Skip to main content
Log in

A brief review and evaluation of earthworm biomarkers in soil pollution assessment

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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:

  1. 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.

  2. 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.

  3. 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.

  4. 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • Aronson J (2005) Biomarkers and surrogate endpoints. Br J Clin Pharmacol 59:491–494

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Calisi A, Lionetto M, Schettino T (2011) Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Sci Total Environ 409:4456–4464

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Depledge MH, Fossi MC (1994) The role of biomarkers in environmental assessment (2). Invertebrates. Ecotoxicology 3:161–172

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kolar L, Kožuh Eržen N, Hogerwerf L, van Gestel CAM (2008) Toxicity of abamectin and doramectin to soil invertebrates. Environ Pollut 151:182–189

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rozman KK, Doull J (2000) Dose and time as variables of toxicity. Toxicology 144:169–178

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vasseur P, Cossu-Leguille C (2003) Biomarkers and community indices as complementary tools for environmental safety. Environ Int 28:711–717

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

Download references

Acknowledgements

This work was financed with resources from the Project 201601D202089 supported by the Natural Science Foundation of Shanxi Province.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Congying Wang.

Additional information

Responsible editor: Philippe Garrigues

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.

Electronic supplementary material

ESM 1

(DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8784-0

Keywords

Navigation