Abstract
Toxic heavy metals persist in agricultural soils and ecosystem for many decades after their application as contaminants in sewage sludge and fertilizer products This study assessed the potential long-term risk of cadmium (Cd), lead (Pb), zinc (Zn), and copper (Cu) in land-applied sewage sludge to food crop contamination. A sewage sludge-amended soil (SAS) aged in the field more than 35 years was used in a greenhouse pot experiment with leafy vegetables (lettuce and amaranth) having strong Cd and Zn accumulation tendencies. Soil media with variable levels of available Cd, Zn, and Cu (measured using 0.01 M CaCl2 extraction) were prepared by diluting SAS with several levels of uncontaminated control soil. Despite long-term aging in the field, the sludge site soil still retains large reserves of heavy metals, residual organic matter, phosphorus, and other nutrients, but its characteristics appear to have stabilized over time. Nevertheless, lettuce and amaranth harvested from the sludge-treated soil had undesirable contents of Cd and Zn. The high plant uptake efficiency for Cd and Zn raises a concern regarding the quality and safety of leafy vegetables in particular, when these crops are grown on soils that have been amended heavily with sewage sludge products at any time in their past.
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Allison, L. E. (1976). Organic carbon. In: C. A. Black (Ed.), Methods of soil analysis: Part 2. Chemical and microbiological properties. American Society of Agronomy (pp. 1367–1378). Madison, Wisconsin.
Bai, Y., Chen, W., Chang, A. C., & Page, A. L. (2010). Uptake of metals by food plants grown on soils 10 years after biosolids application. Journal of Environmental Science and Health. Part. B, 45, 531–539.
De Vos, C. H. R., Schat, H., De Waal, M. A. M., Vooijs, R., & Ernst, W. H. O. (1991). Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiologia Plantarum, 82, 523–528. Copenhagen.
Furr, A. K., Parkinson, T. F., Elfving, D. C., Bache, C. A., Gutenmann, W. H., Doss, G. J., & Lisk, D. J. (1981). Elemental content of vegetables and apple trees grown on Syracuse sludge-amended soils. Journal of Agricultural and Food Chemistry, 29, 156–160.
Jayasinghe, G. Y., Tokashiki, Y., Arachchi, I. D., & Arakaki, M. (2010). Sewage sludge sugarcane trash based compost and synthetic aggregates as peat substitutes in containerized media for crop production. Journal of Hazardous Materials, 174, 700–706.
Kim, B., & McBride, M. B. (2009). Phytotoxic effects of Cu and Zn on soybeans grown in field-aged soils: their additive and interactive actions. Journal of Environmental Quality, 38, 2253–2259.
Lexmond, T. M., & van der Vorm, P. D. J. (1981). The effect of soil pH on copper toxicity to hydroponically grown maize. Netherlands Journal of Agricultural Science, 29, 209–230.
Li, N. Y., Fu, Q. L., Zhuang, P., Guo, B., Zou, B., & Li, Z. A. (2012). Effect of fertilizers on Cd uptake of Amaranthus hypochondriacus, a high biomass, fast growing and easily cultivated potential Cd hyperaccumulator. International Journal of Phytoremediation, 14, 162–173.
Macdonald, C. A., Clark, I. M., Zhao, F.-J., Hirsch, P. R., Singh, B. K., & McGrath, S. P. (2011). Long-term impacts of zinc and copper enriched sewage sludge additions on bacterial, archaeal and fungal communities in arable and grassland soils. Soil Biology and Biogeochemistry, 43, 932–941.
McBride, M. B. (2003). Toxic metals in sewage sludge-amended soils: has promotion of beneficial use discounted the risks? Advances in Environmental Research, 8, 5–19.
McBride, M. B., & Cai, M. (2016). Copper and zinc aging in soils for a decade: changes in metal extractability and phytotoxicity. Environmental Chemistry, 13, 160–167.
McBride, M. B., Richards, B. K., Steenhuis, T., Russo, J. J., & Sauvé, S. (1997). Mobility and solubility of toxic metals and nutrients in soil fifteen years after sludge application. Soil Science, 162, 487–500.
McBride, M. B., Richards, B. K., & Steenhuis, T. (2004). Bioavailability and crop uptake of trace elements in soil columns amended with sewage sludge products. Plant and Soil, 262, 71–84.
McBride, M. B., Simon, T., Tam, G., & Wharton, S. (2013). Lead and arsenic uptake by leafy vegetables grown on contaminated soils: effects of mineral and organic amendments. Water, Air, and Soil Pollution, 224, 1378.
Mellem, J. J., Baijnath, H., & Odhav, B. (2009). Translocation and accumulation of Cr, Hg, As, Pb, Cu and Ni by Amaranthus dubius (Amaranthaceae) from contaminated sites. Journal of Environmental Science and Health, Part A, 44, 568–575.
Moffett, B. F., Nicholson, F. A., Uwakwe, N. C., Chambers, B. J., Harris, J. A., & Hill, T. C. J. (2003). Zinc contamination decreases the bacterial diversity of agricultural soil. FEMS Microbiology Ecology, 43, 13–19.
Nanda Kumar, P. B. A., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction: the use of plants to remove heavy metals from soils. Environmental Science and Technology, 29, 1232–1238.
Nogueira, T. A. R., Franco, A., He, Z., Braga, V. S., Firme, L. P., & Abreu-Junior, C. H. (2013). Short-term usage of sewage sludge as organic fertilizer to sugarcane in a tropical soil bears little threat of heavy metal contamination. Journal of Environmental Management, 114, 168–177.
NYSDEC (2006). NYCRR Part 375-Environmental Remediation Programs. New York State Department of Environmental Conservation. 6.
Rahman, M. M., Azirun, S. M., & Boyce, A. N. (2013). Enhanced accumulation of copper and lead in amaranth (Amaranthus paniculatus), Indian mustard (Brassica juncea) and sunflower (Helianthus annuus). PloS One, 8, e62941.
Richards, B. K., Steenhuis, T. S., Peverly, J. H., & McBride, M. B. (1998). Metal mobility at an old, heavily loaded sludge application site. Environmental Pollution, 99, 365–377.
Sauvé, S., McBride, M. B., Norvell, W. A., & Hendershot, W. H. (1997). Copper solubility and speciation if in situ contaminated soils: effects of copper level, pH and organic matter. Water, Air, and Soil Pollution, 100, 133–149.
Shaheen, S. M., Shams, M. S., Ibrahim, S. M., Elbehiry, F. A., Antoniadis, V., & Hooda, P. S. (2014). Stabilization of sewage sludge by using various by-products: effects on soil properties, biomass production, and bioavailability of copper and zinc. Water Air Soil and Pollution, 225, 2014.
Singh, R. P., & Agrawal, M. (2010). Effect of different sewage sludge applications on growth and yield of Vigna radiata L. field crop: element uptake by plant. Ecological Engineering, 36, 969–972.
Uysal, A., Yilmazel, Y. D., & Demirer, G. N. (2010). The determination of fertilizer quality of the formed struvite from effluent of a sewage sludge anaerobic digester. Journal of Hazardous Materials, 181, 248–254.
Walter, I., Martínez, F., Alonso, L., de Gracia, J., & Cuevas, G. (2002). Extractable soil heavy metals following the cessation of biosolids application to agricultural soil. Environmental Pollution, 117, 315–321.
Wei, S. H., Ji, D. D., & Twardowska, I. (2015). Effect of different nitrogenous nutrients on the cadmium hyperaccumulation efficiency of Rorippa globosa (Turcz.) Thell. Environmental Science and Pollution Research, 223, 1999–2007.
Zorrig, W., El Khouni, A., Ghnaya, T., Davidian, J. C., Abdelly, C., & Berthomieu, P. (2013). Lettuce (Lactuca sativa): a species with a high capacity for cadmium (Cd) accumulation and growth stimulation in the presence of low Cd concentrations. Journal of Horticultural Science and Biotechnology, 88, 783–789.
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Highlights
Long-term risk of toxic metals in land-applied sewage sludge was assessed.
Lettuce and amaranth strongly accumulated Cd and Zn despite 35 years of field aging.
Cadmium presents a singular hazard because of its zootoxicity and persistent bioavailability in soils
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Tai, Y., Li, Z. & Mcbride, M.B. Natural attenuation of toxic metal phytoavailability in 35-year-old sewage sludge-amended soil. Environ Monit Assess 188, 241 (2016). https://doi.org/10.1007/s10661-016-5254-y
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DOI: https://doi.org/10.1007/s10661-016-5254-y