Sublethal effect of synthetic fertilizers (urea and diammonium phosphate) on biomass accumulation and its histological perspicuity on the gut region of the earthworm, Eisenia fetida
Article Main
Abstract
Urea and Diammonium phosphate are commonly used fertilizers in almost every managed agro-ecosystem. The present study assessed the sublethal effect of synthetic fertilizers on biomass accumulation and its histological perspicuity on the gut region of the earthworm, Eisenia fetida. Earthworms, E. fetida (adult), were reared as per the recommendations of the Organization for Economic Co-operation and Development (OECD) guidelines (1984) number 207 for testing the sublethal effect of chemicals in the laboratory. The lethal concentration at which 50% of the worms were dead, i.e., (LC50) was estimated for synthetic fertilizers, urea, and diammonium phosphate by log-probit analysis. The urea LC50 was 862.126 mg/kg, while that of diammonium phosphate was 2098.69 mg/kg in artificial soil. To explore the sublethal effect of synthetic fertilizers on biomass culture (n=10), 1/2 of the LC50 of urea and diammonium phosphate was used. Significant variation in biomass culture was observed in response to the amalgamation of synthetic fertilizers. With in 15 days, in the urea amalgamated culture, the weight of earthworms (n=10), unlike the control group, decreased from 2.86±0.142 g to 2.42±0.120 g, but the weight of the earthworms decreased to 2.72±0.135g after applying DAP. To investigate histological alterations in the gut of earthworms subsequent to exposure, specimens (n=5) were aseptically excised, embedded in paraffin, and subjected to section cutting (thickness- 5µm) after staining with hematoxylin and eosin stain and then examined. Notably, Histological damage was also registered in the chloragogen cells of the gut region of Eisenia fetida (earthworm) on days 15 and 60. Thus, synthetic fertilisers affect earthworms' ability to absorb and digest nutrients and soil health too.
Article Details
Article Details
Keywords
Diammonium phosphate, Earthworm, Eisenia fetida, Gut-region Histology, Lethal concentration (LC50), Synthetic fertilizers, Urea
References
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Aouaichia, K., Grara, N., Bazri, K. E., Barbieri, E., Mamine, N., Hemmami, H., ... & Bellucci, S. (2024). Morphophysiological and histopathological effects of ammonium sulfate fertilizer on Aporrectodea trapezoides (Dugès, 1828) Earthworm. Life, 14(9), 1209. https://doi.org/10.3390/life14091209
Astaykina, A., Streletskii, R., Maslov, M., Krasnov, G. & Gorbatov, V. (2022). Effects of three pesticides on the earthworm Lumbricus terrestris gut microbiota. Frontiers in Microbiology, 13, 853535.
Bhattacharya, A. & Sahu, S. K. (2015). Toxic effect of superphosphate on soil ecosystem using earthworm Drawida willsi as test specimen. Journal of Biodiversity and Environmental Sciences (JBES). ISSN: 2220-6663 (Print), 2222-3045 (Online), 6 (4), 220-226.
Curry, J.P. (2004). Factors affecting the abundance of earthworms in soils; Edwards, C.A., Ecology, E., Eds.; CRC Press: Boca Raton, FL, USA, pp. 91–114.
Esaivani C., Vasanthi K. & Chairman K. (2017). Comparative histological studies in the gut of earthworms exposed to chemical fertilizer and organic manure. Indian Journal of Applied Research. 7(2), 641-644.
Finney, D.J. (1952). Probit analysis (2nd Ed), Journal of the Institute of Actuaries, 78 (3), 388-390.
Gowri, S. & Thangaraj, R. (2020). Studies on the toxic effects of agrochemical pesticide (Monocrotophos) on physiological and reproductive behavior of indigenous and exotic earthworm species. International Journal of Environmental Health Research, 30(2), 212-225.
Hillel, D. & Hatfield, J. L. (2005). Encyclopedia of soils in the environment (Vol. 3). Amsterdam: Elsevier.
Huang, C., Wang, W., Yue, S., Adeel, M. & Qiao, Y. (2020). Role of biochar and Eisenia fetida on metal bioavailability and biochar effects on earthworm fitness. Environmental Pollution, 263, 114586.
Huerta Lwanga, E., Mendoza Vega, J., Ku Quej, V., Chi, J. D. L. A., Sanchez del Cid, L., Chi, C., ... & Geissen, V. (2017)a. Field evidence for transfer of plastic debris along a terrestrial food chain. Scientific Reports, 7(1), 14071.https://doi.org/10.1038/s41598-017-14588-2
Humason, G. (1979). Animal Tissue Techniques. H-Freeman & Company, San Francisco.
Hussain, N., Chatterjee, S. K., Maiti, T. K., Goswami, L., Das, S., Deb, U. & Bhattacharya, S. S. (2021). Metal induced non-metallothionein protein in earthworm: a new pathway for cadmium detoxification in chloragogenous tissue. Journal of Hazardous Materials, 401, 123357. https://doi.org/10.1016/j.jhazmat.2020.123357
Jung, K.H., Kim, J.K., Kim, M.G., Noh, J.H., Eun, J.W., Bae, H.J., Chang, Y.G., Shen, Q., Park, W.S., Lee, J.Y. & Nam, S.W. (2012). Characteristic molecular signature for early detection and prediction of persistent organic pollutants in rat liver. Environ. Sci. Technol., 46, 12882–12889. https://doi.org/10.1021/es302480v.
Kamat, J., Devasagayam, T., Priyadarsini, K. & Mohan, H. (2000). Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications. Toxicology, 155, 55–61.https://doi.org/10.1016/S0300-483X(00)00277-8
Kesic, R., Elliott, J. E., Fremlin, K. M., Gauthier, L., Drouillard, K. G. & Bishop, C. A. (2021). Bishop: Continuing persistence and biomagnification of DDT and metabolites in northern temperate fruit orchard avian food chains. Environmental Toxicology and Chemistry, 40(12), 3379-3391, https://doi.org/10.1002/etc.5220
KilIç, G.A . (2011). Histopathological and biochemical alterations of the earthworm (Lumbricus terrestris) as a biomarker of soil pollution along Porsuk River Basin. (Turkey). Chemosphere., 83, 1175–1180.https://doi.org/10.1016/j.chemosphere.2010.12.091
Li, M., Ma, X., Saleem, M., Wang, X., Sun, L.,Yang, Y.& Zhang, Q. (2020). Response, histopathological change and DNA damage in earthworm (Eisenia fetida) exposed to sulfentrazone herbicide. Ecol. Indic., 115, 106465.https://doi.org/10.1016/j.ecolind.2020.106465
Li, P., Fan, J., Yang, J., Wei, Y., Deng, J., Zheng, J., ... & Liu, D. (2025). Urea Co-exposure Increases glyphosate toxicity in earthworms: Evidence from species with distinct sensitivities. Environmental Science & Technology, https://doi.org/10.1021/acs.est.5c10842
Liang XQ, Li, H, Chen, Y. X, He, MM, Tian, GM & Zhang, ZJ. (2008). Nitrogen loss through lateral seepage in near‐trench paddy fields. Journal of Environmental Quality, 37(2),712-717. https://doi.org/10.2134/jeq2007.0073
Long, W., Ansari, A. & Seecharran, D. (2017). The effect of urea on epigeic earthworm species (Eisenia fetida). Cell Biology and Development, 1(2), 46-50
Luan, L., Jiang, Y., Cheng, M., Dini-Andreote, F., Sui, Y., Xu, Q., ... & Sun, B. (2020). Organism body size structures the soil microbial and nematode community assembly at a continental and global scale. Nature Communications, 11(1), 6406.https://doi.org/10.1038/s41467-020-20271-4
Maenpaa, K. A., Kukkonen, J. V. K. & Lydy, M. J. (2002). Remediation of heavy metal-contaminated soils using phosphorus: evaluation of bioavailability using an earthworm bioassay. Archives of Environmental Contamination and Toxicology, 43, 0389-0398.
Marco, A. & Ortiz-Santaliestra, M. (2009). Pollution: impact of reactive nitrogen on amphibians (nitrogen pollution). Amphibian Biology, 8, 3145-3185.
Mekersi, N., Kadi, K., Casini, S., Addad, D., Amari, A. & Lekmine, S. (2022). Evaluation of the effects of short-term amendment with olive mill pomace on some soil properties. Soil Science Annual, 73(2), 1-6.
Miglani, R. & Bisht, S.S. (2019). World of earthworms with pesticides and insecticides. InterdiscipToxicol, 12(2),71- 82. doi:10.2478/intox-2019-0008.
Mohammed, D & Mosa, A. (2023). Effect of the balanced and nano-composite NPK fertilizer on the vitality of the earthworm Octolasionc yanieum and its effect on the histological composition of the middle of the body. Nativa, 11(2), 241-250. DOI: https://doi.org/10.31413/nativa.v11i2.15905
Molnar, L. (1992). Environmental aspects of the chloragogenous tissue of earthworms. Soil Biology and Biochemistry, 24(12), 1723-1727.https://doi.org/10.10 16/0038-0717(92)90177-Y
Morgan, A.J. (1981). A morphological and electron microprobe study of the inorganic composition of the mineralized secretory product of the calciferous gland and chloragogenous tissue of the earthworm, Lumbricus terrestris L. Cell Tissue Res, 220, 829–844.
Morgan, A.J. & Winters, C. (1982). The elemental composition of the chloragosomes of two earthworm species Lumbricus terrestris and Allolobophora longa determined by electron probe X-ray microanalysis of freeze-dried cryosection. Histochemistry, 73, 589–598.
Mosa Mohammed, A. (2024). Effect of urea fertilizer on the vitality of the earthworm Octolasion cyanieum. NTU Journal of Pure Sciences, 3(2), 9-13 https://doi.org/10.56286/ntujps.v3i2
OECD (1984). Guideline for testing of chemicals No. 207, Earthworm acute-toxicity test (Eisenia fetida/ andrei). Organization for economic co-operation and development (OECD) Chem, 1, 1–9, Paris, France .
Passi, M., Shukla. V & Deswal P. (2021). Effect of chemical and bio-fertilizers on the life table attributes of Eisenia fetida. Journal of Applied and Natural Science, 13(4), 1524- 1530.. https://doi.org/10.31018/jans.v13i4.2973
Paul, S., Goswami, L., Pegu, R., Kumar Chatterjee, S.& Sundar Bhattacharya, S. (2021). Epigenetic regulations enhance adaptability and valorization efficiency in Eisenia fetida and Eudrilus eugeniae during vermicomposting of textile sludge: Insights on repair mechanisms of metal-induced genetic damage and oxidative stress. Bioresour Technol., Feb, 345: 126493. DOI: 10.1016/j.biortech.2021.126493
Pfiffner, L. (2014). Earthworms architects of fertile soils. Their significance and recommendations for their promotion in agriculture. In technical guide on earthworms, International edition; Research Institute of Organic Agriculture: Frick, Switzerland.
Prento, P. (1979). Metals and phosphate in the chloragosomes of Lumbricus terrestris and their possible physiological significance. Cell and Tissue Research, 196(1), 123-134.
Qi, S., Wang, D., Zhu, L., Teng, M., Wang, C., Xue, X. & Wu, L. (2018). Effects of a novel neonicotinoid insecticide cycloxaprid on earthworm, Eisenia fetida. Environmental Science and Pollution Research, 25(14), 14138-14147.
Rai, N., Ashiya, P. & Rathore, D.S. (2014). Comparative study on the effect of chemical fertilizers and organic fertilizers on Eisenia fetida. International J. Innov. Res. Sci. Eng.Technol.,3 (5), 12991-12998.
Rashid, A. (2019). Comparative study of effect of chemical fertilizers or organic fertilizer on earthworm Eisenia fetida.Journal of Emerging Technologies and Innovative Research, 6(6), www.jetir.org (ISSN-2349-5162) JETIR1908300
Samal, S., Sahoo, S. & Mishra, C. S. K. (2017). Morpho-histological and enzymatic alterations in earthworms Drawida willsi and Lampito mauritii exposed to urea, phosphogypsum and paper mill sludge. Chemistry and Ecology, 33(8), 762-776. https://doi.org/10.1080/02757 540.2017.1357700
Senapati, B. K. & Dash, M.C. (1984). Functional role of earthworms in the decomposer subsystem. Tropical Ecology, 25 (2), 54-73.
Singh, J. S. & Gupta, V. K. (2018). Soil microbial biomass: A key soil driver inmanagement of ecosystem functioning. Sci. Total Environment, 634, 497–500. https://doi.org/10.1016/ 1529.
Staley, C., Breuillin-Sessoms, F., Wang, P., Kaiser, T., Venterea, R. T. & Sadowsky, M. J. (2018). Urea amendment decreases microbial diversity and selects for specific nitrifying strains in eight contrasting agricultural soils. Frontiers in Microbiology, 9, 634. https://doi.org/1 0.3389/fmicb.2018.00634
Vogel, J. & Seifert, G. (1992). Histological changes in the chloragogen tissue of the earthworm Eisenia fetida after administration of sublethal concentrations of different fluorides. J. Invert. Pathol. 60, 192–196
Wang, G., Xia, X., Yang, J., Tariq, M., Zhao, J., Zhang, M. & Zhang, W. (2020). Exploring the bioavailability of nickel in a soil system: Physiological and histopathological toxicity study to the earthworms (Eisenia fetida).J. Hazard. Mater, 383, 121169. https://doi.org/10.1016/j.jhazmat.2019.121169
Wang, J., Lv, S., Zhang, M., Chen, G., Zhu, T., Zhang, S., ... & Luo, Y. (2016). Effects of plastic film residues on occurrence of phthalates and microbial activity in soils. Chemosphere, 151, 171-177.https://doi.org/10.10 16/j.chemosphere.2016.02.076
Wang, K., Pang, S., Mu, X., Qi, S., Li, D., Cui, F. & Wang, C. (2015). Biological response of earthworm, Eisenia fetida, to five neonicotinoid insecticides. Chemosphere, 132, 120–126. https://doi.org/10.1016/j.chemos phere.2015.03.002
Winsome, T. (2005). Fauna-In Encyclopedia of Soils in the Environment. (Eds. Hillel, D.). Elseveir. pp. 539-548.
Zhang, S., Ren, S., Pei, L., Sun, Y. & Wang, F. (2022). Ecotoxicological effects of polyethylene microplastics and ZnO nanoparticles on earthworm Eisenia fetida. Applied Soil Ecology, 176, 104469. https://doi.org/10.1016/j.apsoil.2022.104469
Aouaichia, K., Grara, N., Bazri, K. E., Barbieri, E., Mamine, N., Hemmami, H., ... & Bellucci, S. (2024). Morphophysiological and histopathological effects of ammonium sulfate fertilizer on Aporrectodea trapezoides (Dugès, 1828) Earthworm. Life, 14(9), 1209. https://doi.org/10.3390/life14091209
Astaykina, A., Streletskii, R., Maslov, M., Krasnov, G. & Gorbatov, V. (2022). Effects of three pesticides on the earthworm Lumbricus terrestris gut microbiota. Frontiers in Microbiology, 13, 853535.
Bhattacharya, A. & Sahu, S. K. (2015). Toxic effect of superphosphate on soil ecosystem using earthworm Drawida willsi as test specimen. Journal of Biodiversity and Environmental Sciences (JBES). ISSN: 2220-6663 (Print), 2222-3045 (Online), 6 (4), 220-226.
Curry, J.P. (2004). Factors affecting the abundance of earthworms in soils; Edwards, C.A., Ecology, E., Eds.; CRC Press: Boca Raton, FL, USA, pp. 91–114.
Esaivani C., Vasanthi K. & Chairman K. (2017). Comparative histological studies in the gut of earthworms exposed to chemical fertilizer and organic manure. Indian Journal of Applied Research. 7(2), 641-644.
Finney, D.J. (1952). Probit analysis (2nd Ed), Journal of the Institute of Actuaries, 78 (3), 388-390.
Gowri, S. & Thangaraj, R. (2020). Studies on the toxic effects of agrochemical pesticide (Monocrotophos) on physiological and reproductive behavior of indigenous and exotic earthworm species. International Journal of Environmental Health Research, 30(2), 212-225.
Hillel, D. & Hatfield, J. L. (2005). Encyclopedia of soils in the environment (Vol. 3). Amsterdam: Elsevier.
Huang, C., Wang, W., Yue, S., Adeel, M. & Qiao, Y. (2020). Role of biochar and Eisenia fetida on metal bioavailability and biochar effects on earthworm fitness. Environmental Pollution, 263, 114586.
Huerta Lwanga, E., Mendoza Vega, J., Ku Quej, V., Chi, J. D. L. A., Sanchez del Cid, L., Chi, C., ... & Geissen, V. (2017)a. Field evidence for transfer of plastic debris along a terrestrial food chain. Scientific Reports, 7(1), 14071.https://doi.org/10.1038/s41598-017-14588-2
Humason, G. (1979). Animal Tissue Techniques. H-Freeman & Company, San Francisco.
Hussain, N., Chatterjee, S. K., Maiti, T. K., Goswami, L., Das, S., Deb, U. & Bhattacharya, S. S. (2021). Metal induced non-metallothionein protein in earthworm: a new pathway for cadmium detoxification in chloragogenous tissue. Journal of Hazardous Materials, 401, 123357. https://doi.org/10.1016/j.jhazmat.2020.123357
Jung, K.H., Kim, J.K., Kim, M.G., Noh, J.H., Eun, J.W., Bae, H.J., Chang, Y.G., Shen, Q., Park, W.S., Lee, J.Y. & Nam, S.W. (2012). Characteristic molecular signature for early detection and prediction of persistent organic pollutants in rat liver. Environ. Sci. Technol., 46, 12882–12889. https://doi.org/10.1021/es302480v.
Kamat, J., Devasagayam, T., Priyadarsini, K. & Mohan, H. (2000). Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications. Toxicology, 155, 55–61.https://doi.org/10.1016/S0300-483X(00)00277-8
Kesic, R., Elliott, J. E., Fremlin, K. M., Gauthier, L., Drouillard, K. G. & Bishop, C. A. (2021). Bishop: Continuing persistence and biomagnification of DDT and metabolites in northern temperate fruit orchard avian food chains. Environmental Toxicology and Chemistry, 40(12), 3379-3391, https://doi.org/10.1002/etc.5220
KilIç, G.A . (2011). Histopathological and biochemical alterations of the earthworm (Lumbricus terrestris) as a biomarker of soil pollution along Porsuk River Basin. (Turkey). Chemosphere., 83, 1175–1180.https://doi.org/10.1016/j.chemosphere.2010.12.091
Li, M., Ma, X., Saleem, M., Wang, X., Sun, L.,Yang, Y.& Zhang, Q. (2020). Response, histopathological change and DNA damage in earthworm (Eisenia fetida) exposed to sulfentrazone herbicide. Ecol. Indic., 115, 106465.https://doi.org/10.1016/j.ecolind.2020.106465
Li, P., Fan, J., Yang, J., Wei, Y., Deng, J., Zheng, J., ... & Liu, D. (2025). Urea Co-exposure Increases glyphosate toxicity in earthworms: Evidence from species with distinct sensitivities. Environmental Science & Technology, https://doi.org/10.1021/acs.est.5c10842
Liang XQ, Li, H, Chen, Y. X, He, MM, Tian, GM & Zhang, ZJ. (2008). Nitrogen loss through lateral seepage in near‐trench paddy fields. Journal of Environmental Quality, 37(2),712-717. https://doi.org/10.2134/jeq2007.0073
Long, W., Ansari, A. & Seecharran, D. (2017). The effect of urea on epigeic earthworm species (Eisenia fetida). Cell Biology and Development, 1(2), 46-50
Luan, L., Jiang, Y., Cheng, M., Dini-Andreote, F., Sui, Y., Xu, Q., ... & Sun, B. (2020). Organism body size structures the soil microbial and nematode community assembly at a continental and global scale. Nature Communications, 11(1), 6406.https://doi.org/10.1038/s41467-020-20271-4
Maenpaa, K. A., Kukkonen, J. V. K. & Lydy, M. J. (2002). Remediation of heavy metal-contaminated soils using phosphorus: evaluation of bioavailability using an earthworm bioassay. Archives of Environmental Contamination and Toxicology, 43, 0389-0398.
Marco, A. & Ortiz-Santaliestra, M. (2009). Pollution: impact of reactive nitrogen on amphibians (nitrogen pollution). Amphibian Biology, 8, 3145-3185.
Mekersi, N., Kadi, K., Casini, S., Addad, D., Amari, A. & Lekmine, S. (2022). Evaluation of the effects of short-term amendment with olive mill pomace on some soil properties. Soil Science Annual, 73(2), 1-6.
Miglani, R. & Bisht, S.S. (2019). World of earthworms with pesticides and insecticides. InterdiscipToxicol, 12(2),71- 82. doi:10.2478/intox-2019-0008.
Mohammed, D & Mosa, A. (2023). Effect of the balanced and nano-composite NPK fertilizer on the vitality of the earthworm Octolasionc yanieum and its effect on the histological composition of the middle of the body. Nativa, 11(2), 241-250. DOI: https://doi.org/10.31413/nativa.v11i2.15905
Molnar, L. (1992). Environmental aspects of the chloragogenous tissue of earthworms. Soil Biology and Biochemistry, 24(12), 1723-1727.https://doi.org/10.10 16/0038-0717(92)90177-Y
Morgan, A.J. (1981). A morphological and electron microprobe study of the inorganic composition of the mineralized secretory product of the calciferous gland and chloragogenous tissue of the earthworm, Lumbricus terrestris L. Cell Tissue Res, 220, 829–844.
Morgan, A.J. & Winters, C. (1982). The elemental composition of the chloragosomes of two earthworm species Lumbricus terrestris and Allolobophora longa determined by electron probe X-ray microanalysis of freeze-dried cryosection. Histochemistry, 73, 589–598.
Mosa Mohammed, A. (2024). Effect of urea fertilizer on the vitality of the earthworm Octolasion cyanieum. NTU Journal of Pure Sciences, 3(2), 9-13 https://doi.org/10.56286/ntujps.v3i2
OECD (1984). Guideline for testing of chemicals No. 207, Earthworm acute-toxicity test (Eisenia fetida/ andrei). Organization for economic co-operation and development (OECD) Chem, 1, 1–9, Paris, France .
Passi, M., Shukla. V & Deswal P. (2021). Effect of chemical and bio-fertilizers on the life table attributes of Eisenia fetida. Journal of Applied and Natural Science, 13(4), 1524- 1530.. https://doi.org/10.31018/jans.v13i4.2973
Paul, S., Goswami, L., Pegu, R., Kumar Chatterjee, S.& Sundar Bhattacharya, S. (2021). Epigenetic regulations enhance adaptability and valorization efficiency in Eisenia fetida and Eudrilus eugeniae during vermicomposting of textile sludge: Insights on repair mechanisms of metal-induced genetic damage and oxidative stress. Bioresour Technol., Feb, 345: 126493. DOI: 10.1016/j.biortech.2021.126493
Pfiffner, L. (2014). Earthworms architects of fertile soils. Their significance and recommendations for their promotion in agriculture. In technical guide on earthworms, International edition; Research Institute of Organic Agriculture: Frick, Switzerland.
Prento, P. (1979). Metals and phosphate in the chloragosomes of Lumbricus terrestris and their possible physiological significance. Cell and Tissue Research, 196(1), 123-134.
Qi, S., Wang, D., Zhu, L., Teng, M., Wang, C., Xue, X. & Wu, L. (2018). Effects of a novel neonicotinoid insecticide cycloxaprid on earthworm, Eisenia fetida. Environmental Science and Pollution Research, 25(14), 14138-14147.
Rai, N., Ashiya, P. & Rathore, D.S. (2014). Comparative study on the effect of chemical fertilizers and organic fertilizers on Eisenia fetida. International J. Innov. Res. Sci. Eng.Technol.,3 (5), 12991-12998.
Rashid, A. (2019). Comparative study of effect of chemical fertilizers or organic fertilizer on earthworm Eisenia fetida.Journal of Emerging Technologies and Innovative Research, 6(6), www.jetir.org (ISSN-2349-5162) JETIR1908300
Samal, S., Sahoo, S. & Mishra, C. S. K. (2017). Morpho-histological and enzymatic alterations in earthworms Drawida willsi and Lampito mauritii exposed to urea, phosphogypsum and paper mill sludge. Chemistry and Ecology, 33(8), 762-776. https://doi.org/10.1080/02757 540.2017.1357700
Senapati, B. K. & Dash, M.C. (1984). Functional role of earthworms in the decomposer subsystem. Tropical Ecology, 25 (2), 54-73.
Singh, J. S. & Gupta, V. K. (2018). Soil microbial biomass: A key soil driver inmanagement of ecosystem functioning. Sci. Total Environment, 634, 497–500. https://doi.org/10.1016/ 1529.
Staley, C., Breuillin-Sessoms, F., Wang, P., Kaiser, T., Venterea, R. T. & Sadowsky, M. J. (2018). Urea amendment decreases microbial diversity and selects for specific nitrifying strains in eight contrasting agricultural soils. Frontiers in Microbiology, 9, 634. https://doi.org/1 0.3389/fmicb.2018.00634
Vogel, J. & Seifert, G. (1992). Histological changes in the chloragogen tissue of the earthworm Eisenia fetida after administration of sublethal concentrations of different fluorides. J. Invert. Pathol. 60, 192–196
Wang, G., Xia, X., Yang, J., Tariq, M., Zhao, J., Zhang, M. & Zhang, W. (2020). Exploring the bioavailability of nickel in a soil system: Physiological and histopathological toxicity study to the earthworms (Eisenia fetida).J. Hazard. Mater, 383, 121169. https://doi.org/10.1016/j.jhazmat.2019.121169
Wang, J., Lv, S., Zhang, M., Chen, G., Zhu, T., Zhang, S., ... & Luo, Y. (2016). Effects of plastic film residues on occurrence of phthalates and microbial activity in soils. Chemosphere, 151, 171-177.https://doi.org/10.10 16/j.chemosphere.2016.02.076
Wang, K., Pang, S., Mu, X., Qi, S., Li, D., Cui, F. & Wang, C. (2015). Biological response of earthworm, Eisenia fetida, to five neonicotinoid insecticides. Chemosphere, 132, 120–126. https://doi.org/10.1016/j.chemos phere.2015.03.002
Winsome, T. (2005). Fauna-In Encyclopedia of Soils in the Environment. (Eds. Hillel, D.). Elseveir. pp. 539-548.
Zhang, S., Ren, S., Pei, L., Sun, Y. & Wang, F. (2022). Ecotoxicological effects of polyethylene microplastics and ZnO nanoparticles on earthworm Eisenia fetida. Applied Soil Ecology, 176, 104469. https://doi.org/10.1016/j.apsoil.2022.104469
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Sublethal effect of synthetic fertilizers (urea and diammonium phosphate) on biomass accumulation and its histological perspicuity on the gut region of the earthworm, Eisenia fetida. (2026). Journal of Applied and Natural Science, 18(1), 51-58. https://doi.org/10.31018/jans.v18i1.7018
