Abstract
The exploitation of coal is an important resource to generate energy worldwide. However, during the processes of coal extraction, transport, and cargo, dust particles are released into the environment. The aim of this study was to determine the toxicological effects of bituminous coal dust (<38 µm), obtained from a sample collected in a coal mine in Colombia, on the annelid Eisenia fetida. The earthworm culture was standardized under laboratory conditions to evaluate mortality, as well as morphological, physiological and histological changes using concentrations varying from 1 to 4% w/w coal dust in artificial soil, after 7, 14, and 28 days of exposure. In addition, an avoidance assay was carried out after 48-h treatment. Histopathological analysis was performed at the end of the experiment. After the sub-chronic exposure, an increase in mortality was observed at the highest coal dust concentration compared to the untreated group. Alterations in morphology and physiology of the exposed annelids were mostly evidenced at the greatest tested concentrations (3–4%) and exposure times (≥14 days). Changes included loss of weight and color, abundant mucus production, constriction, peeling of the epidermis, clitellum involution, violent movements and lethargy. Avoidance of coal dust-polluted soil followed a concentration-response relationship. Histopathological findings revealed changes on the cuticle, as well as in the circular and longitudinal muscle layers in animals living in soils containing 3 and 4% coal particles. In short, E. fetida exposed to coal dust experienced several pathological changes, suggesting that this pollutant may induce population problems in macroinvertebrates present in coal mining areas.
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Adeel M, Ma C, Ullah S, Rizwan M, Hao Y, Chen C, Jilani G, Shakoor N, Li M, Wang L (2019) Exposure to nickel oxide nanoparticles insinuates physiological, ultrastructural and oxidative damage: a life cycle study on Eisenia fetida. Environ Pollut 254:113032. https://doi.org/10.1016/j.envpol.2019.113032
Alcala-Orozco M, Caballero-Gallardo K, Olivero-Verbel J (2020) Intergenerational effects of coal dust on Tribolium castaneum, Herbst. Environ Res 182:109055. https://doi.org/10.1016/j.envres.2019.109055
Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, Zafar A (2016) In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pak J Pharm Sci 29(3):969–977
ASTM (2008) Standard specification for wire cloth and sieves for testing purposes. Designation: E 11–04, Copyright International, ASTM, West Conshohocken, PA. ftp://ftp.ecn.purdue.edu/olek/PTanikela/To%20Prof.%20Olek/ASTM%20standards/Sieve%20sizes%20ASTM%20E%2011.pdf
Avila-Arias H, Nies LF, Gray MB, Turco RF (2019) Impacts of molybdenum-, nickel, and lithium-oxide nanomaterials on soil activity and microbial community structure. Sci Total Environ 652:202–211. https://doi.org/10.1016/j.scitotenv.2018.10.189
Babić S, Barišić J, Bielen A, Bošnjak I, Klobučar RS, Ujević I, Strunjak-Perović I, Popović NT, Čož-Rakovac R (2016) Multilevel ecotoxicity assessment of environmentally relevant bisphenol A concentrations using the soil invertebrate Eisenia fetida. J Hazard Mater 318:477–486. https://doi.org/10.1016/j.jhazmat.2016.07.017
Berry KL, Hoogenboom MO, Flores F, Negri AP (2016) Simulated coal spill causes mortality and growth inhibition in tropical marine organisms. Sci Rep 6:25894
Bharti S, Banerjee TK (2011) Bioaccumulation of metals in the edible catfish Heteropneustes fossilis (Bloch) exposed to coal mine effluent generated at Northern Coalfield Limited, Singrauli, India. Bull Environ Contam Toxicol 87:393. https://doi.org/10.1007/s00128-011-0371-3
Bielská L, Hovorková I, Kuta J, Machát J, Hofman J (2017) The variability of standard artificial soils: cadmium and phenanthrene sorption measured by a batch equilibrium method. Ecotoxicol Environ Saf 135:17–23. https://doi.org/10.1016/j.ecoenv.2016.09.015
Boughattas I, Hattab S, Boussetta H, Sappin-Didier V, Viarengo A, Banni M, Sforzini S (2016) Biomarker responses of Eisenia andrei to a polymetallic gradient near a lead mining site in North Tunisia. Environ Pollut 218:530–541. https://doi.org/10.1016/j.envpol.2016.07.033
Bustos V, Mondaca P, Verdejo J, Sauvé S, Gaete H, Celis-Diez JL, Neaman A (2015) Thresholds of arsenic toxicity to Eisenia fetida in field-collected agricultural soils exposed to copper mining activities in Chile. Ecotoxicol Environ Saf 122:448–454. https://doi.org/10.1016/j.ecoenv.2015.09.009
Caballero-Gallardo K, Guerrero-Castilla A, Johnson-Restrepo B, de la Rosa J, Olivero-Verbel J (2015) Chemical and toxicological characterization of sediments along a Colombian shoreline impacted by coal export terminals. Chemosphere 138:837–846. https://doi.org/10.1016/j.chemosphere.2015.07.062
Caballero-Gallardo K, Olivero-Verbel J (2016) Mice housed on coal dust-contaminated sand: a model to evaluate the impacts of coal mining on health. Toxicol Appl Pharm 294:11–20. https://doi.org/10.1016/j.taap.2016.01.009
Caballero-Gallardo K, Wirbisky-Hershberger SE, Olivero-Verbel J, de la Rosa J, Freeman JL (2018) Embryonic exposure to an aqueous coal dust extract results in gene expression alterations associated with the development and function of connective tissue and the hematological system, immunological and inflammatory disease, and cancer in zebrafish. Metallomics 10:463–473. https://doi.org/10.1039/C7MT00300E
Delgadillo V, Verdejo J, Mondaca P, Verdugo G, Gaete H, Hodson ME, Neaman A (2017) Proposed modification to avoidance test with Eisenia fetida to assess metal toxicity in agricultural soils affected by mining activities. Ecotoxicol Environ Saf 140:230–234. https://doi.org/10.1016/j.ecoenv.2017.02.038
Demuynck S, Succiu IR, Grumiaux F, Douay F, Leprêtre A (2014) Effects of field metal-contaminated soils submitted to phytostabilisation and fly ash-aided phytostabilisation on the avoidance behaviour of the earthworm Eisenia fetida. Ecotoxicol Environ Saf 107:170–177. https://doi.org/10.1016/j.ecoenv.2014.05.011
EPA (1999) Particulate matter (PM2.5) speciation guidance, first edn. Monitoring and Quality Assurance Group, Emissions, Monitoring, and Analysis Division, Office of Air Quality Planning and Standards, Environmental Protection Agency, Research Triangle Park, NC
García-Santos G, Keller-Forrer K (2011) Avoidance behaviour of Eisenia fetida to carbofuran, chlorpyrifos, mancozeb and metamidophos in natural soils from the highlands of Colombia. Chemosphere 84(5):651–656. https://doi.org/10.1016/j.chemosphere.2011.03.036
Hajdukova Z, Pelclova D, Nakládalová M (2009) The role of exposure to coal mine dust in chronic bronchitis, COPD, and allergic airway diseases among smoking and nonsmoking miners. Chest 136(4):24S. https://doi.org/10.1378/chest.136.4_MeetingAbstracts.24S-b
Harrison JD, Morris DL, Hardcastle JD (1993) Screening for gastric carcinoma in coal miners. Gut 34(4):494–498. https://doi.org/10.1136/gut.34.4.494
Haskins DL, Hamilton MT, Jones AL, Finger Jr JW, Bringolf RB, Tuberville TD (2017) Accumulation of coal combustion residues and their immunological effects in the yellow-bellied slider (Trachemys scripta scripta). Environ Pollut 224:810–819. https://doi.org/10.1016/j.envpol.2017.01.048
He J, Hong P, Tan M, Duan C, Zhou E (2017) Trace element concentration and reduction of typical Chinese bituminous coals via dry physical separation techniques. Fuel 199:662–669. https://doi.org/10.1016/j.fuel.2017.03.036
Heredia R, Dueñas S, Castillo L, Ventura J, Briano MS, del Rio FP, Rodríguez M (2008) Autofluorescence as a tool to study mucus secretion in Eisenia foetida. Comp Biochem Physiol A Mol Integr Physiol 151:407–414. https://doi.org/10.1016/j.cbpa.2007.01.726
Hirano T, Tamae K (2011) Earthworms and soil pollutants. Sensors 11(12):11157–11167. https://doi.org/10.3390/s111211157
Ishtiaq M, Jehan N, Khan SA, Muhammad S, Saddique U, Iftikhar B (2018) Potential harmful elements in coal dust and human health risk assessment near the mining areas in Cherat, Pakistan. Environ Sci Pollut Res 25:14666–14673. https://doi.org/10.1007/s11356-018-1655-5
ISO (2006) Soil quality—avoidance test for testing the quality of soils and the of chemicals—test with earthworms (Eisenia fetida). International Standard Organization Guideline No. 17512-1, Geneve, Switzerland
ISO (2012) ISO 11268-2, ICS 13.080.30. In: Biological properties of soil quality—effects of pollutants on earthworms—Part 2: determination of effects on reproduction of Eisenia fetida/Eisenia Andrei, first edn. http://www.iso.org/standard/53528.html
Iturbe-Requena SL, Prado-Ochoa MG, Muñoz-Guzmán MA, Velázquez-Sánchez AM, Ángeles E, Alba-Hurtado F (2019) Toxic effects of new ethyl-carbamates on the morphology, mortality and acetylcholinesterase activity of Eisenia foetida. Ecotoxicol Environ Saf 176:219–225. https://doi.org/10.1016/j.ecoenv.2019.03.094
Jabłońska M, Kramarczyk M, Smieja-Król B, Janeczek J (2016) Barium concentration in cast roe deer antlers related to air pollution caused by burning of barium-enriched coals in southern Poland. Environ Sci Pollut Res 23(6):5978–5982. https://doi.org/10.1007/s11356-016-6154-y
Karr LL, Drewes CD, Coats JR (1990) Toxic effects of d-limonene in the earthworm Eisenia fetida (Savigny). Pestic Biochem Physiol 36(2):175–186. https://doi.org/10.1016/0048-3575(90)90009-Q
Landen DD, Wassell JT, McWilliams L, Patel A (2011) Coal dust exposure and mortality from ischemic heart disease among a cohort of US coal miners. Am J Ind Med 54:727–733. https://doi.org/10.1002/ajim.20986
Lebedev S, Yausheva E, Galaktionova L, Sizova E (2015) Impact of Zn nanoparticles on growth, survival and activity of antioxidant enzymes in Eisenia Fetida. Math Models Methods Appl Sci 9:34. https://doi.org/10.5539/mas.v9n10p34
Lee BT, Lee SW, Kim KR, Kim KW (2013) Bioaccumulation and the soil factors affecting the uptake of arsenic in earthworm, Eisenia fetida. Environ Sci Pollut Res 20:8326–8333. https://doi.org/10.1007/s11356-013-2087-x
Lourenço J, Silva A, Carvalho F, Oliveira J, Malta M, Mendo S, Gonçalves F, Pereira R (2011) Histopathological changes in the earthworm Eisenia andrei associated with the exposure to metals and radionuclides. Chemosphere 85:1630–1634. https://doi.org/10.1016/j.chemosphere.2011.08.027
Mahbub KR, Krishnan K, Naidu R, Megharaj M (2017) Mercury toxicity to Eisenia fetida in three different soils. Environ Sci Pollut Res 24:1261–1269. https://doi.org/10.1007/s11356-016-7869-5
Masto R, George J, Rout T, Ram L (2017) Multi element exposure risk from soil and dust in a coal industrial area. J Geochem Explor 176:100–107. https://doi.org/10.1016/j.gexplo.2015.12.009
Moreno T, Trechera P, Querol X, Lah R, Johnson D, Wrana A, Williamson B (2019) Trace element fractionation between PM10 and PM2. 5 in coal mine dust: Implications for occupational respiratory health. Int J Coal Geol 203:52–59. https://doi.org/10.1016/j.coal.2019.01.006
Nahmani J, Rossi JP (2003) Soil macroinvertebrates as indicators of pollution by heavy metals. C R Biol 326:295–303. https://doi.org/10.1016/S1631-0691(03)00070-2
Neaman A, Huerta S, Sauvé S (2012) Effects of lime and compost on earthworm (Eisenia fetida) reproduction in copper and arsenic contaminated soils from the Puchuncaví Valley, Chile. Ecotoxicol Environ Saf 80:386–392. https://doi.org/10.1016/j.ecoenv.2012.04.013
Ochiai T, Enoki Y (1981) The molecular architecture and the subunits of earthworm (Eisenia foetida) hemoglobin. Comp Biochem Physiol B Comp Biochem 68:275–279. https://doi.org/10.1016/0305-0491(81)90098-5
Odin M, Ribeyre F, Boudou A (1995) Cadmium and methylmercury bioaccumulation by nymphs of the burrowing mayfly Hexagenia rigida from the water column and sediment. Environ Sci Pollut Res 2:145–152. https://doi.org/10.1007/BF02987527
OECD (1984) Guidelines for the testing of chemicals, draft document. OECD, p 53. https://www.oecd.org/chemicalsafety/testing/44098118.pdf
OECD (2009) Proposal for a new guideline for OECD guidelines for the testing of chemicals bioaccumulation in terrestrial oligochaetes, draft document. OECD, p 53. http://www.oecd.org/general/searchresults/?q=Eisenia%20fetida&cx=012432601748511391518:xzeadub0b0a&cof=FORID:11&ie=UTF-8.%203
Pandey B, Agrawal M, Singh S (2014) Coal mining activities change plant community structure due to air pollution and soil degradation. Ecotoxicology 23(8):1474–1483. https://doi.org/10.1007/s10646-014-1289-4
Pino MR, Val J, Mainar AM, Zuriaga E, Español C, Langa E (2015) Acute toxicological effects on the earthworm Eisenia fetida of 18 common pharmaceuticals in artificial soil. Sci Total Environ 518-519:225–237. https://doi.org/10.1016/j.scitotenv.2015.02.080
Qian Y, Cheng C, Drouillard K, Zhu Q, Feng H, He S, Fang Y, Qiao S, Kolenčíka M, Chang X (2019) Bioaccumulation and growth characteristics of Vallisneria natans (Lour.) Hara after chronic exposure to metal-contaminated sediments. Environ Sci Pollut Res 26:20510–20519. https://doi.org/10.1007/s11356-019-05347-z
Reddy NC, Rao JV (2008) Biological response of earthworm, Eisenia foetida (Savigny) to an organophosphorous pesticide, profenofos. Ecotoxicol Environ Saf 71:574–582. https://doi.org/10.1016/j.ecoenv.2008.01.003
Reinecke SA, Helling B, Reinecke AJ (2002) Lysosomal response of earthworm (Eisenia fetida) coelomocytes to the fungicide copper oxychloride and relation to life-cycle parameters. Environ Toxicol Chem 21(5):1026–1031. https://doi.org/10.1002/etc.5620210519
Rico A, Sabater C, Castillo M-Á (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Saf 127:222–229. https://doi.org/10.1016/j.ecoenv.2016.02.004
Saha T, Chakravarty AK, Chakraborty R (2016) Dynamics of regeneration process in Eisenia Fetida. NBU J Anim Sci 10:79–88. http://nbujas.org/nbu-admin/upload/Research%20Article%204-T%20Saha.pdf
Sanchez-Hernandez J (2006) Earthworm biomarkers in ecological risk assessment. In: Reviews of environmental contamination and toxicology 188. Springer, p 85–126. https://doi.org/10.1007/978-0-387-32964-2_3
Setiawan AA, Budianta D, Suheryanto S, Priadi DP (2018) Pollution due to coal mining activity and its impact on environment. Sriwij J Environ 3:1–5. https://doi.org/10.22135/sje.2018.3.1.1-5
Sforzini S, Moore MN, Boeri M, Bencivenga M, Viarengo A (2015) Effects of PAHs and dioxins on the earthworm Eisenia andrei: a multivariate approach for biomarker interpretation. Environ Pollut 196:60–71. https://doi.org/10.1016/j.envpol.2014.09.015
Shi Y, Shi Y, Zheng L (2020) Individual and cellular responses of earthworms (Eisenia fetida) to endosulfan at environmentally related concentrations. Environ Toxicol Pharm 74:103299. https://doi.org/10.1016/j.etap.2019.103299
Sivakumar S, Subbhuraam C (2005) Toxicity of chromium (III) and chromium (VI) to the earthworm Eisenia fetida. Ecotoxicol Environ Saf 62:93–98. https://doi.org/10.1016/j.ecoenv.2004.08.006
Snyder BA, Hendrix PF (2008) Current and potential roles of soil macroinvertebrates (earthworms, millipedes, and isopods) in ecological restoration. Restor Ecol 16:629–636. https://doi.org/10.1111/j.1526-100X.2008.00484.x
Spurgeon D, Hopkin S, Jones D (1994) Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia fetida (Savigny): assessing the environmental impact of point-source metal contamination in terrestrial ecosystems. Environ Pollut 84:123–130. https://doi.org/10.1016/0269-7491(94)90094-9
Sui W, Cai G, Dong Q (2007) Experimental research on critical percolation gradient of quicksand across overburden fissures due to coal mining near unconsolidated soil layers. JRMGE 26(10):2084–2091
Świątek ZM, van Gestel CA, Bednarska AJ (2017) Toxicokinetics of zinc-oxide nanoparticles and zinc ions in the earthworm Eisenia andrei. Ecotoxicol Environ Saf 143:151–158. https://doi.org/10.1016/j.ecoenv.2017.05.027
Tang H, Yan Q, Wang X, Ai X, Robin P, Matthew C, Qiu J, Li X, Li Y (2016) Earthworm (Eisenia fetida) behavioral and respiration responses to sublethal mercury concentrations in an artificial soil substrate. Appl Soil Ecol 104:48–53. https://doi.org/10.1016/j.apsoil.2015.12.008
Tang Z, Chai M, Cheng J, Jin J, Yang Y, Nie Z, Huang Q, Li Y (2017) Contamination and health risks of heavy metals in street dust from a coal-mining city in eastern China. Ecotoxicol Environ Saf 138:83–91. https://doi.org/10.1016/j.ecoenv.2016.11.003
Tuberville TD, Scott DE, Metts BS, Finger Jr JW, Hamilton MT (2016) Hepatic and renal trace element concentrations in American alligators (Alligator mississippiensis) following chronic dietary exposure to coal fly ash contaminated prey. Environ Pollut 214:680–689. https://doi.org/10.1016/j.envpol.2016.04.003
USNRC (1980) Trace element geochemistry of coal resource development related to environmental quality and health. National Academy Press, US National Research Council, Washington, DC
Venkateswara Rao J, Kavitha P (2004) Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environ Res 96:323–327. https://doi.org/10.1016/j.envres.2004.02.014
Zheng S, Song Y, Qiu X, Sun T, Ackland ML, Zhang W (2008) Annetocin and TCTP expressions in the earthworm Eisenia fetida exposed to PAHs in artificial soil. Ecotoxicol Environ Saf 71:566–573. https://doi.org/10.1016/j.ecoenv.2007.10.025
Zhiqun T, Jian Z, Junli Y, Chunzi W, Danju Z (2017) Allelopathic effects of volatile organic compounds from Eucalyptus grandis rhizosphere soil on Eisenia fetida assessed using avoidance bioassays, enzyme activity, and comet assays. Chemosphere 173:307–317. https://doi.org/10.1016/j.chemosphere.2017.01.004
Zocche JJ, Da Silva LA, Damiani AP, Mendonça RÁ, Peres PB, dos Santos CEI, Debastiani R, Dias JF, de Andrade VM, Pinho RA (2014) Heavy-metal content and oxidative damage in Hypsiboas faber: the impact of coal-mining pollutants on amphibians. Arch Environ Contam Toxicol 66:69–77. https://doi.org/10.1007/s00244-013-9949-6
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This work was supported by the National Program for Doctoral Formation (COLCIENCIAS) grants 567-2012 and 647-2014, Vice-Presidency for Research of the University of Cartagenagrant N119/2018, and Prof. Jesus de la Rosa from the University of Huelva.
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Tirado-Ballestas, I., Caballero-Gallardo, K. & Olivero-Verbel, J. Toxicological effects of bituminous coal dust on the earthworm Eisenia fetida (Oligochaeta: Lumbricidae). Ecotoxicology 29, 1422–1430 (2020). https://doi.org/10.1007/s10646-020-02263-8
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DOI: https://doi.org/10.1007/s10646-020-02263-8