Interactions between sewage sludge-amended soil and earthworms—comparison between Eisenia fetida and Eisenia andrei composting species

Abstract

Vermicomposting is an eco-friendly technology, where earthworms are introduced in the waste, inter alia sewage sludge, to cooperate with microorganisms and enhance decomposition of organic matter. The main aims of the present study was to determine the influence of two different earthworm species, Eisenia fetida and Eisenia andrei, on the changes of selected metallic trace elements content in substratum during vermicomposting process using three different sewage sludge mainly differentiated by their metal contents. Final vermicompost has shown a slight reduction in Cd, Cu, Ni, and Pb, while the Zn concentration tends to increase. Accumulation of particular heavy metals in earthworms’ bodies was assessed. Both species revealed high tendency to accumulate Cd and Zn, but not Cu, Ni, and Pb, but E. andrei has higher capabilities to accumulate some metals. Riboflavin content, which content varies depending on metal pollution in several earthworms species, was measured supravitaly in extruded coelomocytes. Riboflavin content decreased slightly during the first 6 weeks of exposure and subsequently restored till the end of the 9-week experiment. Selected agronomic parameters have also been measured in the final product (vermicompost) to assess the influence of earthworms on substratum.

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

Fig. 1
Fig. 2
Fig 3
Fig 4

References

  1. APHA (1999) Standard methods for the examination of water and wastewater, 20th edn. APHA, Washington DC

    Google Scholar 

  2. Bernard F, Brulle F, Douay F, Lemiere S, Demuynck S, Vandenbulcke F (2010) Metallic trace element body burdens and gene expression analysis of biomarker candidates in Eisenia fetida, using an “exposure/depuration” experimental scheme with field soils. Ecotoxicol Environ Saf 73:1034–45

    Article  CAS  Google Scholar 

  3. Brulle F, Mitta G, Leroux R, Lemiere S, Lepretre A, Vandenbulcke F (2007) The strong induction of metallothionein gene following cadmium exposure transiently affects the expression of many genes in Eisenia fetida: a trade-off mechanism? comparative biochemistry and physiology. Toxicol Pharmacol : CBP 144:334–41

    CAS  Google Scholar 

  4. Dai J (2004) Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biol Biochem 36:91–98

    Article  CAS  Google Scholar 

  5. Demuynck S, Grumiaux F, Mottier V, Schikorski D, Lemiere S, Lepretre A (2007) Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comp Biochem Physiol Toxicol Pharmacol : CBP 145:658–68

    Article  CAS  Google Scholar 

  6. Dominguez J, Edwards CA (2011) Biology and ecology of earthworm species used for vermicomposting. In: Edwards CA, Sherman RL (eds) Vermiculture technology: earthworms, organic wastes, and environmental management. CRC Press, USA

    Google Scholar 

  7. Domínguez-Crespo MA, Sánchez-Hernández ZE, Torres-Huerta AM, Negrete-Rodríguez MLX, Conde-Barajas E, Flores-Vela A (2011) Effect of the heavy metals Cu, Ni, Cd and Zn on the growth and reproduction of epigeic earthworms (E. Fetida) during the vermistabilization of municipal sewage sludge. Water Air Soil Pollut 223:915–931

    Article  Google Scholar 

  8. Edwards CA (1988) Examines the earthworm through morphology, taxonomy, biology and look at its environmental role. In: Neuhauser CAEEF (ed) Earthworms in waste and environmental management. SPB Academic Publ. Co, The Hague, pp 21–31

    Google Scholar 

  9. Edwards CA, Bater JE (1992) The use of earthworms in environmental management. Soil Biol Biochem 24:1683–1689

    Article  Google Scholar 

  10. Elvira C, Sampedro L, Benítez E, Nogales R (1998) Vermicomposting of sludges from paper mill and dairy industries with Eisenia Andrei: a pilot-scale study. Bioresour Technol 63:205–211

    Article  CAS  Google Scholar 

  11. Fritsch C, Giraudoux P, Cœurdassier M, Douay F, Raoul F, Pruvot C, Waterlot C, Ad V, Scheifler R (2010) Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties, and risk for wildlife. Chemosphere 81:141–155

    Article  CAS  Google Scholar 

  12. Garg P, Gupta A, Satya S (2006) Vermicomposting of different types of waste using Eisenia foetida: a comparative study. Bioresour Technol 97:391–5

    Article  CAS  Google Scholar 

  13. Gogoi A, Biswas S, Bora J, Bhattacharya SS, Kumar M (2015) Effect of vermicomposting on copper and zinc removal in activated sludge with special emphasis on temporal variation. Ecohydrol Hydrobiol 15:101–107

    Article  Google Scholar 

  14. Hait S, Tare V (2011) Vermistabilization of primary sewage sludge. Bioresour Technol 102:2812–20

    Article  CAS  Google Scholar 

  15. Hernstein R (1981) Utilization of earthworms and microorganisms in stabilization, decontamination and detoxification of residual sludges from treatment of wastewater. National Science Foundation, Washington, DC

    Google Scholar 

  16. Homa J, Rorat A, Kruk J, Cocquerelle C, Plytycz B, Vandenbulcke F (2015) Dermal exposure of Eisenia Andrei earthworms: effects of heavy metals on metallothionein and phytochelatin synthase gene expressions in coelomocytes. Environ Toxicol Chem 34:1397–1404

    Article  CAS  Google Scholar 

  17. ISO (6878:2004) Water quality -- Determination of phosphorus -- Ammonium molybdate spectrometric method

  18. Koziol B, Markowicz M, Kruk J, Plytycz B (2006) Riboflavin as a source of autofluorescence in Eisenia fetida coelomocytes. Photochem Photobiol 82:570–3

    Article  CAS  Google Scholar 

  19. Lavelle P, Spain AV (2001) Soil ecology. Kluwer Academic Publishers, Dordrecht, p 654

    Book  Google Scholar 

  20. Liu X, Hu C, Zhang S (2005) Effects of earthworm activity on fertility and heavy metal bioavailability in sewage sludge. Environ Int 31:874–879

    Article  CAS  Google Scholar 

  21. Maboeta MS, Rensburg LV (2003) Vermicomposting of industrially produced woodchips and sewage sludge utilizing Eisenia fetida. Ecotoxicol Environ Saf 56:265–270

    Article  CAS  Google Scholar 

  22. Manna MC, Jha S, Ghosh PK, Acharya CL (2003) Comparative efficacy of three epigeic earthworms under different deciduous forest litters decomposition. Bioresour Technol 88:197–206

    Article  CAS  Google Scholar 

  23. Mazur AI, Klimek M, Morgan AJ, Plytycz B (2011) Riboflavin storage in earthworm chloragocytes and chloragocyte-derived eleocytes and its putative role as chemoattractant for immunocompetent cells. Pedobiologia 54:S37–S42

    Article  CAS  Google Scholar 

  24. Mitchell MJ, Mulligan RM, Hartenstein R, Neuhauser EF (1977) Conversion of sludges into “topsoils” by earthworms. Compost Sci 18:28–32

    CAS  Google Scholar 

  25. Mitchell MJ, Hornor SG, Abrams BI (1980) Decomposition of sewage sludge in drying beds and the potential role of the earthworm, Eisenia foetida1. J Environ Qual 9:373–378

    Article  Google Scholar 

  26. Mohee R, Soobhany N (2014) Comparison of heavy metals content in compost against vermicompost of organic solid waste: past and present. Resour Conserv Recycl 92:206–213

    Article  Google Scholar 

  27. Morgan JE, Morgan AJ (1992) Heavy metal concentrations in the tissues, ingesta and faeces of ecophysiologically different earthworm species. Soil Biol Biochem 24:1691–1697

    Article  CAS  Google Scholar 

  28. Morgan JE, Morgan AJ (1998) The distribution and intracellular compartmentation of metals in the endogeic earthworm Aporrectodea caliginosa sampled from an unpolluted and a metal-contaminated site. Environ Pollut 99:167–75

    Article  CAS  Google Scholar 

  29. Ndegwa PM, Thompson SA (2000) Effects of C-to-N ratio on vermicomposting of biosolids. Bioresour Technol 75:7–12

    Article  CAS  Google Scholar 

  30. Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR (1994) Bioconcentration and biokinetics of heavy metals in the earthworm. Environ Pollut 89:293–301

    Article  Google Scholar 

  31. OECD (1984) OECD guideline for testing chemicals. Section 2: effects on biotic systems, Method, 207, Earthworm, acute toxicity tests, Paris, France

  32. OECD (2007) OECD Annual Report 2007, OECD Publishing

  33. Olchawa E, Bzowska M, Sturzenbaum SR, Morgan AJ, Plytycz B (2006) Heavy metals affect the coelomocyte-bacteria balance in earthworms: environmental interactions between abiotic and biotic stressors. Environ Pollut 142:373–81

    Article  CAS  Google Scholar 

  34. Pattnaik S, Reddy MV (2011) Heavy metals remediation from urban wastes using three species of earthworm (Eudrilus eugeniae, Eisenia fetida and Perionyx excavatus). J Environ Chem Ecotoxicol 3:345–356

    CAS  Google Scholar 

  35. Pauwels M, Frérot H, Souleman D, Vandenbulcke F (2013) Using biomarkers in an evolutionary context: lessons from the analysis of biological responses of oligochaete annelids to metal exposure. Environ Pollut 179:343–350

    Article  CAS  Google Scholar 

  36. Peijnenburg WJGM, Baerselman R, de Groot AC, Jager T, Posthuma L, Van Veen RPM (1999) Relating environmental availability to bioavailability: soil-type-dependent metal accumulation in the oligochaete Eisenia Andrei. Ecotoxicol Environ Saf 44:294–310

    Article  CAS  Google Scholar 

  37. Plytycz B, Lis-Molenda U, Cygal M, Kielbasa E, Grebosz A, Duchnowski M, Andre J, Morgan AJ (2009) Riboflavin content of coelomocytes in earthworm (Dendrodrilus rubidus) field populations as a molecular biomarker of soil metal pollution. Environ Pollut 157:3042–50

    Article  CAS  Google Scholar 

  38. Plytycz B, Kielbasa E, Grebosz A, Duchnowski M, Morgan AJ (2010) Riboflavin mobilization from eleocyte stores in the earthworm dendrodrilus rubidus inhabiting aerially-contaminated Ni smelter soil. Chemosphere 81:199–205

    Article  CAS  Google Scholar 

  39. Plytycz B, Klimek M, Klimek BA, Szymanski W, Kruk J, Morgan AJ (2011) Riboflavin content in the coelomocytes of contrasting earthworm species is differentially affected by edaphic variables including organic matter and metal content. Pedobiologia 54:S43–S48

    Article  CAS  Google Scholar 

  40. PN-ISO (10694:2002) Soil quality - determination of organic and total carbon after dry combustion (‘elementary analysis’)

  41. PN-ISO (11261:2002) Soil quality - determination of total nitrogen - modified Kjeldahl method

  42. Prakash M, Karmegam N (2010) Vermistabilization of pressmud using perionyx ceylanensis Mich. Bioresour Technol 101:8464–8468

    Article  CAS  Google Scholar 

  43. Reynolds JW, Wetzel MJ (2004) Nomenclatura oligochaetologica. Supplementum quartum, A catalogue of names, descriptions and type specimens of the Oligochaeta. Illinois Natural History Survey Special Publication, Illinois

    Google Scholar 

  44. Roodbergen M, Klok C, van der Hout A (2008) Transfer of heavy metals in the food chain earthworm black-tailed godwit (limosa limosa): comparison of a polluted and a reference site in the Netherlands. Sci Total Environ 406:407–12

    Article  CAS  Google Scholar 

  45. Rorat A, Kacprzak M, Vandenbulcke F, Płytycz B (2013) Soil amendment with municipal sewage sludge affects the immune system of earthworms Dendrobaena veneta. Appl Soil Ecol 64:237–244

    Article  Google Scholar 

  46. Rorat A, Kachamakova-Trojanowska N, Jozkowicz A, Kruk J, Cocquerelle C, Vandenbulcke F, Santocki M, Plytycz B (2014) Coelomocyte-derived fluorescence and DNA markers of composting earthworm species. Journal of experimental zoology. A Ecol Genet Physiol 321:28–40

    Article  CAS  Google Scholar 

  47. Singh RP, Embrandiri A, Ibrahim MH, Esa N (2011) Management of biomass residues generated from palm oil mill: vermicomposting a sustainable option. Resour Conserv Recycl 55:423–434

    Article  Google Scholar 

  48. Soobhany N, Mohee R, Garg VK (2015) Comparative assessment of heavy metals content during the composting and vermicomposting of municipal solid waste employing eudrilus eugeniae. Waste Manag 39:130–145

    Article  CAS  Google Scholar 

  49. Spurgeon DJ, Hopkin SP (1996) Risk assessment of the threat of secondary poisoning by metals to predators of earthworms in the vicinity of a primary smelting works. Sci Total Environ 187:167–183

    Article  CAS  Google Scholar 

  50. Spurgeon DJ, Hopkin SP (1999) Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils. Appl Soil Ecol 11:227–243

    Article  Google Scholar 

  51. Suthar S, Singh S (2008) Vermicomposting of domestic waste by using two epigeic earthworms (Perionyx excavatus and Perionyx sansibaricus). Int J Environ Sci Technol 5:99–106

    Article  CAS  Google Scholar 

  52. Suthar S, Singh S (2009) Bioconcentrations of metals (Fe, Cu, Zn, Pb) in earthworms (Eisenia fetida), inoculated in municipal sewage sludge: do earthworms pose a possible risk of terrestrial food chain contamination? Environ Toxicol 24:25–32

    Article  CAS  Google Scholar 

  53. Wang L, Hung Y-T, Li K (2009) Vermicomposting process. In: Wang L, Pereira N, Hung Y-T (eds) Biological treatment processes. Handbook of environmental engineering. Humana Press, Totowa, pp 715–732

    Google Scholar 

  54. Yadav A, Garg VK (2009) Feasibility of nutrient recovery from industrial sludge by vermicomposting technology. J Hazard Mater 168:262–8

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The project was financed with National Center for Science grant based on DEC-2013/09/N/NZ9/01937, by K/ZDS/001955 from the Jagiellonian University, the French Agence National de la Recherche, and by BS PB/401/304/11 and BS MN/401/304/12 from Czestochowa University of Technology (CUT). H. Suleiman was supported by Syrian Ministry of Higher Education. A. Rorat was supported by a doctoral fellowship from Lille 1 University and CUT. Agnieszka Rorat is a beneficient of the project “DoktoRIS – Scholarship Program for Innovative Silesia” funded by the European Union.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Agnieszka Rorat.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rorat, A., Suleiman, H., Grobelak, A. et al. Interactions between sewage sludge-amended soil and earthworms—comparison between Eisenia fetida and Eisenia andrei composting species. Environ Sci Pollut Res 23, 3026–3035 (2016). https://doi.org/10.1007/s11356-015-5635-8

Download citation

Keywords

  • Vermicomposting
  • Metallic trace elements
  • Riboflavin
  • Accumulation
  • Eisenia sp
  • Sewage sludge