Assessing the Impact of Pesticides on Earthworm Health: A Comprehensive Review

Mohamed Riad Fouad

Department of Pesticide Chemistry and Technology, Faculty of Agriculture, Alexandria University, Aflaton St., 21545, El-Shatby, Alexandria, Egypt

Abstract | This review consolidates recent global research on pesticide production, usage patterns, and their ecological impacts on earthworms, emphasizing their role as bioindicators of soil health. The main objective is to identify key pesticide groups and biomarkers associated with adverse effects on earthworm physiology and ecology, filling existing knowledge gaps in understanding mechanisms of toxicity. We introduce a conceptual framework linking pesticide classes to specific biochemical markers and ecological consequences, highlighting how certain pesticide groups (such as neonicotinoids and organophosphates) pose significant risks. Our synthesis reveals that sub-lethal effects, including enzyme activity disruptions, DNA damage, and reproductive impairments, are crucial indicators of environmental health. These findings advance current understanding by pinpointing sensitive biomarkers and emphasizing the importance of sustainable pesticide management strategies to mitigate ecological harm and protect terrestrial ecosystems.

Novelty Statement | This study presents a comprehensive synthesis of recent research on the effects of various pesticides on earthworm health, highlighting novel insights into the mechanisms of toxicity and ecological implications that have not been systematically reviewed before.

Article History

Received: August 19, 2025

Revised: October 05, 2025

Accepted: October 18, 2025

Published: December 08, 2025

Keywords

Biochemical, Earthworms, Genotoxic, Growth, Histopathological, Pesticides

Copyright 2025 by the authors. Licensee ResearchersLinks Ltd, England, UK. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Corresponding author: Mohamed R. Fouad

[email protected], [email protected]

To cite this article: Fouad, M.R., 2025. Assessing the impact of pesticides on earthworm health: A comprehensive review. Punjab Univ. J. Zool., 40(2): 209-224. https://dx.doi.org/10.17582/journal.pujz/2025/40.2.209.224

Introduction

The widespread use of synthetic pesticides has greatly increased the agricultural productivity by reducing losses resulted from presence of weeds, insects, and diseases (Wang et al., 2012; El-Aswad et al., 2019; Gowri and Thangaraj, 2020). However, this intensification has led to declining biodiversity in farm ecosystems (Lackmann et al., 2023; Fouad and Abdel-Raheem, 2024). Pesticide droplets often settle on both pests and non-target organisms, affecting a broad range of species sharing similar traits (Yatoo et al., 2022). Despite efforts to limit their spread, pesticides drift, volatilize, runoff, and penetrate soil, impacting surrounding environments (Abd-Eldaim et al., 2023; Fouad et al., 2025a, b; Mostafa et al., 2025). These pesticides (including insecticides, herbicides, fungicides, and others) target specific pests but can harm soil and environmental life at even trace levels, posing ecological and health risks (Chen et al., 2018; Velki et al., 2019; Abdelkhalek et al., 2024; El-Aswad et al., 2024a-c; Hussein et al., 2024; Ibrahim et al., 2024). Most pesticides contaminate air, water, and soil, with less than 0.1% reaching intended targets, leading to accumulation in ecosystems and entering the food chain. Recognizing soil’s vital ecological role (supporting food production, nutrient cycling, carbon storage, and biodiversity) is increasingly important. Yet, agricultural and industrial activities intensify pressure on this finite resource, especially as pesticides contaminate soil directly or via runoff (Treder et al., 2020; Fouad, 2023a-e; Shamsan et al., 2023). Earthworms, key soil inhabitants, are particularly vulnerable they absorb pesticides through skin contact and ingestion, depending on chemical adsorption and soil conditions (Fouad et al., 2023a-b; Abdul-Malik et al., 2024; El-Ossaily et al., 2024; Sebaiy et al., 2024a, b). Moving up to 6.3 tons of soil per hectare annually, earthworms process organic and mineral matter, influencing soil health profoundly (Mosleh et al., 2003a, b). Pesticides can harm earthworms by reducing cocoon production, juvenile density, and growth, and increasing mortality and tissue damage; they also induce genetic, biochemical, and physiological stress (Zhang et al., 2014a). Despite developing some defenses, earthworms remain sensitive bioindicators of soil contamination ideal for ecotoxicological assessments due to their ease of study and consistent responses (Reddy and Rao, 2008). Their burrowing and casting activities enhance soil structure, nutrient cycling, and plant growth, making them vital for sustainable agroecosystems (Lackmann et al., 2023). As key ecosystem engineers, earthworms support soil fertility and help process pollutants, with their abundance reflecting soil health and contamination levels (Tiwari et al., 2016). Consequently, they are frequently used to evaluate the ecotoxic effects of pesticides, highlighting the importance of understanding and mitigating chemical impacts on soil biodiversity (Fouad et al., 2024a-e).

Methodology

The methodology for assessing the impact of pesticides on earthworm health in a comprehensive review involves a systematic approach to gather, evaluate, and synthesize existing research. Initially, a thorough literature search is conducted across multiple scientific databases such as PubMed, Scopus, Web of Science, and Google Scholar to identify relevant studies spanning all years. Inclusion criteria are established to select peer-reviewed articles, experimental studies, field surveys, and meta-analyses that investigate various aspects of pesticide exposure and earthworm health. Data extraction involves collecting information on pesticide types, concentrations, application methods, duration of exposure, earthworm species studied, and health parameters assessed (e.g., survival rate, reproduction, behavioral changes, physiological and biochemical markers). The review critically analyzes experimental designs, methodologies, and results to identify patterns, correlations, and disparities across different studies. Additionally, the methodology may include a quality assessment of the selected studies to ensure reliability and validity. Synthesis of data involves qualitative and quantitative approaches, such as meta-analysis if applicable, to derive overarching conclusions about the effects of pesticides on earthworms. Overall, this methodology aims to provide a comprehensive understanding of how pesticides influence earthworm health over time and across various environmental contexts. While numerous reviews have addressed the general effects of pesticides on soil organisms, many lack a focused synthesis on earthworms, particularly in relation to emerging pesticide formulations and application methods. This review uniquely consolidates recent data on the sub-lethal and long-term impacts of various pesticide classes on earthworm physiology, behavior, and reproductive success, highlighting inconsistencies and gaps in current methodologies.

Pesticide production and consumption in the world

In 2022, global pesticide active ingredient use reached 3.7 million tons up 4% from 2021, 13% over the past decade, and three times more than in 1990. Compared to the 1990s, pesticide use has increased by 48% for insecticides, 54% for fungicides and bactericides, and 121% for herbicides. During this period, herbicides’ share of total pesticide use grew from 40–50%, while insecticides decreased from 26% to 22%, and fungicides and bactericides from 25% to 22% (see Figure 1). In 2022, pesticide exports totaled approximately 6.9 million tonnes (down 1% from 2021) but their value rose by 13% to USD 48.8 billion. Between 2013 and 2022, exports increased by 50%, and their value grew by 53%. The top five pesticide-consuming countries, from most to least, are China, the United States, Argentina, Thailand, and Brazil (FAO, 2024; Yatoo et al., 2022).

 

Ecological classification of earthworms

Over 7,000 earthworm species have been described globally, spread among 23 families and 700 genera. There are three categories into which earthworms fall depends on the area of soil that earthworms live in, as well as their feeding and burrowing habits. Lumbricus castaneus is an example of an epigeic species, which live and feed on soil surface. Anecic earthworms, such as Lumbricus terrestris, may emerge from their permanent vertical burrows in soil to feed onto surface litter. Endogeic species, such as Allolobophora chlorotica, feed on soil and dwell in transient horizontal burrows (Eisenhauer and Eisenhauer, 2020). Each category uniquely supports ecosystem services, with epigeic focusing on surface processes, anecic on vertical mixing and aeration, and endogeic on subsurface soil health. Together, they play vital roles in maintaining soil fertility and ecosystem productivity.

LC50 of pesticides on earthworms

Eisenia fetida

Tables 1 and 2, the LC50 values of different pesticides on Eisenia foetida are shown using filter paper contact technique and soil mixing technique. E. fetida exposed to atrazine (0.1–5 µg/cm²) had a mean 96-h LC50 of 2.9 µg/cm². For cyanazine (0.5–10 µg/cm²), the LC50 was 4.9 µg/cm², and for chlorpyrifos (1–15 µg/cm²), it was slightly higher at 8.3 µg/cm² (Lydy and Linck, 2003). LC50 value of chlorpyrifos was 0.047 and 0.037 µg/cm2 at 24 and 48 hours by Rao et al. (2003). The LC50 of azodrin was 0.46 µg/cm² via paper contact after 48 hours, and 132 mg/kg in artificial soil after 14-d (Rao and Kavitha, 2004). Lindane was more toxic than deltamethrin to E. fetida over 14-d, with LC50 values of 162.1 mg/kg and 432.9 mg/kg soil, respectively (Shi et al., 2007). The LC50 values for benomyl, carbendazim and lambda-cyhalthrin were 633, >1000, and 23.9 mg/kg into tropical artificial soil, 22, 5.8, and 99.8 mg/kg into artificial soil, 14.6, 4.1, and 139.9 mg/kg into loamy sand soil, respectively (Garcia et al., 2008). The LC50 values for profenofhos were 4.56 and 3.55 µg/cm2 after 24 and 48 hours, respectively (Reddy and Rao, 2008). Wang et al. (2012) found that insect growth regulators were moderately toxic to worms (LC50: 117.6–564.6 µg/cm² at 48 hours), pyrethroids were highly toxic (LC50: 10.55–25.7 µg/cm²), and neonicotinoids were extremely toxic (LC50: 0.0088–0.45 µg/cm²). Using an artificial soil bioassay, neonicotinoids exhibited greater acute toxicity than antibiotics, carbamates, insect growth regulators, organophosphates, and pyrethroids, which were the least hazardous. Terbuthylazine herbicide was the most ecologically harmful to E. fetida, followed by galition (fenitrothion and malathion) insecticides, and metaldehyde limacid (Jovana et al., 2014). The 96-h acute toxicity test in natural soil showed that carbendazim was more toxic than captan (Mandal et al., 2015). The LC50 of acetamiprid, imidacloprid, nitenpyram, thiacloprid and clothianidin was 2.69, 3.05, 4.34, 2.68 and 0.93 mg/kg artificial soil, respectively (Wang et al., 2015a, b). It was found that carbendazim is highly toxic to E. fetida, with a 14-day LC50 of 2 mg/kg. Dimethoate shows moderate toxicity (LC50 of 28 mg/kg), whereas trichlorfon, tebuconazole, and prochloraz exhibit relatively low toxicity (Rico et al., 2016). According to Chen et al. (2018), tribenuron-methyl exhibited low toxicity to E. fetida in studies using contact filter paper and artificial soil. Isoprocarb increased mortality in a dose-dependent manner, with LC50 values of 8.2 μg/cm² (48-h) on filter paper and 3.37 mg/kg (14-d) in soil (Gu et al., 2021). In the artificial soil, the 14-day LC50 value of flupyradifurone was 157.6502 mg/kg for juvenile E. fetida and 186.9773 mg/kg to adult E. fetida (Qiao et al., 2022). Acetamiprid was 167.9-times more toxic for E. fetida than tetraconazo after a 7-day break. Likewise, acetamiprid’s toxicity was 142.2 times greater than tetraconazo’s over a 14-d interval (An et al., 2025).

 

Table 1: LC50 of pesticides to Eisenia foetida by filter paper contact (µg/cm2) technique.

Pesticide	Time (h)	LC50	Ref.
Chlorpyrifos, Atrazine, Cyanazine	96	8.3, 2.9, 4.9	Lydy and Linck, 2003
Chlorpyrifos	24 and 48	0.047 and 0.037	Rao et al., 2003
Azodrin	48	0.46	Rao and Kavitha, 2004
Profenofos	24 and 48	4.56 and 3.55	Reddy and Rao, 2008
Acetamiprid, Clothianidin, Imidacloprid, Nitenpyram, Thiacloprid, Abamectin, Emamectin benzoate, Ivermectin, Buprofezin, Chlorfluazuron, Hexaflumuron, Tebufenozide, Cyhalothrin, Cypermethrin, Fenpropathrin, Lambda-cyhalthrin, Carbosulfan, Isoprocarb, Metolcarb, Promecarb, Chlorpyrifos, Phoxim, Pyridaphenthion, Triazophos	48	0.0088, 0.28, 0.027, 0.22, 0.45, 23.08, 30.2, 4.40, 564.6, 536.2, 117.6, 508.1, 24.30, 10.63, 10.55, 25.7, 75.75, 3.64, 9.18, 10.58, 14.19, 54.65, 3.84, 14.21	Wang et al., 2012
Tribenuron-methyl, Tebuconazole	24 and 48	377.9 and 9.4 –135.6 and 5.7	Chen et al., 2018
Isoprocarb	24 and 48	32.04 and 8.20	Gu et al., 2021

 

Table 2: LC50 of pesticides to Eisenia foetida by soil mixing (mg/kg soil) technique.

Pesticide	Soil type	Time (d)	LC50	Ref.
Azodrin	Artificial	7 and 14	171 and 132	Rao and Kavitha, 2004
lindane, deltamethrin	Artificial	14	162.1, 432.9	Shi et al., 2007
Benomyl, Carbendazim, Lambda-cyhalthrin	Tropical artificial	2	633, >1000, 23.9	Garcia et al., 2008
	Artificial		22.0, 5.8, 99.8
	Loamy sand		14.6, 4.1, 139.9
Acetamiprid, Clothianidin, Imidacloprid, Nitenpyram, Thiacloprid, Abamectin, Emamectin benzoate, Ivermectin, Buprofezin, Chlorfluazuron, Hexaflumuron, Tebufenozide, Cyhalothrin, Cypermethrin, Fenpropathrin, Lambda-cyhalthrin, Carbosulfan, Isoprocarb, Metolcarb, Promecarb, Chlorpyrifos, Phoxim, Pyridaphenthion, Triazophos	Artificial	7 and 14	1.72 and 1.52 –7.44 and 6.06, 3.15 and 2.82, 4.42 and 3.91, 12.13 and 10.96, 31.50 and 27.86, 196.2 and 175.3, 68.11 and 56.34, 425.1 and 363.3, 406.5 and 381.8, 420.1 and 374.2, 434.8 and 386.7, 1530 and 1369, 1467 and 1272, 1532 and 1246, 1623 and 1370, 146.8 and 130.1, 69.4 and 60.8, 108.1 and 93.8, 31.23 and 28.43, 421.3 and 384.9, 1083 and 901.5, 273.3 and 243.7, 381.4 and 347.5	Wang et al., 2012
Galition, Fenitrothion+Malathion, Terbuthylazine, Metaldehyde	Artificial	14	368.25, 1.264, 3.66	Jovana et al., 2014
Carbendazim, Captan	Natural	4	5.38, 10.41	Mandal et al., 2015
Imidacloprid, Acetamiprid, Nitenpyram, Clothianidin, Thiacloprid	Artificial	14	3.05, 2.69, 4.34, 0.93, 2.68	Wang et al., 2015a, b
Trichlorfon, Dimethoate, Carbendazim, Tebuconazole, Prochloraz	Artificial	14	122, 28, 2, 180, 261	Rico et al., 2016
Tribenuron-methyl, Tebuconazole	Artificial	7 and 14	1007.3 and 746.3, 511.0 and 287.9	Chen et al., 2018
Isoprocarb	Artificial	7 and 14	6.95 and 3.37	Gu et al., 2021
Flupyradifurone	Artificial	14	186.9773 (adult) and 157.6502 (juveniles)	Qiao et al., 2022
Acetamiprid, Tetraconazo	Artificial	7 and 14	1.96 and 1.54, 329 and 219	An et al., 2025

 

Eisenia andrei

LC50 values of various pesticides against E. andrei under different exposure regimes are shown in Table 3. The LC50 values were 492-154, 23.4-13.5, and 7.10-38.9 mg/kg in artificial soil, while they were 481-106, 8.46-11.9, and 2.70-41.5 mg/kg in loamy sand soil for chlorpyrifos, carbofuran, and carbendazim at 20 and 26°C, respectively (De Silva et al., 2009). The toxicity for mixture of chlorpyrifos, and cypermethrin (LC50= 35.06) was significantly higher than either of cypermethrin (LC50 = 86.04), and chlorpyrifos (LC50 = 116) individually onto Eisenia fetida Andrei (Zhou et al., 2011). The LC50 value is 25.34 mg/kg at 14-day for organophosphate azinphos-methyl on E. Andrei (Jordaan et al., 2012). Quantified impact of imidacloprid, thiametoxam, fipronil, and captan (thiram + carboxin) on reproduction, survival, and behavior of E. andrei, with exception of imidacloprid (LC50 = 53.25 mg/kg soil), none of pesticides tested caused mortality (Alves et al., 2013). LC50 values were 102.035, 10.149, 249.804, and 558.376 mg/kg dry soil after 1-d of treatment for thiacloprid, esfenvalerate, dimethenamid-p, and prosulfocarb, respectively (Lackmann et al., 2023).

Aporrectodea caliginosa

Mosleh et al. (2003a) studied toxicity of cypermethrin, profenofos, aldicarb, atrazine, metalaxyl and chlorfluazuron to earthworms, A. caligenosa. The result was that aldicarb (LC50 = 0.68) was the most toxic to A. caligenosa in artificial soil after 28 days, followed in order by cypermethrin (LC50 = 72.96), profenofos (LC50 = 127), chlorfluazuron (LC50 = 139.9), atrazine (LC50 = 381.2), and metalaxyl (LC50 = 518) (Table 4). The LC50 value of acetamiprid was 0.199 and 0.009 after 5 and 10 day for A. caliginosa in alluvial soil (Abdel-Raheem et al., 2023). The LC50 values were (334.27 and 55.45 mg/kg) into clay soil, and (415.9 and 25 mg/kg) into sandy clay loam soil for fenitrothion after 5 and 10 days of exposure. LC50 values were (0.93 and 0.41 mg/kg) into clay soil, and (55.28 and 10.65 mg/kg) into sandy clay loam soil after 5 and 10 day of exposure for thiobencarb (El-Aswad et al., 2023a-b). Atrazine had higher intrinsic toxicity than metribuzin to earthworms (A. caligenosa), with LC50 of 1.693 and 0.026 μg/cm2 after 48 and 72 hours by filter paper contact test. LC50 was reduced from 11.121 to 3.118 and 164.824 to 19.113 mg/kg into clay soil, from 32.221 to 17.33 and 324.141 to 41.028 mg/kg into clay soil: Sandy clay loam soil (1:1), and from 41.234 to 30.804 and 462.255 to 70.902 mg/kg into sandy clay loam soil of atrazine, and metribuzin after 5 and 10 days (Fouad et al., 2023b).

 

Table 3: LC50 of pesticides to Eisenia andrei, in different exposure techniques.

Pesticides	Exposure method	Time (d)	LC50	Ref.
Chlorpyrifos, Carbofuran, Carbendazim	In artificial soil (mg/kg dry soil) at 20 and 26 °C	28	492 and 154, 23.4 and 13.5, 7.10 and 38.9	De Silva et al., 2009
	In loamy sand soil (mg/kg dry soil) at 20 and 26 °C		481 and 106, 8.46 and 11.9, 2.70 and 41.5
Cypermethrin, Chlorpyrifos, Cypermethrin+Chlorpyrifos	In artificial soil (mg/kg dry soil)	14	86.04, 116.00, 35.06	Zhou et al., 2011
Azinphos-methyl	In artificial soil (mg/kg dry soil)	14	25.34	Jordaan et al., 2012
Imidacloprid, Thiametoxam, Fipronil, Carboxin+Thiram	In artificial soil (mg/kg dry soil)	14	25.53, >1000, >1000, >1000	Alves et al., 2013
Difenoconazole+Fludioxonil, Fluopyram+Tebuconazole, Pyrimethanil, Thiram+Carboxin, Flutriafol+Thiabendazole, Fluroxypyr-meptyl, Thiamethoxam	On filter paper (µg/cm2)	1, 2 and 3	1.4, 0.6 and 0.3, 5.9, 2.9 and 1.0, 40.9, 6.5 and 2.7, 31.8, 8.2 and 1.1, 74.3, 16.2 and1.2, 19.7, 17.3 and 14.1, 724.0, 110.3 and 19.2	Velki et al., 2019
Thiacloprid, Esfenvalerate, Dimethenamid-p, Prosulfocarb	In artificial soil (mg/kg dry soil)	2	102.035, 10.149, 249.804, 558.376	Lackmann et al., 2023

 

Lumbricus terrestris

L. terrestris were exposed for commercial formulations of aldicarb and endosulfan at 2, 7, 15 days, with LC50 were 12.29, 5.82 and 3.36 mg/kg for endosulfan, 3.09, 1.51 and 1.5 mg/kg for aldicarb (Mosleh et al., 2003b). The LC50 value was 26.804 and 7.001 mg/kg on earthworms in sandy loam soil after 21 and 42 days of glyphosate exposure (Table 4) (Stellin et al., 2018).

Effect of pesticides on enzyme activities in earthworms

Acetylcholinesterase

Carbamate and organophosphorus pesticides primarily inhibit acetylcholinesterase (AChE). Using a standardized paper contact method, E. fetida shows a time-dependent decrease in AChE activity when exposed to azodrin and chlorpyrifos (Tiwari et al., 2016). As chlorpyrifos and imidacloprid concentrations increased, AChE activity in E. foetida was progressively suppressed (Teng et al., 2022). Azodrine also decreased AChE activity in a concentration-dependent manner (Rao and Kavitha, 2004). Diazinon reduced AChE activity in E. fetida body wall and gut (Zawisza-Raszka and Dolezych, 2013), with the lowest activity observed at 120 ng/cm² of temephos after 1 and 2 hours (Hackenberger et al., 2008). Methiocarb significantly decreased AChE activity (Tiwari et al., 2016), while ethyl-4-chlorophenyl, ethyl-4-bromophenyl carbamates, and propoxur caused weak inhibition (Iturbe-Requena et al., 2019). Isoprocarb also decreased AChE activity (Gu et al., 2021), and compounds like carbendazim, trichlorfon, dimethoate, prochloraz, and tebuconazole significantly inhibited AChE in artificial soil (Rico et al., 2016). Exposure to imidacloprid over 3 to 21 days reduced AChE activity in E. fetida by up to 46.7%, with inhibition rates of 28.9–46.7% (Wang et al., 2015b). Flupyradifurone at 25 and 50 mg/kg maintained AChE inhibition over 28 days (Qiao et al., 2022). Conversely, atrazine exposure increased AChE activity in E. fetida (Lammertyn et al., 2021). In E. andrei, carbaryl primarily inhibits AChE competitively (Gambi et al., 2007). Organophosphates like diazinon and chlorpyrifos suppressed AChE by 72–87% within a day and remained suppressed in A. caliginosa for 14-d (Booth et al., 1998). Parathion caused rapid AChE inhibition (~70%) within three days, reaching 80–90% after a week; similar patterns were observed in A. chlorotica, though at a slower pace (Rault et al., 2008). AChE activity in A. caliginosa and A. caligenosa was inhibited after exposure to lambda-cyhalothrin, chlorpyrifos-ethyl, and fungicides like myclobutanil and folpet within three days (Reinecke and Reinecke, 2007; Schreck et al., 2008). L. terrestris showed significant AChE inhibition as an indirect measure of chlorpyrifos bioavailability (Martínez Morcillo et al., 2013). Conversely, Dendrobaena veneta exhibited increased AChE activity after a week of glyphosate exposure at 2.16 mg/kg soil (Hackenberger et al., 2018). Chlorpyrifos and cypermethrin suppressed AChE in Eudrilus eugeniae in a dose and region-dependent manner, while glyphosate had no significant effect on AChE activity in E. eugeniae, Libyodrilus violaceus, and Alma millsoni (Owagboriaye et al., 2020). Variations in AChE response are likely influenced by pesticide type and concentration, earthworm species, and soil properties (Yatoo et al., 2022).

Glutathione-S-transferase

When glutathione is used, glutathione-S-transferase (GST) plays a vital role in detoxifying electrophilic chemicals (Yatoo et al., 2022). Elevated GST levels can enhance defense against pesticides, making GST a potential biomarker for pollution monitoring (Tiwari et al., 2016). Studies show that earthworms exposed to chemicals like glyphosate, QYR301, aldrin, endosulfan, and lindane exhibit significantly increased GST activity (Owagboriaye et al., 2020). Similarly, GST activity in

 

Table 4: LC50 of pesticides to Aporrectodea caliginosa and Lumbricus terrestris in different exposure systems.

Earthworms	Pesticides	Exposure method	Exposure time	LC50	Ref.
A. caliginosa	Aldicarb, Cypermethrin, Profenofos, Chlorfluazuron, Atrazine, Metalaxyl	In artificial soil (mg/kg dry soil)	28 days	0.68, 72.96, 127.00, 139.90, 381.20, 518.00	Mosleh et al., 2003a
	Acetamiprid	In alluvial soil (µg/g soil)	5 and 10 days	0.199 and 0.009	Abdel-Raheem et al., 2023
	Fenitrothion, Thiobencarb	On filter paper (µg/cm2)	48 and 72 hours	83.16 and 24.67, 288.26 and 39.98	El-Aswad et al., 2023a
		In clay soil (µg/g soil)	5 and 10 days	334.27 and 55.45, 0.93 and 0.41
		In sandy clay loam soil (µg/g soil)		415.90 and 25.00, 55.28 and 10.65
	Atrazine, Metribuzin	On filter paper (µg/cm2)	24, 48 and 72 hours	43.007, 10.260 and 0.910, 65.620, 1.693 and 0.063	Fouad et al., 2023b
		In clay soil (µg/g soil)	5 and 10 days	11.121 and 3.118, 164.824 and 19.113
		In sandy clay loam soil (µg/g soil)		41.234 and 30.408, 462.255 and 70.902
		In a mixture of clay soil and sandy clay loam soil (µg/g soil)		32.221 and 17.330, 324.141 and 41.028
L. terrestris	Endosulfan, Aldicarb	In artificial soil (mg/kg dry soil)	2, 7 and 15 days	12.29, 5.82 and 3.36, 3.09, 1.51 and 1.50	Mosleh et al., 2003b
	Glyphosate	In sandy loam soil (g/m2)	21 and 42 days	26.804 and 7.001	Stellin et al., 2018

 

E. fetida rises upon exposure to compounds such as flupyradifurone, azoxystrobin, fomesafen, sulfentrazone, and pyraclostrobin (Han et al., 2014; Zhang et al., 2014b; Li et al., 2020; Qiao et al., 2022). Long-term exposure to cyflumetofen also activates GST (Shi et al., 2023). Conversely, some chemicals like cyantraniliprole initially decrease and later increase GST activity, while thifluzamide inhibits it (Qiao et al., 2019; Yao et al., 2020). Soil contamination with oxyfluorfen causes significant GST reductions in earthworms such as Allolobophora molleri, E. fetida, and L. terrestris (Tejada et al., 2016). Similarly, exposure to lambda-cyhalothrin, chlorpyrifos-ethyl, and other pesticides over 14-d suppresses GST activity in A. caliginosa nocturnus, especially at higher concentrations (Schreck et al., 2008).

Superoxide dismutase

Superoxide dismutase (SOD) is the primary antioxidant enzyme defending against reactive oxygen species. Owagboriaye et al. (2020) found that glyphosate-treated earthworms (L. violaceus, E. eugeniae, A. millsoni) exhibited significantly higher SOD activity than unexposed ones. Conversely, Liu et al. (2020) observed different SOD responses in E. fetida after trifloxystrobin exposure. Other studies reported significant variations in SOD activity in E. eugeniae and E. fetida when exposed to nitenpiram, malathion, triflumezopyrim, and sulfoxaflor (Zhang et al., 2020a-b; Jeyaprakasam et al., 2021; Wen et al., 2021; Zhang et al., 2021). Exposure to azoxystrobin, QYR30, and flupyradifurone increased SOD activity in E. fetida, indicating detoxification and oxidative stress mitigation (Qiao et al., 2022). SOD activity also rose with higher sulfentrazone levels, showing a dose-dependent effect (Li et al., 2020). A maximum dose of spirotetramat (2.5 mg/kg) significantly elevated SOD activity during exposure (Zhang et al., 2015). Conversely, atrazine and thifluzamide inhibited SOD activity, while increasing concentrations of isoprocarb reduced it (Song et al., 2009; Gu et al., 2021). Responses to cyantraniliprole varied, with initial decreases followed by increases in SOD activity (Qiao et al., 2019).

Catalase

Catalase (CAT) converts hydrogen peroxide into oxygen and water, reducing its toxicity (Yatoo et al., 2022). In E. fetida, CAT activity decreases at higher chlorpyrifos doses but remains unaffected at low levels (Zhu et al., 2020). Tebuconazole (0.5, 5, 50 mg/kg soil) showed no significant impact on CAT activity (Zhang et al., 2020a), and azoxystrobin did not increase CAT activity (Han et al., 2014). Exposure to atrazine and isoprocarb reduced CAT activity, while diazinon increased it (Gu et al., 2021; Zawisza-Raszka and Dolezych, 2013). Triflumisopyrim initially elevated CAT activity, which normalized after 28 days (Wen et al., 2021). Similarly, flupyradifurone increased CAT activity (Qiao et al., 2022). Some fungicides, like spirotetramat, pyraclostrobin, thifluzamide, and QYR301, initially activated CAT but inhibited it over time (Zhang et al., 2015; Yao et al., 2020). Cyantraniliprole caused an initial decrease followed by an increase in CAT activity (Qiao et al., 2019). During 7-21 days, sulfentrazone increased CAT activity at all concentrations, while at 7 and 28 days, there was no significant change (Li et al., 2020). In A. caligenosa nocturnus, seven days of exposure to lambda-cyhalothrin, chlorpyrifos-ethyl, folpet, fosetyl-Al, myclobutanil, and metalaxyl decreased CAT activity (Schreck et al., 2008).

Cellulase

Cellulase is a digestive enzyme involved in cellulose breakdown. Acute deltamethrin exposure decreased E. fetida cellulase activity, while lindane increased it (Shi et al., 2007). Fomesafen at 500 mg/kg for 14 days markedly inhibited cellulase activity in E. fetida (Zhang et al., 2014b), and high-dose spirotetramat also significantly reduced activity during exposure (Zhang et al., 2015). Sublethal doses of dichlorovos and endosulfan significantly inhibited cellulase activity in E. foetida (Farrukh, 2017). Exposure to imidacloprid and acetamiprid increased cellulase activity, peaking at 14 days before returning to normal. Combined chlorpyrifos with these insecticides caused initial activation after one day, with levels normalizing after seven days (Teng et al., 2022). Patnaik and Dash (1993) reported reduced cellulose activity in three earthworm species (Drawida willsi, Lampito mauritii, and Octochaetona surensis) after malathion exposure.

Effect of pesticides on histology in earthworms

Cellular and tissue damage in earthworms exposed to hazardous pesticides has been documented through histopathological studies. Imidacloprid induces dose and time dependent genotoxicity in coelomocytes of Metaphire posthuma and E. eugeniae, with midgut cells showing abnormal nuclei, reduced cytoplasm, and cellular breakdown as exposure increases (Dittbrenner et al., 2011; Kaur et al., 2023). Multiple neonicotinoids (including thiamethoxam, dinotefuran, acetamiprid, clothianidin, nitenpyram, and thiacloprid) damage midgut and epidermal tissues (Yan et al., 2021; Elango et al., 2023), with acetamiprid causing severe structural disintegration (Elango et al., 2023). Acetamiprid also induces alterations in epidermal, muscle, and vascular tissues of Aporrectodea giardi (Berrouk et al., 2021). Other pesticides, such as abamectin, cause posterior segment loss, fragmentation, and body thinning in E. andrei across all tested concentrations (Nunes et al., 2016). Lindane exposure results in vacuolation and muscle-epidermis separation, effects that intensify with higher doses of dimethoate and chlorpyrifos, leading to cellular destruction in A. caliginosa (Mukherjee and Parida, 2015; Abdel-Aziz et al., 2023; Ahmed and Yahya, 2023). Dimethoate affects neurosecretory cell morphology and urosecretory processes in Eudichogaste Kinneari (Lakhani, 2015). Profenofos treatment causes body rupture, bleeding, glandular proliferation, and muscle disintegration in E. fetida (Reddy and Rao, 2008). Exposure to triazophos and deltamethrin damages the post-clitellar region of E. eugeniae, causing tissue rupture and necrosis (Singh et al., 2019). Monocrotophos induces rupture, necrosis, and tissue fusion in earthworm body walls, while also negatively impacting intestinal histology and microbial populations in L. mauritii (Gowri and Thangaraj, 2020; Kavitha et al., 2020). High concentrations of monocrotophos and glyphosate cause lesions, skin undulation, and deformities in E. eugeniae, with glyphosate damaging intestinal tissue in Pheretima elongata (Morowati, 2000; Samal et al., 2019). Glyphosate exposure leads to cuticular degeneration, cytolysis, vacuolization, and muscle damage in Nsukkadrilus mbae (Stanley and Joy, 2014). Similarly, atrazine causes vacuolation, loss of nuclei, and tissue disorganization in N. mbae (Oluah et al., 2010). Exposure to butachlor results in vacuolation and glandular enlargement in Perionyx sansibaricus and E. fetida (Muthukaruppan et al., 2005; Gobi and Gunasekaran, 2010). Sulfentrazone damages the digestive and epidermal tissues of E. fetida after 21 days, with cellular disintegration observed (Li et al., 2020). Triazole fungicides cause destruction of epidermal cells and disorganization of muscle layers, with higher concentrations inducing cytoplasmic staining and cell death (Gao et al., 2013).

Genotoxic effects of pesticides on earthworms

E. fetida exhibits antioxidant responses to lipid peroxidation and DNA damage caused by subchronic exposure to acetamiprid and imidacloprid (Li et al., 2018). Imidacloprid at 0.1–2 mg/kg soil can induce DNA damage after 21 days, as shown by sperm deformity assessments (Wang et al., 2015b). Nitenpyram also causes notable DNA damage in E. fetida, with effects increasing dose-dependently (Zhang et al., 2021). DNA damage metrics, such as tail moment, rise with higher cyantraniliprole concentrations and longer exposure (Xue et al., 2023). Endosulfan and triflumezopyrim similarly induce DNA damage (Wen et al., 2021), while deltamethrin + triazophos and profenofos + cypermethrin show moderate genotoxicity (Bhargavi et al., 2020). Chlorpyriphos increases DNA damage and reactive oxygen species levels, leading to oxidative stress at low concentrations (Casabé et al., 2007; Zhu et al., 2020). Glyphosate formulations are cytotoxic and genotoxic both in vivo and ex vivo (Curieses et al., 2018), but glyphosate alone shows no clear DNA harm risk in Pheretima peguana (Casabé et al., 2007). Conversely, paraquat is clastogenic and aneugenic (Muangphra et al., 2014), and atrazine damages E. foetida DNA (Song et al., 2009). Sulfentrazone and QYR301 induce oxidative stress, lipid peroxidation, and DNA damage in E. fetida (Li et al., 2020). Short-term exposure to diuron (0–5 mg/kg) causes minimal oxidative stress and DNA damage (Wang et al., 2023), while chloridazon, oxadiazon, bentazone, and pendimethalin increase DNA damage and chromosomal abnormalities in Eisenia hortensis (Ulukütük and Ciğerci, 2020; Ciğerci et al., 2022). Azostrobin triggers oxidative stress and DNA damage in E. fetida (Han et al., 2014), and carbendazim and metalaxyl-M cause significant DNA damage in E. foetida coelomocytes, with effects related to dose and exposure duration (Liu et al., 2014; Huan et al., 2016).

Effects of pesticides on growth of earthworms

Although glyphosate is relatively non-toxic to Aporrectodea trapezoides, Aporrectodea rosea, A. caliginosa, and Aporrectodea longa in field studies, it has been shown to reduce A. caliginosa growth in laboratory settings, decrease cocoon viability, and lower juvenile counts in the field. It also affects reproduction and development in E. foetida (Dalby et al., 1995), leading to fewer juveniles. Similarly, glyphosate decreases cocoon viability and juvenile production in E. fetida (Casabé et al., 2007). Laboratory tests reveal that 2,4-D and glyphosate significantly impact E. foetida reproduction and development, with treated soils lacking cocoons and juveniles (Correia and Moreira, 2010). These chemicals, along with carbendazim, dimethoate, and copper oxychloride, cause dose-dependent reductions in E. fetida growth (Yasmin and D’Souza, 2010). Both glyphosate and chlorpyrifos reduce E. fetida andrei feeding activity in field and lab conditions, though low chlorpyrifos concentrations do not affect reproduction (Casabé et al., 2007). The weight of E. fetida is more sensitive than mortality to methamidophos and acetochlor exposure (Zhou et al., 2006). Increased butachlor concentrations decrease E. fetida biomass and cocoon formation (Gobi and Gunasekaran, 2010), and inhibit P. sansibaricus growth and cocoon production (Muthukaruppan et al., 2005). Lindane exposure reduces the biomass of E. eugeniae (Mukherjee and Parida, 2015). Pesticides such as chlorpyrifos, diazinon, aldicarb, profenofos, cypermethrin, chlorfluazuron, metalaxyl, and atrazine slow the growth of A. caliginosa (Booth et al., 2000; Yasmin and D’Souza, 2010), with diazinon and chlorpyrifos notably reducing growth during exposure (Booth et al., 2000). Endosulfan significantly decreases juvenile A. trapezoides weight within 35-days when applied at normal rates, while fenamiphos has similar effects only in the field. Malathion reduces E. foetida weight and sperm viability, with parathion also impairing E. andrei growth (Yasmin and D’Souza, 2010). Neonicotinoids such as imidacloprid, nitenpyram, acetamiprid, thiacloprid, and clothianidin are highly toxic to E. fetida, significantly inhibiting fecundity (Wang et al., 2015a, b), with high doses adversely affecting reproduction, growth, and physiology of M. posthuma and E. eugeniae (Kaur et al., 2023). Acetamiprid induces mortality in A. giardi proportional to dose and exposure time (Berrouk et al., 2021). Elevated abamectin levels decrease E. andrei reproductive efficiency (Nunes et al., 2016), and cyantraniliprole exposure dramatically reduces E. fetida weights, likely due to loss of proteins, fats, and glycogen (Qiao et al., 2019).

Effect of pesticides on the behavior of earthworms

These sublethal, organism-wide effects can occur even at low pesticide exposures, making behavioral changes highly sensitive and ecologically relevant (Lackmann et al., 2023). Earthworms play a crucial role in soil structure and aeration; their soil preference or avoidance can indicate soil quality issues (Pereira et al., 2010). Avoidance behavior is a well-established, sensitive indicator of soil pesticide contamination, as pesticides have been shown to influence earthworm avoidance responses. For instance, exposure to sulcotrione and penoxsulam affected avoidance in standardized soils (Marques et al., 2009), while 2.5 and 5 mg/kg esfenvalerate increased avoidance (Lackmann et al., 2023). Similarly, E. fetida and E. andrei avoided glyphosate-treated soils (Casabé et al., 2007), though low chlorpyrifos concentrations showed no effect. Elevated doses of deltamethrin + triazophos or profenofos + cypermethrin altered earthworm behavior, causing body folding and reduced activity (Bhargavi et al., 2020). Additionally, imidacloprid significantly affected burrow depth, length, and branching in Aporrectodea nocturna and Allolobophora icterica.

Conclusion

This review underscores the complex and multifaceted threats that pesticides pose to earthworm populations and, consequently, to soil health and ecosystem stability. Analysis of the existing literature reveals several consistent patterns: organophosphates and carbamates emerge as the most acutely toxic pesticide classes, exhibiting high mortality rates in earthworms at recommended agricultural doses, while certain neonicotinoids, though less immediately lethal, induce sub-lethal effects such as impaired reproduction and growth over time. Among various biomarkers, reductions in reproductive output, alterations in antioxidant enzyme activities (such as catalase and superoxide dismutase), and increased DNA damage measured via comet assays are the most sensitive indicators of pesticide-induced stress, signaling early and sustained biological impacts before mortality occurs. Pesticides can also induce significant histopathological alterations, including degeneration of the epidermis and gut epithelium, alongside genotoxic effects that compromise cellular integrity and genetic stability, potentially impairing earthworm populations and their ecological functions. To address these issues, policymakers should implement strict regulations to limit or ban the use of the most toxic pesticide classes, promote integrated pest management strategies that prioritize biological control and biopesticides, mandate regular environmental monitoring using sensitive biomarkers for early detection, and educate farmers and stakeholders about the ecological costs of pesticide overuse and sustainable soil management practices. Future research should focus on longitudinal field studies to elucidate chronic and cumulative effects, standardize biomarker protocols for cross-study comparison, investigate potential bioaccumulation and transfer of pesticides through soil food webs, and develop earthworm-based bioassays as rapid, cost-effective soil health assessment tools. By synthesizing these patterns and translating them into targeted actions and research priorities, we can better safeguard earthworm populations, preserve vital ecosystem services, and promote sustainable agricultural practices for future generations.

Declarations

Funding

Not applicable.

IRB approval

The review was approved by the Department of Chemistry and Pesticide Technology.

Ethical statement

The study is a literature review on pesticides’ effects on earthworms, involving no direct experimentation. It uses publicly available, peer-reviewed sources, properly cites all data, and adheres to ethical standards. No ethical approval was needed since it does not involve new experiments or fieldwork.

Consent for publication

The review contains no such material that may be unlawful, defamatory, or which would, if published, in any way whatsoever, violate the terms and conditions as laid down in the agreement.

Generative AI and AI-assisted technology statement

No Generative AI and AI-assisted technologies wer used in the writing process.

Conflict of interest

The author has declared no conflict of interest.

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