The aim of this study was to evaluate the usefulness of Phalaris arundinacea, Salix viminalis and Zea mays to the phy- toremediation of the soil contaminated with nickel. A 2-year microplot experiment was carried out with plants growing on Ni-contaminated soil. Microplots (1 m × 1 m deep) were filled with Haplic Luvisols soil. Simulated soil contamination with −1 Ni was introduced in the following doses: 0—no metals, Ni—60, Ni —100 and Ni —240 mg kg . The phytoremedia- 1 2 3 tion potential of plants was evaluated using a tolerance index, bioaccumulation factor, and translocation factor. None of the tested plants was a species with high Ni phytoremediation potential. All of them demonstrated a total lack of usefulness for phytoextraction; however, they can be in some way useful for phytostabilization. Z. mays accumulated large amounts of Ni in the roots, which made it useful for phytostabilization, but, at the same time, showed little tolerance to this metal. For this reason, it can be successfully used only on soils medium-contaminated with Ni, where a large yield decrease did not occur. Its biomass may be safely used as cattle feed, as the Ni transfer from roots to shoots was strongly restricted. P. arundinacea and S. viminalis accumulated too little Ni in the roots to be considered as typical phytostabilization plants. However, they may be helpful for phytostabilization due to their high tolerance to Ni. These plants can grow in the soil contaminated with Ni, acting as a protection against soil erosion or the spread of contamination. Keywords Soil contamination · Nickel · Phytostabilization · Maize · Reed canary grass · Willow Introduction The total average Ni concentration in the soil is about −1 20 mg kg (Kabat-Pendias and Mukherjee 2007), and the Nickel, although necessary for living organisms in small allowable maximum limit is generally set at the level of −1 amounts, is toxic to humans, animals, and plants after 100 mg kg (Regulation of the Minister of the Environ- exceeding its tolerable level (Kabta-Pendias and Mukherjee ment 2016; Tóth et al. 2016). Soil contamination with Ni is 2007). This element gets into the environment from a number not very common, but there are areas where human activity of anthropogenic sources, such as combustion of fossil fuels, has led to its excessive accumulation. Literature data report mining and refining processes, nickel alloy manufacturing of numerous places in the world where Ni exceeds the per- (steel), electroplating, incineration of municipal wastes and missible limit. For example, the Ni concentration of the soil −1 sewage sludge (Ahmad and Ashraf 2011; Gaj et al. 2007). was 1600–2150 mg kg at Sudbury smelting area in Canada −1 Nickel contamination is highly probable to occur on the soils (Adamo et al. 2002; Narendrula et al. 2012), 303 mg kg at in the vicinity of metal smelters steel and mines. Plovdiv non-ferrous metal smelter in Bulgaria (Bacon and −1 Dinev 2005), 267 mg kg around the Selebi Phikwe Cu–Ni −1 mine in Botswana (Ngole and Ekosse 2012), 212 mg kg at the former sludge disposal site in Denmark (Algreen et al. Editorial responsibiility: M. Abbaspour. −1 2014) and 122 mg kg at the area of a former waste incin- * J. Korzeniowska eration plant in Czech Republic (Kacalkova et al. 2014). email@example.com Ni-contaminated areas require remediation. One of the new, rapidly growing remediation methods, which uses Department of Weed Science and Soil Tillage Systems in Wroclaw, Institute of Soil Science and Plant Cultivation plants, is phytoremediation. Its main advantage is positive - State Research Institute in Pulawy, ul. Orzechowa 61, effect on such soil parameters as fertility, biological activity 50-540 Wrocław, Poland Vol.:(0123456789) 1 3 International Journal of Environmental Science and Technology and structure, as well as its lower cost compared to other for phytoextraction (Cheraghi et al. 2011; McGrath and Zhao remediation techniques (Ghosh and Singh 2005; Mulligan 2003), while plants with a high bioaccumulation factor for et al. 2001).roots (BF > 1) and, simultaneously, with a low translocation roots The two most common phytoremediation techniques factor (TF < 1) are appropriate for phytostabilization (Cheraghi are phytoextraction and phytostabilization. Phytoextraction et al. 2011; Roccotiello et al. 2010). involves extracting contaminates from the soil by plants The use of energy plants for the Ni phytoremediation may through incorporating them in their tissues and then removing be a beneficial solution. The cultivation of these plants on con- them from the soil together with the harvested crops. Phyto- taminated lands can serve both for the remediation and for the stabilization involves using plants to immobilize the contami- production of biomass. Consequently, it is essential to identify nants in the soil. Metals are absorbed and accumulated by the the tolerance of the most used energy species such as willow, roots, adsorbed on the roots, or precipitated in the rhizosphere reed canary grass or maize to the excess of Ni in the soil and (Karczewska et al. 2013; Stanislawska-Glubiak et al. 2012). to investigate the Ni transfer from the roots to the aboveground This reduces the mobility of contaminants, making it difficult organs, which is important from the point of view of plants for them to migrate to groundwater and air, as well as lowers suitability for phytoremediation. So far no studies have been their bioavailability, thereby preventing their spread through- done on the potential for reed canary grass in areas contami- out the food chain. Plants used in phytostabilization reduce the nated with Ni, despite the fact that this plant produces a lot of amount of water percolating through the soil, thus minimizing biomass and is often used as a source of energy. On the other the hazardous leaching and preventing soil erosion, and hence, hand, research on the potential of Ni phytoremediation of other stop the distribution of toxic metals to other areas (Srivastava species, mainly willow and maize, was mostly carried out in 2016; Thakur et al. 2016). In the case of Ni, wind erosion pots, or more often, in hydroponics, which does not reflect field poses the biggest threat. Ni is especially dangerous when it conditions in which these plants actually grow (Antonkiewicz enters the body through dust inhalation (WHO 2000). Inhala- et al. 2016; Drzewiecka et al. 2012; Kopittke et al. 2010; Seregin tion exposure to Ni causes toxic effects in the respiratory tract et al. 2003). The only available study on willow and maize con- and immune system. Human and animal data provide strong ducted under field conditions was on the soils contaminated with evidence that inhalation exposure to some nickel compounds several metals jointly, which did not allow to draw conclusions can induce lung cancer (Tokar et al. 2011). about the Ni exclusively (Algreen et al. 2014; Kacalkova et al. Ni toxicity to plants is manifested by the decrease in 2014; Mleczek et al. 2009). All in all, there is a lack of research germination efficiency (Yusuf et al. 2011), the inhibition of that could be a reliable basis for the assessment of the suitability growth and root branching (Seregin et al. 2003), the reduc- of mentioned species for the phytoremediation of sites polluted tion of nutrient absorption by roots (Ahmad and Ashraf with Ni. Therefore, our study, the objective of which is to assess 2011), damage to the photosynthetic apparatus (Shafeeq the suitability of these species for Ni phytoremediation under et al. 2012), and the induction of oxidative stress (Ali et al. conditions similar to the actual field, is a novelty. In this study, 2003). All these negative processes result in a significant we hypothesized that three energy plants such as reed canary decrease in yields. grass (Phalaris arundinacea), maize (Zea mays) and willow Plant sensitivity to high Ni concentration in soil can hin- (Salix viminalis) can be useful for phytoextraction or phytosta- der the application of phytoremediation techniques, hence the bilization of soils contaminated with nickel. search for the tolerant species suitable for Ni extraction or Ni This study was carried out during 2009–2010 in Institute stabilization is an issue of great practical importance. The use- of Soil Science and Plant Cultivation-State Research Insti- fulness of plants for metal phytoremediation is evaluated on tute in Pulawy Poland. the basis of several parameters such as: (1) the tolerance of the plants to the metal associated with producing suc ffi iently high yields, (2) metal bioaccumulation in the aboveground parts and Materials and methods roots measured by the bioaccumulation factor (BF aboveground and BF ) and (3) the transfer of metal from roots to the Microplot experiment parts roots aboveground parts measured by the translocation factor (TF) (Raskin and Ensley 2000). BF (also called BAF or BCF) is The 2-year experiment was conducted at the Experimental defined as the ratio of metal concentration in aboveground Station Baborowko near Poznan (middle-west Poland) in four parts or roots to the metal in the soil, whereas TF as the ratio replicates with three tested plants: reed canary grass (Phala- of the metal in aboveground parts to the metal in roots (Golda ris arundinacea), maize (Zea mays) and willow (Salix vimi- and Korzeniowska 2016; Masarovicova et al. 2010; Melo et al. nalis). In the year preceding the planting/seeding plants, con- 2009; Stanislawska-Glubiak et al. 2015). crete-framed microplots (1 m × 1 m deep without bottom) Plants with a high biomass and high bioaccumulation factor in the open air were filled with Haplic Luvisols soil—the for aboveground parts (B F > 1) are appropriate most common type of soil in Poland. It was a coarse-textured aboveground parts 1 3 International Journal of Environmental Science and Technology soil with a low content of clay, low pH, and low content of while root biomass—on the basis of two rows of plants— organic matter (Table 1). The soil in microplots was artifi- removed from a plot (0.2 m ). In the second season, the bio- cially contaminated with Ni in the autumn in the year before mass of the aboveground parts and roots was evaluated based the introduction of plants. During the winter microplots on the plants remaining per plot (0.8 m ). P. arundinacea was were exposed to precipitation. The following doses of nickel harvested at the heading stage, giving only 1 biomass cut in were applied: 0-the control (no metals), Ni-40, Ni -80 and the first growing season (September 25, 2009) and 3 cuts in the 1 2 −1 Ni -160 mg kg . In total, 48 microplots were used (3 plants second season ( July 23/ August 8/ August 23, 2010). × 4 treatments × 4 replicates). Nickel doses were established The samples of the plants for chemical analyses were col- on the basis on the previous authors studies and literature lected during the harvest: Z. mays—(1) stems with leaves, (2) data (Korzeniowska et al. 2007, Poulik 1997). ears, (3) roots, P. arundinacea—(1) shoots, (2) roots, S. vimi- Nickel in the form of sulfate was dissolved in water and nalis—(1) twigs, (2) leaves, (3) roots. All plant samples were applied to the microplots using a hand liquid spreader. To carefully washed, dried at 60 ◦C, and finely ground. thoroughly mix the metal with the soil, it was first intro- Soil samples were collected during each autumn after the duced into the 15–30 cm soil layer, mixed, and then into the harvest using an Eijkelkamp soil sampler of the diameter size 0–15 cm layer, where it was carefully mixed again. 2.5 cm. The sample from each microplot consisted of carefully The plants were planted or sown in the spring, 1 year after mixed five subsamples, taken randomly across the plot from the introduction of Ni into the soil. All the test plants, apart depth 0–30 cm. Air-dry samples were passed through a sieve from P. arundinacea, were initially planted in higher density, with the mesh size of 2 mm. and after 2 months, plant thinning was performed, leaving 5 plants of S. viminalis and 12 of Z. mays on the microplot. In Calculation of TI, BF and TF the case of P. arundinacea, 6 g of seeds was sown per plot. In two growing seasons of the study, basic NPK ferti- Tolerance of Z. mays, P. arundinacea and S. viminalis to the lization was applied in the spring at 10: 2: 8 g per plot, excess of Ni was compared using tolerance index (TI), which respectively. The plants on microplots were hand-weeded reflected resistance to contamination. To compare the accumu- and watered during the periods of insufficient rainfall. lation and distribution of Ni in the tested plants, three param- The biomass of the aboveground parts and roots of Z. mays eters were used: bioaccumulation factor for aboveground parts and S. viminalis were determined by collecting the plants from and roots (BF) and translocation factor (TF). the area of 1 m . Root biomass of S. viminalis was determined TI was calculated as the ratio of biomass yield in the metal only for the second growing season. There was no possibility treatment to biomass in the control treatment according to the of determining root biomass in the first season due to the fact Wilkins (1978) formula in authors modification: that S. viminalis is a perennial plant. Z. mays was collected −2 mean yield of 3 doses of metal gm on September 6, 2009, and September 3, 2010 (stems with TI = × 100 leaves and cobs), while S. viminalis on October 25, 2009, and −2 control yield gm October 6, 2010 (branches with leaves), respectively, in the first and second growing season. BF and TF were calculated for each Ni concentration by the The biomass of the aboveground parts of P. arundinacea in following formulas according to Melo et al. (2009) in authors the first growing season was determined on the basis of 1 m , modification: BF Table 1 Chemical and physical properties of experimental soil before aboveground parts the introduction of nickel (0–30 cm) −1 metal concentration in aboveground parts mg kg Feature Value −1 metal concentration in soil mg kg pH in KCl 5.6 −1 Soil fraction 0.1–0.02 mm (%) 24 metal concentration in roots mg kg BF = roots Sol fraction < 0.02 mm (%) 16 −1 metal concentration in soil mg kg C org. (%) 0.8 a −1 P (mg kg ) 85 −1 metal concentration in aboveground parts mg kg a −1 K (mg kg ) 116 TF = −1 b −1 metal concentration in roots mg kg Mg (mg kg ) 51 c −1 Ni (mg kg ) 7.6 Egner Schachtschabel aqua regia 1 3 International Journal of Environmental Science and Technology slightly higher than doped probably due to the doping pro- Measurement of net photosynthesis rate cess and soil homogenization; however, differences in rela- tion to the expected values were low. The average concentra- Net photosynthesis rate was measured in the first growing −1 season, at the beginning of July (9 July and 10 July) using tion of this metal in Ni ranged from 49.9 to 58.2 mg kg , −1 in Ni —from 89.5 to 111 mg kg , while in Ni treatment— a portable Li 6400 recorder (LI-COR). The measurements 2 3 −1 were taken under comparable ambient conditions: in the from 182 to 186 mg kg , depending on the plant species. These concentrations corresponded to, respectively, weak, morning (9.00–12.00 am) at the constant PAR radiation −2 −1 −1 1200 μmol m s, CO concentration 390 mg kg , and medium and heavy contamination level according to the limits of soil contamination with heavy metals by Kabata- temperature 23–26 °C. Net photosynthesis was measured on randomly selected, youngest fully formed leaves in 12 Pendias et al. (1993). This assessment takes into account soil features such as soil fraction < 0.02 mm and soil pH replicates (3 measurements for each replicate). (Table 3). According to the Polish standards (Regulation of the Minister of the Environment 2016), the total Ni concen- Chemical analyses tration in the soil on agricultural areas should not exceed −1 100 mg kg , which coincides with the upper limit of the All chemical analyses were done by the Central Laboratory of the Institute of Soil Science and Plant Cultivation-State Research average soil contamination acc. to Kabata-Pendias et al. (1993). In the present study, the Ni concentration exceeded Institute, certie fi d by the Polish Centre of Accreditation accord - ing to PN-EN ISO/IEC 175 17025 (certificate no. AB 339). the allowable limit only in the treatment Ni . P and K in soil were determined by Egner–Riehm method (PN-R-04023:1996 and PN-R-04022:1996 adequately), Mg Plant biomass by Schachtschabel method (PN-R-04020:1994), total organic carbon (TOC) by Tiurin method using potassium dichro- Ni phytotoxicity, manifested by the reduction in biomass yields, varied depending on the plant species and the level of soil con- mate (ISO 14235:2003), pH—potentiometrically in 1 mol −3 KCl.dm (ISO 10390:2005), and texture by the aerometric tamination Ni –Ni (Table 4). Plants responded to the Ni reduc- 1 3 tion of both the biomass of the aboveground parts and roots. method (PN-R-04033:1998). The Ni concentration in the soil was determined using The biomass of the aboveground parts of each tested spe- cies systematically decreased relative to the control, together aqua regia (ISO 11466:1995). After the digestion, Ni was determined using the FAAS method. with increasing Ni in the soil. It was noticed in both growing seasons (Table 4, Fig. 1). However, the differences between Nickel in plant tissue was determined by the FAAS method, having first dry ashed the material in a muffle fur - the seasons in plant responses to Ni should be considered nace and digested it with 20% nitric acid (PN-R-04014:1991). Table 2 Total nickel concentration in soil at the end of the growing A standard reference material IPE 952 (International Plant- −1 seasons (mg kg ) Analytical Exchange) from Wageningen (Netherlands) was used for quality control purposes. The recovery values ranged Plant Treatment I season II season Mean Contam- ination from 88 to 106%, which were considered satisfactory. level Statistical analyses Z. mays 0 8.3 ± 0.5 6.5 ± 0.5 7.4 a 0 Ni 67.5 ± 5 48.9 ± 2 58.2 b II/III The results of plant biomass and Ni concentration were Ni 74.9 ± 8 104 ± 9 89.5 c III given as the means from four replications, and for net pho- Ni 187 ± 6 180 ± 9 184 d IV tosynthesis as a mean from 12 replications. ANOVA calcu- P. arundinacea 0 7.1 ± 0.3 6.0 ± 0.4 6.6 a 0 lations were performed using the Statgraphics v 5.0 soft- Ni 45.5 ± 4 61.1 ± 7 53.3 b II/III ware. Multiple comparisons among groups were made with Ni 86.6 ± 9 136 ± 11 111 c III/IV Tukey’s honestly significant difference (P < 0.05). Ni 181 ± 14 192 ± 10 186 d IV S. viminalis 0 7.5 ± 0.4 6.1 ± 0.4 6.8 a 0 Ni 50.1 ± 0.4 49.6 ± 3 49.9 b II Results and discussion Ni 100 ± 6 80.5 ± 6 90.3 c III Ni 185 ± 9 180 ± 17 182 d IV Nickel concentration in the soil Same letters for each plant-year combination indicate the lack of sig- nificant differences according to Tukey’s test (P < 0.05). The concen- Ni concentration in the soil after plant harvest remained at a trations in I and II season are average values of 4 replicates ± standard similar level in both growing seasons (Table 2). The concen- error tration of Ni in soil at the end of both growing seasons was acc. Kabata-Pendias et al. 1993 1 3 International Journal of Environmental Science and Technology die ff rently for an annual plant Z. mays than for perennials, P. S. viminalis exhibited a much lower sensitivity to high arundinacea and S. viminalis. The biggest reduction in the concentrations of Ni in the soil than P. arundinacea and aboveground parts was recorded for Z. mays. The biomass of Z. mays. A significant reduction in the aboveground parts this plant in the first growing season decreased significantly, in Ni3 treatment for S. viminalis did not exceed 35% in by 19% in N , and by 71% in N . It was similar in the second both growing seasons, while for other two plants was much 2 3 season, where the reduction was 13 and 83%, respectively. higher, especially in the first season. The biomass of the aboveground parts of the perennial Soil contamination with Ni resulted not only in the reduc- grass P. arundinacea decreased only in Ni , whereas in the tion in the aboveground parts, but also the reduction in the second growing season, this reduction was significantly growth of roots, with the exception of S. viminalis (Table 4, smaller (28%) in comparison with the first season (56%). Fig. 2). Particularly large reductions were recorded for Z. The authors believe that this may be related to the age and mays. In the first growing season, the root biomass of this length of roots. It can be assumed that in the second season, plant decreased significantly by 21% in N and by 77% in the roots of grass reached the deeper, into the uncontami- N treatment, while in the second season, by 64% in N in 3 3 nated soil layers. Microplots used in our experiment were relation to the control. The impact of Ni on the restriction 1 m deep, while Ni was introduced to a depth of 30 cm only. Korzeniowska and Stanisławska-Glubiak (2015) recorded a c b c b similar phenomenon in another grass (Spartina pectinata); c c bc 80 c a b there was a smaller yield decline under the influence of Ni b b in the second year than in the first year of growth. Table 3 Nickel contamination assessment of light sandy soil accord- ing. Reproduced with permission from Kabata-Pendias et al. (1993) −1 0Ni1 Ni2Ni3 0Ni1 Ni2Ni3 0Ni1 Ni2Ni3 Contamination level Ni in mg kg Z. mays P. arundinacea S. viminalis 0—background content < 10 I season II season I—increased content 11–30 II—weak contamination 31–50 Fig. 1 Relative aboveground biomass of tested plants: Z. III—medium contamination 51–100 mays − steams + ears, P. arundinacea − sum of 3 cuts of above- IV—heavy contamination 101–400 ground parts, S. vinimalis − twigs. Control values were taken as V—very heavy contamination > 400 100%. Same letters for each plant-year combination indicate the lack of significant differences according to Tukey’s test (P < 0.05) Content of soil fraction < 0.02 mm: 10–20%, pH < 5.5 Table 4 Biomass of tested Plant I season II season plants at the end of growing seasons (g m ) Z. mays Steams Ears Roots Steams Ears Roots 0 752 ± 12 d 1050 ± 26 c 191 ± 8 c 671 ± 9 d 790 ± 13 c 173 ± 2 b Ni 683 ± 26 c 1007 ± 20 bc 186 ± 4 c 630 ± 15 c 816 ± 23 c 163 ± 3 b Ni 526 ± 16 b 942 ± 22 b 150 ± 12 b 549 ± 17 b 726 ± 16 b 162 ± 2 b Ni 207 ± 63 a 309 ± 93 a 44 ± 15 a 99 ± 39 a 144 ± 54 a 62 ± 5 a P. arundinacea Shoots Roots Shoots Roots 0 754 ± 15 c 545 ± 17 c 1464 ± 11 c 825 ± 54 c Ni 747 ± 14 c 569 ± 11 c 1394 ± 41 c 821 ± 11 c Ni 621 ± 7 b 498 ± 16 b 1295 ± 12 b 697 ± 24 b Ni 333 ± 32 a 337 ± 41 a 1048 ± 41 a 595 ± 49 a S. viminalis Twigs Roots Twigs Roots 0 740 ± 5 c x 3008 ± 142 b 430 ± 17 ab Ni 698 ± 22 bc x 2918 ± 209 b 438 ± 21 ab Ni 674 ± 6 b x 3100 ± 177 b 440 ± 35 b Ni 508 ± 41 a x 1960 ± 165 a 400 ± 35 a sum of 3 cuts x-not collected. Same letters for each plant organ-year combination indicate the lack of significant dif- ferences according to Tukey’s test (P < 0.05). The results in the table are average values of 4 repli- cates ± standard error 1 3 % International Journal of Environmental Science and Technology of the growth of the Z. mays roots was confirmed by other However, hydroponic and pot studies allow to compare authors who, under hydroponic conditions, found that Ni the tolerance of several species between themselves to Ni. accumulated in the roots restricted their branching (Seregin A high sensitivity of Z. mays to Ni found in our studies has et al. 2003) and a length (Maksimovic et al. 2007). been confirmed by Antonkiewicz et al. (2016). These authors In the species P. arundinacea, soil contamination with Ni found that the hydroponically grown Z. mays responded with caused a reduction in the biomass of roots only at the level of a bigger reduction of the aboveground parts to the increase Ni . In both seasons, growth reduction was, respectively, 38 in Ni concentration in the culture medium (80% compared and 28% compared to the control. It should be noted that in to control) than beans (60%) or lettuce (23%). this perennial grass, in the first season, the reduction in bio- mass yields caused by an excessive Ni in the soil, was bigger Photosynthesis rate for the aboveground parts (the decrease by 58%) than for the roots (38%), while in the second season, it was similar for Nickel decreased the net photosynthesis rate of all the tested the two parts (28% each). plant species (Table 6). A significant decrease occurred with Tolerance indices, calculated for both aboveground parts Z. mays in Ni and Ni and with P. arundinacea and S. vimi- 2 3 and roots of the tested plants, indicate that Z. mays is the nalis in N treatment. most sensitive species to excessive Ni in the soil, while S. These results are consistent with the above-mentioned viminalis is the most tolerant one (Table 5). biomass decrease in the aboveground parts of the tested There are no studies in field condition that would confirm species. The inhibition of photosynthesis rate was the big- our results of high tolerance of S. vinimalis and low toler- gest with Z. mays, while the smallest with S. viminalis. ance of Z. mays for Ni. The field studies with S. viminalis Physiological studies confirm that Ni damages the photo- were conducted by Ali et al. (2003), Algreen et al. (2014), synthetic apparatus at almost every level of its organiza- and Kacalkova et al. (2014), but only on soils contaminated tion (Chen et al. 2009). Shafeeq et al. (2012), in pot experi- with several heavy metals jointly, so it was not possible to ments, recorded a systematic decrease photosynthetic rate assess the impact of the Ni exclusively on the formation of of wheat together with an increasing dose of Ni from 50 to −1 willow biomass. 300 mg kg . It is possible to find some information about tolerance of S. viminalis and Z. mays to Ni exclusively, but obtained Ni concentration in plants on the basis of pot or hydroponic experiments. Torres et al. (2016), in the pot experiment, observed a 40% bio- Ni concentration in organs of Z. mays was in the follow- mass reduction in 50-day shoots of Z. mays at a dose of ing order: ears < steams < roots (Table 7). Ears contained −3 −1 −1 10 mg dm Ni. A significant tolerance of S. viminalis to Ni 1.7–5.4 mg kg , while stems 1.1–10.7 mg kg Ni, depend- in hydroponic conditions was demonstrated by Drzewiecka ing on the level of contamination of the soil and the growing et al. (2012). According to these authors, this plant can be season. These concentrations do not exceed the maximal grown on soils heavily contaminated with Ni. It should be tolerable dietary level of this metal for beef cattle and dairy −1 noted, however, that the bioavailability of metals from nutri- cattle, which is 50 mg kg dm. (NRC 1996; NCR 2001). ent solutions or pots is much higher than that of field soils, The roots contained a dozen or even several dozen times and such studies cannot be used to assess the actual suit- more Ni than the aerial parts. At the highest level of con- ability of plants for phytoremediation. tamination of Ni , the roots contained, respectively, 16 and 12 times more Ni than the stems, and 44 and 24 times more Ni than the ears, respectively, for the first and second season. ab b b c b Ni concentration in the aboveground parts of P. arundinacea ab b a −1 c c was higher than in Z. mays, amounting to 10.1–31.6 mg kg , b a Table 5 Tolerance index in % Plant I season II season 0 Aboveground Roots Aboveground Roots 0Ni1 Ni2Ni3 0Ni1 Ni2Ni3 0Ni1 Ni2Ni3 parts parts Z. mays P. arundinaceaS. viminalis Z. mays 68 66 68 75 I season II season P. arundinacea 75 86 85 85 S. viminalis 85 x 88 99 Fig. 2 Relative roots biomass of tested plants. Control values were taken as 100%. Same letters for each plant-year combination indicate Aboveground parts: Z. mays − steams + ears. P. arundinacea − sum the lack of significant differences according to Tukey’s test (P < 0.05) of 3 cuts of aboveground parts. S. vinimalis − twigs 1 3 % International Journal of Environmental Science and Technology depending on the level of contamination and a season, but it leaves, and 7.5 and 6.5 times higher compared to the twigs, never exceeded the maximal tolerable dietary level. In their depending on the growing season. roots, the plants accumulated only a few times more Ni than In our study, Z. mays showed the highest ability to accu- in aboveground parts. The roots contained about 4–5 times mulate Ni in the roots among the plants tested. These results more Ni than the aboveground parts, regardless of the level of are confirmed by Antonkiewicz et al. (2016), who found that contamination of Ni –Ni or the growing season. hydroponically growing Z. mays accumulated 30 times more 1 3 Ni concentration in the organs of S. viminalis was in the Ni in the roots than in the stems at the concentration of 10 mg −3 following order: twigs < leaves < roots. Twigs contained dcm Ni in nutrient solution. There is a lack of reports on −1 −1 2.1–6.2 mg kg , while leaves 3.5–10.4 mg kg Ni, depend- the response of P. arundinacea to Ni. Only Vymazal et al. ing on the level of Ni and a season. The roots had a sev- (2011) found a higher Ni concentration in the roots than in eral times higher Ni concentration than the leaves or twigs. the aboveground parts of the grass growing in a constructed At the level of Ni , it was 7.5 and 2.5 times higher than in wetland treated with municipal sewage. Other authors also observed a higher Ni concentration in the roots in comparison with the aboveground parts of other plant species (Ahmad Table 6 Net photosynthesis rate of leaves (I vegetation season) et al. 2007; Al Chami et al. 2015; Antonkiewicz et al. 2016). 2 −1 Plant Treatmentμmol CO m s % Similarly as in our research on S. viminalis, Drzewiecka et al. (2012), under hydroponic conditions, observed the Z. mays 0 23.2 ± 2 a 100 smallest Ni concentration in the twigs, higher in leaves, Ni 24.1 ± 2 a 104 while the highest in the roots. In the study of Kacalkova et al. Ni 17.3 ± 1 b 75 (2014), willow growing on soils naturally contaminated with Ni 14.2 ± 1 c 61 several metals jointly, accumulated more Ni in the leaves P. arundinacea 0 15.4 ± 1 a 100 than in the twigs. Moreover, willow leaves contained more Ni 17.0 ± 1 a 110 Ni compared with the leaves of maize, sunflower, or poplar. Ni 15.5 ± 2 a 101 A significant accumulation of Ni in the leaves of S. viminalis Ni 8.2 ± 0.8 b 53 was also emphasized by Mleczek et al. (2009), even though S. viminalis 0 14.4 ± 1 a 100 the concentration of this metal in the roots was higher. Ni 15.8 ± 1 a 110 Ni 15.5 ± 2 a 108 Ni accumulation and translocation Ni 12.0 ± 0.9 b 83 The results in the table are average values of 12 replicates ± standard The tested plants showed a various ability to accumulate error. Same letter for each plant indicate the lack of significant differ - Ni, as measured by bioaccumulation factor (BF) (Table 8). ences according to Tukey’s test (P < 0.05) S. viminalis accumulated small amounts of Ni, both in Table 7 Ni concentration in Plant Treatment I season II season plants in the end of the growing −1 seasons (mg kg ) Z. mays Steams Ears Roots Steams Ears Roots 0 1.7 ± 0.1 a 0.8 ± 0.04 a 1.6 ± 0.1 a 0.9 ± 0.03 a 0.3 ± 0.03 a 2.1 ± 0.2 a Ni 2.7 ± 0.1 b 1.7 ± 0.1 b 60.4 ± 5 b 1.1 ± 0.04 b 2.1 ± 0.1 b 29.5 ± 2 b Ni 5.4 ± 0.3 c 2.5 ± 0.1 c 91.4 ± 6 c 2.6 ± 0.1 c 3.3 ± 0.1 c 80.4 ± 8 c Ni 10.4 ± 0.4 d 3.8 ± 0.2 d 169 ± 14 d 10.7 ± 0.5 d 5.4 ± 0.2 d 132 ± 12 d P. arundinacea Shoots Roots Shoots Roots 0 1.1 ± 0.1 a 3.0 ± 0.2 a 0.9 ± 0.04 a 1.6 ± 0.2 a Ni 10.1 ± 0.6 b 42.2 ± 2 b 13.7 ± 0.2 b 50.9 ± 5 b Ni 14.0 ± 0.4 c 67.5 ± 5 c 21.2 ± 1 c 65.5 ± 5 c Ni 24.9 ± 1 d 133 ± 11 d 31.6 ± 0.8 d 133 ± 11 d S. viminalis Twigs Leaves Roots Twigs Leaves Roots 0 2.2 ± 0.1 a 0.7 ± 0.04 a 2.6 ± 0.1 a 0.6 ± 0.1 a 0.5 ± 0.05 a 1.3 ± 0.1 a Ni 2.6 ± 0.2 ab 3.5 ± 0.1 b 4.9 ± 0.2 b 2.1 ± 0.2 b 5.6 ± 0.3 b 10.1 ± 0.9 b Ni 2.7 ± 0.2 b 5.7 ± 0.5 c 15.0 ± 1 c 2.4 ± 0.1 b 7.4 ± 0.3 c 11.6 ± 0.8 b Ni 6.2 ± 0.4 c 9.3 ± 0.5 d 46.6 ± 4 d 4.1 ± 0.2 c 10.4 ± 0.4 d 26.6 ± 2 c Mean over 3 cuts. The results in the table are average values of 4 replicates ± standard error. Same let- ter for each plant-year combination indicate the lack of significant differences according to Tukey’s test (P < 0.05) 1 3 International Journal of Environmental Science and Technology the aboveground parts and in the roots (mean BF and 0.20–0.28, while TF and TF for S. viminalis were twigs twigs leaves BF ≤ 0.09, BF ≤ 0.19). Among the tested plants, P. 0.18–0.20 and 0.34–0.52, respectively, depending on the leaves roots arundinacea showed the highest ability to bioaccumulate growing season. Ni by the aboveground parts and relatively high by roots (mean BF = 0.17–0.18, BF = 0.67–0.81). Z. mays shoots roots accumulated the least Ni in the aboveground parts, and at Conclusion the same time, the most Ni in the roots (mean BF and steams BF ≤ 0.06, BF = 0.7–1.0). The efficiency of phytoremediation depends on the toler - ears roots Other authors confirm the low bioaccumulation of Ni by ance of plant species to contamination and their ability to the aboveground parts of maize. accumulate metals in aboveground organs and roots. Metal Fargasova (2012) and Antonkiewicz et al. (2016) showed phytoextraction from the soil can be performed by tolerant a lower BF value for Z. mays than for Viciasativa, Raphanus plants with high biomass production and BF > 1, aboveground part sativus, Synapsis alba, lettuce and field bean. while phytostabilization by plants without a significant bio- In our study, all the plants accumulated more mass reduction and having BF > 1 and TF < 1. None of roots Ni in the roots than in the aboveground parts the tested plants was a species with high Ni phytoremedia- (BF > BF ). At the same time, all tion potential, as they did not meet the necessary above- roots aboveground parts BF were much lower than 1.0, indicating a total mentioned criteria. aboveground parts lack of usefulness of the tested plants for phytoextraction Z. mays showed a relatively high ability to bioaccumulate (McGrath and Zhao 2003). At the same time, the value of Ni in the roots (BF ~ 1), and at the same time, a unique roots BF close to 1.0 for Z. mays suggests its suitability for ability to prevent its transfer to the aboveground parts roots phytostabilization (Cheraghi et al. 2011). (TF ≤ 0.08). Due to this mechanism, Ni concentration in the Ni transport from the roots to the aboveground parts of all tissues of the aboveground parts does not exceed the maxi- three species tested was limited, as evidenced by the values mal tolerable dietary level for cattle, even under heavy soil of TFs < 1 (Table 9). However, TFs values for Z. mays were contamination. These traits may indicate a high phytostabi- significantly lower than for P. arundinacea and S. viminalis, lization potential of Z. mays. Unfortunately, on the heavily oscillating from 0.02 to 0.08. It means that plants transferred contaminated soils, this plant showed the lowest tolerance to only 2–8% Ni from the roots to the aboveground parts. Also, Ni among the three species, which was reflected by a signifi- in the studies of Fargasova (2012) and Antonkiewicz et al. cant, up to 83%, biomass reduction. However, Z. mays can be (2016), the values of TFs for Z. mays were lower than for successfully used for phytostabilization of the soils medium- other species investigated plants. According to Seregin et al. contaminated with Ni, while biomass collected annually can (2003), Z. mays belongs to excluder plants, as its roots con- be safely used as feed for cattle. stitute a barrier limiting Ni transport to the shoots. Perennial P. arundinacea and S. viminalis showed a P. arundinacea and S. viminalis showed higher TF values higher Ni tolerance than Z. mays, whereas this tolerance than Z. mays. The mean T F for P. arundinacea were increased in the second growing season compared to the shoots Table 8 Bioaccumulation factor Plant Treatment I season II season (BF) Z. mays Steams Ears Roots Steams Ears Roots Ni 0.04 0.02 0.89 0.02 0.04 0.60 Ni 0.07 0.03 1.22 0.02 0.03 0.77 Ni 0.06 0.02 0.90 0.06 0.03 0.73 mean 0.06 0.02 1.00 0.03 0.03 0.70 P. arundinacea Shoots Roots Shoots Roots Ni 0.22 0.93 0.22 0.83 Ni 0.16 0.78 0.16 0.48 Ni 0.14 0.73 0.16 0.69 mean 0.17 0.81 0.18 0.67 S. viminalis Twigs Leaves Roots Twigs Leaves Roots Ni 0.05 0.07 0.10 0.04 0.11 0.20 Ni 0.03 0.06 0.15 0.03 0.09 0.14 Ni 0.04 0.06 0.31 0.03 0.07 0.18 mean 0.04 0.06 0.19 0.03 0.09 0.17 Mean over 3 cuts 1 3 International Journal of Environmental Science and Technology Table 9 Translocation factor (TF) References Plant Treatment I season II season Adamo P, Dudka S, Wilson MJ, McHardy WJ (2002) Distribu- tion of trace elements in soils from the Sudbury smelting area Z. mays Steams Ears Steams Ears (Ontario, Canada). 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