vegetation fertilization (in the first year) with macro- and micronutrients was determined taking into consideration initial nutrient contents in substrates, after liming reaching the following levels (in mg dm-3): N 200, P 120, K 250, Mg 100, Fe 50, Mn 20, B 1.5 and Mo 1.5. All macro- and micronutrients were introduced in the form of solutions using chemically pure reagents (potassium mono-phosphate, potassium nitrate, ammonium nitrate, magnesium saltpeter, magnesium sulfate, iron sulfate, copper sulfate, zinc sulfate, manganese sulfate, ammonium molybdate, borax). In the second year of the experiment, an identical experimental design was used as in the first year. After plant cutting in the first year of the experiment the containers with polluted substrates were stored in an unheated tunnel to the next vegetation year (the second year of the study). In the second year of the study, in March, prior to the beginning of vegetation substrate samples were collected and chemical analyses were performed to determine nutrient contents. On this basis nutrient fertilization was established (leading to nutrient contents at the same levels, which were applied in the first year of the experiment). Nutrients in substrates were determined using the "Universal" method (Kozik and Golcz 2011) in CH3COOH extraction solution at a concentration of 0.03 mol dm-3, pH in water was determined by the potentiometric method (the substrate to water ratio of 1:2), while the conductivity method was applied to determine EC (mS cm-1), (the substrate to water ratio of 1:2) (Golcz 2011). The following nutrient determination techniques were applied: N ­ NH4 and N ­ NO3 by micro-distillation (Bremner modified by Starck), P by colorimetry using the vanadiummolybdenum method, K, Ca and Na by flame photometry, Mg by atomic absorption (AAS), Cl and S ­ SO4 by nephelometry (Kozik and Golcz 2011). In October in each year of the studies prior to harvest, plant height was measured. Dry weight of plants was recorded and samples of plant material were collected for analyses. Harvested plant material (entire aboveground mass) was dried in an extraction drier at a temperature of 105ºC for 48 h. Next the material was ground and at the amount of 2.5 g taken from each sample it was digested in a mixture of concentrated HNO3 (ultra pure) and HClO4 (analytically pure) at a 3:1 ratio (Bosiacki and Roszyk 2010). Content of nickel in the plant material was determined by flame atomic absorption spectrophotometry (FAAS), using AAS-3 spectrophotometer by Zeiss. Moreover, the content of nickel in the reference material (Pseudevernia furfuracea BCR®-482/2009, certified by the Institute for Reference Materials and Measurements in Belgium), was determined as well (Table 1). Table 1. Contents of nickel in reference materials Pseudevernia furfuracea (mg kg-1 dry weight) Reference material certified content mg kg-1 Ni 2.47 +/0.07 mg kg-1 2.37 recovery (%) 95.95 Digestion difference (mgkg-1) -0.10 difference (%) -4.05 Metal In the first and second year of the studies samples of the substrate were collected after harvest. Nickel was extracted from them using modified Lindsay's solution containing 5 g EDTA (ethylenediaminetetraacetic acid), 9 cm3 25% NH4OH solution, 4 g citric acid and 2 g Ca(CH3COO)2 2H2O in 1 dm3 (Nowosielski 1988). The ratio of the soil to the extraction solution was 1:4 (50 cm3 : 200 cm3). Next this metal was determined by flame atomic absorption spectrophotometry (FAAS) in AAS-3 spectrophotometer by Zeiss. Results of the nickel content in substrates and aboveground parts of Miscanthus × giganteus and results of plant dry weight, and height were elaborated statistically in the Statobl program applying a one-way analysis of variance for orthogonal factorial experiments, with differences between means determined at a significance level p < 0.05. Results and discussion Nickel is characterized by high mobility in ecosystems and it is generally readily absorbed by plants, typically in proportion to its content in soil (Kabata-Pendias and Pendias 1999). According to Antoniewicz and Jasiewicz (2002) the translocation of nickel to aboveground parts is limited, while Drkiewicz (1994) claimed that this metal penetrating to the soil as an industrial or agricultural pollutant is readily absorbed by the root system and transported to stems and leaves with xylem sap. In the opinion of Drkiewicz (1994), nickel in plants is found in complexes with organic compounds, while at excess Ni+2 it may be found in plants in the cation form (Knypl 1980) inhibiting plants growth (Reeves and Baker 2000, Nadgórska-Socha and Ciepal (2009), as well as their metabolism (Sheoran et al. 1990, Van Assche and Clijsters 1990). In the conducted investigations mineral soil polluted with increasing doses of nickel did not have a significant effect on plant dry weight in the first year of growth (Table 2). In mineral soil with an addition of peat, the lowest weight was found at a nickel dose of 600 mg dm-3, while it was highest at the 150 mg dm-3 dose of nickel, which did not differ significantly from the weight obtained in the control substrate (with no Ni added). In the first year of growth, in the mineral soil, the lowest plants were reported at a nickel dose of 150 mg dm-3, while doses of 75 and 600 mg Ni dm-3 did not have a significant effect on plant growth in comparison to plants growing in the soil, to which no nickel was introduced (Table 2). In a mixture of soil with peat, nickel introduced at 600 mg dm-3 caused the production of the lowest plants, which did not differ significantly from those growing in this substrate contaminated with 75 mg Ni dm-3. In the second year of growth, in mineral soil, a dose of 600 mg Ni dm-3 had a significant effect on the production of the greatest dry matter in plants, while in a mixture of soil with peat, both the lowest dry matter content and the lowest plants were obtained at this dose (Table 3). No effect of increasing nickel doses introduced to mineral soil was found on plant height in the second year of growth (Table 3). Table 2. Dry weight of above-ground parts of Miscanthus × giganteus (g plant-1) and height of plants (cm) in the first year of growth Dose of Ni mg dm-3 control Dry weight Mean control Height 75 150 600 Mean 44­48 35­54 23­49 44­48 4 19 26 4 44.2 a 75 150 600 Substrates Mineral soil min.-max. range 69­89 39­85 67­80 69­89 Range R 20 46 13 20 73.5 a 1.4 7.3 9.6 1.6 45.7 b 49.5 bc 35.5 a 46.3 b 60­66 54­65 60­66 47­72 6 11 6 25 60.2 b Standard deviation 7.0 15.2 5.3 7.8 Mean 77.0 a 65.2 a 72.8 a 79.0 a min. max. range 125­175 105­145 125­175 60­90 Mineral soil + high-moor peat Range R 50 40 50 30 125.7 b 2.3 3.5 2.2 9.2 63.2 e 59.2 de 62.7 e 55.7 cd Standard deviation 16.5 16.6 16.4 12.1 Mean 148.8 c 126.8 b 149.0 c 78.3 a Irrespective of nickel doses, both in the first and second year of growth of Miscanthus × giganteus a greater dry matter and plant height were recorded in a mixture of the soil with peat. The effect of nickel on the growth of ornamental plants was investigated by many researchers. Adhikari (2012) observed a growth inhibition in Ricinus communis only at a dose of 250 mg Ni dm-3. In turn, Ahmad et al. (2011) recorded a toxic effect of nickel on Helianthus annuus already at 10, 20, 30 and 40 mg Ni dm-3. Bosiacki and Wojciechowska (2012) obtained a lower total yield of above-ground parts in Tagetes erecta at all the applied nickel doses (from 25 to 300 mg dm-3). The same authors observed a stimulatory effect of nickel on the total yield of above-ground parts in Amaranthus caudatus, recorded in a substrate to which 150 mg Ni dm-3 were introduced. Phytoextraction assumes the use of the so-called hyperaccumulators, i.e. plants, which are genetically and physiologically capable of accumulating considerable amounts of heavy metals with no symptoms of their toxicity (Boyd and Martens 1994, Boyd 1998). The term hyper-accumulator of Ni was devised by many authors (Jaffré et al. 1976, Reeves 1992, Baker et al. 2000, Reeves and Baker 2000, McGrath and Zhao 2003). They claimed that a hyper-accumulator of Ni is a plant in which a Ni concentration of at least 1 000 g·g-1 (1 000 mg·kg-1) has been recorded in the dry matter of any above-ground tissue in at least one specimen growing in its natural habitat. According to Van der Ent et al. (2013) only plant leaves (or fronds) are to be considered in establishing hyper-accumulator status. Miscanthus sp. is a plant having the ability to accumulate large amounts of heavy metals in contaminated soil (Pogrzeba et al. 2011). Higher content of Cd, Pb and Ni in triploid than diploid Miscanthus biomass was found (Kalembasa and Malinowska 2009a). Kalembasa and Malinowska (2009a) also claimed that mineral fertilization (NPK) influences cadmium content in biomass of diploid genotypes and nickel in biomass of diploid and triploid genotypes, while the contents of Cd, Pb and Ni were dependent on a harvest date. The highest nickel concentration was recorded in Miscanthus biomass at the beginning of July. In the conducted investigations, the highest content of nickel was observed in the second year of growth, in plants growing in mineral soil contaminated with the highest levels of this metal (Table 4). When comparing the content of nickel in above-ground parts of plants in the first and second year of growth, significant differences in Ni contents were recorded only in plants growing in substrates with the highest nickel content (600 mg dm-3). In the above-ground parts of Miscanthus × giganteus growing in mineral soil contaminated with 600 mg Ni dm-3 a significantly higher content of nickel was detected in the second year of growth. The same dependence was found for nickel contents in above-ground parts of Miscanthus × giganteus growing in a mixture of soil and peat. Both in the first and second year of Miscanthus × giganteus growth higher nickel contents were observed in plants growing in the mineral soil. In the conducted analyses the nickel concentration index was calculated for above-ground parts of Miscanthus × giganteus. The metal concentration index was caluclated from the formula C=a:b a ­ content in a plant growing in a polluted substrate b ­ content in a plant growing in an unpolluted substrate (Bosiacki and Wojciechowska 2012). Nickel concentration index in the above-ground parts of Miscanthus × giganteus of over 100 was recorded both in the first and second year of plant growth in mineral soil and in a mixture of soil with peat which was contaminated with nickel at 600 mg dm-3 (Table 5). According to Kalembasa (2006) in ash of Miscanthus sinensis Thumb. the content of individual heavy metals ranks in the following decreasing levels: Zn>Cd>Pb>Ni>Cu>Cr. Miscanthus × giganteus is a more tolerant species to the total contamination of soil with Zn and Pb than mallow and Table 3. Dry weight of above-ground parts of Miscanthus × giganteus (g plant-1) and height of plants (cm) in the second year of growth Dose of Ni mg dm-3 control Dry weight Mean control Height 75 150 600 Mean 51­68 54­69 38­63 54­82 17 15 25 28 59.9 a 75 150 600 Substrates Mineral soil min.-max. range 50­92 72­114 60­111 117­135 Range R 42 42 51 18 97.9 a 6.8 6.6 9.0 9.6 59.8 a 61.5 a 55.0 a 63.3 a 67­90 63­120 60­96 48­58 23 57 36 10 72.2 b Standard deviation 15.5 15.5 21.4 7.4 Mean 80.5 b 100.0 b 86.7 b 124.5 c min.-max. range 122­180 116­147 115­170 21­83 Mineral soil + high-moor peat Range R 58 31 55 62 121.7 b 7.7 19.9 12.0 3.7 76.5 b 82.0 b 76.5 b 53.8 a Standard deviation 19.2 11.9 19.9 20.2 Mean 149.3 d 138.0 cd 143.0 cd 56.3 a greater amounts of macronutrients and lower amounts of heavy metals (Kalembasa and Malinowska 2009a, Kalembasa and Malinowska 2009b). Some researchers showed an effect of fertilization on changes in individual heavy metal content in the successive years of growth. In comparison to osier, Miscanthus is characterized by lower tolerance to high concentrations of heavy metals and as it is reported by Kabala et al. (2010), they need to be further tested in terms of phytoremediation capacity of individual cultivars of Miscanthus. phytoextraction of Zn and Pb from the soils contaminated with these metals are much higher for Miscanthus than for Virginia mallow (Koco and Matyka 2012). As reported by Kabala et al. (2010). Miscanthus may be grown on soils weakly contaminated with heavy metals on condition they are provided with adequate abundance of nutrients and water. In turn, on soils with medium and strong heavy metal contamination selected clones of osier are recommended. In comparison to osier, wood straw of Miscanthus grown on uncontaminated soils contains Table 4. Contents of Ni (mg kg-1 dry weight) in above-ground parts of Miscanthus × giganteus growing in substrates polluted with nickel Year of cultivation Substrate Dose of metal (mg dm-3) Control Mineral soil Ni 75 Ni 150 Ni 600 Mineral soil + high-moor peat Control Ni 75 Ni 150 Ni 600 1st year min.-max. range 3.2­4.0 24.9­49.3 198.3­269.1 389.2­467.3 3.3­4.1 22.1­28.2 212.3­280.6 333.3­403.7 range R 0.8 24.4 70.8 78.1 0.8 6.1 68.3 70.4 SD 0.3 9.5 26.8 27.9 0.3 2.1 26.7 27.0 mean 3.5 a 42.9 bc 244.8 d 426.0 f 3.7 a 25.7 ab 265.9 d 375.5 e min.-max. range 3.3­4.8 45.6­52.5 241.8­272.0 423.6­494.2 3.8­4.2 19.3­29.4 198.8­301.3 378.8­471.2 2nd year range R 1.5 6.9 30.2 70.6 0.4 10.1 102.5 92.4 SD 0.6 2.7 10.9 26.8 0.1 3.4 35.2 35.8 mean 4.0 a 50.9 c 261.5 d 476.0 g 4.00a 23.8 ab 265.2 d 446.5 f *homogeneous groups were identified using the Duncan test, p < 0.05 (values denoted with identical letters do not differ significantly) Table 5. Metal concentration indexes in above-ground parts of Miscanthus × giganteus Substrates Metal Dose of metal (mg dm-3) 75 Ni 150 600 Mineral soil The first year of growth 12.3 69.9 121.7 The second year of growth 12.7 65.4 119.0 Mineral soil + high-moor peat The first year of growth 6.9 71.9 101.5 The second year of growth 5.9 66.3 111.6 Table 6. Contents of nickel (extracted with Lindsay solution) in substrates (in mg dm-3) after the completion of plant growth in the first and the second years of analyses Type of pollution Control (native content of Ni mg dm-3) Weak pollution (Ni 75 mg dm-3) Medium pollution (Ni 150 mg dm-3) Strong pollution (Ni 600 mg dm-3) Substrate mineral soil soil + peat mineral soil soil + peat mineral soil soil + peat mineral soil soil + peat Year of growth 1st year 2.4 c 0.7 a 44.3 d 25.6 b 87.3 c 56.5 b 269.6 c 193.4 ab 2nd year 1.5 b 0.6 a 29.8 c 20.7 a 64.6 b 37.5 a 211.7 b 161.3 a Both in soil and in a mixture of soil with peat a lower nickel content was found after the second year of growth (Table 6). In all experimental combinations a lower nickel content was detected in the substrate being a mixture of soil and peat in comparison to that found in mineral soil. A lower content of soluble forms of nickel in that substrate results from the uptake of greater amounts of this metal in the biomass yield produced in that substrate. Moreover, as it was reported by Bosiacki and Tyksiski (2006) an addition of organic substance to soil results in a reduced availability of soluble heavy metal forms. Conclusions 1. Miscanthus × giganteus growing in contaminated mineral soil turned out to be a species tolerant to high nickel concentrations. 2. Miscanthus × giganteus accumulated a considerable amount of nickel in biomass. 3. Miscanthus × giganteus needs to be further tested in terms of nickel phytoextraction capacity from contaminated soil in natural habitat. Acknowledgments The study was financed from funds for science in the years 2008­2011 as a research project no. N N305 085535.

Journal

Archives of Environmental Protection – de Gruyter

Published: Mar 1, 2015

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