Skip to main content

Agro-industrial wastes as effective amendments for ecotoxicity reduction and soil health improvement in aided phytostabilization

Environmental Science and Pollution Research volume 21, pages 10036–10044 (2014)Cite this article

Abstract

Aided phytostabilization is a technology that uses metal tolerant plants and organic and/or inorganic amendments to reduce soil metal bioavailability, while improving soil health. Our objective was to determine the effects of the application of amendments [sheep manure (SHEEP), poultry litter (POULTRY), cow slurry (COW), and paper mill sludge mixed with poultry litter (PAPER)], together with the growth of a metallicolous Festuca rubra L. population, on (i) chemical and microbial indicators of soil health and (ii) soil ecotoxicity, during the aided phytostabilization of a Zn/Pb contaminated mine soil. Amendment application led to an increase in soil pH, organic matter content, and inorganic salts, resulting in a decrease in Pb and Zn CaCl2-extractable concentrations in soil, which, in turn, contributed to lower ecotoxicity and a stimulation of plant growth and soil microbial communities. The factor most affecting the metal extractability was probably soil pH. POULTRY was the best amendment in terms of increasing plant growth, chlorophylls content, and soil microbial biomass and activity, but resulted in higher levels of phytoavailable Pb and Zn. SHEEP and PAPER were more effective at reducing metal CaCl2-extractability and, consequently, led to lower values of metal accumulation in plant tissues, thereby reducing the risk of metals entering into the food chain. When combined with the application of organic amendments, the metallicolous F. rubra population studied here appears an excellent candidate for aided phytostabilization. Our results indicate that the application of organic amendments is essential for the short-term recovery of highly contaminated metalliferous soils during aided phytostabilization.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

References

  • Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142

    CAS  Article  Google Scholar 

  • Alvarenga P, Gonçalves AP, Fernandes RM, de Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2009) Organic residues as immobilizing agents in aided phytostabilization: (I) Effects on soil chemical characteristics. Chemosphere 74:1292–1300

    CAS  Article  Google Scholar 

  • Anderson TH, Domsch KH (1985) Determination of eco-physiological maintenance requirements of soil microorganisms in a dormant state. Biol Fertil Soil 1:81–89

    CAS  Article  Google Scholar 

  • Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soils from a metallurgical site. Sci Total Environ 319:13–25

    CAS  Article  Google Scholar 

  • Ariz I, Esteban R, García-Plazaola JI, Becerril JM, Aparicio-Tejo PM, Moran JF (2010) High irradiance induces photoprotective mechanisms and a positive effect on NH4 + stress in Pisum sativum L. J Plant Physiol 167:1038–1045

    CAS  Article  Google Scholar 

  • Barrutia O, Epelde L, García-Plazaola JI, Garbisu C, Becerril JM (2009) Phytoextraction potential of two Rumex acetosa L. accessions collected from metalliferous and non-metalliferous sites: Effect of fertilization. Chemosphere 74:259–264

    CAS  Article  Google Scholar 

  • Barrutia O, Artetxe U, Hernández A, Olano JM, García-Plazaola JI, Garbisu C, Becerril JM (2011) Native plant communities in an abandoned Pb-Zn mining area of northern Spain: Implications for phytoremediation and germplasm preservation. Int J Phytoremediat 13:256–270

    CAS  Article  Google Scholar 

  • Boluda R, Roca-Pérez L, Marimón L (2011) Soil plate bioassay: an effective method to determine ecotoxicological risks. Chemosphere 84:1–8

    CAS  Article  Google Scholar 

  • Bosshard C, Sørensen P, Frossard E, Dubois D, Mäder P, Nanzer S, Oberson A (2009) Nitrogen use efficiency of 15 N-labelled sheep manure and mineral fertilizer applied to microplots in long-term organic and conventional cropping systems. Nutr Cycle Agroecosyst 83:271–287

    Article  Google Scholar 

  • Dilly O (2006) Ratios of microbial biomass estimates to evaluate microbial physiology in soil. Biol Fert Soil 42:241–246

    Article  Google Scholar 

  • Directive 86/278/EC, of 12 June 1986, on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture (DOCE no. L 181, of 4 July 1986). Brussels, Belgium

  • Epelde L, Becerril JM, Hernández-Allica J, Barrutia O, Garbisu C (2008) Functional diversity as indicator of the recovery of soil health derived from Thlaspi caerulescens growth and metal phytoextraction. Appl Soil Ecol 39:299–310

    Article  Google Scholar 

  • Epelde L, Becerril JM, Mijangos I, Garbisu C (2009) Evaluation of the efficiency of a phytostabilization process with biological indicators of soil health. J Environ Qual 38:2041–2049

    CAS  Article  Google Scholar 

  • Epelde L, Becerril JM, Barrutia O, González-Oreja JA, Garbisu C (2010) Interactions between plant and rhizosphere microbial communities in a metalliferous soil. Environ Pollut 158:1576–1583

    CAS  Article  Google Scholar 

  • Ernst WHO (2005) Phytoextraction of mine wastes—Options and impossibilities. Chem der Erde 65:29–42

    Article  Google Scholar 

  • Foged, Lyngsø H, Flotats X, Blasi AB, Palatsi J, Magri A, Schelde KM (2011) Inventory of manure processing activities in Europe. Technical Report No. I concerning “Manure Processing Activities in Europe” to the European Commission, Directorate-General Environment

  • García-Plazaola JI, Becerril JM (2001) Seasonal changes, photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: Implications for tree decline diagnosis. Aust J Plant Physiol 28:225–232

    Google Scholar 

  • Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378

    CAS  Article  Google Scholar 

  • Hartz TK, Mitchell JP, Giannini C (2000) Nitrogen and carbon mineralization dynamics of manures and composts. HortScience 35:209–212

    Google Scholar 

  • Hernández-Allica J, Becerril JM, Zárate O, Garbisu C (2006) Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 281:147–158

    Article  Google Scholar 

  • Houba VJG, Lexmond TM, Novozamsky I, van der Lee JJ (1996) State of the art and future developments in soil analysis for bioavailability assessment. Sci Total Environ 178:21–28

    CAS  Article  Google Scholar 

  • Houba VJG, Temminghoff EJM, Gaikhorst GA, vanVark W (2000) Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Commun Soil Sci Plant Anal 31:1299–1396

    CAS  Google Scholar 

  • ISO 10390 (2005) Soil quality. Determination of pH, Geneva

    Google Scholar 

  • ISO 16072 (2002) Soil quality. Laboratory methods for determination of microbial soil respiration, Geneva

    Google Scholar 

  • ISO 17155 (2002) Soil quality. Determination of abundance and activity of soil microflora using respiration curves, Geneva

    Google Scholar 

  • Karlen DL, Andrews SS, Weinhold BJ, Doran JW (2003) Soil quality: Humankind’s foundation for survival. J Soil Water Conserv 58:171–179

    Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—a review. Waste Manage 28:215–225

    CAS  Article  Google Scholar 

  • Liu L, Chen H, Cai P, Liang W, Huang Q (2009) Immobilization and phytotoxicity of Cd in contaminated soil amended with chicken manure compost. J Hazard Mater 163:563–567

    CAS  Article  Google Scholar 

  • MAPA (1994) Official methods of analysis. Volume III. General Technical Secretary, Ministry of Agriculture, Fisheries and Food, Madrid

    Google Scholar 

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

    CAS  Article  Google Scholar 

  • Moreno-Jiménez E, Esteban E, Carpena-Ruiz RO, Lobo MC, Peñalosa JM (2012) Phytostabilization with Mediterranean shrubs and liming improved soil quality in a pot experiment with a pyrite mine soil. J Hazard Mater 201–202:52–59

    Article  Google Scholar 

  • Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc Environ 15:327–337

    Google Scholar 

  • Novozamsky I, Lexmond TM, Houba VJG (1992) A single extraction procedure of soil for evaluation of uptake of some heavy metals by plants. Int J Environ An Ch 51:47–58

    Article  Google Scholar 

  • Ohm H, Marschner B, Broos K (2011) Respiration and priming effects after fructose and alanine additions in two copper- and zinc-contaminated Australian soils. Biol Fert Soil 47:523–532

    CAS  Article  Google Scholar 

  • Rashid MT, Barry D, Goss M (2006) Paper mill biosolids application to agricultural lands: benefits and environmental concerns with special reference to situation in Canada. Soil Environ 25:85–98

    Google Scholar 

  • Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228

    CAS  Article  Google Scholar 

  • van der Werf A, Nagel OW (1996) Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose: Opinion. Plant Soil 185:21–32

    Article  Google Scholar 

  • 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 Res 16:765–794

    CAS  Article  Google Scholar 

  • Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780

    CAS  Article  Google Scholar 

  • Zhao F, McGrath SP, Crosland AR (1994) Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectroscopy (ICP-AES). Commun Soil Sci Plant Anal 25:407–418

    CAS  Google Scholar 

Download references

Acknowledgments

This work has been financially supported by the following projects: Etortek-BERRILUR III, UPV/EHU-GV IT-299-07, and MINECO AGL2012-39715-CO3-01/02. M.A. Galende is the recipient of a postdoctoral fellowship from the University of the Basque Country (UPV/EHU), and M.T. Gómez-Sagasti is the recipient of a predoctoral fellowship from the Department of Education, Universities and Research, Basque Government. SGIker technical and human support by Dr. Juan Carlos Raposo and Dr. Azucena González (University of the Basque Country) is gratefully acknowledged.

Author information

Affiliations

  1. Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), P.O. box 644, 48080, Bilbao, Spain

    María A. Galende, José M. Becerril, María T. Gómez-Sagasti, Oihana Barrutia & Antonio Hernández

  2. NEIKER-Tecnalia, Basque Institute of Agricultural Research and Development, Soil Microbial Ecology Group, c/Berreaga 1, 48160, Derio, Spain

    Carlos Garbisu

Authors
  1. María A. Galende
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José M. Becerril
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María T. Gómez-Sagasti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oihana Barrutia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos Garbisu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Antonio Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María A. Galende.

Additional information

Responsible editor: Zhihong Xu

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Galende, M.A., Becerril, J.M., Gómez-Sagasti, M.T. et al. Agro-industrial wastes as effective amendments for ecotoxicity reduction and soil health improvement in aided phytostabilization. Environ Sci Pollut Res 21, 10036–10044 (2014). https://doi.org/10.1007/s11356-014-2752-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-2752-8

Keywords

  • Biological indicators
  • Festuca rubra
  • Organic amendment
  • CaCl2-extractable metal
  • Mine soil
  • Phytoremediation