Skip to main content
Log in

Setal-epidermal, muscular and enzymatic anomalies induced by certain agrochemicals in the earthworm Eudrilus eugeniae (Kinberg)

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

Abstract

Eudrilus eugeniae, the vermicomposing worm, is found in considerable numbers in agricultural fields in India due to their eventual transfer through vermimanure. These worms are very often exposed to pesticides, herbicides, chemical fertilisers and other soil amendments. This paper reports the effects of variable concentrations of urea, phosphogypsum (PG), paper mill sludge (PMS) and two organophosphorus agrochemicals, monocrotophos and glyphosate, on certain morphological, histological and biochemical parameters of E. eugeniae. Results indicated setal anomalies, epidermal lesions, clitellar swelling and constriction of the body. Disintegration of connective tissue, vacuolation of dermis and significant alterations in protein, lipid peroxidation levels and activities of lactate dehydrogenase, acetylcholinesterase and catalase have also been observed in the treated worms. It is proposed that setae, connective tissue, protein and enzymes in E. eugeniae could be useful markers to evaluate toxicity due to the test chemicals.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agronika (2005) Official publication of Government of Odisha. Ind fertil dos:541–550

  • Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1):1–12

    Article  Google Scholar 

  • Augenfeld JM (1966) Lactic dehydrogenase activities in invertebrates in relation to environment and mode of gas exchange. Comp Biochem Physiol 18:983–985

    Article  CAS  Google Scholar 

  • Bangarusamy V, Karpagam S, Martin P (2014) Toxicity and histopathological effect of different organic waste on the earthworms (Eudrillus eugeniae and Eisenia fetida) under laboratory conditions. Int J Ethnomed Pharm Res 2(1):18–22

    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 

  • Bednarska AJ, Choczyński M, Laskowski R, Walczak M (2017) Combined effects of chlorpyriphos, copper and temperature on acetylcholinesterase activity and toxicokinetics of the chemicals in the earthworm Eisenia fetida. Environ Pollut 220:567–576

    Article  CAS  Google Scholar 

  • Belinato TA, Martins AJ, Lima JBP, Lima-Camara TND, Peixoto AA, Valle D (2009) Effect of the chitin synthesis inhibitor triflumuron on the development, viability and reproduction of Aedes aegypti. Mem Inst Oswaldo Cruz 104(1):43–47

    Article  CAS  Google Scholar 

  • Bhattacharya A, Sahu SK (2014) Lethal effect of urea on soil biota. A laboratory study on earthworm (Drawida willsi). J Biol Environ Sci 4(6):64–72

    Google Scholar 

  • Cabaud PG, Wróblewski F, Ruggiero V (1958) Colorimetric measurement of lactic dehydrogenase activity of body fluids. Am J Clin Pathol 30(3):234–236

    Article  CAS  Google Scholar 

  • Canbek M, Ozen A, Yerli N, Uyano M, Arslan N (2012) Histopathology of the tissue of a tubicid worm (Limnodrilus homeisteri) exposed to cadmium. Canka Univ J Sci Eng 9(1):69–73

    Google Scholar 

  • Cataldo R, Hidalgo L, Neaman A, Gaete O (2011) Use of molecular biomarkers in Eisenia foetida to assess copper toxicity in agricultural soils affected by mining activities. J Soil Sci Plant Nutr 11(3):57–70

    Google Scholar 

  • Cohen E (1993) Chitin synthesis and degradation as targets for pesticide action. Arch Insect Biochem Physiol 22(1–2):245–261

    Article  CAS  Google Scholar 

  • Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34(1):30–38

    Article  CAS  Google Scholar 

  • Correia FV, Moreira JC (2010) Effects of glyphosate and 2, 4-D on earthworm (Eisenia foetida) in laboratory tests. Bull Environ Contam Toxicol 85:264–268

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88IN191–88I9095

    Article  Google Scholar 

  • Enuneku A, Ezemonye L, Ajieh M (2014) Histopathological effects of spent oil based drilling mud and cuttings on the earthworm, Aporrectodea longa. J Sci Pract Pharm 1(1):20–24

    Google Scholar 

  • Eseigbe FJ, Doherty VF, Sogbanmu T, Otitoloju AA (2013) Histopathology alterations and lipid peroxidation as biomarkers of hydrocarbon-induced stress in the earthworm, Eudrilus eugeniae. Environ Monit Assess 185(3):2189–2196

    Article  CAS  Google Scholar 

  • Gobi M, Gunasekaran P (2009) Effect of butachlor herbicide on earthworm Eisenia fetida-its histological perspicuity. Appl Environ Soil Sci 2010:4. https://doi.org/10.1155/2010/850758

  • Govindarajan B, Vigneeswaran M, Rameshkumar G, Prabakaran V (2011) Bioaccumulation studies of heavy metal on impact towards polluted soil using earthworm Lampito mauritii and Eisenia fetida. J Ecobiotechnol 2(11):6–12

    Google Scholar 

  • Ifemeje JC, Udedi SC, Okechukwu AU et al (2015) Determination of total protein, superoxide dismutase, catalase activity and lipid peroxidation in soil macro-fauna (earthworm) from Onitsha municipal open waste dump. J Sci Res Rep 6(5):394–403

    Google Scholar 

  • Ismail S, Ahmed Y, Mosleh Y, Ahmed T (1997) The activities of some proteins and protein related enzymes of earthworms as biomarker for atrazine exposure. Toxicol Environ Chem 63:141–148

    Article  CAS  Google Scholar 

  • Kavitha V, Ramalingam R, Anandi V (2008) Effect of endosulfan on the bacterial and fungal populations in the gut of the Indian earthworm Lampito mauritii (Kinberg). J Sci Trans Environ Technov 2(2):78–81

    Google Scholar 

  • Leighton T, Marks E, Leighton F (1981) Pesticides: insecticides and fungicides are chitin synthesis inhibitors. Science 213(4510):905–907

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Calisi A, Giordano ME, Erroi E, Schettino T (2016) Biomonitoring of water and soil quality: a case study of ecotoxicological methodology application to the assessment of reclaimed agroindustrial wastewaters used for irrigation. Rend Lincei Sci Fis 27(1):105–112

    Article  Google Scholar 

  • Lourenço JI, Pereira RO, Silva AC, Morgado JM, Carvalho FP, Oliveira JM, Malta MP, Paiva AA, Mendo SA, Gonçalves FJ (2011) Genotoxic endpoints in the earthworms sub-lethal assay to evaluate natural soils contaminated by metals and radionuclides. J Haz Mat 186:788–795

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Ma T, Wu L, Zhang H, Luo Y (2016) Oxidative stress, cytotoxicity and genotoxicity in earthworm Eisenia fetida at different di-n-butyl phthalate exposure levels. PLoS One 11(3):e0151128

    Article  CAS  Google Scholar 

  • McIntyre NE, Rango J, Fagan WF, Faeth SH (2001) Ground arthropod community structure in a heterogeneous urban environment. Landsc Urban Plan 52:257–274

    Article  Google Scholar 

  • Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Ins Sci 20(2):121–138

    Article  CAS  Google Scholar 

  • Mosleh Y, Paris-Palacios S, Couderchet M, Vernet G (2003) Acute and sublethal effects of two insecticides on earthworms (Lumbricusterrestris L.) under laboratory conditions. Environ Toxicol 18:1–8

    Article  CAS  Google Scholar 

  • Mukherjee R, Parida P (2015) Effect of lindane on Eudrilus eugeniae. Ind J Appl Res 5(9):279–282 ISSN - 2249-555X

    Google Scholar 

  • Muthukaruppan G, Janardhanan S, Vijayalakshmi GS (2005) Sublethal toxicity of the herbicide butachlor on the earthworm Perionyx sansibaricus and its histological changes. J Soils Sediments 5:82–86

    Article  CAS  Google Scholar 

  • Nayak S, Mishra CSK, Guru BC, Rath M (2011) Effect of phosphogypsum amendment on soil physico-chemical properties, microbial load and enzyme activities. J Environ Biol 32:613–617

    Google Scholar 

  • Nayak S, Mishra CSK, Guru BC, Samal S (2018). Histological anomalies and alterations in enzyme activities of the earthworm Glyphidrillus tuberosus exposed to high concentrations of phosphogypsum. Environ Monit Assess 190:529. https://doi.org/10.1007/s10661-018-6933-7

    Article  CAS  Google Scholar 

  • Nunes MET, Daam MA, Espíndola ELG (2016) Survival, morphology and reproduction of Eisenia andrei (Annelida, Oligochaeta) as affected by Vertimec® 18 EC (a.i. abamectin) in tests performed under tropical conditions. Appl Soil Ecol 100(2016):18–26

    Article  Google Scholar 

  • O' Brien RD (1967) Insecticides, action and metabolism. Academic Press, New York

    Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  Google Scholar 

  • Oluah NS, Obiezue RN, Ochulor AJ, Onuoha E (2010) Toxicity and histopathological effect of atrazin herbicides on the earthworm Nsukkadrilus mbae under laboratory condition. Anim Res Int 7(3):1287–1293

    Google Scholar 

  • Oni AA, Hassan AT (2013) Acute and sub-lethal toxic effects of a contaminated dumpsite soil to the earthworm, Eisenia fetida (Savigny, 1826). J Sci Res Rep 2:544–558

    Google Scholar 

  • Patnaik HK, Dash MC (1992) Brain and muscle cholinesterase response in earthworms exposed to sublethal concentrations of an organophosphorous insecticide. J Ecotoxicol Environ Monit 2:279–282

    Google Scholar 

  • Paulina S, Hernán G, María EH (2011) Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Lat Am J Aquat Res 39(2):280–285

    Article  Google Scholar 

  • Pradhan SC, Mishra PC (1998) Inhibition and recovery kinetics of acetylcholine esterase activity in Drawidacalebi and Ocotchaetonasurensis, the tropical earthworms exposed to carbaryl insecticide. Bull Environ Contam Toxicol 60:904–908

    Article  CAS  Google Scholar 

  • Rao JV, Pavan YS, Madhavendra SS (2003) Toxic effects of chorpyriphos on morphology and acetylcholinesterase activity in the earthworm Eisenia foetida. Ecotoxicol Environ Saf 54:296–301

    Article  CAS  Google Scholar 

  • Reddy NC, Rao JV (2008) Biological response of earthworm Eisenia foetida (Savigny) to an organophosphorous pesticide, profenofos. Ecotoxicol Environ Saf 71:574–582

    Article  CAS  Google Scholar 

  • Ribeiro S, Sousa JP, Nogueira AJ et al (2001) Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotoxicol Environ Safe 49(2):131–138

    Article  CAS  Google Scholar 

  • Rico A, Sabater C, Castillo MÁ (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Saf 127:222–229

    Article  CAS  Google Scholar 

  • Samal S, Sahoo S, Mishra CSK (2017) Morpho-histological and enzymatic alterations in earthworms Drawida willsi and Lampito mauritii exposed to urea, phosphogypsum and paper mill sludge. Chem Ecol 33(8):762–776

    Article  CAS  Google Scholar 

  • Santorufo L, Van Gestel CA, Rocco A, Maisto G (2012) Soil invertebrates as bioindicators of urban soil quality. Environ Pollut 161:57–63

    Article  CAS  Google Scholar 

  • Shahzad A, Pawar SS (2017) Mortality (LC50) by standardization artificial soil test mathod for estimation of toxic effect of dieldrine and cythion on earthworm, Eisenia fetida. Int J Innov Res Adv Stud 4(3):148–152

    Google Scholar 

  • Sharma VJ, Satyanarayan S (2011) Effects of selected heavy metals on the histopathology of different tissues of earthworm Eudrilus eugeniae. Environ Monit Assess 180:257–267

    Article  CAS  Google Scholar 

  • Singh AP, Narayanan K (2015) Impact of economic growth and population on agrochemical use: evidence from post-liberalization India. Environ Dev Sustain 17(6):1509–1525

    Article  Google Scholar 

  • Stanley ON, Ochulor AJ (2014) Histopathological Effects of Glyphosate and Its Toxicity to the Earthworm Nsukkadrilus mbae. Brit Biotech J 4(2):149

  • Sivasankari B, Indumathi S, Anandharaj M (2013) A study on life cycle of earthworm Eudrilus eugeniae. Int J Res Pharm Life Sci 1:64–67

    Google Scholar 

  • Tiwari RK, Singh S, Pandey RS, Sharma B (2016) Enzymes of earthworm as indicators of pesticide pollution in soil. Adv Enzym Res 4(04):113

    CAS  Google Scholar 

  • Tripathi G, Kachhwaha N, Dabi I (2009) Impact of phorate on malate dehydrogenases, lactate dehydrogenase and proteins of epigeic, anecic and endogeic earthworms. Pestic Biochem Phys 95:100–105

    Article  CAS  Google Scholar 

  • Tripathi G, Kachhwaha N, Dabi I, Bandooni N (2011) Temperature-dependent alterations in metabolic enzymes and proteins of three ecophysiologically different species of earthworms. Braz Arch Biol Technol 54(4):769–776

    Article  CAS  Google Scholar 

  • Van Gestel CAM, Ortiz MD, Borgman E, Verweij RA (2011) The bioaccumulation of molybdenum in the earthworm Eisenia andrei: influence of soil properties and ageing. Chemosphere 82:1614–1619

    Article  CAS  Google Scholar 

  • Veltman K, Huijbregts MAJ, Vijver MG, Peijnenburg WJGM, Hobbelen PHF, Koolhaas JE, Van Gestel CAM, Van Vliet PCJ, Hendriks AJ (2007) Metal accumulation in the earthworm Lumbricus rubellus. Model predictions compared to field data. Environ Pollut 146:428–436

    Article  CAS  Google Scholar 

  • Vijaya TM, Middha SK, Usha T, Aruna HK, Bharathi R, Saini D, Govindaraj G (2012) Morphological and histological studies on the vermicomposting Indian earthworm Eudrilus eugeniae. World J Zool 7(2):165–170

    Google Scholar 

  • Youn JA (2005) Assessing soil ecotoxicity of methyl tert-butyl ether using earthworm bioassay; closed soil microcosm test for volatile organic compounds. Environ Pollut 134(2):181–186

    Article  CAS  Google Scholar 

  • Yvan C, Rault M, Costagliola G, Mazzia C (2005) Lethal and sublethal effects of imidacloprid on two earthworm species (Aporrectodea nocturna and Allolobophora icterica). Biol Fertil Soils 41(3):135–143

    Article  CAS  Google Scholar 

  • Zhang X, Lu Y, Shi Y, Chen C, Yang Z, Li Y, Feng Y (2009) Antioxidant and metabolic responses induced by cadmium and pyrene in the earthworm Eisenia fetida in two different systems: contact and soil tests. Chem Ecol 25(3):205–215

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Science and Technology Department, Government of Odisha, India for financial support.

Funding

This study was funded by Science and Technology Department, Government of Odisha, India (Grant number ST-Bio-15/2014/1191).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suryasikha Samal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 4742 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samal, S., Mishra, C.S.K. & Sahoo, S. Setal-epidermal, muscular and enzymatic anomalies induced by certain agrochemicals in the earthworm Eudrilus eugeniae (Kinberg). Environ Sci Pollut Res 26, 8039–8049 (2019). https://doi.org/10.1007/s11356-019-04204-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04204-3

Keywords

Navigation