Skip to main content

Advertisement

Log in

Effects of sewage sludge fertilizer on heavy metal accumulation and consequent responses of sunflower (Helianthus annuus)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Use of sewage sludge, a biological residue produced from sewage treatment processes in agriculture, is an alternative disposal technique of waste. To study the usefulness of sewage sludge amendment for Helianthus annuus, a pot experiment was conducted by mixing sewage sludge at 2.5, 5, and 7.5 % (w/w) amendment ratios to the agricultural soil. Soil pH decreased whereas electrical conductivity, organic matter, total N, available P, and exchangeable Na, K, and Ca increased in soil amended with sewage sludge in comparison to unamended soil. Sewage sludge amendment led to significant increase in Pb, Ni, Cu, Cr, and Zn concentrations of soil. The increased concentration of heavy metals in soil due to sewage sludge amendment led to increases in shoot and root concentrations of Cr, Cu, Ni, and Zn in plant as compared to those grown on unamended soil. Accumulation was more in roots than shoots for most of the heavy metals. Moreover, high metal removal for the harvestable parts of the crops was recorded. Sewage sludge amendment increased root and shoot length, leaves number, biomass, and antioxidant activities of sunflower. Significant increases in the activities of antioxidant enzymes and in the glutathione, proline, and soluble sugar content in response to amendment with sewage sludge may be defense mechanisms induced in response to heavy metal stress.

Origin, fate and behavior of sewage sludge fertilizer

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrawal M, Singh D (2003) Physiological and biochemical and SO2, singly and in combination. Environ Pollut 121:189–197

    Article  CAS  Google Scholar 

  • Ahmed P, Jaleel CA, Azooz MM, Nabi G (2009) Generation of ROS and non enzymatic antioxidants during abiotic stress in plants. Bot Res Int 2(1):11–20

    Google Scholar 

  • Angin I, Aslantas R, Kose M, Karakurt H, Ozkan G (2012) Changes in chemical properties of soil and sour cherry as a result of sewage sludge application. Hortic Sci 39(2):61–66

    CAS  Google Scholar 

  • Arenas-Lago D, Vega FA, Silva LFO, Andrade ML (2013) Soil interaction and fractionation of added cadmium in some Galician soils. Micro chem J 110:681–690

    Article  CAS  Google Scholar 

  • Bates LS, Waldran RP, Teare ID (1973) Rapid determination of proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bekaert C, Femer V (2002) Evaluation of toxic and genotoxic potential of stabilized industrial waste and contaminated soils. J Waste Manag 22:241–247

    Article  CAS  Google Scholar 

  • Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaıbi W, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linumus itatissimum L. Ecotoxicol Environ Saf 73:1004–1011

    Article  CAS  Google Scholar 

  • Bergkvist P, Jarvis N, Berggren D, Carlgren K (2003) Long-term effects of sewage sludge applications on soil properties, cadmium availability, and distribution in arable soil. Agric Ecosyst Environ 97:167–179

    Article  CAS  Google Scholar 

  • Brooks RR, Robinson BH (1998) Aquatic phytoremediation by accumulator plants. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals: their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining. CAB International, New York, pp. 203–266

    Google Scholar 

  • Cerqueira B, Vega FA, Serra C, Silva LF, Andrade ML (2011) Time of flight secondary ion mass spectrometry and high-resolution transmission electron microscopy/energy dispersive spectroscopy: a preliminary study of the distribution of Cu2+ and Cu2+/Pb2+ on a Bt horizon surfaces. J Hazard Mater:422–431

  • Cerqueira B, Vega FA, Silva LF, Andrade L (2012) Effects of vegetation on chemical and mineralogical characteristics of soils developed on a decantation bank from a copper mine. Sci Total Environ 421-422:220–229

    Article  CAS  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal MH, Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effect on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147

    Article  CAS  Google Scholar 

  • Davies FT, Puryear JD, Newton RJ, Egilla JN, Saraivagrossi JA (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J. Plant Physiol 158:777–786

    Article  CAS  Google Scholar 

  • De Vos CH, Ten Bookum WM, Vooijs R, Schat H, DeKok LJ (1993) Effect of copper on fatty acid composition and peroxidation of lipids in the roots of copper tolerant and sensitive Silene cucubalus. Plant Physiol Biochem 31:151–158

    Google Scholar 

  • Drazkiewicz M, Baszynski T (2005) Growth parameters and photosynthetic pigments in leaf segments of Zea mays exposed to cadmium, as related to protection mechanisms. J Plant Physiol 162:1013–1021

    Article  CAS  Google Scholar 

  • Ekmekci Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

    Article  CAS  Google Scholar 

  • Ekmekci Y, Tanyolac D, Ayhan B (2009) A crop tolerating oxidative stress induced by excess Pb: maize. Acta Physiol Plant 31:319–330

    Article  CAS  Google Scholar 

  • Elloumi N, Ben Abdallah F, Rhouma A, Ben Rwina B, Mezghani I, Boukhris M (2007) Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiol Plant 29:57–62

    Google Scholar 

  • Elloumi N, Zouari M, Chaari L, Jomni C, Ben Rouina B, Ben Abdallah F (2014a) Ecophysiological responses of almond (Prunus dulcis) seedlings to cadmium stress. Biologia 69(5):604–609

    Article  CAS  Google Scholar 

  • Elloumi N, Zouari M, Chaari L, Jomni C, Marzouk B, Ben Abdallah F (2014b) Effects of cadmium on lipids of almond seedlings (Prunus dulcis). Bot Stud 55:61–68

    Article  Google Scholar 

  • Fotovat A, Naidu R, Sumner ME (1997) Water: soil ratio influences aqueous phase chemistry of indigenous copper and zinc in soils. Aust J Soil Res 35:687–710

    Article  CAS  Google Scholar 

  • Gupta AK, Sinha S (2006) Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants. Chemosphere 64:161–173

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photooxidation in isolated chloroplast. I. Kinetics and stoichiometric of fatty acids peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Homme PM, Conalez B, Billard J (1992) Carbohydrate content, fructose and sucrose, enzyme activities in roots, stubble and leaves of rye grass (Lolium perenne L.) as affected by source/sink modification after cutting. J Plant Physiol 140:282–291

    Article  Google Scholar 

  • Jha AB, Dubey RS (2004) Carbohydrate metabolism in growing rice seedling under arsenic toxicity. J Plant Physiol 161:867–872

    Article  CAS  Google Scholar 

  • Kholodova V, Volkov K, Abdeyeva A, Kuznetsov V (2011) Water status in Mesembryanthemum crystallinum under heavy metal stress. Environ Exp Bot 71:382–389

    CAS  Google Scholar 

  • Kjeldahl JZ (1883) A new method for the determination of nitrogen in organic matter. Anal Chem 22:366

    Article  Google Scholar 

  • Knorzer OC, Durner J, Boger P (1996) Alterations in the antioxidative system of suspension cultured soy bean cells (Glycine max) induced by oxidative stress. Physiol Plant 97:388–396

    Article  Google Scholar 

  • Komilis DP, Tziouvaras IS (2009) A statistical analysis to assess the maturity and stability of six composts. Waste Manag 29:1504–1513

    Article  CAS  Google Scholar 

  • Krishnaraj S, Dan TV, Saxena PK (2000) A fragrant solution to soil remediation. Int J Phytoremediation 2:117–132

    Article  Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120

    Article  CAS  Google Scholar 

  • Lee JH, Hossner LR, Attrep Jr M, Kung KS (2002) Uptake and translocation of plutonium in two plant species using hydroponics. Environ Pollut 117:61–68

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lou LQ, Shen ZG, Li XD (2004) The copper tolerance mechanisms of Elsholtziahaichowensis, a plant from copper-enriched soils. Environ Exp Bot 51:111–120

    Article  CAS  Google Scholar 

  • Marchiol L, Assolari S, Sacro P, Zerbia G (2004) Phytoremediation of heavy metals by canola (Brassica napus) and radish (Raplanus sativus) grown on multi contaminated soil. Environ Pollut 132:21–27

    Article  CAS  Google Scholar 

  • Marchiol L, Fellet G, Perosa D, Zerbi G (2007) Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: a field experience. Plant Physiol Biochem 45:379–387

    Article  CAS  Google Scholar 

  • Masoudi-Sadaghiani F, Abdollahi Mandoulakani B, Zardoshti MR, Rasouli-Sadaghiani MH, Tavakoli A (2011) Response of proline, soluble sugars, photosynthetic pigments and antioxidant enzymes in potato (Solanum tuberosum L.) to different irrigation regimes in greenhouse condition. Aust J Crop Sci 5(1):55–60

    Google Scholar 

  • McGrath SP, Cuncliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798

    Article  CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MN (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopamonnieri L. Plant. Physiol Biochem 44:25–37

    CAS  Google Scholar 

  • Mithofer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    Article  CAS  Google Scholar 

  • Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22

    Article  CAS  Google Scholar 

  • Moreira RS, Mincato RL, Santos BR (2013) Heavy metals availability and soil fertility after land application of sewage sludge on dystroferric red latosol. Ciêncagrotec 37(6):512–520

    CAS  Google Scholar 

  • Muchuweti M, Birkett JW, Chinyanga E, Zvauya R, Scrimshaw MD, Lester JN (2006) Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agric Ecosyst Environ 112:41–48

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhury MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Naidu R, Oliver D, McConnell S (2003) Heavy metal phytotoxicity in soils. In: Langley A, Gilbey M, Kennedy B, (eds), Proceedings of the fifth national workshop on the assessment of site contamination national environment protection council service corporation

  • Nouairi I, Ammar WB, Youssef NB, Ben Miled DD, Ghobal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica nepus) under cadmium stress. Acta Physiol Plant 31(2):237–247

    Article  CAS  Google Scholar 

  • NT 106.20 (2002) Matières fertilisantes- Boues des ouvrages de traitement des eaux usées urbaines. Normes Tunisiens Enregistrée 12:38

    Google Scholar 

  • Ostos JC, Lopez-Garrido R, Murillo JM, Lopez R (2008) Substitution of peat for municipal solid waste-and sewage sludge-basedccompsts in nursery growind media: Effects on growth and nutrition of the native shrub Pistacia lentiscus L. Biores Technol 99:1793–1800

  • Qasim M, Javed N, Himayatullah SM (2001) Effect of sewage sludge on the growth of maize crop. J Biol Sci 1:52–54

    Article  Google Scholar 

  • Rao Madhava KV, Sresty TV (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rejeb S, Gharbi F, Mouneimne AH, Ghorbal MH (2011) Effects of sludge on the metals levels of various edible crops grown in the field. J Agric Biol Sci 6:8

    Google Scholar 

  • Scott TA, Melvin EH (1956) Anthrone colorimetric method. In: Whistler RL, Walfrom ML (eds) Methods in carbohydrate chemistry, Vol. 1. Academic Press, New York, London, p. 384

    Google Scholar 

  • Sharma P, Dubey RS (2005) Pb toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 1–26

  • Siddaramaiah RK, Ramakrishnaiah H, Subramanya S (1998) Assessment of toxicity of heavy metal rich industrial effluents using germination and chlorophyll content tests. J Ind Pollut Control 14:27–35

    CAS  Google Scholar 

  • Silva JD, Tamara TB, Leal Araújoa AS, Araujoa RM, Gomes RL, Melo WJ, Singh RP (2010) Effect of different tannery sludge compost amendment rates on growth, biomass accumulation and yield responses of capsicum plants. Waste Manag 30:1976–1980

    Article  Google Scholar 

  • Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240

    Article  CAS  Google Scholar 

  • Singh RP, Agrawal M (2009) Use of sewage sludge as fertilizer supplement for Abelmoschuse sculentus plants: physiological, biochemical and growth responses. Int J Environ Waste Manag 3:91–106

    Article  CAS  Google Scholar 

  • Singh A, Agrawal M (2010) Effects of municipal waste water irrigation on availability of heavy metals and morpho-physiological characteristics of Beta vulgaris L. J Environ Biol 31:727–736

    CAS  Google Scholar 

  • Singh S, Sinha S (2004) Scanning electron microscopic studies and growth response of the plants of Helianthus annuus L. grown on tannery sludge amended soil. Environ Int 30:389–395

    Article  Google Scholar 

  • Singh S, Sinha S (2005) Accumulation of metals and its effect in Brassica juncea (L.) grown on various amendments of tannery waste. Ecotoxicol Environ Saf 62:118–127

    Article  CAS  Google Scholar 

  • Singh S, Saxena R, Pandey K, Bhatt K, Sinha S (2004a) Response of antioxidants in sunflower (Helianthus annuus L.) grown on different amendments of tannery sludge: its metal accumulation potential. Chemosphere 57:1663–1673

    Article  CAS  Google Scholar 

  • Singh S, Sinha S, Saxena R, Pandey K, Bhatt K (2004b) Translocation of metals and its effects in the tomato plants grown on the various amendments of tannery waste: evidence for involvement of antioxidants. Chemosphere 57:91–99

    Article  CAS  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Biol 51:49–81

    Article  CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 281:1057–1060

    Article  Google Scholar 

  • Soudek P, Petrova Š, Vankova R, Song J, Vanek T (2014) Accumulation of heavy metals using Sorghum sp. Chemosphere 104:15–24

    Article  CAS  Google Scholar 

  • Srivastava S, Srivastava AK, Suprasanna PD, Souza SF (2009) Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. In response to arsenic exposure reveals mechanisms of stress perception and tolerance. J Exp Bot 60(12):3419–3431

    Article  CAS  Google Scholar 

  • Sukreeyapongse O, Holm PE, Strobel BW, Panichsakpatana S, Magid J, Hansen HC (2002) pH-dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J Environ Qual 31:1901–1909

    Article  CAS  Google Scholar 

  • Tanaka K, Suda Y, Kondo N, Sugahara K (1985) O3 tolerance and ascorbate dependent H2O2 decomposing systems in chloroplasts. Plant Cell Physiol 26:1425–1431

    CAS  Google Scholar 

  • USEPA (1996) Ecological effects test guidelines. OPPTS 850.4100 terrestrial plant toxicity. Tier I (seedling emergence). EPA712-C-96-153. United States Environmental Protection Agency

  • Verma S, Dubey RS (2003) Pb toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    Article  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37

    Article  CAS  Google Scholar 

  • Yadav SK (2009) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Zavoda J, Cutright T, Szpak J, Fallon E (2001) Uptake, selectivity and inhibition of hydroponic treatment of contaminants. J Environ Eng 127:502–508

    Article  CAS  Google Scholar 

  • Zucconi F, Monaco A, Forte M, deBertoldi M (1985) Phytotoxins during the stabilization of organic matter. In: Gasser JKR, editor. Composting of agricultural and other wastes.London: Elsevier Applied Science Pub 1: 73–86

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dalel belhaj.

Additional information

Responsible editor: Zhihong Xu

Dalel Belhaj and Nada Elloumi contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

belhaj, D., Elloumi, N., Jerbi, B. et al. Effects of sewage sludge fertilizer on heavy metal accumulation and consequent responses of sunflower (Helianthus annuus). Environ Sci Pollut Res 23, 20168–20177 (2016). https://doi.org/10.1007/s11356-016-7193-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7193-0

Keywords

Navigation