Abstract
Bioremediation is very efficient in biodegrading petroleum hydrocarbons. However, the decrease in these target contaminants in soils is not necessarily followed by a decrease in toxicity. The remaining contaminants can be enough to retain toxicity, while incomplete degradation of several compounds can generate sub-products, which can be even more toxic. In this context, the aim of this study was to assess acute and chronic toxicity in Eisenia andrei exposed to soil contaminated with 5% spent lubricant oil before and after 22 months of bioremediation in 150 L aerobic reactors. Applied bioremediation strategies were biostimulation (BIOS), bioaugmentation by adding mature compost from municipal solid waste (BIOA1) and bioaugmentation by adding non-mature compost from municipal solid waste (BIOA2). After 22 months, total petroleum hydrocarbons (TPH) were reduced 71% in BIOS and 73% in both BIOA1 and BIOA2. Polycyclic aromatic hydrocarbons (PAH) were reduced in about 98% in all treatments (BIOS, BIOA1 and BIOA2). At the 14th day of exposure, mortality rates were 7 ± 2, 20 ± 0, 75 ± 25, 93 ± 12 and 100 ± 0% for Eisenia andrei exposed to CONT (soil with no oil addition), BIOS, OLU (soil newly contaminated with 5% spent oil), BIOA1 and BIOA2, respectively. After 14 days, surviving specimens in both BIOS and OLU soils exhibited anatomic deformations, less biomass than the controls, and decrease in juvenile forms and coelomocytes. After 28 days, the mortality rate for BIOS and OLU soils increased to 97 and 100%, respectively. Therefore, even with a reduction of 71–73% for TPH and 98% for PAH, toxic effects remained in all soils bioremediated, probably due to the remaining hydrocarbons and/or hydrocarbon biodegradation products. The results indicate that both chemical analyses and toxicological monitoring are required to follow-up soil remediation progress.
Similar content being viewed by others
References
An YJ (2005) Assessing soil ecotoxicity of methyl tert-butyl ether using earthworm bioassay; closed soil microcosm test for volatile organic compounds. Environ Pollut 134:181–186. https://doi.org/10.1016/j.envpol.2004.08.012
de Andréa MM (2010) Use of earthworms as bioindicators of soil contamination. Acta Zool Mex 26:95–107
Blouin M, Hodson ME, Delgado EA et al. (2013) A review of earthworm impact on soil function and ecosystem services: earthworm impact on ecosystem services. Eur J Soil Sci 64:161–182. https://doi.org/10.1111/ejss.12025
Bonnard M, Eom I-C, Morel J-L, Vasseur P (2009) Genotoxic and reproductive effects of an industrially contaminated soil on the earthworm Eisenia Fetida. Environ Mol Mutagen 50:60–67. https://doi.org/10.1002/em.20436
Bremnner JM (1960) Determination of nitrogen in soil by Kjeldahl method. J Agric Sci 55:11–33
Ceccanti B, Masciandaro G, Garcia C et al. (2006) Soil bioremediation: combination of earthworms and compost for the ecological remediation of a hydrocarbon polluted soil. Water, Air, Soil Pollut 177:383–397. https://doi.org/10.1007/s11270-006-9180-4
Chachina SB, Voronkova NA, Baklanova ON (2015) Biological remediation of the engine lubricant oil-contaminated soil with three kinds of Earthworms, Eisenia Fetida, Eisenia Andrei, Dendrobena Veneta, and a Mixture of Microorganisms. Procedia Eng 113:113–123. https://doi.org/10.1016/j.proeng.2015.07.302
Chaineau CH, Yepremian C, Vidalie JF et al. (2003) Bioremediation of a crude oil-polluted soil: biodegradation, leaching and toxicity assessments. Water Air Soil Poll 144:419–440
CONAMA. Resolution no. 420, December 2009 (in Portuguese). National Environmental Council, Brazil
Correia FV, Moreira JC (2010) Effects of glyphosate and 2,4-D on earthworms (Eisenia foetida) in laboratory tests. Bull Environ Contam Toxicol 85:264–268. https://doi.org/10.1007/s00128-010-0089-7
Di Marzio WD, Sáenz ME, Montivero C et al. (2007) Genotoxicity of acqueous elutions of industrial soils. Bull Environ Contam Toxicol 79:483–487. https://doi.org/10.1007/s00128-007-9284-6
Dorn PB, Vipond TE, Salanitro JP, Wisniewski HL (1998) Assessment of the acute toxicity of crude oils in soils using earthworms; Microtox and plants. Chemosphere 37:845–860
Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd ed. Chapman and Hall, London, UK
Ernandez-Castellanos B, Zavala-Cruz J, Marinez-Hernandez S et al. (2013) Earthworm populations in an aged hydrocarbon contaminated soil. Res J Environ Sci 7:27–37
Eyambe GS, Goven AJ, Fitzpatrick LC et al. (1991) A non-invasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Lab Anim 25:61–67. https://doi.org/10.1258/002367791780808095
Gainer A, Cousins M, Hogan N, Siciliano SD (2018) Petroleum hydrocarbon mixture toxicity and a trait‐based approach to soil invertebrate species for site‐specific risk assessments. Environ Toxicol Chem 2018(37):2222–2234
Geissen V, Gomez-Rivera P, Huerta Lwanga E et al. (2008) Using earthworms to test the efficiency of remediation of oil-polluted soil in tropical Mexico. Ecotoxicol Environ Saf 71:638–642. https://doi.org/10.1016/j.ecoenv.2008.02.015
Hentati O, Lachhab R, Ayadi M, Ksibi M (2013) Toxicity assessment for petroleum-contaminated soil using terrestrial invertebrates and plant bioassays. Environ Monitor Assess 185:2989–2998. https://doi.org/10.1007/s10661-012-2766-y
Hubálek T, Vosáhlová S, Matějů V et al. (2007) Ecotoxicity monitoring of hydrocarbon-contaminated soil during bioremediation: a case study. Arch Environ Contam Toxicol 52:1–7. https://doi.org/10.1007/s00244-006-0030-6
Innemanová P, Filipová A, Michalíková K, Wimmerová L, Cajthaml T (2018) Bioaugmentation of PAH-contaminated soils: A novel procedure for introduction of bacterial degraders into contaminated soil. Ecol Eng 118:93–96. https://doi.org/10.1016/j.ecoleng.2018.04.014
ISO (1993) Soil Quality - Effects of pollutants on earthworms - Part 1: Determination of acute toxicity using artificial soil substrate. ISO 11268-1. International Organization for Standardization, Geneve
ISO (1998) Soil Quality - Effects of pollutants on earthworms - Part 2: Determination of effects on reproduction. ISO 11268-2. International Organization for Standardization, Geneve
Khan MAI, Biswas B, Naidu ESR, Megharaj M (2018) Toxicity assessment of fresh and weathered petroleum hydrocarbons in contaminated soil- a review. Chemosphere 212:755–767. https://doi.org/10.1016/j.chemosphere.2018.08.094
Kuppusamy S, Palanisami T, Megharaj M, Venkateswarlu K, Naidu R (2016) In-situ remediation approaches for the management of contaminated sites: a comprehensive overview. In: de Voogt P (ed) Reviews of Environmental Contamination and Toxicology, vol 236. Reviews of Environmental Contamination and Toxicology (Continuation of Residue Reviews), Springer, Carolina, USA
Klute A, Page AL (eds) (1982) Methods of soil analysis, 2nd ed. American Society of Agronomy. Soil Science Society of America, Madison, Wis
Kriipsalu M, Marques M, Hogland W, Nammari DR (2008) Fate of polycyclic aromatic hydrocarbons during composting of oily sludge. Environ Technol 29:43–53. https://doi.org/10.1080/09593330802008735
Lackmann C, Velki M, Seiler T-B, Hollert H (2018) Herbicides diuron and fluazifop-p-butyl affect avoidance response and multixenobiotic resistance activity in earthworm Eisenia andrei. Chemosphere 210:110–119. https://doi.org/10.1016/j.chemosphere.2018.07.008
Lee YB, Lorenz N, Dick LK, Dick RP (2007) Cold storage and pretreatment incubation effects on soil microbial properties. Soil Sci Soc Am J 71:1299. https://doi.org/10.2136/sssaj2006.0245
Leet JK, Richards SM (2009) Genetic ecotoxicology. In: Santos EB (Eds) Ecotoxicology research developments. Nova Science Publishers, Portland, p 61–87
Lionetto MG, Calisi A, Schettino T (2012) Earthworm biomarkers as tools for soil pollution assessment. Soil Health Land Use Manag 16:305–332
Lopes PRM, Montagnolli RN, de Fátima Domingues R, Bidoia ED (2010) Toxicity and biodegradation in sandy soil contaminated by lubricant oils. Bull Environ Contam Toxicol 84:454–458. https://doi.org/10.1007/s00128-010-9945-8
Lors C, Perie F, Grand C, Damidot D (2009) Benefits of ecotoxicological bioassays in the evaluation of a field biotreatment of PAHs polluted soil. Glob Nest J 11:251–259
Lourenço JI, Pereira RO, Silva AC et al. (2011) Genotoxic endpoints in the earthworms sub-lethal assay to evaluate natural soils contaminated by metals and radionuclides. J Hazard Mater 186:788–795. https://doi.org/10.1016/j.jhazmat.2010.11.073
Martinkosky L, Barkley J, Sabadell G, Gough H, Davidson S (2017) Earthworms (Eisenia fetida) demonstrate potential for use in soil bioremediation by increasing the degradation rates of heavy crude oil hydrocarbons. Sci Total Environ 580:734–743. https://doi.org/10.1016/j.scitotenv.2016.12.020
Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediationapproaches for organic pollutants: A critical perspective. Environ Int 37:1362–1375. https://doi.org/10.1016/j.envint.2011.06.003
Mehlich A (1953) Determination of P, Ca, Mg, K, Na and NH4 by North Carolina soil testing laboratories. Raleigh, N.C.
Molina-Barahona L, Vega-Loyo L, Guerrero M et al. (2005) Ecotoxicological evaluation of diesel-contaminated soil before and after a bioremediation process: ecotoxicology of a diesel-contaminated soil. Environ Toxicol 20:100–109. https://doi.org/10.1002/tox.20083
Newman MC (2010) Fundamentals of ecotoxicology. CRC Press, Boca Raton
Nocentini M, Pinelli D, Fava F (2000) Bioremediation of a soil contaminated by hydrocarbon mixtures: the residual concentration problem. Chemosphere 41:1115–1123. https://doi.org/10.1016/S0045-6535(00)00057-6
Płaza G, Nałęcz-Jawecki G, Ulfig K, Brigmon RL (2005) The application of bioassays as indicators of petroleum-contaminated soil remediation. Chemosphere 59:289–296. https://doi.org/10.1016/j.chemosphere.2004.11.049
Płaza GA, Jangid K, Łukasik K et al. (2008) Reduction of petroleum hydrocarbons and toxicity in refinery wastewater by bioremediation. Bull Environ Contam Toxicol 81:329–333. https://doi.org/10.1007/s00128-008-9411-z
Pohren RS, Rocha JAV, Horn KA, Vargas VMF (2019) Bioremediation of soils contaminated by PAHs: mutagenicity as a tool to validate environmental quality. Chemosphere 214:659–668. https://doi.org/10.1016/j.chemosphere.2018.08.020
Ramadass K, Megharaj M, Venkateswarlu K, Naidu R (2015) Ecological implications of motor oil pollution: earthworm survival and soil health. Soil Biol Biochem 85:72–81. https://doi.org/10.1016/j.soilbio.2015.02.026
Rincón J, Cañizares P, García MT (2007) Regeneration of used lubricant oil by ethane extraction. J Supercrit Fluids 39:315–322. https://doi.org/10.1016/j.supflu.2006.03.007
Salanitro JP, Dorn PB, Huesemann MH, Moore KO, Rhodes IA, Jackson LMR (1997) Crude oil hydrocarbon bioremediation and soil ecotoxicity assessment. Environ Sci Technol 31:1769–1776. https://doi.org/10.1021/es960793i
Saterbak A, Toy RJ, McMain BJ, Williams MP, Dorn PB (2000) Ecotoxicological and analytical assessment of effects of bioremediation on hydrocarbon-containing soils. Environ Toxicol Chem 19:2643–2652
Sforzini S, Boeri M, Dagnino A et al. (2012) Genotoxicity assessment in Eisenia andrei coelomocytes: a study of the induction of DNA damage and micronuclei in earthworms exposed to B[a]P- and TCDD-spiked soils. Mutat Res/Genet Toxicol Environ Mutagen 746:35–41. https://doi.org/10.1016/j.mrgentox.2012.02.011
Shen W, Zu N, Cui J, Wang H, Dang Z, Wu P et al. (2016) Ecotoxicity monitoring and bioindicator screening of oil-contaminated soil during bioremediation. Ecotoxicol Environ Saf 124:120–8. https://doi.org/10.1016/j.ecoenv.2015.10.005
Shin KH, Kim KW (2001) Ecotoxicity monitoring of hydrocarbon-contaminated soil using earthworm (Eisenia foetida). Environ Monit Assess 70:93–103
Sherman R (2003) Raising earthworms successfully. North Carolina Cooperative Extension Service. Publication number: EBAE 103-83, North Carolina University, Raleigh, NC, USA
Song Y et al. (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biol Biochem 41(5):905–909
Stephenson GL, Kuperman RG, Linder GL (2002) Toxicity test for assessing contaminated soils and groundwater. In: Sunahara GI, Renoux AY, Thellen C, Gaudet CL, Pilon A (eds) Environmental analysis of contaminated sites. Wiley, New York, pp 25–44
Tang JC, Wang M, Wang F, Sun Q, Zhou QX (2001) Eco-toxicity of petroleum hydrocarbon contaminated soil. J Environ Sci 23:845–851. https://doi.org/10.1016/S1001-0742(10)60517-7
Trindade PVO, Sobral LG, Rizzo ACL et al. (2005) Bioremediation of a weathered and a recently oil-contaminated soils from Brazil: a comparison study. Chemosphere 58:515–522. https://doi.org/10.1016/j.chemosphere.2004.09.021
USEPA. (2007) Microwave acid digestion of sediments, sludges, soils, and oils. Rev. 1. United States Safety Environmental Protection Agency, Washington DC
van Gestel CAM, van Dis WA (1988) The influence of soil characteristics on the toxicity of four chemicals to the earthworm Eisenia fetida andrei (Oligochaeta). Biol Fertil Soils 6:262–265
Walkley A (1946) A critical examination of a rapid method for determining organic carbon in soils: effects of variations in digestion conditions and organic soils constituents. Soil Sci 63:251–263
Wu S, Zhang H, Zhao S et al. (2012) Biomarker responses of earthworms (Eisenia fetida) exposured to phenanthrene and pyrene both singly and combined in microcosms. Chemosphere 87:285–293. https://doi.org/10.1016/j.chemosphere.2011.11.055
Acknowledgements
The authors acknowledge financial support from The Carlos Chagas Filho Research Support Foundation-FAPERJ and The National Council for Scientific and Technological Development-CNPq.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Soroldoni, S., Silva, G., Correia, F.V. et al. Spent lubricant oil-contaminated soil toxicity to Eisenia andrei before and after bioremediation. Ecotoxicology 28, 212–221 (2019). https://doi.org/10.1007/s10646-018-02013-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-018-02013-x