Abstract
We tested the suitability of Salix viminalis for phytoextraction with the analysis of selected elements in soil, root, and leaf, and by visual tree condition assessment in an area with varying levels of contamination. Bioconcentration factor (BCF) and translocation factor (TF) were used to assess the phytoextraction potential of willows. The middle part of the study area was strongly contaminated, while the northern and southern parts were moderately contaminated. We found increasing element concentrations toward deeper layers. Mean concentrations of elements in roots were similar among the three parts, while in leaves the highest concentrations were found in the strongly contaminated part of the study area. Tree condition scores were the lowest in the strongly contaminated part of the study area, which was caused by Al, Ca, K, Mg, Ni, Sr, and Zn concentration. These elements induced leaf disease and leaf feeders. The highest BCF values were found for Cu, Fe, Mn, and Zn in root, and for Cd and Zn in leaves, indicating that S. viminalis had high accumulation potential of these elements. Furthermore, TF values were high for Cd, Mn, Sr, and Zn. Our results also demonstrated that soil element composition has major influence on the condition of S. viminalis individuals. Furthermore, visual condition assessment was found to be a useful tool to assess the phytoextraction potential of trees.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad MS, Ashraf M (2011) Essential roles and hazardous effects of nickel in plants. Rev Environ Contam T 214:125–167
Anh BTK, Ha NTH, Danh LT, Van Minh V, Kim DD (2017) Phytoremediation applications for metal-contaminated soils using terrestrial plants in Vietnam. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation, pp 157–181. https://doi.org/10.1007/978-3-319-52381-1_6
Algreen M, Trapp S, Rein A (2014) Phytoscreening and phytoextraction of heavy metals at Danish polluted sites using willow and poplar trees. Environ Sci Pollut R 21(15):8992–9001. https://doi.org/10.1007/s11356-013-2085-z
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Balogh Z, Harangi S, Gyulai I, Braun M, Hubay K, Tóthmérész B, Simon E (2017) Exploring river pollution based on sediment analysis in the upper Tisza region (Hungary). Environ Sci Pollut Res 24(5):4851–4859. https://doi.org/10.1007/s11356-016-8225-5
Begley D, McCracken AR, Dawson WM, Watson S (2009) Interaction in short rotation coppice willow, Salix viminalis genotype mixtures. Biomass Bioenergy 33(2):163–173. https://doi.org/10.1016/j.biombioe.2008.06.001
Boisvert S, Joly D, Leclerc S, Govindachary S, Harnois J, Carpentier R (2007) Inhibition of the oxygen-evolving complex of photosystem-II and depletion of extrinsic polypeptides by nickel. Biometals 20(6):879–889. https://doi.org/10.1007/s10534-007-9081-z
Borišev M, Pajević S, Nikolić N, Krstić B, Župunski M, Kerbert M, Pilipović A, Orlović S (2012) Response of Salix alba L. to heavy metals and diesel fuel contamination. Afr J Biotechnol 11:14313–14319
Borišev M, Pajević S, Nikolić N (2016) Magnesium and iron deficiencies alter Cd accumulation is Salix viminalis L. Int J Phytoremediat 18(2):164–170. https://doi.org/10.1080/15226514.2015.1073670
Budak F, Zaimoğlu Z, Başcı N (2011) Uptake and translocation of hexavalent chromium by selected species of ornamental plants. Polish J Environ Stud 20:857–862
Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. Clean-Soil Air Water 37(4-5):304–313. https://doi.org/10.1002/clen.200800199
Chen M, Tang YL, Ao J (2012) Effects of strontium on photosynthetic characteristics of oilseed rape seedlings. Russ J Plant Physl 59(6):772–780. https://doi.org/10.1134/S1021443712060052
Cloutier-Hurteau B, Turmel MC, Mercier C, Courchesne F (2014) The sequestration of trace elements by willow (Salix purpurea)—which soil properties favor uptake and accumulation? Environ Sci Pollut R 21(6):4759–4771. https://doi.org/10.1007/s11356-013-2450-y
Colle C, Madoz-Escande C, Leclerc E (2009) Foliar transfer into the biosphere: review of translocation factors to cereal grains. J Environ Radioact 100(9):683–689. https://doi.org/10.1016/j.jenvrad.2008.10.002
Cosio C, Vollenweider P, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.) I. Macrolocalization and phytotoxic effects of cadmium. Environ Exp Bot 58(1-3):64–74. https://doi.org/10.1016/j.envexpbot.2005.06.017
Courchesne F, Turmel MC, Cloutier-Hurteau B, Tremblay G, Munro L, Masse J, Labrecque M (2017) Soil trace element changes during a phytoremediation trial with willows in southern Québec, Canada. Int J Phytoremediat 19(7):632–642. https://doi.org/10.1080/15226514.2016.1278422
Dimitriou I, Eriksson J, Adler A, Aronsson A, Verwijst T (2006) Fate of heavy metals after application of sewage sludge and wood–ash mixtures to short-rotation willow coppice. Environ Pollut 142(1):160–169. https://doi.org/10.1016/j.envpol.2005.09.001
Ding C, Li X, Zhang T, Ma Y, Wang X (2014) Phytotoxicity and accumulation of chromium in carrot plants and the derivation of soil thresholds for Chinese soils. Ecotox Environ Safe 108:179–186. https://doi.org/10.1016/j.ecoenv.2014.07.006
Drzewiecka K, Mleczek M, Gansecka M, Magdziak Z, Goliński P (2012) Changes in Salix viminalis L. cv ‘Cannabina’ morphology and physiology in response to nickel ions—hydroponic investigations. J Hazard Mater 217–218:429–438. https://doi.org/10.1016/j.jhazmat.2012.03.056
Evlard A, Sergeant K, Printz B, Guignard C, Renaut J, Campanella B, Paul R, Hausman JF (2014) A multiple-level study of metal tolerance in Salix fragilis and Salix aurita clones. J Proteome 101:113–129. https://doi.org/10.1016/j.jprot.2014.02.007
Ferreiro-Domínguez N, Rigueiro-Rodríguez A, Bianchetto E, Mosquera-Losada MR (2014) Effect of lime and sewage sludge fertilisation on tree and understory interaction in a silvopastoral system. Agric Ecos Environ 188:72–79. https://doi.org/10.1016/j.agee.2014.02.007
Gobran GR, Fenn LB, Persson H (1993) Nutrition response of Norway spruce and willow to varying levels of calcium and aluminium. Fert Res 34(2):181–189. https://doi.org/10.1007/BF00750113
Greger M, Landberg T (2015) Novel field data on phytoextraction: pre-cultivation with Salix reduces cadmium in wheat grains. Int J Phytoremediat 17(10):917–924. https://doi.org/10.1080/15226514.2014.1003785
Guo TR, Yao CP, Zhang ZD, Wang JJ, Wang M (2012) Involvement of antioxidative defense system in rice seedlings exposed to aluminium toxicity and phosphorus deficiency. Rice Sci 19(3):207–212. https://doi.org/10.1016/S1672-6308(12)60042-0
Hafsi C, Debez A, Abdelly C (2014) Potassium deficiency in plants: effects and signaling cascades. Acta Physiol Plant 36(5):1055–1070. https://doi.org/10.1007/s11738-014-1491-2
Heintzman RL, Titus JE, Zhu WX (2015) Effects of roadside deposition on growth and pollutant accumulation by willow (Salix miyabeana). Water Air Soil Pollut 226(2):11. https://doi.org/10.1007/s11270-014-2270-9
Heiri O, Lotter AF, Lemcke G (2001) Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol 25(1):101–110. https://doi.org/10.1023/A:1008119611481
Hodson MJ (2012) Metal toxicity and tolerance in plants. Biochemist 34:28–32
Huber H, Chen X, Hendriks M, Keijsers D, Voesenek LACJ, Pierik R, Poorter H, de Kroon H, Visser EJW (2012) Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage. New Phytol 194(2):572–582. https://doi.org/10.1111/j.1469-8137.2012.04075.x
Ignatowicz K (2016) Using phytoremediation and bioremediation for protection soil near graveyard. J. Ecol Eng 17(3):87–90. 10.12911/22998993/63313
Irshad M, Ahmad S, Pervez A, Inoue M (2015) Phytoaccumulation of heavy metals in natural plants thriving on wastewater effluent at Hattar industrial estate, Pakistan. Int J Phytoremediat 17(2):154–158. https://doi.org/10.1080/15226514.2013.862208
Janssen J, Weyens N, Croes S, Beckers B, Meiresonne L, Van Peteghem P, Carleer R, Vangronsveld J (2015) Phytoremediation of metal contaminated soil using willow: exploiting plant-associated bacteria to improve biomass production and metal uptake. Int J Phytoremediat 17(11):1123–1136. https://doi.org/10.1080/15226514.2015.1045129
Kaczynski KM, Cooper DJ (2013) The role of potential future climate change on willow dieback. Forest Ecol Manag 305:223–228. https://doi.org/10.1016/j.foreco.2013.06.002
Karimaei M, Poozesh V (2016) Effects of aluminum toxicity on plant height, total chlorophyll (Chl a+b), potassium and calcium contents in spinach (Spinacia oleracea L.) Intl J Farm & Alli Sci 5:76–82
Kozhevnikova AD, Seregin IV, Bystrova EI, Belyaeva AI, Kataeva MN, Ivanov VB (2009) The effects of lead, nickel, and strontium nitrates on cell division and elongation in maize roots. Russ J Plant Physl+ 56:242–250
Kubátová P, Hejcman M, Száková J, Vondráčková S, Tlustoš P (2016) Effects of sewage sludge application on biomass production and concentrations of Cd, Pb and Zn in shoots of Salix and Populus clones: improvement of phytoremediation efficiency in contaminated soils. Bioenerg Res 9(3):809–819. https://doi.org/10.1007/s12155-016-9727-1
Kuzovkina YA, Knee M, Quigley MF (2004) Cadmium and copper uptake and translocation in five willow (Salix L.) species. Int J Phytoremediat 6(3):269–287. https://doi.org/10.1080/16226510490496726
Landberg T, Greger M (1996) Differences in uptake and tolerance to heavy metals in Salix from unpolluted and polluted areas. Appl Geochem 11(1-2):175–180. https://doi.org/10.1016/0883-2927(95)00082-8
Liu W, Ni J, Zhou Q (2013) Uptake of heavy metals by trees: prospects for phytoremediation. Mater Sci Forum 743–744:768–781
Mahar A, Wang P, Ali A, Kumar Awasthi M, Hussain Lahori A, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotox Environ Safe 126:111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023
Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad, Pakistan. Pak J Bot 42:291–301
Maxted AP, Black CR, West HM, Crout NMJ, McGrath SP, Young SD (2007) Phytoextraction of cadmium and zinc by Salix from soil historically amended with sewage sludge. Plant Soil 290(1-2):157–172. https://doi.org/10.1007/s11104-006-9149-5
Ministry of the Environment, Finland (2007) Government decree on the assessment of soil contamination and remediation needs (214/2007, March 1, 2007) http://www.finlex.fi/fi/laki/kaannokset/2007/en20070214.pdf
Mleczek M, Kozlowska M, Kaczmarek Z, Chadzinikolau T, Golinski P (2012) Influence of Ca/Mg ratio on phytoextraction properties of Salix viminalis I. The effectiveness of Cd, Cu, Pb, and Zn bioaccumulation and plant growth. Int J Phytoremediat 14(1):75–88. https://doi.org/10.1080/15226514.2011.573824
Moyen C, Roblin G (2010) Uptake and translocation of strontium in hydroponically grown maize plants, and subsequent effects on tissue ion content, growth and chlorophyll a/b ratio: comparison with Ca effects. Environ Exp Bot 68(3):247–257. https://doi.org/10.1016/j.envexpbot.2009.12.004
Nagajyoti PC, Lee KD, Sreekanth TMV (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216. https://doi.org/10.1007/s10311-010-0297-8
Ndeda LA, Manohar S (2014) Bio concentration factor and translocation ability of heavy metals within different habitats of hydrophytes in Nairobi dam, Kenya. J Environ Sci Toxicol. Food Technol 8:42–45
Ngole VM, Ekosse GIE (2012) Copper, nickel and zinc contamination in soils within the precincts of mining and landfilling environments. Int J Environ Sci Technol 9(3):485–494. https://doi.org/10.1007/s13762-012-0055-5
Padmavathiamma PK, Ahmed M, Rahman HA (2014) Phytoremediation—a sustainable approach for contaminant remediation in arid and semi-arid regions—a review. Emir J Food Agric 26(9):757–772. https://doi.org/10.9755/ejfa.v26i9.18202
Panda SK, Baluska F, Matsumoto H (2009) Aluminium stress signaling in plants. Plant Signal Behav 4(7):592–597. https://doi.org/10.4161/psb.4.7.8903
Placek A, Grobelak A, Kacprzak M (2016) Improving the phytoremediation of heavy metals contaminated soil by use of sewage sludge. Int J Phytoremediat 18(6):605–618. https://doi.org/10.1080/15226514.2015.1086308
Rooney CP, Zhao FJ, McGrath SP (2007) Phytotoxicity of nickel in a range of European soils: influence of soil properties, Ni solubility and speciation. Environ Pollut 145(2):596–605. https://doi.org/10.1016/j.envpol.2006.04.008
Rout GR, Das P (2009) Effect of metal toxicity on plant growth and metabolism: I. Zinc. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Dordrecht, pp 873–884. https://doi.org/10.1007/978-90-481-2666-8_53
Rout GR, Samantaray S, Das P (2001) Aluminium toxicity in plants: a review. Agronomie 21(1):3–21. https://doi.org/10.1051/agro:2001105
Różanowski B, Michałowski M, Tora B, Cablik V, Cernotova L (2012) Effectiveness of the use of willow tree (Salix viminalis) for wastewater treatment. AGH J Min Geoeng 36:159–164
Rudnick RL, Gao S (2004) Composition of the continental crust. In: Holland HD, Turekian KK (eds) Treatise on geochemistry, vol 3. Elsevier, Amsterdam, pp 1–64
Ruttens A, Boulet J, Weyens N, Smeets K, Adriaensen K, Meers E, Van Slycken S, Tack FMG, Meiresonne L, Thewys T, Witters N, Carleer R, Dupae J, Vangronsveld J (2011) Short rotation coppice culture of willows and poplars as energy crops on metal contaminated agricultural soils. Int J Phytoremediat 13(sup1):194–207. https://doi.org/10.1080/15226514.2011.568543
Saba G, Parizanganeh AH, Zamani A, Saba J (2015) Phytoremediation of heavy metals contaminated environments: screening for native accumulator plants in Zanjan—Iran. Int J Environ Res 9:309–316
Shi X, Wang S, Sun H, Chen Y, Wang D, Pan H, Zou Y, Liu J, Zheng L, Zhao X, Jiang Z (2017) Comparative of Quercus spp. and Salix spp. for phytoremediation of Pb/Zn mine tailings. Environ Sci Pollut Res 24(4):3400–3411. https://doi.org/10.1007/s11356-016-7979-0
Silva S (2012) Aluminium toxicity targets in plants. J Bot 2012:1–8. https://doi.org/10.1155/2012/219462
Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11(3):229–254. https://doi.org/10.1007/s10311-013-0407-5
Sinha S, Mishra RK, Sinam G, Mallick S, Gupta AK (2013) Comparative evaluation of metal phytoremediation potential of trees, grasses, and flowering plants from tannery-wastewater-contaminated soil in relation with physicochemical properties. Soil Sediment Contam 22(8):958–983. https://doi.org/10.1080/15320383.2013.770437
Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium—a functional plant nutrient. Crc Cr Rev Plant Sci 22:391–416
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl− ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61(15):4449–4459. https://doi.org/10.1093/jxb/erq251
Tlustoš P, Száková J, Vysloužilová M, Pavlíková D, Weger J, Javorská H (2007) Variation in the uptake of arsenic, cadmium, lead, and zinc by different species of willows Salix spp. grown in contaminated soils. Cent Eur J Biol 2:254–275
Toome M, Heinsoo K, Holm B (2010) The influence of canopy density on willow leaf rust (Melampsora epitea) severity in willow short rotation coppice. Biomass Bioenergy 34(8):1201–1206. https://doi.org/10.1016/j.biombioe.2010.03.012
Tóth G, Hermann T, Da Silva MR, Montanarella L (2016) Heavy metals in agricultural soils of the European Union with implications for food safety. Environ Int 88:299–309. https://doi.org/10.1016/j.envint.2015.12.017
Vaca R, Lugo J, Martínez R, Esteller MV, Zavaleta H (2011) Effects of sewage sludge and sewage sludge compost amendment on soil properties and Zea mays L. plants (heavy metals, quality and productivity). Rev Int Contam Ambie 27:303–311
Vandecasteele B, Meers E, Vervaeke P, De Vos B, Quataert P, Tack FMG (2005) Growth and trace metal accumulation of two Salix clones on sediment-derived soils with increasing contamination levels. Chemosphere 58(8):995–1002. https://doi.org/10.1016/j.chemosphere.2004.09.062
Vandecasteele B, Quataert P, Piesschaert F, Lettens S, De Vos B, Du Laing G (2015) Translocation of Cd and Mn from bark to leaves in willows on contaminated sediments: delayed budburst in related to high Mn concentrations. Land 4(2):255–280. https://doi.org/10.3390/land4020255
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut R 16(7):765–794. https://doi.org/10.1007/s11356-009-0213-6
Vassilev A, Nikolova A, Koleva L, Lidon F (2011) Effects of excess Zn on growth and photosynthetic performance of young bean plants. J Phytol 3:58–62
Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55(1):35. https://doi.org/10.1186/1999-3110-55-35
Von Fircks Y, Rosén K, Sennerby-Forsse L (2002) Uptake and distribution of 137Cs and 90Sr in Salix viminalis plants. J Environ Radioactiv 63(1):1–14. https://doi.org/10.1016/S0265-931X(01)00131-X
Wahsha M, Bini C, Argese E, Minello F, Fontana S, Wahsheh H (2012) Heavy metals accumulation in willows growing on Spolic Technosols from the abandoned Imperina Valley mine in Italy. J Geochem Explor 123:19–24. https://doi.org/10.1016/j.gexplo.2012.07.004
Webster BL (1978) Guide to judging the condition of a shade tree. J Arboric 4:247–249
Wieshammer G, Unterbrunner R, Bañares Garcia T, Zivkovic M, Puschenreiter M, Wenzel WW (2007) Phytoextraction of Cd and Zn from agricultural soils by Salix Ssp. and intercropping of Salix caprea and Arabidopsis halleri. Plant Soil 298(1–2):255–264. https://doi.org/10.1007/s11104-007-9363-9
Wind C, Arend M, Fromm J (2004) Potassium-dependent cambial growth in poplar. Plant Biol 6(1):30–37. https://doi.org/10.1055/s-2004-815738
Yang W, Wang Y, Zhao F, Ding Z, Zhang X, Zhu Z, Yang X (2014) Variation in copper and zinc tolerance and accumulation in 12 willow clones: implications for phytoextraction. J Zhejiang Univ Sci B 15(9):788–800. https://doi.org/10.1631/jzus.B1400029
Yang W, Zhao F, Zhang X, Ding Z, Wang Y, Zhu Z, Yang X (2015) Variations of cadmium tolerance and accumulation among 39 Salix clones: implications for phytoextraction. Environ Earth Sci 73(7):3263–3274. https://doi.org/10.1007/s12665-014-3636-4
Zacchini M, Pietrini F, Mugnozza GS, Iori V, Pietrosanti L, Massacci A (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut 197(1-4):23–34. https://doi.org/10.1007/s11270-008-9788-7
Zaltauskaite J, Judeikyte S, Sujetoviene G, Dagiliute R (2015) Sewage sludge application effects to first year willow (Salix viminalis L.) growth and heavy metal bioaccumulation. Proceedings of the 14th International Conference on Environmental Science and Technology, Rhodes, Greece, 3–5 September 2015
Zárubová P, Hejcman M, Vondráčková S, Mrnka L, Száková J, Tlustoš P (2015) Distribution of P, K, Ca, Mg, Cd, Cu, Fe, Mn, Pb and Zn in wood and bark age classes of willows and poplars used for phytoextraction on soils contaminated by risk elements. Environ Sci Pollut R 22(23):18801–18813. https://doi.org/10.1007/s11356-015-5043-0
Zhao H, Wu L, Chai T, Zhang Y, Tan J, Ma S (2012) The effects of copper, manganese and zinc on plant growth and elemental accumulation in the manganese-hyperaccumulator Phytolacca americana. J Plant Physiol 169(13):1243–1252. https://doi.org/10.1016/j.jplph.2012.04.016
Acknowledgements
We wish to thank Anjan Kumar Prusty for critical reading of the article and his useful statements and proposals. The research was partially supported by the TÁMOP 4.2.1./B-09/1/KONV-2010-0024 project and by the SROP-4.2.2.B-15/1/KONV20150001 project. Research was partly supported by OTKA K 116639 project. We acknowledge Agilent Technologies and Novo-Lab Ltd. (Hungary) for providing the MP-AES 4200.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Tőzsér, D., Harangi, S., Baranyai, E. et al. Phytoextraction with Salix viminalis in a moderately to strongly contaminated area. Environ Sci Pollut Res 25, 3275–3290 (2018). https://doi.org/10.1007/s11356-017-0699-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0699-2