Skip to main content
Log in

Assessment of Trace Element Accumulation by Earthworms in an Orchard Soil Remediation Study Using Soil Amendments

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

This study assessed potential bioaccumulation of various trace elements in grasses and earthworms as a consequence of soil incorporation of organic amendments for in situ remediation of an orchard field soil contaminated with organochlorine and Pb pesticide residues. In this experiment, four organic amendments of differing total organic carbon content and quality (two types of composted manure, composted biosolids, and biochar) were added to a contaminated orchard field soil, planted with two types of grasses, and tested for their ability to reduce bioaccumulation of organochlorine pesticides and metals in earthworms. The experiment was carried out in 4-L soil microcosms in a controlled environment for 90 days. After 45 days of orchardgrass or perennial ryegrass growth, Lumbricus terrestris L. were introduced to the microcosms and exposed to the experimental soils for 45 days before the experiment was ended. Total trace element concentrations in the added organic amendments were below recommended safe levels and their phytoavailablity and earthworm availability remained low during a 90-day bioremediation study. At the end of the experiment, total tissue concentrations of Cu, Cd, Mn, Pb, and Zn in earthworms and grasses were below recommended safe levels. Total concentrations of Pb in test soil were similar to maximum background levels of Pb recorded in soils in the Eastern USA (100 mg kg−1 d.w.) because of previous application of orchard pesticides. Addition of aged dairy manure compost and presence of grasses was effective in reducing the accumulation of soil-derived Pb in earthworms, thus reducing the risk of soil Pb entry into wildlife food chains.

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
Fig. 5

Similar content being viewed by others

References

  • Andrade, N. A., Centofanti, T., McConnell, L. L., Hapeman, C. J., Torrents, A., Nguyen, A., Beyer, W. N., Chaney, R. L., Novak, J. M., Anderson, M. O., & Cantrell, K. B. (2014). Utilizing thin-film solid-phase extraction to assess the effect of organic carbon amendments on the bioavailability of DDT and dieldrin to earthworms. Environmental Pollution, 185, 307–313.

    Article  CAS  Google Scholar 

  • Baiocchi, G., & Distaso, W. (2003). GRETL: econometric software for the GNU generation. Journal of Applied Econometrics, 18, 105–110.

    Article  Google Scholar 

  • Basta, N. T., Ryan, J. A., & Chaney, R. L. (2005). Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. Journal of Environmental Quality, 34, 49–63.

    Article  CAS  Google Scholar 

  • Beyer, W. N., & Gale, R. (2013). Persistence and changes in bioavailability of dieldrin, DDE, and heptachlor epoxide in earthworms over 45 years. Ambio, 42, 83–89.

    Article  CAS  Google Scholar 

  • Beyer, W. N., & Stafford, C. (1993). Survey and evaluation of contaminants in earthworms and in soils derived from dredged material at confined disposal facilities in the Great Lakes Region. Environmental Monitoring and Assessment, 24, 151–165.

    Article  CAS  Google Scholar 

  • Beyer, W. N., & Cromartie, E. J. (1987). A survey of Pb, Cu, Zn, Cd, As, and Se in earthworms and soil from diverse sites. Environmental Monitoring and Assessment, 8, 27–36.

    Article  CAS  Google Scholar 

  • Beyer, W. N., Chaney, R. L., & Mulhern, M. (1982). Heavy metal concentrations in earthworms from soil amended with sewage sludge. Journal of Environmental Quality, 11, 381–385.

    Article  CAS  Google Scholar 

  • Beyer, W. N., & Gish, C. D. (1980). Persistence in earthworms and potential hazards to birds of soil applied DDT, dieldrin and heptachlor. Journal of Applied Ecology, 17, 295–307.

    Article  CAS  Google Scholar 

  • Ball, D.M., Collins, M., Lacefield, G.D., Martin, N.P., Mertens, D.A., Olson, K.E., Putnam, D.H., Undersander, D.J., Wolf, M.W. Understanding forage quality. American Farm Bureau Federation Publication 1, no. 01 (2001)

  • Bolan, N. S., & Duraisamy, V. P. (2003). Role of inorganic and organic soil amendments on immobilisation and phytoavailability of heavy metals: a review involving specific case studies. Soil Research, 41, 533–555.

    Article  CAS  Google Scholar 

  • Brown, S. L., & Chaney, R. L. (2016). Use of amendments to restore ecosystem function to metal mining impacted sites; tools to evaluate efficacy. Current Pollution Reports. doi:10.1007/s40726-016-0029-1.

    Google Scholar 

  • Brown, S, Chaney, RL, Sprenger, M, Compton, H (2002a). Assessing impact to wildlife at biosolids remediated sites. BioCycle, 43, 50-58.

  • Brown, S, Chaney, RL, Sprenger, M, Compton, H (2002b). Soil remediation using biosolids. BioCycle, 43, 41-44.

  • Brown, S. L., Henry, C. L., Chaney, R., Compton, H., & DeVolder, P. S. (2003). Using municipal biosolids in combination with other residuals to restore metal-contaminated mining areas. Plant and Soil, 249, 203–215.

    Article  CAS  Google Scholar 

  • Centofanti, T., Andrade, N. A., McConnell, L. L., Chaney, R. L., Hapeman, J. C., Torrents, A., Beyer, N. W., Nguyen, A., Anderson, M. O., Novak, J. M., & Jackson, D. (2016). Organic amendments for risk mitigation of organochlorine pesticide residues in old orchard soils. Environmental Pollution, 120, 182–191.

    Article  Google Scholar 

  • Chaney, R.L. (2010). Cadmium and Zinc. In Hooda, P.S. (Ed.), Trace Elements in Soils (pp. 409-440). John Wiley & Sons, Ltd.

  • Chaney, R.L., Mahoney, M. (2014). Phytostabilization and phytomining: Principles and successes. Meeting Proceedings. Proc. Life of Mines Conference, July 15-17, 2014, Brisbane Australia. Paper 104.

  • Chaney, R. L., Malik, M., Li, Y. M., Brown, S. L., Brewer, E. P., Angle, J. S., & Baker, A. J. M. (1997). Phytoremediation of soil metals. Current Opinion in Biotechnology, 8, 279–284.

    Article  CAS  Google Scholar 

  • Chaney, R. L., Ryan, J. A., & O’Connor, G. A. (1996). Organic contaminants in municipal biosolids: risk assessment, quantitative pathways analysis, and current research priorities. Science of the Total Environment, 185, 187–216.

    Article  CAS  Google Scholar 

  • Chaney, R.L., Sterrett, S.B., Mielke, H.W. (1984). The potential for heavy metal exposure from urban gardens and soils. In Proc. Symp. Heavy Metals in Urban Gardens. pp. 37-84.

  • Conder, J. M., Lanno, R. P., & Basta, N. T. (2001). Assessment of metal availability in smelter soil using earthworms and chemical extractions. Journal of Environmental Quality, 30, 1231–1237.

    Article  CAS  Google Scholar 

  • Ernst, G., Zimmermann, S., Christie, P., & Frey, B. (2008). Mercury, cadmium and lead concentrations in different ecophysiological groups of earthworms in forest soils. Environmental Pollution, 156, 1304–1313.

    Article  CAS  Google Scholar 

  • Kennette, D., Hendershot, W., Tomlin, A., & Sauvé, S. (2002). Uptake of trace metals by the earthworm Lumbricus terrestris L. in urban contaminated soils. Applied Soil Ecology, 19, 191–198.

    Article  Google Scholar 

  • Kızılkaya, R. (2004). Cu and Zn accumulation in earthworm Lumbricus terrestris L. in sewage sludge amended soil and fractions of Cu and Zn in casts and surrounding soil. Ecological Engineering, 22, 141–151.

    Article  Google Scholar 

  • Korthals, G. W., Popovici, I., Iliev, I., & Lexmond, T. M. (1998). Influence of perennial ryegrass on a copper and zinc affected terrestrial nematode community. Applied Soil Ecology, 10, 73–85.

    Article  Google Scholar 

  • Kukier, U., Chaney, R. L., Ryan, J. A., Daniels, W. L., Dowdy, R. H., & Granato, T. C. (2010). Phytoavailability of cadmium in long-term biosolids amended soils. Journal of Environmental Quality, 39, 519–530.

    Article  CAS  Google Scholar 

  • Latif, R., Malek, M., & Mirmonsef, H. (2013). Cadmium and lead accumulation in three endogeic earthworm species. Bulletin of Environmental Contamination and Toxicology, 90, 456–459.

    Article  CAS  Google Scholar 

  • Mehlich, A. (1984). Mehlich-3 soil test extractant: a modification of Mehlich-2 extractant. Communications in Soil Science and Plant Analysis, 15, 1409–1416.

    Article  CAS  Google Scholar 

  • Marschner, H. (2011). Marschner’s mineral nutrition of higher plants. Academic press.

  • Morris, B., & Morgan, A. J. (1986). Calcium-lead interactions in earthworms: observations on Lumbricus terrestris L. sampled from a calcareous abandoned leadmine site. Bulletin of Environmental Contamination and Toxicology, 37, 226–233.

    Article  CAS  Google Scholar 

  • Morgan, J. E., & Morgan, A. J. (1990). The distribution of cadmium, copper, lead, zinc and calcium in the tissues of the earthworm Lumbricus rubellus sampled from one uncontaminated and four polluted soils. Oecologia, 84, 559–566.

    Article  Google Scholar 

  • Nahmani, J., Hodson, M. E., & Black, S. (2007). A review of studies performed to assess metal uptake by earthworms. Environmental Pollution, 145, 402–424.

    Article  CAS  Google Scholar 

  • Nannoni, F., Rossi, S., & Protano, G. (2014). Soil properties and metal accumulation by earthworms in the Siena urban area (Italy). Applied Soil Ecology, 77, 9–17.

    Article  Google Scholar 

  • National Research Council. Mineral tolerance of animals: second revised edition. Washington, DC: The National Academies Press, 2005.

  • OECD. 2004. Guideline for testing of chemical n 222. Earthworm reproduction Test (Eisenia fetida / Eisenia andrei), acute toxicity tests, Adopted 13 April 2004.

  • Park, J. H., Lamb, D., Paneerselvam, P., Choppala, G., Bolan, N., & Chung, J. (2011). Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. Journal of Hazardous Materials, 185, 549–574.

    Article  CAS  Google Scholar 

  • Pearson, M. S., Maenpaa, K., Pierzynski, G. M., & Lydy, M. J. (2000). Effects of soil amendments on the bioavailability of lead, zinc, and cadmium to earthworms. Journal of Environmental Quality, 29, 1611–1617.

    Article  CAS  Google Scholar 

  • Peryea, F. J., & Creger, T. L. (1994). Vertical distribution of lead and arsenic in soils contaminated with lead arsenate pesticide residues. Water, Air, and Soil Pollution, 78, 297–306.

    Article  CAS  Google Scholar 

  • Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.

    Article  CAS  Google Scholar 

  • Richardson, J. B., Görres, J. H., Jackson, B. P., & Friedland, A. J. (2015). Trace metals and metalloids in forest soils and exotic earthworms in northern New England, USA. Soil Biology and Biochemistry, 85, 190–198.

    Article  CAS  Google Scholar 

  • Robinson, B., Green, S., Mills, T., Clothier, B., Van Der Velde, M., Laplane, R., Fung, L., Deurer, M., Hurst, S., Thayalakumaran, T., & Van Den Dijssel, C. (2003). Phytoremediation: using plants as biopumps to improve degraded environments. Australian Journal of Soil Research, 41, 599–611.

    Article  Google Scholar 

  • Sizmur, T., Palumbo-Roe, B., Watts, M. J., & Hodson, M. E. (2011). Impact of the earthworm Lumbricus terrestris (L.) on As, Cu, Pb and Zn mobility and speciation in contaminated soils. Environmental Pollution, 159, 742–748.

    Article  CAS  Google Scholar 

  • Spokas, K. A., Cantrell, K. B., Novak, J. M., Archer, J. W., Ippolito, J. A., Collins, H. P., Boateng, A. A., Lima, I. M., Lamb, M. C., McAloon, A. J., Lentz, R. D., & Nichols, K. A. (2012). Biochar: a synthesis of its agronomic impact beyond carbon sequestration. Journal of Environmental Quality, 41, 973–989.

    Article  CAS  Google Scholar 

  • Smith, D.B., Cannon, W.F., Woodruff, L.G., Solano, Federico, Kilburn, J.E., and Fey, D.L. (2013). Geochemical and mineralogical data for soils of the conterminous United States: U.S. Geological Survey Data Series 801, 19 p., http://pubs.usgs.gov/ds/801/.

  • U.S. Department of Agriculture. (2009). Biological availability study report: BARC 4/19. Document Accession Number: F-24-0454. Beltsville Agricultural Research Center Information Repository (http://www.ars.usda.gov/superfund, accessed 12/10/15)

  • U.S. EPA (2003). Guidance for developing ecological soil screening levels—review of background concentrations for metals. OSWER Dir. 92857-55 pp. 31.

  • van Herwijnen, R., Laverye, T., Poole, J., Hodson, M. E., & Hutchings, T. R. (2007). The effect of organic materials on the mobility and toxicity of metals in contaminated soils. Applied Geochemistry, 22, 2422–2434.

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Ms. Marya Orf Anderson, Dr. Natasha Andrade, and Mr. Christopher Jennings for their assistance during field and laboratory operations. In addition, a special thank you to Ms. Ann Ngyuen and Dr. Carrie Green for their invaluable analytical and technical contribution to this study. Funding for this study was received from the US Environmental Protection Agency, Region III Green Remediation Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiziana Centofanti.

Ethics declarations

Disclaimer

Mention of specific products is for identification and does not imply endorsement by the US Department of Agriculture or the US Geological Survey to the exclusion of other suitable products or suppliers.

Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Centofanti, T., Chaney, R.L., Beyer, W.N. et al. Assessment of Trace Element Accumulation by Earthworms in an Orchard Soil Remediation Study Using Soil Amendments. Water Air Soil Pollut 227, 350 (2016). https://doi.org/10.1007/s11270-016-3055-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-016-3055-0

Keywords

Navigation