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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

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Abstract

Fast-growing clones of Salix and Populus species have been studied for phytoremediation of soils contaminated by risk elements (REs) using short-rotation coppice plantations. Biomass yield, accumulation and removal of RE (Cd, Pb and Zn) by highly productive willow (S1—(Salix schwerinii × Salix viminalis) × S. viminalis, S2—Salix × smithiana) and poplar (P1—Populus maximowiczii × Populus nigra, P2—P. nigra) clones were investigated with and without sewage sludge (SS) application. The precise field experiment was established in April 2008 on moderately Cd-, Pb- and Zn-contaminated soil. Initially, shoots were harvested after four seasons in February 2012 and then after two more seasons in February 2014. The application of SS limited plant growth during the first years of the experiment in the majority of treatments, mainly due to weed competition and higher concentrations of available soil nutrients causing lower yields than those of control (C) treatments. Well-developed roots were able to take advantage of SS applications, and shoot yield was mainly higher in SS treatments in the second harvest, reaching up to 15 t dry matter (DM) ha−1. Willows performed better than poplars. Application of SS reduced RE shoot concentrations compared to the C treatment. The removal of RE was significantly higher in the second harvest for all clones and elements (except the P2 clone), and the biomass yield was the major driving force for the amount of RE removed by shoots. Well-developed plantations of fast-growing trees showed better suitability for the phytoextraction of moderately contaminated soils for Cd and partly for Zn but not for Pb, which was less available to plants. From the four tested clones, S2 showed the best removal of Cd (up to 0.94 %) and Zn (up to 0.34 %) of the total soil element content, respectively, and this clone is a good candidate for phytoextraction. SS can be a suitable source of nutrients for Salix clones without any threat to the food chain in terms of biomass contamination, but its application to the soil can result in an increased incidence of some weeds during the first years of plantation.

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References

  1. Santos FS, Magalhaes MOL, Mazur N, Amaral Sabrinho NMB (2007) Chemical amendment and phytostabilization of an industrial residue contaminated with Zn and Cd. Sci Agric 64:506–512

    Article  Google Scholar 

  2. Melo ÉEC, Nascimento CWA, Accioly AMA, Santos ACQ (2008) Phytoextraction and fractionality of heavy metals in soil after multiple application of natural chelants. Sci Agric 65:61–68

    Article  Google Scholar 

  3. Wenzel WW, Lombi E, Adriano D (1999) Biogeochemical processes in the rhizosphere: role in phytoremediation of metal-polluted soils. In: Prasad N, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer Verlag, Heidelberg, p 401

    Google Scholar 

  4. Pulford ID, Dickinson NM (2006) Phytoremediation technologies using trees. In: Prasad MNV, Sajwan KS, Naidu R (eds) Trace elements in the environment: biochemistry, biotechnology and bioremediation. CRC Press, Boca Raton, pp 375–395

    Google Scholar 

  5. Vysloužilová M, Tlustoš P, Száková J (2003) Cadmium and zinc phytoextraction potential of seven clones of Salix spp. planted on heavy metal-contaminated soils. Plant Soil Environ 49:542–547

    Google Scholar 

  6. Vysloužilová M, Tlustoš P, Száková J, Pavlíková D (2003) As, Cd, Pb and Zn uptake by Salix spp. clones grown in soils enriched by high loads of these elements. Plant Soil Environ 49:191–196

    Article  Google Scholar 

  7. Fischerová Z, Tlustoš P, Száková J, Šichorová K (2006) A comparison of phytoremediation capability of selected plant species for given trace elements. Environ Pollut 144:93–100

    Article  PubMed  Google Scholar 

  8. Jensen JK, Holm PE, Nejrup J, Larsen MB, Borggaard OK (2009) The potential of willow for remediation of heavy metal-polluted calcareous urban soils. Environ Pollut 157:931–937

    Article  CAS  PubMed  Google Scholar 

  9. Lonardo DS, Capuana M, Arnetoli M, Gabbrielli R, Gonnelli C (2011) Exploring the metal phytoremediation potential of three Populus alba L. clones using an in-vitro screening. Environ Sci Pollut Res 18:82–90

    Article  CAS  Google Scholar 

  10. Dos Santos Utmazian MN, Wieshammer G, Vega R, Wenzel WW (2007) Hydroponic screening for metal resistance and accumulation of cadmium and zinc in 20 clones of willows and poplars. Environ Pollut 148:155–165

    Article  PubMed  Google Scholar 

  11. 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 290:157–172

    Article  CAS  Google Scholar 

  12. Laureysens I, De Temmerman L, Hastir T, Van Gysel M, Ceulemans R (2005) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: II. Vertical distribution and phytoextraction potential. Environ Pollut 133:541–551

    Article  CAS  PubMed  Google Scholar 

  13. Laturnus F, von Arnold K, Grøn C (2007) Organic contaminants from sewage sludge applied to agricultural soils. Environ Sci Pollut Res 14:53–60

    Article  CAS  Google Scholar 

  14. Hartman M, Pohořelý M, Trnka O (2006) Chemical and fuel characteristics of anaerobically stabilized sewage sludge and its ash. Chem List 100:813–820 [in Czech]

    CAS  Google Scholar 

  15. Pagliai M, Antisari LV (1993) Influence of waste organic matter on soil micro- and macrostructure. Bioresour Technol 43:205–213

    Article  CAS  Google Scholar 

  16. Garrido T, Mendoza J, Arriagada F (2012) Changes in the sorption, desorption, distribution and availability of copper, induced by application of sewage sludge on Chilean soils contaminated by mine tailings. J Environ Sci 24:912–918

    Article  CAS  Google Scholar 

  17. Shaheen SM, Tsadilas CD, Rinklebe J (2013) A review of the distribution coefficients of trace elements in soils: influence of sorption system, element characteristics and soil colloidal properties. Adv Colloid Interface Sci 201–202:43–56

    Article  PubMed  Google Scholar 

  18. Tlustoš P, Balík J, Dvořák P, Száková J, Pavlíková D (2001) Zinc and lead uptake by three crops planted on different soils treated by sewage sludge. Rostl Výr 47:129–134

    Google Scholar 

  19. Shaheen SM, Tsadilas CD (2010) Influence of fly ash and sewage sludge application on cadmium and lead sorption by an acidic Alfisol. Pedosphere 20:436–445

    Article  CAS  Google Scholar 

  20. Hanč A, Tlustoš P, Száková J, Balík J (2007) The changes of cadmium and zinc mobility in sewage sludges after their treatment. Chem List 101:807–810 [in Czech]

    Google Scholar 

  21. Chaney RL, Li Y-M, Angle JS, Baker AJM, Reeves RD, Brown SL, Homer FA, Malik M, Chin M (1999) Improving metal-hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry N, Bańuelos GS (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Rat, p 408

    Google Scholar 

  22. McBride MB (2003) Toxic metals in sewage sludge-amended soils: has promotion of beneficial use discounted the risks? Environ Res 8:5–19

    Article  CAS  Google Scholar 

  23. Havlíčková K, Suchý J, Weger J, Šedivá J, Táborská M, BurešM, Hána J, Nikl M, Jirásková L, Petruchová J, Knápek J, Vašíček J, Gallo P, Strašil Z (2010) Analysis of biomass production potential in the Czech Republic. VÚKOZ v. v. i., Průhonice. [in Czech]

  24. Weih M, Nordh NE (2002) Characterising willows for biomass and phytoremediation: growth, nitrogen and water use of 14 willow clones under different irrigation and fertilisation regimes. Biomass Bioenergy 23:397–413

    Article  Google Scholar 

  25. Sevel L, Nord-Larsen T, Ingerslev M, Jørgensen U, Raulund-Rasmussen K (2014) Fertilisation of SRC willow: I. Biomass production response. Bioenergy Res 7:319–328

    Article  CAS  Google Scholar 

  26. Kidd P, Mench M, Álvarez-López V, Bert V, Dimitriou I, Friesl-Hanl W, Herzig R, Jansen JO, Kolbas A, Müller I, Neu S, Renella G, Ruttens A, Vangronsveld J, Puschenreiter M (2015) Agronomic practices for improving gentle remediation of trace element-contaminated soils. Int J Phytoremediation 17:1005–1037

    Article  CAS  PubMed  Google Scholar 

  27. 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 Res 22:18801–18813

    Article  Google Scholar 

  28. Tlustoš P, Száková J, Vysloužilová M, Pavlíková P, 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 2:254–428

    Google Scholar 

  29. Weger J (2008) Yield of selected poplar and willow clones after 9 years of coppicing. Acta Pruhoniciana 89:5–10 [in Czech]

    Google Scholar 

  30. Weger J (2009) The evaluation of the influence of a rotation length of short-rotation coppice on production and growth characteristics of poplar clone Max-4 (Populus nigra L. × P. maximowiczii Henry). Acta Pruhoniciana 92:5–11 [in Czech]

    Google Scholar 

  31. Weger J, Bubeník J (2011) The evaluation of yield and growth of native willows after 14 years of short-rotation coppice. Acta Pruhoniciana 97:39–46 [in Czech]

    Google Scholar 

  32. Komárek M, Tlustoš P, Száková J, Chrastný V (2008) The use of poplar during a 2-year-induced phytoextraction of metals from contaminated agricultural soils. Environ Pollut 151:27–38

    Article  PubMed  Google Scholar 

  33. Laureysens I, Bogaert J, Blust R, Ceulemans R (2004) Biomass production of 17 poplar clones in a short-rotation coppice culture on a waste disposal site and its relation to soil characteristics. For Ecol Manag 187:295–309

    Article  Google Scholar 

  34. Casler MD, Vermerris W, Dixon RA (2015) Replication concepts for bioenergy research experiments. Bioenergy Res 8:1–16

    Article  CAS  Google Scholar 

  35. Anonymous (1994) Public notice No. 13/1994 for the management of soil protection. Czech Ministry of the Environment, Prague [In Czech]

  36. Mehlich A (1984) Mehlich-3 soil test extractant: a modification of Mehlich-2 extractant. Commun Soil Sci Plant Anal 15:1409–1416

    Article  CAS  Google Scholar 

  37. Mader P, Száková J, Miholová D (1998) Classical dry ashing of biological and agricultural materials: part II. Losses of analytes due to their retention in an insoluble residue. Analysis 26:121–129

    Article  CAS  Google Scholar 

  38. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

  39. Hejcman M, Vondráčková S, Müllerová V, Červená K, Száková J, Tlustoš P (2012) Effect of quick lime and superphosphate additives on emergence and survival of Rumex obtusifolius seedlings in acid and alkaline soils contaminated by As, Cd, Pb and Zn. Plant Soil Environ 58(12):561–567

    CAS  Google Scholar 

  40. Clay DV, Dixon FL (1997) Effect of ground-cover vegetation on the growth of poplar and willow short-rotation coppice. Asp Appl Biol 49:53–60

    Google Scholar 

  41. Larsen SU, Jørgensen U, Lærke PU (2014) Willow yield is highly dependent on clone and site. Bioenergy Res 7:1280–1292

    Article  Google Scholar 

  42. Al Afas N, Marron N, Van Dongen S, Laureysens I, Ceulemans R (2008) Dynamics of biomass production in a poplar coppice culture over three rotations (11 years). For Ecol Manag 255:1883–1891

    Article  Google Scholar 

  43. Fortier J, Gagnon D, Truax B, Lambert F (2010) Biomass and volume yield after 6 years in multiclonal hybrid poplar riparian buffer strips. Biomass Bioenergy 34:1028–1040

    Article  Google Scholar 

  44. Pulford ID, Riddell-Black D, Stewart C (2002) Heavy metal uptake by willow clones from sewage sludge-treated soil: the potential for phytoremediation. Int J Phytoremediation 4:59–72

    Article  CAS  Google Scholar 

  45. Van de Walle I, Van Camp N, Van de Casteele L, Verheyen K, Lemeur R (2007) Short-rotation forestry of birch, maple, poplar and willow in Flanders (Belgium): I. Biomass production after 4 years of tree growth. Biomass Bioenergy 31:267–275

    Article  Google Scholar 

  46. Armstrong A, Johns C, Tubby I (1999) Effects of spacing and cutting cycle on the yield of poplar grown as an energy crop. Biomass Bioenergy 17:305–314

    Article  CAS  Google Scholar 

  47. Bullard MJ, Mustill SJ, McMillan SD, Nixon PMI, Carver P, Britt CP (2002) Yield improvements through modification of planting density and harvest frequency in short-rotation coppice Salix spp:–1. Yield response in two morphologically diverse varieties. Biomass Bioenergy 22:15–25

    Article  Google Scholar 

  48. Benetka V, Pilařová P, Kozliková K (2009) Yield potential analysis of black poplar in the course of three coppice rotations at two different plant spacings. Acta Pruhoniciana 92:13–17 [in Czech]

    Google Scholar 

  49. Tinker PB, MacPherson A, West TS (1981) Levels, distribution and chemical forms of trace elements in food plants. Philos Trans R Soc B 294:41–55

    Article  CAS  Google Scholar 

  50. Hejcman M, Szaková J, Schellberg J, Tlustoš P (2010) The Rengen grassland experiment: relationship between soil and biomass chemical properties, amount of elements applied and their uptake. Plant Soil 333:163–179

    Article  CAS  Google Scholar 

  51. Laureysens I, Blust R, De Temmermanc L, Lemmensa C, Ceulemans R (2004) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seasonal variation in leaf, wood and bark concentrations. Environ Pollut 131:485–494

    Article  CAS  PubMed  Google Scholar 

  52. Schmidt U (2003) Enhancing phytoextraction: the effect of chemical soil manipulation on mobility, plant accumulation and leaching of heavy metals. J Environ Qual 32:1939–1954

    Article  CAS  PubMed  Google Scholar 

  53. Dickinson NM, Pulford ID (2005) Cadmium phytoextraction using short-rotation coppice Salix: the evidence trail. Environ Int 31:609–613

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by National Agency of Agriculture Sciences (NAZV QJ 1210211) and Czech University of Life Sciences, Prague, from CIGA project no. 20142005.

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Correspondence to Pavel Tlustoš.

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Kubátová, P., Hejcman, M., Száková, J. et al. 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, 809–819 (2016). https://doi.org/10.1007/s12155-016-9727-1

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