Abstract
Olive oil industry is economically important in Mediterranean countries. Disposal of olive mill waste (OMW) presents an environmental concern in those countries due to its high salinity and its high level of polyphenols. In order to reuse OMW, those properties have to change either through the filtration process and addition of adsorbents or by composting. One of the most important organisms in composting of organic wastes is earthworms. However, data on the effects of OMW on earthworms are scarce. The main aim of our study was to investigate whether OMW contaminated soil (OMW CS) causes adverse effects on molecular and organism level in epigeic earthworm Dendrobaena veneta and on microbiological activity. Changes of measured biochemical biomarkers (AChE, CAT, GST, lipids, MDA) varied depending on the quantity of added OMW CS and the exposure duration. Oxidative stress occurred after 7 days of exposure, while in most cases enzyme activity recovered after 28 days. At the highest ratio of contaminated soil (50%), reproduction was completely inhibited. The second aim was to investigate the impact of earthworms on phenol degradation and microbial activity, indicating an important role in the bioremediation of contaminated soils. Our results show that above a certain quantity an OMW CS has an adverse effect on earthworms, while the impact of earthworms on soil microbial activity was positive but transient. Yet, as the results also imply that earthworms have an impact on phenol degradation, they can be used to help remediation of OMW CS and its subsequent usage in agriculture. However, the quantity of OMW CS that can be safely added should be determined first.
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References
Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33(7–8):943–951
Asses N, Ayed L, Bouallagui H, Rejeb IB, Gargouri M, Hamdi M (2009) Use of Geotrichum candidum for olive mill wastewater treatment in submerged and static culture. Biores Technol 100(7):2182–2188. https://doi.org/10.1016/j.biortech.2008.10.048
Babić S, Malev O, Pflieger M, Lebedev AT, Mazur DM, Kužić A, ... Trebše P (2019) Toxicity evaluation of olive oil mill wastewater and its polar fraction using multiple whole-organism bioassays. Sci Total Environ 686:903–914. https://doi.org/10.1016/j.scitotenv.2019.06.046
Bi YM, Tian GL, Wang C, Feng CL, Zhang Y, Zhang LS, Sun ZJ (2016) Application of leaves to induce earthworms to reduce phenolic compounds released by decomposing plants. Eur J Soil Biol 75:31–37. https://doi.org/10.1016/j.ejsobi.2016.04.007
Box JD (1981) Investigation of the Folin-Ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17(5):511–525
Butenschoen O, Marhan S, Langel R, Scheu S (2009) Carbon and nitrogen mobilisation by earthworms of different functional groups as affected by soil sand content. Pedobiologia 52(4):263–272. https://doi.org/10.1016/j.pedobi.2008.11.001
Campani T, Caliani I, Pozzuoli C, Romi M, Fossi MC, Casini S (2017) Assessment of toxicological effects of raw and bioremediated olive mill waste in the earthworm Eisenia fetida: a biomarker approach for sustainable agriculture. Appl Soil Ecol 119:18–25. https://doi.org/10.1016/j.apsoil.2017.05.016
Chalkia C, Vavoulidou E, Koubouris G, Chatzipavlidis I, Kalaitzaki A, Perdikis D (2020) Spreading raw olive mill wastewater is compatible with the growth and the beneficial functions of the earthworm Octodrilus complanatus. Appl Soil Ecol 153:103625. https://doi.org/10.1016/j.apsoil.2020.103625
Charan AA, Charan AI, Verma OMP, Naushad SS (2015) Profiling of antioxidant enzymes in cat fish (Clarias batrachus) exposed to phenolic compounds. Asian J Bio Sci 10(1):6–14. https://doi.org/10.15740/HAS/AJBS/10.1/6-14
Chouchene A, Jeguirim M, Khiari B, Zagrouba F, Trouvé G (2010) Thermal degradation of olive solid waste: influence of particle size and oxygen concentration. Resour Conserv Recycl 54(5):271–277. https://doi.org/10.1016/j.resconrec.2009.04.010
Chtourou M, Ammar E, Nasri M, Medhioub K (2004) Isolation of a yeast, Trichosporon cutaneum, able to use low molecular weight phenolic compounds: application to olive mill waste water treatment. J Chem Technol Biotechnol 79(8):869–878. https://doi.org/10.1002/jctb.1062
Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods of oxygen radical research, p 283e284
Danellakis D, Ntaikou I, Kornaros M, Dailianis S (2011) Olive oil mill wastewater toxicity in the marine environment: alterations of stress indices in tissues of mussel Mytilus galloprovincialis. Aquat Toxicol 101:358–366. https://doi.org/10.1016/j.aquatox.2010.11.015
Davies LC, Vilhena AM, Novais JM, Martins-Dias S (2004) Olive mill wastewater characteristics: modelling and statistical analysis. Grasas Aceites 55(3):233–241. https://doi.org/10.3989/gya.2004.v55.i3.171
Djerdj T, Hackenberger DK, Hackenberger DK, Hackenberger BK (2020) Observing earthworm behavior using deep learning. Geoderma 358:113977. https://doi.org/10.1016/j.geoderma.2019.113977
Doula MK, Moreno-Ortego JL, Tinivella F, Inglezakis VJ, Sarris A, Komnitsas K (2017) Olive mill waste: recent advances for the sustainable development of olive oil industry. In: Olive Mill Waste. Academic Press, pp 29–56. https://doi.org/10.1016/B978-0-12-805314-0.00002-9
Duan W, Meng F, Cui H, Lin Y, Wang G, Wu J (2018) Ecotoxicity of phenol and cresols to aquatic organisms: a review. Ecotoxicol Environ Saf 157:441–456. https://doi.org/10.1016/j.ecoenv.2018.03.089
Ellman GL, Courtney KD, Andreas Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88e95
Frings CS, Fendley TW, Dunn RT, Queen CA (1972) Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 18(7):673–674
Gagné F (2014) Biochemical ecotoxicology: principles and methods. Elsevier
Galliou F, Markakis N, Fountoulakis MS, Nikolaidis N, Manios T (2018) Production of organic fertilizer from olive mill wastewater by combining solar greenhouse drying and composting. Waste Manage 75:305–311. https://doi.org/10.1016/j.wasman.2018.01.020
Gamba C, Piovanelli C, Papini R, Pezzarossa B, Ceccarini L, Bonari E (2005) Soil microbial characteristics and mineral nitrogen availability as affected by olive oil waste water applied to cultivated soil. Commun Soil Sci Plant Anal 36:937–950
Gambardella C, Mesarič T, Milivojević T, Sepčić K, Gallus L, Carbone S, … Faimali M (2014) Effects of selected metal oxide nanoparticles on Artemia salina larvae: evaluation of mortality and behavioural and biochemical responses. Environ Monit Assess 186(7):4249–4259
García-Carmona M, Romero-Freire A, Aragón MS, Garzón FM, Peinado FM (2017) Evaluation of remediation techniques in soils affected by residual contamination with heavy metals and arsenic. J Environ Manage 191:228–236. https://doi.org/10.1016/j.jenvman.2016.12.041
Golby S, Ceri H, Gieg LM, Chatterjee I, Marques LLR, Turner RJ (2012) Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond. FEMS Microbiol Ecol 79:240–250. https://doi.org/10.1111/j.1574-6941.2011.01212
Habig WH, Pabst MJ, Jakobi W (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130e7139
Hachicha S, Cegarra J, Sellami F, Hachicha R, Drira N, Medhioub K, Ammar E (2009) Elimination of polyphenols toxicity from olive mill wastewater sludge by its co-composting with sesame bark. J Hazard Mater 161(2–3):1131–1139. https://doi.org/10.1016/j.jhazmat.2008.04.066
Hackenberger DK, Stjepanović N, Lončarić Ž, Hackenberger BK (2018) Acute and subchronic effects of three herbicides on biomarkers and reproduction in earthworm Dendrobaena veneta. Chemosphere 208:722–730. https://doi.org/10.1016/j.chemosphere.2018.06.047
Hentati O, Oliveira V, Sena C, Bouji MSM, Wali A, Ksibi M (2016) Soil contamination with olive mill wastes negatively affects microbial communities, invertebrates and plants. Ecotoxicology 25:1500–1513. https://doi.org/10.1007/s10646-016-1700-4
Holmstrup M, Sørensen JG, Overgaard J, Bayley M, Bindesbøl AM, Slotsbo S, … Asmund G (2011) Body metal concentrations and glycogen reserves in earthworms (Dendrobaena octaedra) from contaminated and uncontaminated forest soil. Environ Pollut 159(1):190–197. https://doi.org/10.1016/j.envpol.2010.09.005
Jarboui R, Sellami F, Azri C, Gharsallah N, Ammar E (2010) Olive mill wastewater evaporation management using PCA method: case study of natural degradation in stabilization ponds (Sfax, Tunisia). J Hazard Mater 176(1–3):992–1005. https://doi.org/10.1016/j.jhazmat.2009.11.140
Kapellakis IE, Tsagarakis KP, Avramaki C, Angelakis AN (2006) Olive mill wastewater management in river basins: a case study in Greece. Agric Water Manag 82(3):354–370. https://doi.org/10.1016/j.agwat.2005.08.004
Karaouzas I, Cotou E, Albanis, Triantafyllos A, Kamarianos A, Skoulikidis, Nikolaods T, Giannakou U (2011) Bioassays and biochemical biomarkers for assessing olive mill and citrus processing wastewater toxicity. Environ Toxicol 26:669–676. https://doi.org/10.1002/tox.20606
Kavvadias V, Doula MK, Komnitsas K, Liakopoulou N (2010) Disposal of olive oil mill wastes in evaporation ponds: effects on soil properties. J Hazard Mater 182(1–3):144–155. https://doi.org/10.1016/j.jhazmat.2010.06.007
Komnitsas KA, Zaharaki D (2016) Morphology of modified biochar and its potential for phenol removal from aqueous solutions. Front Environ Sci 4:26. https://doi.org/10.3389/fenvs.2016.00026
Kurtz MP, Peikert B, Brühl C, Dag A, Zipori I, Shoqeir JH, Schaumann GE (2015) Effects of olive mill wastewater on soil microarthropods and soil chemistry in two different cultivation scenarios in Israel and Palestinian Territories. Agriculture 5(3):857–878. https://doi.org/10.3390/agriculture5030857
Lam PK, Gray JS (2001) Predicting effects of toxic chemicals in the marine environment. Mar Pollut Bull 42(3):169–173. https://doi.org/10.1016/S0025-326X(00)00178-8 https://doi.org/10.1016/j.ecoenv.2019.03.025
Lin Z, Zhen Z, Ren L, Yang J, Luo C, Zhong L, … Zhang D (2018) Effects of two ecological earthworm species on atrazine degradation performance and bacterial community structure in red soil. Chemosphere 196:467–475. https://doi.org/10.1016/j.chemosphere.2017.12.177
Lowry Oh, Nj R, Al F, Rj R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275 (PMID: 14907713)
Martins F, Gomes-Laranjo J, Amaral C, Almeida J, Peixoto F (2008) Evaluation of olive oil mill wastewaters acute toxicity: a study on the mitochondrial bioenergetics. Ecotoxicol Environ Saf 69(3):480–487. https://doi.org/10.1016/j.ecoenv.2007.05.008
Mekki A, Dhouib A, Sayadi S (2007) Polyphenols dynamics and phytotoxicity in a soil amended by olive mill wastewaters. J Environ Manage 84(2):134–140. https://doi.org/10.1016/j.jenvman.2006.05.015
Mekki A, Dhouib A, Feki F, Sayadi S (2008) Assessment of toxicity of the untreated and treated olive mill wastewaters and soil irrigated by using microbiotests. Ecotoxicol Environ Saf 69:488–495. https://doi.org/10.1016/j.ecoenv.2007.04.008
Mekki A, Aloui F, Dhouib A, Sayadi S (2012) Effects of Phanerochaete chrysosporium on biologic activity of soil amended with olive mill wastewaters. J Soil Sci Environ Manag 3:1–8. https://doi.org/10.5897/JSSEM11.092
Melgar R, Benitez E, Nogales R (2009) Bioconversion of wastes from olive oil industries by vermicomposting process using the epigeic earthworm Eisenia andrei. J Environ Sci Health B 44(5):488–495. https://doi.org/10.1080/03601230902935444
Mkhinini M, Boughattas I, Alphonse V, Livet A, Bousserrhine N, Banni M (2019) Effect of treated wastewater irrigation in East Central region of Tunisia (Monastir governorate) on the biochemical and transcriptomic response of earthworms Eisenia andrei. Sci Total Environ 647:1245–1255
Natal-da-Luz T, Lee I, Verweij RA, Morais PV, Van Velzen MJ, Sousa JP, Van Gestel CA (2012) Influence of earthworm activity on microbial communities related with the degradation of persistent pollutants. Environ Toxicol Chem 31(4):794–803. https://doi.org/10.1002/etc.1738
OECD (2004) Test no. 222: earthworm reproduction test (Eisenia fetida/Eisenia andrei), OECD Publishing, Paris. https://doi.org/10.1787/9789264070325-en
Piotrowska A, Iamarino G, Rao MA, Gianfreda L (2006) Short-term effects of olive mill waste water (OMW) on chemical and biochemical properties of a semiarid Mediterranean soil. Soil Biol Biochem 38(3):600–610
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 〈https://www.R-projec-t.org/〉
R Studio Team (2016) RStudio. Integrated Development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com
Rivier PA, Havranek I, Coutris C, Norli HR, Joner EJ (2019) Transfer of organic pollutants from sewage sludge to earthworms and barley under field conditions. Chemosphere 222:954–960. https://doi.org/10.1016/j.chemosphere.2019.02.010
Saadi I, Laor Y, Raviv M, Medina S (2007) Land spreading of olive mill wastewater: effects on soil microbial activity and potential phytotoxicity. Chemosphere 66:75–83. https://doi.org/10.1016/j.chemosphere.2006.05.019
Sáez JA, Pérez-Murcia MD, Vico A, Martínez-Gallardo MR, Andreu-Rodríguez FJ, López MJ, … Moral R (2020) Olive mill wastewater-evaporation ponds long term stored: integrated assessment of in situ bioremediation strategies based on composting and vermicomposting. J Hazard Mater 402:123481. https://doi.org/10.1016/j.jhazmat.2020.123481
Sanchez-Hernandez JC, Sáez JA, Vico A, Moreno J, Moral R (2020) Evaluating earthworms’ potential for remediating soils contaminated with olive mill waste sediments. Appl Sci 10(7):2624. https://doi.org/10.3390/app10072624
Santadino M, Coviella C, Momo F (2014) Glyphosate sublethal effects on the population dynamics of the earthworm Eisenia fetida (Savigny, 1826). Water Air Soil Pollut 225(12):1–8
Sassi AB, Boularbah A, Jaouad A, Walker G, Boussaid A (2006) A comparison of olive oil mill wastewaters (OMW) from three different processes in Morocco. Process Biochem 41(1):74–78
Schmitt CJ, Whyte JJ, Roberts AP, Annis ML, May TW, Tillitt DE (2007) Biomarkers of metals exposure in fish from lead-zinc mining areas of southeastern Missouri, USA. Ecotoxicol Environ Saf 67:31–47. https://doi.org/10.1016/j.ecoenv.2006.12.011
Singhal SS, Singh SP, Singhal P, Horne D, Singhal J, Awasthi S (2015) Antioxidant role of glutathione S-transferases: 4-hydroxynonenal, a key molecule in stress-mediated signaling. Toxicol Appl Pharmacol 289(3):361–370. https://doi.org/10.1016/j.taap.2015.10.006
Sultana T, Begum A, Akhter H (2019) Effect of pesticides on exopolysaccharide (EPS) production, antibiotic sensitivity and phosphate solubilization by rhizobial isolates from Sesbania bispinosa in Bangladesh. Afr J Agric Res 14:1845–1854. https://doi.org/10.5897/AJAR2019.14304
Suthar S (2014) Toxicity of methyl parathion on growth and reproduction of three ecologically different tropical earthworms. Int J Environ Sci Technol 11(1):191–198
Tavazzi B, Di Pierro D, Amorini AM, Fazzina G, Tuttobene M, Giardina B, Lazzarino G (2000) Energy metabolism and lipid peroxidation of human erythrocytes as a function of increased oxidative stress. Eur J Biochem 267(3):684–689. https://doi.org/10.1046/j.1432-1327.2000.01042.x
Toyota K, Kimura M (2000) Microbial community indigenous to the earthworm Eisenia foetida. Biology and Fertility of Soil 31:187–190. https://doi.org/10.1007/s003740050644
Varadarajan R, Philip B (2016) Antioxidant responses and lipid peroxidation in Mozambique tilapia (Oreochromis mossambicus) exposed to phenol and m-cresol. Indian J Fish 63(2). https://doi.org/10.21077/ijf.2016.63.2.20575-12
Vivas A, Moreno B, Garcia-Rodriguez S, Benitez E (2009) Assessing the impact of composting and vermicomposting on bacterial community size and structure, and microbial functional diversity of an olive-mill waste. Biores Technol 100(3):1319–1326. https://doi.org/10.1016/j.biortech.2008.08.014
Zhang XJ, Yang L, Zhao Q, Caen JP, He HY, Jin QH, … Shi YF (2002) Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Differ 9(8):790–800
Acknowledgements
This research was conducted in the framework of the DEFENSoil project (Diverse Effects of Environmentally Relevant Metal-based Nanoparticle and Pesticide Mixtures on Soil Fauna: A Novel Issue for Risk Assessment) financed by the Croatian Science Foundation (HrZZ) (contract number: IP-09-2014-4459). We are grateful to the members of the Subdepartment of Quantitative Ecology who supported our work.
Funding
This research was financially supported through DEFENSoil project (Diverse Effects of Environmentally Relevant Metal-based Nanoparticle and Pesticide Mixtures on Soil Fauna: A Novel Issue for Risk Assessment) financed by the Croatian Science Foundation (HrZZ) (contract number: IP-09–2014-4459).
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All authors contributed to the study conception and design. Resource acquisition, funding and visualization were performed by ST, AK and BKH. The investigation and formal analysis were performed by ST, DKH, MK, NS and GP. The first draft of the manuscript was written by ST, MK and NS, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Highlights
• Responses of biomarkers were correlated with exposure time and OMW CS ratio.
• The highest applied dose of OMW CS (50%) prevented reproduction of D. veneta.
• A change in soil microbial activity indicated a transient stimulatory effect by earthworms.
• Earthworms stimulated a degradation of phenolic compounds.
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Trigui, S., Hackenberger, D.K., Kovačević, M. et al. Effects of olive mill waste (OMW) contaminated soil on biochemical biomarkers and reproduction of Dendrobaena veneta. Environ Sci Pollut Res 29, 24956–24967 (2022). https://doi.org/10.1007/s11356-021-17593-1
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DOI: https://doi.org/10.1007/s11356-021-17593-1