Abstract
The tropical endogeic earthworm Pontoscolex corethrurus, a non-standard species used in ecotoxicity, has been found in crude oil-contaminated habitats. We estimated the removal of total hydrocarbons from heavy crude “Maya” oil on an artificially contaminated soil with a median lethal concentration of P. corethrurus and an addition of oil palm bagasse. P. corethrurus had a high survival rate, and the addition of oil palm bagasse led to a greater growth and an increase in abundance of bacteria and fungi. The activity of P. corethrurus and the nutritional quality of oil palm bagasse had a significant impact on the removal of a larger amount of petroleum hydrocarbons from contaminated soil. We concluded that the endogeic earthworm P. corethrurus and oil palm bagasse acted synergistically to achieve a more effective removal of total petroleum hydrocarbons from soil. These results show the potential for using P. corethrurus to remove, either directly or indirectly, crude oil from soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alves PRL, Niemeyer JC, Cardoso EJBN (2017) Section I: Terrestrial invertebrates as experimental models chapter 1. He uses of non-standardized inverteberates in soil ecotoxicology, pp 1–10. https://doi.org/10.1039/9781788010573-00001
Anyaoha KE, Sakrabani R, Patchigolla K, Mouazen AM (2018) Critical evaluation of oil palm fresh fruit bunch solid wastes as soil amendments: prospects and challenges. Resour Conserv Recycl 136:399–409. https://doi.org/10.1016/j.resconrec.2018.04.022
Boukirat D, Maatoug M (2021) Bioremediation of lead contaminated soils for sustainable agriculture. In: Jhariya MK, Meena RS, Barnerjee A (eds) Ecological intensification of natural resources for sustainable agriculture. Springer, Singapore. https://doi.org/10.1007/978-981-33-4203-3_10
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 Pollution 177:383–397. https://doi.org/10.1007/S11270-006-9180-4
Cuevas-Díaz MC, Vázquez-Luna D, Martínez-Hernández S, Gumán-López O, Ortiz-Ceballos AI (2017) Sensitivity of the endogeic tropical earthworm Pontoscolex corethrurus to presence of heavy crude oil. Bull Environ Contam Toxicol 99(2):154–160. https://doi.org/10.1007/s00128-017-2126-2
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, et al (2018) A global atlas of the dominat bacteria found in soil. Science 359:320–325. https://doi.org/10.1126/science.aap9516
Ekperusi OA, Aigbodion FI (2015) Bioremediation of petroleum hydrocarbons from crude oil-contaminated soil with the earthworm: Hyperiodrilus africanus. 3 Biotech 5(6):957–965. https://doi.org/10.1007/s13205-015-0298-1
Fiedler S, Siebe C, Herre A, Roth B, Cram S, Stahr K (2009) Contribution of oil industry activities to environmental loads of heavy metals in the Tabasco Lowlands, Mexico. Water Air Soil Pollut 197(1–4):35–47. https://doi.org/10.1007/s11270-008-9789-6
García-Segura D, Castillo-Murrieta IM, Martínez-Rabelo F, Gomez-Anaya A, Rodríguez-Campos J, Hernández-Castellanos B, Contreras-Ramos SM, Barois I (2018) Macrofauna and mesofauna from soil contaminated by oil extraction. Geoderma 332:180–189. https://doi.org/10.1016/j.geoderma.2017.06.013
Hamzah A, Phan CW, Yong PH, Hayati N, Ridzuan M (2014) Oil palm empty fruit bunch and sugarcane bagasse enhance the bioremediation of soil artificially polluted by crude oil. Soil Sedim Contam 23(7):751–762. https://doi.org/10.1080/15320383.2014.870528
Harmsen J, Rietra RPJJ (2018) 25 years monitoring of PAHs and petroleum hydrocarbons biodegradation in soil. Chemosphere 207:229–238. https://doi.org/10.1016/j.chemosphere.2018.05.043
Herbert RA (1990) Methods for enumerating microorganisms and determining biomass in natural environments. Academic Press Methods in Microbiology 22:1–40
Hernández-Castellanos B, Ortíz-Ceballos AI, Martínez-Hernández S, Noa-Carrazana JC, Luna-Guido M, Dendooven L, Contreras-Ramos SM (2013) Removal of benzo (a) pyrene from soil using an endogenic earthworm Pontoscolex corethrurus (Müller, 1857). Appl Soil Ecol 70:62–69. https://doi.org/10.1016/j.apsoil.2013.04.009
Hickman ZA, Reid BJ (2008a) Earthworm assisted bioremediation of organic contaminants. Environ Int 34(7):1072–1081. https://doi.org/10.1016/j.envint.2008.02.013
Hickman ZA, Reid BJ (2008b) Increased microbial catabolic activity in diesel contaminated soil following addition of earthworms (Dendrobaena veneta) and compost. Soil Biol Biochem 40(12):2970–2976. https://doi.org/10.1016/j.soilbio.2008.08.016
Hickman ZA, Reid BJ (2008c) The co-application of earthworms (Dendrobaena veneta) and compost to increase hydrocarbon losses from diesel contaminated soils. Environ Int 34(7):1016–1022. https://doi.org/10.1016/j.envint.2008.03.004
Hoang SA, Sarkar B, Seshadri B, Lamb D, Wijesekara H, Vithanage M, Liyanage C, Kilivabandara PA, Rinklebe J, Lam SS, Vinu A, Wang H, Kirkham MB, Bolan NS (2021) Mitigation of petroleum-hydrocarbon-contaminated hazardous soils using organic amendments: a review. J Hazard Mater 416:125702. https://doi.org/10.1016/j.jhazmat.2021.125702
Khan MAI, Biswas B, Smith E, Naidu R, 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
Lorch HJ, Benckiesser G, Ottow JCG (1998) Basic methods for counting microorganisms in soil and water. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 146–161
Ortiz-Ceballos AI, Pérez-Staples D, Pérez-Rodríguez P (2016) Nest site selection and nutritional provision through excreta: a form of parental care in a tropical endogenic earthworm. PeerJ 4:e2032. https://doi.org/10.7717/peerj.2032
Ortiz-Ceballos AI, Ortiz-Gamino D, Andrade-Torres A, Pérez-Rodríguez P, López-Ortega M (2019) Pontoscolex corethrurus: a homeless invasive tropical earthworm? PLoS ONE 14(9):e0222337. https://doi.org/10.1371/journal.pone.0222337
Parkinson D, Gray TRG, Williams ST (1971) Methods for studying the ecology of soil microorganism, IBP-Handbook No 19. Blackwell, Oxford
Patowary R, Patowary K, Devi A, Kalita MC, Deka S (2017) Uptake of total petroleum hydrocarbon (TPH) and polycyclic aromatic hydrocarbons (PAHs) by Oryza sativa L. grown in soil contaminated with crude oil. Bull Environ Contam Toxicol 98(1):120–126. https://doi.org/10.1007/s00128-016-1990-5
Rodríguez-Campos J, Perales-Garcia A, Hernandez-Carballo J, Martinez-Rabelo F, Hernández-Castellanos B, Barois I, Contreras-Ramos SM (2019) Bioremediation of soil contaminated by hydrocarbons with the combination of three technologies: bioaugmentation, phytoremediation, and vermiremediation. J Soils Sediments 19(4):1981–1994. https://doi.org/10.1007/s11368-018-2213-y
Rupani PF, Embrandiri A, Ibrahim MH, Shahadat M, Hansen SB, Mansor NNA (2017) Bioremediation of palm industry wastes using vermicomposting technology: its environmental application as green fertilizer. 3 Biotech 7(3):1–8. https://doi.org/10.1007/s13205-017-0770-1
Sabrina DT (2012) Oil palm empty-fruit bunch application effects on the earthworm population and phenol contents under field conditions. Afr J Biotech 11(19):4396–4406. https://doi.org/10.5897/ajb11.3582
Schaefer M, Juliane F (2007) The influence of earthworms and organic additives on the biodegradation of oil contaminated soil. Appl Soil Ecol 36(1):53–62. https://doi.org/10.1016/j.apsoil.2006.11.002
Schaefer M, Petersen SO, Filser J (2005) Effects of Lumbricus terrestris, Allolobophora chlorotica and Eisenia fetida on microbial community dynamics in oil-contaminated soil. Soil Biol Biochem 37(11):2065–2076. https://doi.org/10.1016/j.soilbio.2005.03.010
Sims JL, Sims RC, Mattews JE (1989) Bioremediation of contaminated surface soils. United States Environmental Protection Agency
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(4):423–434. https://doi.org/10.1016/j.resconrec.2010.11.005
Sivaram AK, Logeshwaran P, Lockington R, Naidu R, Megharaj M (2019) Phytoremediation efficacy assessment of polycyclic aromatic hydrocarbons contaminated soils using garden pea (Pisum sativum)and earthworms (Eisenia fetida). Chemosphere 229:227–235. https://doi.org/10.1016/j.chemosphere.2019.05.005
Šrut M, Menke S, Höckner M, Sommer S (2019) Earthworms and cadmium – heavy metal resistant gut bacteria as indicators for heavy metal pollution in soils? Ecotoxicol Environ Saf 171:843–853. https://doi.org/10.1016/j.ecoenv.2018.12.102
Taheri S, Pelosi C, Dupont L (2018) Harmful or useful? A case study of the exotic peregrine earthworm morpho species Pontoscolex corethrurus. Soil Biol Biochem 116:277–289. https://doi.org/10.1016/j.soilbio.2017.10.030
The Jamovi Project (2021) Jamovi (Version 1.6) Computer Software. https://www.jamovi.org
Trejo-Hernández MR, Ortiz A, Okoh AI, Morales D, Quintero R (2007) Biodegradation of heavy crude oil Maya using spent compost and sugar cane bagasse wastes. Chemosphere 68(5):848–855. https://doi.org/10.1016/j.chemosphere.2007.02.023
van Groenigen JW, Lubbers IM, Vos HMJ, Brown GG, De Deyn GB, Van Groenigen KJ (2014) Earthworms increase plant production: a meta-analysis. Sci Rep 4:6365. https://doi.org/10.1038/srep06365
Villalobos M, Avila-Forcada AP, Gutierrez-Ruiz ME (2008) An improved gravimetric method to determine total petroleum hydrocarbons in contaminated soils. Water Air Soil Pollut 194(1–4):151–161. https://doi.org/10.1007/s11270-008-9704-1
Wang SJ, Yan ZG, Guo GL, Lu GL, Wang QH, Li FS (2010) Ecotoxicity assessment of aged petroleum sludge using a suite of effects-based end points in earthworm Eisenia fetida. Environmental Monitoring and Assessment 169(1–4):417–428. https://doi.org/10.1007/s10661-009-1184-2
Zavala-Cruz J, Trujillo-Capistran F, Ortiz-Ceballos OC, Ortiz-Ceballos AI (2013) Tropical endogeic earthworm population in pollution gradient with weathered crude oil. Environ Sci 7(1):15–26
Zeb A, Li S, Wu J, Lian J, Liu W, Sun Y (2020) Insights into the mechanisms underlying the remediation potential of earthworms in contaminated soil: a critical review of research progress and prospects. Sci Total Environ 740:140145. https://doi.org/10.1016/j.scitotenv.2020.140145
Acknowledgements
This research was supported by the PRODEP-SEP (CA-UVER-173 and CA-UVER-332) and Mexican CONACYT (CB-2007-01/83600). In addition, we are grateful to anonymous reviewers and Alberto Ortiz Brito for careful revision of the manuscript.
Author information
Authors and Affiliations
Corresponding author
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
del Carmen Cuevas-Díaz, M., Ramos-Morales, F.R., Castro-Luna, A. et al. Synergy of the Tropical Earthworm Pontoscolex corethrurus and Oil Palm Bagasse in the Removal of Heavy Crude Oil. Bull Environ Contam Toxicol 108, 956–962 (2022). https://doi.org/10.1007/s00128-022-03475-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-022-03475-w