Abstract
Earthworm biomarker response to pollutants has been widely investigated in the assessment of soil pollution. However, whether and how the earthworm biomarker-approach can be actually applied to soil pollution assessment is still a controversial issue. This review is concerned about the following points:
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1.
Despite much debate, biomarker is valuable to ecotoxicology and biomarker approach has been properly used in different fields. Earthworm biomarker might be used in different scenarios such as large-scale soil pollution survey and soil pollution risk assessment. Compared with physicochemical analysis, they can provide more comprehensive and straightforward information about soil pollution at low cost.
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2.
Although many earthworm species from different ecological categories have been tested, Eisenia fetida/andrei is commonly used. Many earthworm biomarkers have been screened from the molecular to the individual level, while only a few biomarkers, such as avoidance behavior and lysosomal membrane stability, have been focused on. Other aspects of the experimental design were critically reviewed.
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3.
More studies should focus on determining the reliability of various earthworm biomarkers in soil pollution assessment in future research. Besides, establishing a database of a basal level of each biomarker, exploring biomarker response in different region/section/part of earthworm, and other issues are also proposed.
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4.
A set of research guideline for earthworm biomarker studies was recommended, and the suitability of several earthworm biomarkers was briefly evaluated with respect to their application in soil pollution assessment.
This review will help to promote further studies and practical application of earthworm biomarker in soil pollution assessment.
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References
Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730–741
Aronson J (2005) Biomarkers and surrogate endpoints. Br J Clin Pharmacol 59:491–494
Asensio V, Rodríguez-Ruiz A, Garmendia L, Andre J, Kille P, Morgan AJ, Soto M, Marigómez I (2013) Towards an integrative soil health assessment strategy: a three tier (integrative biomarker response) approach with Eisenia fetida applied to soils subjected to chronic metal pollution. Sci Total Environ 442:344–365
Bartlett MD, Briones MJI, Neilson R, Schmidt O, Spurgeon D, Creamer RE (2010) A critical review of current methods in earthworm ecology: from individuals to populations. Eur J Soil Biol 46:67–73
Calisi A, Lionetto M, Schettino T (2011) Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Sci Total Environ 409:4456–4464
Chen SC, Fitzpatrick LC, Goven AJ, Venables BJ, Cooper EL (1991) Nitroblue tetrazolium dye reduction by earthworm (Lumbricus terrestris) coelomocytes: an enzyme assay for nonspecific immunotoxicity of xenobiotics. Environ Toxicol Chem 10:1037–1043
Chen C, Zhou Q, Liu S, Xiu Z (2011) Acute toxicity, biochemical and gene expression responses of the earthworm Eisenia fetida exposed to polycyclic musks. Chemosphere 83:1147–1154
Demuynck S, Lebel A, Grumiaux F, Pernin C, Leprêtre A, Lemière S (2016) Comparative avoidance behaviour of the earthworm Eisenia fetida towards chloride, nitrate and sulphate salts of Cd, Cu and Zn using filter paper and extruded water agar gels as exposure media. Ecotoxicol Environ Saf 129:66–74
Dendooven L, Alvarez-Bernal D, Contreras-Ramos SM (2011) Earthworms, a means to accelerate removal of hydrocarbons (PAHs) from soil? A mini-review. Pedobiologia 54(Supplement):S187–S192
Denoyelle R, Rault M, Mazzia C, Mascle O, Capowiez Y (2009) Cholinesterase activity as a biomarker of pesticide exposure in Allolobophora chlorotica earthworms living in apple orchards under different management strategies. Environ Toxicol Chem 26:2644–2649
Depledge MH, Fossi MC (1994) The role of biomarkers in environmental assessment (2). Invertebrates. Ecotoxicology 3:161–172
Dong L, Gao J, Xie X, Zhou Q (2012) DNA damage and biochemical toxicity of antibiotics in soil on the earthworm Eisenia fetida. Chemosphere 89:44–51
Du L, Li G, Liu M, Li Y, Yin S, Zhao J, Zhang X (2015) Evaluation of DNA damage and antioxidant system induced by di-n-butyl phthalates exposure in earthworms (Eisenia fetida). Ecotoxicol Environ Saf 115:75–82
Edwards CA (2004) Earthworm ecology. CRC Press
EEA (2014) Progress in Management of Contaminated Sites
FAO (2015) Status of the World’s Soil Resources (main Report)
Ferreira NG, Santos MJ, Domingues I, Calhôa CF, Monteiro M, Amorim MJ, Soares AM, Loureiro S (2010) Basal levels of enzymatic biomarkers and energy reserves in Porcellionides pruinosus. Soil Biol Biochem 42:2128–2136
Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280
Gambi N, Pasteris A, Fabbri E (2007) Acetylcholinesterase activity in the earthworm Eisenia andrei at different conditions of carbaryl exposure. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 145:678–685
Garcia M, Rombke J, de Brito MT, Scheffczyk A (2008) Effects of three pesticides on the avoidance behavior of earthworms in laboratory tests performed under temperate and tropical conditions. Environ Pollut 153:450–456
Gomes SIL, Hansen D, Scott-Fordsmand JJ, Amorim MJB (2015) Effects of silver nanoparticles to soil invertebrates: oxidative stress biomarkers in Eisenia fetida. Environ Pollut 199:49–55
Hagger JA, Jones MB, Leonard D, Owen R, Galloway TS (2006) Biomarkers and integrated environmental risk assessment: are there more questions than answers? Integr Environ Assess Manag 2:312–329
Heemsbergen D, Warne M, McLaughlin M, Kookana R (2009) The Australian methodology to derive ecological investigation levels in contaminated soils. CSIRO Land and Water Science Report 43/09
Herrick JE (2000) Soil quality: an indicator of sustainable land management? Appl Soil Ecol 15:75–83
Hu S, Zhang W, Li J, Lin K, Ji R (2016) Antioxidant and gene expression responses of Eisenia fetida following repeated exposure to BDE209 and Pb in a soil-earthworm system. Sci Total Environ 556:163–168
Irizar A, Izagirre U, de Cerio OD, Marigómez I, Soto M (2014) Zonation in the digestive tract of Eisenia fetida: implications in biomarker measurements for toxicity assessment. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 160:42–53
Irizar A, Rodríguez M, Izquierdo A, Cancio I, Marigómez I, Soto M (2015) Effects of soil organic matter content on cadmium toxicity in Eisenia fetida: implications for the use of biomarkers and standard toxicity tests. Arch Environ Contam Txicology 68:181–192
ISO (1993) Soil quality—effects of pollutants on earthworms (Eisenia fetida). Part 1: Determination of acute toxicity using artificial soil substrate. No. 11268–1. IOS, Geneva, Switzerland.
ISO (1998): Soil quality—effects of pollutants on earthworms (Eisenia fetida). Part 2: determination of effects on reproduction. No. 11268. ISO, Geneva, Switzerland.
ISO (2008): Soil quality—avoidance test for evaluation the quality of soils and the toxicity of chemicals. Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei). ISO, Geneva, Switzerland.
Jager T (1998) Mechanistic approach for estimating bioconcentration of organic chemicals in earthworms (oligochaeta). Environ Toxicol Chem 17:2080–2090
Jager T, Fleuren RH, Hogendoorn EA, De Korte G (2003) Elucidating the routes of exposure for organic chemicals in the earthworm, Eisenia andrei (oligochaeta). Environ Sci Technol 37:3399–3404
Jemec A, Drobne D, Tišler T, Sepčić K (2010) Biochemical biomarkers in environmental studies - lessons learnt from enzymes catalase, glutathione S-transferase and cholinesterase in two crustacean species. Environ Sci Pollut Res 17:571–581
Khan M, Cheema S, Tang X, Hashmi M, Shen C, Park J, Chen Y (2013) A battery of bioassays for the evaluation of phenanthrene biotoxicity in soil. Arch Environ Contam Toxicol 65:47–55
Kolar L, Kožuh Eržen N, Hogerwerf L, van Gestel CAM (2008) Toxicity of abamectin and doramectin to soil invertebrates. Environ Pollut 151:182–189
Lanno R, Wells J, Conder J, Bradham K, Basta N (2004) The bioavailability of chemicals in soil for earthworms. Ecotoxicol Environ Saf 57:39–47
Lin D, Zhou Q, Xie X, Liu Y (2010) Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida). Chemosphere 81(10):1328–1333
Li D, Hockaday WC, Masiello CA, Alvarez PJJ (2011) Earthworm avoidance of biochar can be mitigated by wetting. Soil Biol Biochem 43:1732–1737
Lionetto MG, Calisi A, Schettino T (2012) Earthworm biomarkers as tools for soil pollution assessment. INTECH Open Access Publisher
Li Y, Zhang F, Ai X, Wang X, Robin P, Cavanagh J, Matthew C, Qiu J (2015) Antioxidant and behavior responses of earthworms after introduction to a simulated vermifilter environment. Ecol Eng 81:218–227
Liu S, Zhou Q, Chen C (2012) Antioxidant enzyme activities and lipid peroxidation in earthworm Eisenia fetida exposed to 1,3,4,6,7,8-hexahydro-4,6,6,7,8,8-hexamethyl-cyclopenta-γ-2-benzopyran. Environ Toxicol 27:472–479
Lukkari T, Taavitsainen M, Soimasuo M, Oikari A, Haimi J (2004) Biomarker responses of the earthworm Aporrectodea tuberculata to copper and zinc exposure: differences between populations with and without earlier metal exposure. Environ Pollut 129:377–386
Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424
OECD (1984) Earthworm, acute toxicity tests. Guideline for testing chemicals. No. 207. OECD, Paris, France
OECD (2004) Earthowrm reproduction test. Guideline for testing chemicals. No. 222. OECD, Paris, France.
Panzarino O, Hyršl P, Dobeš P, Vojtek L, Vernile P, Bari G, Terzano R, Spagnuolo M, de Lillo E (2016) Rank-based biomarker index to assess cadmium ecotoxicity on the earthworm Eisenia andrei. Chemosphere 145:480–486
Paone JF, Phillip Waalkes T, Robinson Baker R, Shaper JH (1980) Serum UDP-galactosyl transferase as a potential biomarker for breast carcinoma. J Surg Oncol 15:59–66
Reinecke AJ, van Wyk M, Reinecke SA (2016) The influence of soil characteristics on the toxicity of oil refinery waste for the springtail Folsomiacandida (Collembola). Bull Environ Contam Toxicol 96:804–809
Rocco A, Scott-Fordsmand JJ, Maisto G, Manzo S, Salluzzo A, Jensen J (2011) Suitability of lysosomal membrane stability in Eisenia fetida as biomarker of soil copper contamination. Ecotoxicol Environ Saf 74:984–988
Rodriguez-Campos J, Dendooven L, Alvarez-Bernal D, Contreras-Ramos SM (2014) Potential of earthworms to accelerate removal of organic contaminants from soil: a review. Appl Soil Ecol 79:10–25
Rozman KK, Doull J (2000) Dose and time as variables of toxicity. Toxicology 144:169–178
Sanchez W, Porcher J-M (2009) Fish biomarkers for environmental monitoring within the water framework directive of the European Union. TrAC Trends Anal Chem 28:150–158
Sanchez-Hernandez J (2006) Earthworm biomarkers in ecological risk assessment. Rev Environ Contam Toxicol:85–126
Scott-Fordsmand JJ, Weeks JM (2000) Biomarkers in earthworms. Rev Environ Contam Toxicol 165:117–159
Shi Z, Xu L, Wang N, Zhang W, Li H, Hu F (2013) Pseudo-basal levels of and distribution of anti-oxidant enzyme biomarkers in Eisenia fetida and effect of exposure to phenanthrene. Ecotoxicol Environ Saf 95:33–38
Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biol Biochem 41(5):905–909
Spurgeon DJ, Ricketts H, Svendsen C, Morgan AJ, Kille P (2005) Hierarchical responses of soil invertebrates (earthworms) to toxic metal stress. Environ Sci Technol 39:5327–5334
Svendsen C, Spurgeon D, Hankard P, Weeks J (2004) A review of lysosomal membrane stability measured by neutral red retention: is it a workable earthworm biomarker? Ecotoxicol Environ Saf 57:20–29
USEPA (2003) Guidance for developing ecological soil screening levels, Office of Solid Waste and Emergency Response, Washington DC
Usman AR, Lee SS, Awad YM, Lim KJ, Yang JE, Ok YS (2012) Soil pollution assessment and identification of hyperaccumulating plants in chromated copper arsenate (CCA) contaminated sites, Korea. Chemosphere 87:872–878
Vasseur P, Cossu-Leguille C (2003) Biomarkers and community indices as complementary tools for environmental safety. Environ Int 28:711–717
Velki M, Hackenberger BK (2013) Biomarker responses in earthworm Eisenia andrei exposed to pirimiphos-methyl and deltamethrin using different toxicity tests. Chemosphere 90:1216–1226
Velki M, Hackenberger BK, Lončarić Ž, Hackenberger DK (2014) Application of microcosmic system for assessment of insecticide effects on biomarker responses in ecologically different earthworm species. Ecotoxicol Environ Saf 104:110–119
Wang Z, Cui Z (2016) Accumulation, biotransformation, and multi-biomarker responses after exposure to arsenic species in the earthworm Eisenia fetida. Toxicol Res 5:500–510
Wang J, Wang J, Wang G, Zhu L, Wang J (2016) DNA damage and oxidative stress induced by imidacloprid exposure in the earthworm Eisenia fetida. Chemosphere 144:510–517
Wu S, Wu E, Qiu L, Zhong W, Chen J (2011) Effects of phenanthrene on the mortality, growth, and anti-oxidant system of earthworms (Eisenia fetida) under laboratory conditions. Chemosphere 83(4):429–434
Wu S, Zhang H, Zhao S, Wang J, Li H, Chen J (2012) Biomarker responses of earthworms (Eisenia fetida) exposured to phenanthrene and pyrene both singly and combined in microcosms. Chemosphere 87:285–293
Xiao NW, Song Y, Ge F, Liu XH, Ou-Yang ZY (2006) Biomarkers responses of the earthworm Eisenia fetida to acetochlor exposure in OECD soil. Chemosphere 65:907–912
Xu D, Li C, Wen Y, Liu W (2013) Antioxidant defense system responses and DNA damage of earthworms exposed to perfluorooctane sulfonate (PFOS). Environ Pollut 174:121–127
Xue Y, Wang X, Gu X, Sun C (2009) Acute toxicity of tetrabromobisphenol A to earthworms Eisenia fetida and its effects on antioxidant defense system enzymes. Asian J Ecotoxi 4:93–100
Yang X, Song Y, Kai J, Cao X (2012) Enzymatic biomarkers of earthworms Eisenia fetida in response to individual and combined cadmium and pyrene. Ecotoxicol Environ Saf 86:162–167
Zhang W, Song Y, Sun T (2007a) Influence of phenanthrene and pyrene on cytochrome P450 and antioxidant enzymes in earthworms (Eisenia fetida). Environ Chem (Beijing) 26(2):202–206
Zhang W, Song Y, Sun T, Liu M, Ackland M, Galina B (2007b) Effects of low dosage pyrene pollution on biochemical characters of earthworm (Eisenia fetida) in soil.J Appl Ecol (China) 2007, 18(9):2097–2103
Zhang L, Hu C, Wang W, Ji F, Cui Y, Li M (2014) Acute toxicity of multi-walled carbon nanotubes, sodium pentachlorophenate, and their complex on earthworm Eisenia fetida. Ecotoxicol Environ Saf 103:29–35
Zhu S, Zhu L, Liu M, Chang C (2010) Toxicity of commercial penta-BDE and Cd in soil on anti-oxidant defensive responses of earthworms. Environ Sci Techno (China) 33:10–16
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This work was financed with resources from the Project 201601D202089 supported by the Natural Science Foundation of Shanxi Province.
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Highlights
• Despite debate, earthworm biomarkers are valuable for real soil pollution survey and assessment.
• Many earthworm biomarkers studies exist but lack comparability, preventing practical use.
• More effects should focus on the reliability of various biomarkers in real soil pollution assessment.
• The guidelines for earthworm biomarker studies and suitability of several biomarkers were discussed.
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Shi, Z., Tang, Z. & Wang, C. A brief review and evaluation of earthworm biomarkers in soil pollution assessment. Environ Sci Pollut Res 24, 13284–13294 (2017). https://doi.org/10.1007/s11356-017-8784-0
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DOI: https://doi.org/10.1007/s11356-017-8784-0