Table 1 Biomarker studies using earthworms as sentinels in the assessment of environmentally
relevant soil contaminants
Earthworm
species
Type of exposure
Tested biomarkers
Ref.
Pesticides
Several agriculture
pesticides
Lumbricus
terrestris (A)
Field study. Conventional vs organic
orchard
CEs in 3 tissues of the
gastrointestinal tract
[18]
Carbamate
(Pirimor
®
) and OP
(Lorsban
®
)
insecticides
Aporrectodea
caliginosa (En)
Spiked soil for 1, 2,
3, 4 and 7 days
AChE in whole tissue
and nerve conduction
velocity (NCV) assay
in medial giant fibres
[19]
Ethyl-parathion
Allolobophora
chlorotica
(En) and
A. caliginosa
(En)
Up to 7-day soil
spiked (0.1, 1 and
10 mg kg
À1
) under
lab exposure
AChE, CE activities,
behaviour responses
(burrowing, casting,
feeding)
[20]
OP pesticides:
dimethoate and
pirimiphos-methyl
E. andrei (Ep)
Filter paper contact
test
AChE, CE activities
in whole tissue vs
coelomocyte extracts
[21]
Commercial formulations of glyphosate
(GLF), tembotrione
(TBT) and
nicosulfuron (NCS)
Dendrobaena
veneta (Ep)
Three concentrations
of each formulation
using filter paper
contact test. Measures
at 7 and 28 days
AChE, CAT and GST
activities and LPO
(malondialdehyde
(MDA)) levels
[22]
Bifenthrin
(pyrethroid)
E. fetida (Ep)
Soil-spiked test. After
3, 7, 14, 21 and
28 days
ROS formation,
guaiacol peroxidase
(POD), SOD, CAT,
GST and EROD
activities
[23]
Roundup
® Alphée
(glyphosate-based
herbicide)
Alma millsoni
(Ep), Eudrilus
eugeniae
(Ep) and
Libyodrilus
violaceus (Ep)
Soil exposure after 1-,
2-, 4-, 6- and 8-week
herbicide application
Activities of GST,
MT, AChE, LDH,
SOD and GPX.
Levels of GSH and
LPO
[24]
Tebuconazole
(fungicide)
E. fetida (Ep)
Soil spiked at 0.5,
5 and 50 mg kg
À1 for
7 days
Biochemical (SOD,
CAT, GSH and
LPO), mRNA (SOD,
CAT, TCPP and
ANN-related genes)
and untargeted
metabolomics (NMR)
[25]
Dinotefuran
(neonicotinoid insecticide) and two
metabolites: UF and
DN
E. fetida (Ep)
Filter paper contact
test for acute toxicity
(mortality) and soil
exposure (0.1, 0.5,
1 and 2 mg kg
À1
) for
2, 7, 14 and 28 days
Enzyme determinations (SOD, CAT),
LPO 8-OHdG levels,
gene expression
Hsp70 and annetocin
(ANN)
[26]
(continued)
Biomarkers in Earthworms
317
relevant soil contaminants
Earthworm
species
Type of exposure
Tested biomarkers
Ref.
Pesticides
Several agriculture
pesticides
Lumbricus
terrestris (A)
Field study. Conventional vs organic
orchard
CEs in 3 tissues of the
gastrointestinal tract
[18]
Carbamate
(Pirimor
®
) and OP
(Lorsban
®
)
insecticides
Aporrectodea
caliginosa (En)
Spiked soil for 1, 2,
3, 4 and 7 days
AChE in whole tissue
and nerve conduction
velocity (NCV) assay
in medial giant fibres
[19]
Ethyl-parathion
Allolobophora
chlorotica
(En) and
A. caliginosa
(En)
Up to 7-day soil
spiked (0.1, 1 and
10 mg kg
À1
) under
lab exposure
AChE, CE activities,
behaviour responses
(burrowing, casting,
feeding)
[20]
OP pesticides:
dimethoate and
pirimiphos-methyl
E. andrei (Ep)
Filter paper contact
test
AChE, CE activities
in whole tissue vs
coelomocyte extracts
[21]
Commercial formulations of glyphosate
(GLF), tembotrione
(TBT) and
nicosulfuron (NCS)
Dendrobaena
veneta (Ep)
Three concentrations
of each formulation
using filter paper
contact test. Measures
at 7 and 28 days
AChE, CAT and GST
activities and LPO
(malondialdehyde
(MDA)) levels
[22]
Bifenthrin
(pyrethroid)
E. fetida (Ep)
Soil-spiked test. After
3, 7, 14, 21 and
28 days
ROS formation,
guaiacol peroxidase
(POD), SOD, CAT,
GST and EROD
activities
[23]
Roundup
® Alphée
(glyphosate-based
herbicide)
Alma millsoni
(Ep), Eudrilus
eugeniae
(Ep) and
Libyodrilus
violaceus (Ep)
Soil exposure after 1-,
2-, 4-, 6- and 8-week
herbicide application
Activities of GST,
MT, AChE, LDH,
SOD and GPX.
Levels of GSH and
LPO
[24]
Tebuconazole
(fungicide)
E. fetida (Ep)
Soil spiked at 0.5,
5 and 50 mg kg
À1 for
7 days
Biochemical (SOD,
CAT, GSH and
LPO), mRNA (SOD,
CAT, TCPP and
ANN-related genes)
and untargeted
metabolomics (NMR)
[25]
Dinotefuran
(neonicotinoid insecticide) and two
metabolites: UF and
DN
E. fetida (Ep)
Filter paper contact
test for acute toxicity
(mortality) and soil
exposure (0.1, 0.5,
1 and 2 mg kg
À1
) for
2, 7, 14 and 28 days
Enzyme determinations (SOD, CAT),
LPO 8-OHdG levels,
gene expression
Hsp70 and annetocin
(ANN)
[26]
(continued)
Biomarkers in Earthworms
317