Abstract
The application of municipal sewage sludge on energy crops is an alternative form of recycling nutrients, food materials, and organic matter from waste. Municipal sewage sludge constitutes a potential source of heavy metals in soil, which can be partially removed by the cultivation of energy crops. The aim of the research was to assess the effect of municipal sewage sludge on the uptake of heavy metals by monocotyledonous energy crops. Sewage sludge was applied at doses of 0, 10, 20, 40, and 60 Mg DM · ha−1 once, before the sowing of plants. In a 6-year field experiment, the effect of four levels of fertilisation with sewage sludge on the uptake of heavy metals by two species of energy crops, reed canary grass (Phalaris arundinacea L.) of ‘Bamse’ cultivar and giant miscanthus (Miscanthus × giganteus GREEF et DEU), was analysed. It was established that the increasing doses of sewage sludge had a considerable effect on the increase in biomass yield from the tested plants. Due to the increasing doses of sewage sludge, a significant increase in heavy metals content in the energy crops was recorded. The heavy metal uptake with the miscanthus yield was the highest at a dose of 20 Mg DM · ha−1, and at a dose of 40 Mg DM · ha−1 in the case of reed canary grass. Research results indicate that on account of higher yields, higher bioaccumulation, and higher heavy metal uptake, miscanthus can be selected for the remediation of sewage sludge.
This is a preview of subscription content, access via your institution.
References
Act on waste (2012) Act on wastes dated 14 December 2012. J Law Poland. Item 21. http://isap.sejm.gov.pl/DetailsServlet?id=WDU20130000021
Ahmad MSA, Ashraf M (2011) Essential roles and hazardous effects of nickel in plants. Rev Environ Contam Toxicol 214:125–167. doi:10.1007/978-1-4614-0668-6_6
Ahmed HK, Fawy HA, Abdel-Hady ES (2010) Study of sewage sludge use in agriculture and its effect on plant and soil. Agric Biol J N Am 1(5):1044–1049. doi:10.5251/abjna2010.1.5.1044.1049
Antonkiewicz J (2014) Effect of fly ashes and sewage sludge on Fe, Mn, Al, Si and Co uptake by grass mixture. J Ecol Eng 15(3):6–13. doi:10.12911/22998993.1109115
Antonkiewicz J, Para A (2015) The use of dialdehyde starch derivatives in the phytoremediation of soils contaminated with heavy metals. Int J Phytoremediation. doi:10.1080/15226514.2015.1078771
Aşık BB, Katkat AV (2010) Evaluation of wastewater sludge for possible agricultural use. Environ Eng Manag J 9(6):819–826. http://omicron.ch.tuiasi.ro/EEMJ/
Audet P, Charest C (2007) Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 147:231–237. doi:10.1016/j.envpol.2006.08.011
Barbu CH, Pavel BP, Sand C, Pop MR (2010) Miscanthus sinensis × gigantheus behaviour on soils polluted with heavy metals. University of Sibiu, Faculty Of Agricultural Sciences, Food Industry And Environmental Protection. Romania, pp. 5. http://www.rutsolmeg.ro/raport02.pdf
Barrera I, Andrés P, Alcaňiz JM (2001) Sewage sludge application on soil: effects on two earthworm species. Water Air Soil Pollut 129:319–332. doi:10.1023/A:1010335816237
Boominathan R, Saha-Chaudhury NM, Sahajwalla V, Doran PM (2004) Production of nickel bio-ore from hyperaccumulator plant biomass: applications in phytomining. Biotechnol Bioeng 86(3):243–250. doi:10.1002/bit.10795
Borkowska H, Molas R (2012) Two extremely different crops, Salix and Sida, as sources of renewable bioenergy. Biomass Bioenergy 36:234–240. doi:10.1016/j.biombioe.2011.10.025
Borkowska H, Molas R (2013) Yield comparison of four lignocellulosic perennial energy crop species. Biomass Bioenergy 51:145–153. doi:10.1016/j.biombioe.2013.01.017
Březinová T, Vymazal J (2015) Evaluation of heavy metals seasonal accumulation in phalaris arundinacea in a constructed treatment wetland. Ecol Eng 79:94–99. doi:10.1016/j.ecoleng.2015.04.008
Casado-Vela J, Sellés S, Navarro J, Bustamante MA, Mataix J, Guerrero C, Gomez I (2006) Evaluation of composted sewage sludge as nutritional source for horticultural soils. Waste Manag 26:946–952. doi:10.1016/j.wasman.2005.07.016
Catalogue of Waste (2014) Regulation of the minister of the natural environment on catalog of wastes dated 9 December 2014. J. Law Poland, Item 1923. http://isap.sejm.gov.pl/DetailsServlet?id=WDU20140001923
Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Environ Biotechnol 8:279–284. doi:10.1016/S0958-1669(97)80004-3
Christian DG, Yates NE, Riche AB (2006) The effect of harvest date on the yield and mineral content of Phalaris arundinacea L. (reed canary grass) genotypes screened for their potential as energy crops in southern England. J Sci Food Agric 86:1181–1188. doi:10.1002/jsfa.2437
Collura S, Azambre B, Finqueneisel G, Zimny T, Weber JV (2006) Miscanthus × giganteus straw and pellets as sustainable fuels. Combustion and emission tests. Environ Chem Lett 4:75–78. doi:10.1007/s10311-006-0036-3
Directive 2009/28/EC of the European Parliament and of the Council of 23 April 2009 on the promotion of the use of energy from renewable sources and amending and subsequently repealing Directives 2001/77/EC and 2003/30/EC
Environment (2015) Statistical information and elaborations. GUS, Warsaw, p 565
Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794. doi:10.1016/j.soilbio.2008.04.001
Fernández JM, Plaza C, Garcia-Gil JC, Polo A (2009) Biochemical properties and barley yield in a semiarid Mediterranean soil amended with two kinds of sewage sludge. Appl Soil Ecol 42(1):18–24. doi:10.1016/j.apsoil.2009.01.006
Fernando AL, Godovikova V, Oliveira JFS (2004) Miscanthus x giganteus: contribution to a sustainable agriculture of a future/present-oriented biomaterial. Mater Sci Forum 455–456:437–441. doi:10.4028/www.scientific.net/MSF.455-456.437
Fischer TB, Potter K, Donaldson S, Scott T (2011) Municipal waste management strategies, strategic environmental assessment and the consideration of climate change in England. J Environ Assess Policy Manag 13(4):541–565. doi:10.1142/S1464333211004000
Gardea-Torresdey J, Peralta-Videa J, Rosa G, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797–1810. doi:10.1016/j.ccr.2005.01.001
Ghosh M, Singh SP (2005) A review of phytoremediation of heavy metals and utilization of its byproducts. Appl Ecol Environ Res 3(1):1–18. http://aloki.hu/indvol03_1.htm
Gondek K (2012) Effect of fertilization with farmyard manure, municipal sewage sludge and compost from biodegradable waste on yield and mineral composition of spring wheat grain. J Elem 2(2012):231–245. doi:10.5601/jelem.2012.17.2.06
Hseu ZY, Su SW, Lai HY, Guo HY, Chen TC, Chen ZS (2010) Remediation techniques and heavy metal uptake by different rice varieties in metal-contaminated soils of Taiwan: new aspects for food safety regulation and sustainable agriculture. Soil Sci Plant Nutr 56:31–52. doi:10.1111/j.1747-0765.2009.00442.x
Jones JB, Case VW (1990) Soil testing and plant analysis. 3rd ed. Soil Sci. Soc. Am. SSSA, Chapter 15
Kołodziej B, Antonkiewicz J, Stachyra M, Bielińska EJ, Wiśniewski J, Luchowska K, Kwiatkowski C (2015) Use of sewage sludge in bioenergy production—a case study on the effects on sorghum biomass production. Eur J Agron 69:63–74. doi:10.1016/j.eja.2015.06.004
Komilis DP, Ham RK (2004) Live-cycle inventory of municipal solid waste and yard waste windrow composting in the United States. J Environ Eng 130(11):1390–1400. doi:10.1061/(ASCE)0733-9372(2004)130:11(1390)
Korzeniowska J, Stanisławska-Glubiak E (2015) Phytoremediation potential of Miscanthus x giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res 22(15):11648–11657. doi:10.1007/s11356-015-4439-1
Kusznierewicz B, Bączek-Kwinta R, Bartoszek A, Piekarska A, Huk A, Manikowska A, Antonkiewicz J, Namieśnik J, Konieczka P (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata F. Alba). Environ Toxicol Chem 31(11):2482–2489. doi:10.1002/etc.1977
Ladd JN, Butler JHA (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4(1):19–30. doi:10.1016/0038-0717(72)90038-7
Lewandowski I, Scurlock JMO, Lindvall E, Christou M (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25:335–361. doi:10.1016/S0961-9534(03)00030-8
Li C, Xiao B, Wang QH, Yao SH, Wu JY (2014) Phytoremediation of Zn- and Cr-contaminated soil using two promising energy grasses. Water Air Soil Pollut 225:2027. doi:10.1007/s11270-014-2027-5
Lindvall E, Gustavsson A, Palmborg C (2012) Establishment of reed canary grass with perennial legumes or barley and different fertilization treatments: effects on yield, botanical composition and nitrogen fixation. Global Change Biol Bioenergy 4:661–670. doi:10.1111/j.1757-1707.2012.01178.x
Lindvall E, Gustavsson A, Ramuelsson R, Magnusson T, Palmborg C (2015) Ash as a phosphorus fertilizer to reed canary grass: effects of nutrient and heavy metal composition on plant and soil. Global Change Biol Bioenergy 7:553–564. doi:10.1111/gcbb.12161
Liu CY, Gong XF, Tang YP, Chen CL (2015) Lead sequestration in iron plaques developed on Phalaris arundinacea Linn. and Carex cinerascens Kukenth. from Poyang Lake (China). Aquat Bot 122:54–59. doi: 10.1016/j.aquabot.2014.12.007
Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13. doi:10.1016/j.envexpbot.2009.10.011
McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol 14(2):94–104. doi:10.1007/BF01569890
Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162. doi:10.1016/S1369-5266(99)00054-0
Milinovic J, Vidal M, Lacorte S, Rigol A (2014) Leaching of heavy metals and alkylphenolic compounds from fresh and dried sewage sludge. Environ Sci Pollut Res 21:2009–2017. doi:10.1007/s11356-013-2100-4
Monti A, Di Virgilio N, Venturi G (2008) Mineral composition and ash content of six major energy crops. Biomass Bioenergy 32:216–223. doi:10.1016/j.biombioe.2007.09.012
Nsanganwimana F, Pourrut B, Mench M, Douai F (2014) Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review. J Environ Manag 143:123–134. doi:10.1016/j.jenvman.2014.04.027
Ostrowska A, Gawliński S, Szczubiałka Z (1991) Methods of analysis and assessment of soil and plant properties. A catalgoue. Publisher: Institute of Environmental Protection – National Research Institute, Warsaw, p 334
Otero M, Calvo LF, Gil MV, García AI, Morán A (2008) Co-combustion of different sewage sludge and coal: a non-isothermal thermogravimetric kinetic analysis. Bioresour Technol 99:6311–6319. doi:10.1016/j.biortech.2007.12.011
Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Water Air Soil Pollut 184(1–4):105–126. doi:10.1007/s11270-007-9401-5
Page K, Harbottle MJ, Cleall PJ, Hutchings TR (2014) Heavy metal leaching and environmental risk from the use of compost-like output as an energy crop growth substrate. Sci Total Environ 487:260–271. doi: 10.1016/j.scitotenv.2014.04.021
Pavel PB, Puschenreiter M, Wenzel WW, Diacu E, Barbu CH (2014) Aided phytostabilization using Miscanthus sinensis × giganteus on heavy metal-contaminated soils. Sci Total Environ 479–480:125–131. doi:10.1016/j.scitotenv.2014.01.0977
Pidlisnyuk V, Stefanovska T, Lewis EE, Ericsson LE, Davis LC (2014) Miscanthus as a productive biofuel crop for phytoremediation. Crit Rev Plant Sci 33(1):1–19. doi:10.1080/07352689.2014.847616
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. doi:10.1146/annurev.arplant.56.032604.144214
Pogrzeba M, Krzyżak J, Sas-Nowosielska A, Majtkowski M, Małkowski E, Kita A (2011) A heavy metal environmental threat resulting from combustion of biofuels of plant origin. In: Simeonov LI, Kochubovski MV, Simeonova BG (eds) Environmental heavy metal pollution and effects on child mental development. Risk Assessment and Prevention Strategies, Springer Science + Business Media B.V., pp 213–225. doi:10.1007/978-94-007-0253-0_13
Polish Soil Classification (2011) Soil Sci Annu 62(3):1–193. http://www.ptg.sggw.pl
Regasa TH, Wortmann CS (2014) Sweet sorghum as a bioenergy crop: literature review. Biomass Bioenergy 64:348–355. doi:10.1016/j.biombioe.2014.03.052
Regulation (2002) Regulation of the minister of the natural environment on municipal sewage sludge dated 1 September 2002. J Law Poland, 134, Item 1140
Regulation (2015) Regulation of the minister of the natural environment on municipal sewage sludge dated 6 February 2015. J Law Poland, Item 257. http://isap.sejm.gov.pl/DetailsServlet?id=WDU20150000257
Sahramaa M, Jauhiainen L (2003) Characterization of development and stem elongation of reed canary grass under northern conditions. Ind Crop Prod 18:155–169. doi:10.1016/S0926-6690(03)00044-X
Sastre I, Vicente MA, Lobo MC (1996) Influence of the application of sewage sludges on soil microbial activity. Bioresour Technol 57:19–23. doi:10.1016/0960-8524(96)00035-1
Sheaffer CC, Rosen CJ, Gupta SC (2008) Reed canary grass forage yield and nutrient uptake on a year-round wastewater application site. J Agron Crop Sci 194:465–469. doi:10.1111/j.1439-037X.2008.00327.x
Sidle RC, Hook JE, Kardos LT (1976) Heavy metals application and plant uptake in a land disposal system for waste water. J Environ Qual 5(1):97–102. doi:10.2134/jeq1976.00472425000500010023x
Singh RP, Agrawal M (2008) Potential benefits and risks of land application of sewage sludge. Waste Manag 28:347–358. doi:10.1016/j.wasman.2006.12.010
Singh RP, Sing P, Ibrahim MH, Hashim R (2011) Land application of sewage sludge: physicochemical and microbial response. Rev Environ Contam Toxicol 214:41–61. doi:10.1007/978-1-4614-0668-6_3
Soil Survey Staff (2014) Keys to soil taxonomy, 12th edn. USDA-Natural Resources Conservation Service, Washington, DC
Suchkova N, Tsiripidis I, Alifragkis D, Ganoulis J, Marakas E, Sawidis T (2014) Assessment of phytoremediation potential of native plants during the reclamation of an area affected by sewage sludge. Ecol Eng 69:160–169. doi:10.1016/j.ecoleng.2014.03.029
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1(4):301–307. doi:10.1016/0038-0717(69)90012-1
Thalmann A (1968) Zur methodik der bestimmung der dehydrogenaseaktivit ~ tt im boden mittels triphenyltetrazoliumchlorid (TTC). Landwirtsch Forsch 21:249–258
Vymazal J, Švehla J, Kröpfelová L, Chrastný V (2007) Trace metals in Phragmites australis and Phalaris arundinacea growing in constructed and natural wetlands. Sci Total Environ 380:154–162. doi:10.1016/j.scitotenv.2007.01.057
Wang AS, Angle JS, Chaney RL, Delorme TA, Macintosh M (2006) Changes in soil biological activities under reduced soil pH during Thlaspi caerulescens phytoextraction. Soil Biol Biochem 38(6):1451–1461. doi:10.1016/j.soilbio.2005.11.001
Zantua MI, Bremner JM (1975) Comparison of methods of assaying urease activity in soils. Soil Biol Biochem 7(4–5):291–295. doi:10.1016/0038-0717(75)90070-X
Acknowledgments
This study was performed partially with the financial support of the Ministry of Science and Higher Education, Poland, (Grant No. NN310080336) and the research results carried out within the subject No. 3101 were financed from the subsidy for science granted by the Polish Ministry of Science and Higher Education.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Antonkiewicz, J., Kołodziej, B. & Bielińska, E.J. The use of reed canary grass and giant miscanthus in the phytoremediation of municipal sewage sludge. Environ Sci Pollut Res 23, 9505–9517 (2016). https://doi.org/10.1007/s11356-016-6175-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-6175-6
Keywords
- Reed canary grass
- Giant miscanthus
- Heavy metals
- Content
- Uptake
- Phytoremediation
- Sewage sludge