CARBENDAZIM, BENOMYL, AND THIOPHANATE-METHYL
Summary
Identity, physical and chemical properties, and
analytical methods
Sources of human and environmental exposure
Environmental transport, distribution, and transformation
Environmental levels and human exposure
Effects on other organisms in the laboratory and the field
Evaluation of effects on the environment
Risk evaluation
Aquatic environment
Terrestrial environment
Bibliography
1. Summary
Carbendazim, benomyl, and thiophanate-methyl are evaluated
together because benomyl and thiophanate-methyl are rapidly converted
mainly to carbendazim in the environment. Benomyl has an aerobic
half-life of 2 h in water and 19 h in soil; thiophanate-methyl has an
aerobic half-life of less than one day in soil and two days in water.
2. Identity, physical and chemical properties, and analytical methods
Carbendazim is an odourless, white crystalline solid with a
melting-point of 302-307°C and a vapor pressure of 1 × 10-7 Pa (< 1
× 10-9 mbar) at 20°C; the technical grade has a melting-point of >
295°C. It has low water solubility, 8 mg/litre at 24°C and pH 7, and a
low n-octanol:water partition coefficient (log Pow, about 1.5).
Carbendazim is hydrolytically stable at pH 5-7 at ambient temperatures
(22-25°C). It is capable of strong dust explosion, but is not
flammable or auto-flammable. Analyses for residues and environmental
contamination are performed by high-performance liquid chromatography
(HPLC). Benomyl has a melting-point of 140°C, a vapour pressure of <
5.0 × 10-6 Pa at 25°C, a water solubility of 3.6 mg/litre at pH 5,
and a log Pow value of 23.4-32.0. HPLC and immunoassays have been
used to analyse for benomyl. Thiophanate-methyl has a melting-point of
177°C, a vapour pressure of 1.30 × 10-5 kPa, a water solubility of
21.8 mg/litre at 25°C, and a log Pow value of 25-34.
3. Sources of human and environmental exposure
Carbendazim has been produced commercially since 1970. It is a
systemic fungicide with a broad spectrum of activity on many
economically important phytopathogens of the Ascomycetes,
Deuteromycetes, and Basidiomycetes groups. It is used on agricultural
crops (e.g. cereals, rice, grapes, cucurbits, tomatoes, pome fruits,
stone fruits, and strawberries) and horticultural plants and in
forestry and home gardening. Pest resistance has been seen, e.g. apple
scab, eyespot, and Botrytis In order to combat resistance,
carbendazim is combined with other fungicides with different modes of
action.
Benomyl and thiophanate-methyl degrade primarily to methyl-2-
benzimidazole carbamate (carbendazim), which is also fungicidal. The
mode of action of carbendazim involves interference in the
biosynthesis of DNA during fungal cell division. As benomyl and
thiophanate-methyl have a highly specific mode of action, resistant
strains of fungal pathogens have been developed.
The application rates and the number of treatments allowed per
crop vary with the chemical (see Table 1). Overall, the rates are
0.18-0.60 kg/ha per application for carbendazim, 0.14-1.12 kg/ha for
benomyl, and 0.22-2.13 kg/ha for thiophanate-methyl.
Table 1. Uses and application rates (kg active ingredient/ha) and numbers of treatments allowed
Commodity Carbendazim Benomyl Thiophanate-methyl
Application No. of treatments Application No. of treatments Application No. of treatments
rate rate rate
Apples 0.3-0.6 4 0.45 3 1.35 > 9
Vineyards 0.28-0.56 4 0.45 4
Stone fruits 0.3-0.6 2 0.45 3 1.35-2.13 4
Curcurbits 0.30 2 0.30 3 0.22-0.50 ?
Tomatoes 0.60 4 0.30 3
Rice 1.12 2
Wheat 0.25 1 (cereals) 1.12 1.5 0.9 1
Bananas 0.15 6
Citrus 1.12 2
Caneberries 0.42 5
Celery 0.28 6
Conifers 0.56 5
Peanuts 0.14 12 0.50 Unspecified
Soya bean 1.12 1 0.5-0.9 2
Strawberries 0.60 2 0.56 5 0.7-0.9 Unspecified
Beans 060 1 1.70-2.24 2 0.90-1.53 2
Nut crops
Pecans 0.28-0.56 > 4 0.50-0.90 ?
Almonds 0.56-0.84 2 1.35-1.80 2
Sugar beets 0.21-0.28 ? 0.29-0.38 ?
Sugar cane 0.21-0.28 ? 0.38 ?
4. Environmental transport, distribution, and transformation
Carbendazim has a half-life to hydrolysis of 25 weeks. In the
environment, it has half-lives of 6-12 months on bare soil, 3-6 months
on turf, and 1-2 months in a water-sediment system under aerobic
conditions and 25 months under anaerobic conditions. In aerobic river
sediment containing water, thiophanate-methyl degraded with a
half-life of 15-20 days. Residues of carbendazim and its metabolites
are strongly bound or incorporated into soil organic matter. In
laboratory studies of soil containing labelled carbendazim, the
molecules remained in the topsoil. Residues of carbendazim and its
metabolites that are bound or incorporated into soil are probably due
to the imidazole ring of the molecule, as the Koc is relatively low.
Benomyl is hydrolysed rapidly, in < 2 h at pH 5, 7, and 9; it is
rapidly degraded in water, with half-lives of < 4 h in sun or
darkness, and on soil, at less than four days on silt loam soil. In a
field study, the degradation half-life was 5.2 h in light and 5.7 h in
the dark, indicating that photolysis is not a significant degradation
pathway but that hydrolysis is the controlling factor.
Under anaerobic conditions, 98% of carbendazim residues partition
into sediment after seven days. The half-life of carbendazim was 743
days, and after one year 36% of the radiolabel was bound to sediment.
Under aerobic conditions, the half-life in non-sterile sediment was 61
days. After 30 days, 22% of the radiolabelled carbendazim was bound to
sediments, and < 1% of the amount applied was evolved as carbon
dioxide. Anaerobic degradation in soil and water is slower than
aerobic degradation.
Carbendazim was susceptible to photolysis in natural daylight and
was broken down to dimethyloxalate, quinidine, and mono- and
dicarbomethoxyguanidine. No photolysis products were detected in
extracts of leaves of treated corn plants after exposure to sunlight
for 18 h. After aerobic incubation, 3-10 mg/kg carbendazim had
disappeared within 250 days, with only 5-13% remaining. After 224
days, 57% was in the form of non-extractable residue; after 250 days,
4-8% was converted to 2-amine-1 H-benzimidazole and 30-40% to carbon
dioxide.
When carbendazim was applied directly to two German water-
sediment systems, the label disappeared rapidly from water, with
half-lives of 31 days in Rhine River water and 22 days in pond water.
The average half-life of carbendazim in an aquatic system was about 26
days. In the total soil-water system, 98.3% carbendazim was eliminated
from Rhine River water and 95.9% from pond water after 91 days. In
contrast to English and Mississippi sediments, formation of
14C-carbon dioxide was extensive, amounting to 61.2% in Rhine River
water and 40.3% in pond water after 91 days of incubation.
Two other benomyl degradates, dibutylurea and 1-butylisocyanate,
are formed under hot, humid conditions in greenhouses. These two
compounds are being studied for phytotoxicity to vascular plants.
Carbendazim, thiophanate-methyl, and benomyl are absorbed by
sprouts, leaves, and roots and are translocated within the
transpiration system in the plants xylem. They inhibit the development
of fungal germ tubes, the formation of appressoria, and the growth of
mycelia. Their fungitoxic action is based on blockage of nuclear
division during mitosis and destabilization of fungal cell structures.
Carbendazim, thiophanate-methyl, and benomyl persist on leaf surfaces
and in leaf litter. The conversion of benomyl to carbendazim on leaf
surfaces varies with the leaf surface, light intensity, and other
environmental factors. About 50% of a 50% wettable powder formulation
of benomyl remained on apple leaves after five days.
Bioconcentration of carbendazim in fish is not expected to be
significant: > 94% of residue was lost from whole fish, viscera, and
muscle during a 14-day depuration phase. The bioconcentration factors
for bluegill sunfish ( Lepomis microlophus) were 27 (0.018 mg/litre)
and 23 (0.17 mg/litre). After exposure of rainbow trout ( Salmo
gairdneri) and bluegill sunfish to 45 µg/litre for 96 h, rainbow
trout had the highest uptake rate constant (1.78 per hour) and
bioconcentration factor (159). Channel catfish ( Ictalurus punctatus)
accumulated less residue (0.44 µg/g) but died after 48 h of exposure.
The bioconcentration factors in whole fish were 23-27, and radiolabel
was concentrated in the viscera, the peak viscera bioconcentration
factors being 380-460; very little radiolabel was concentrated in
muscle (bioconcentration factor, < 4) or the remaining carcass
(< 7). When the fish were placed in clean water, > 94% of the peak
level of radiolabel was lost from the whole fish, viscera, and muscle
after two weeks; the rate of loss from the carcass was 77-82% at that
time.
5. Environmental levels and human exposure
Carbendazim residues are expected to persist on leaf surfaces and
in leaf litter and to increase with each successive application. When
a 50% wettable powder benomyl fungicide was applied to apple trees in
three successive treatments at a rate of 1.7 kg/ha, benomyl residues
on foliage had fallen by 50% on day 5 after application, whereas those
of carbendazim had doubled and increased with each successive benomyl
application. A similar pattern for residues of thiophanate-methyl can
be expected.
Thiophanate-methyl residues were monitored in water and in
crayfish after application of Topsin M(R), a 70% wettable powder
formulation, twice to rice fields. No thiophanate-methyl residues were
detected in crayfish tails (detection limit, 0.05 ppm), and no adverse
effects on the crayfish were observed. In rice water effluent sampled
three to four weeks after the second application of 0.85 kg/ha, no
thiophanate-methyl residues were found; carbendazim was detected at
0.01-0.006 ppm in the field, 0.01-0.007 in the drainage ditch, and
0.004-0.005 ppm at the receiving stream.
In long-term studies of field dissipation, fallow and cropped
fields received two treatments of Topsin M(R) at 1.57 kg/ha per
application, and soil samples were collected for one year at depths of
0-10, 10-20, and 20-30 cm. The fields were tilled by standard practice
for the area. The residues of thiophanate-methyl and carbendazim were
low, even on the day of application. Thiophanate-methyl readily
degraded to carbendazim in all soils, and the carbendazim residues
declined to < 0.1 ppm in almost all plots after one to three months.
Thiophanate-methyl was not detectable in soil sections of < 10 cm,
and, after four months, carbendazim was not detected at > 0.02 ppm in
the 20-30-cm soil section. Soil binding of carbendazim increased with
the organic matter content of the soil. Dissipation of thiophanate-
methyl did not occur below 0-10 cm, and carbendazim was essentially
undetectable in the 20-30-cm layer. Dissipation of carbendazim in
water was rapid.
6. Effects on other organisms in the laboratory and the field
Carbendazim is highly acutely toxic to channel catfish (LC50,
0.007-> 0.56 mg/litre), aquatic invertebrates (0.087-0.46 mg/litre),
mysid shrimp (0.098 mg/litre), and rainbow trout (0.1-> 1.8 mg/litre),
and moderately to slightly toxic to bluegill sunfish (> 3.20-
55 mg/litre) in the laboratory. In a study of the early life stage of
rainbow trout, the maximum acceptable toxicant concentration (MATC)
was 0.019 mg/litre. In a two-generation study of reproductive toxicity
in Daphnia magna, the MATC was 0.0040 mg/litre. In a study of the
life cycle of Mysidopsis bahia, the MATC was 0.0354 mg/litre.
The toxicity of carbendazim in green algae appears to be
species-dependent, with median effective concentration (EC50) values
ranging from 0.34 mg/litre for Chlorella pyrenoidosa to 419 mg/litre
for Scenedesmus subspicatus. Carbendazim was algicidal to
Raphidocellis subcapitata, with an EC50 of 1.6 mg/litre and a
no-observed-effect concentration (NOEC) of 0.5 mg/litre.
Significant inhibition of the Egyptian soil fungi Aspergillus
sp. occurred when carbendazim was applied at the recommended field
application rate; however, the nitrification activities of
Nitrosomonas sp. and Nitrobacter agilis were not inhibited in
suspension cultures with up to 100 mg/litre carbendazim. The mud ditch
organisms Escherichia coli and Salmonella typhimurium were not
adversely affected at up to 1000 mg/litre.
Results of laboratory studies with terrestrial organisms are
summarized in Table 2. The tests with natural arthropod enemies of
pests, hover flies, ladybirds, and predatory mites, were conducted
with only one dose of benomyl, so that the concentrations that had an
effect cannot be calculated. Concentrations well below most
recommended field rates, however, affected reproduction in at least
one mite and one insect species.
Several field studies of earthworms, in which benomyl or
carbendazim were applied at rates near or below the maximal
recommended field rates, are summarized in EHC 148 and EHC 149. In
most of the reports, effects were recorded on numbers, biomass, cast
production, and/or removal of litter. In a study in apple orchards,
benomyl was applied at 0.28 kg/ha five to seven times a year for three
years and thiophanate-methyl at 0.78 kg/ha seven times a year for two
years. The numbers and biomass of the earthworm populations were
seriously diminished, Lumbricus terrestris and Allolobophora
chlorotica being the most affected. Populations of other earthworm
species recovered within two years after spraying ended. Earthworm
populations adjacent to the orchards were unaffected, perhaps due to
the immobility of benomyl in soil (Stringer & Lyons, 1974).
Field studies with soil and litter microorganisms show only
transient or no effects of benomyl and carbendazim when applied at
recommended field rates. Pronounced but transient effects (< 40 days)
were observed on soil fungi by Abdel-Fattah et al. (1982), and
Torstensson & Wessén (1984) found pronounced effects only in sandy
soils at 2 kg/ha. No field studies were available on other non-target
terrestrial organisms.
Carbendazim has low toxicity for birds, with an acute oral LD50
value of > 2250 mg/kg bw for bobwhite quail. In five-day dietary
studies, the LC50 values were > 10 000 mg/kg diet for mallard ducks
and bobwhite quail. Owing to its low octanol:water partition
coefficient, bioaccumulation is expected to be minimal. In a 90-day
study of reproduction in Japanese quail, the NOEL for carbendazim was
160 mg/kg diet (mean daily intake, 20 mg/kg bw); the reproductive NOEC
was 400 ppm, equivalent to a mean daily intake of about 50 mg/kg bw.
Benomyl has low toxicity for birds, with an acute oral LD50
value of > 2250 mg/kg bw for bobwhite quail. In five-day dietary
studies, the LC50 values were > 10 000 mg/kg bw for mallard ducks
and bobwhite quail and > 5000 for Japanese quail. Because of its low
octanol:water partition coefficient, its bioaccumulation is expected
to be low. No studies are available on the effects of benomyl on avian
reproduction.
Thiophanate-methyl has low, toxicity for birds, with acute oral
LD50 values of > 4640 mg/kg diet for bobwhite quail and mallard
ducks. In five-day dietary studies, the LC50 values were >
10 000 mg/kg for mallard ducks and bobwhite quail. Owing to its low
octanol:water partition coefficient, bioaccumulation is expected to be
low. In 24-week studies of reproduction, the no-effect concentrations
in diets were 500 mg/kg for bobwhite quail and 103 mg/kg for mallard
ducks.
Table 2. Toxicity of carbendazim, benomyl, and thiophanate-methyl to terrestrial organisms
Organism Study type Exposure End-point, result (nominal
concentration of active ingredient)
Carbendazim
Soil microorganisms Oxygen consumption 15 days EC50 > 100 mg/litre
Nitrobacter agilis and Nitrification and NOEC > 100 mg/litre
Nitrosomonas spp. witrification
Escherichia coli and NOEC > 1000 mg/litre
Salmonella typhimurium
Aspergillis Growth 5 and 40 Significant inhibition
Worms
Compost worm (Eisenia andrei) Acute, artificial soil 3 weeks LC50 5.7 mg/kg
Compost worm (Eisenia andrei) Reproduction, artificial soil 8 weeks EC50 2.9 mg/kg soil; NOEC,
Insects 0.6 mg/kg
Springtail (Folsomia candida) Reproduction, artificial soil 4 weeks EC50 > 1000 mg/kg soil
Honey bee (Apis mellifera) Contact 48 h LD50 > 50 µg/bee
Carabid beetle (Ptesrostichus melanarius) Contact, spray, soil/sand 6 days NOEC > 1250 g/ha
Birds Dietary 5 days LC50 > 15.59-2250 mg/kg feed
Reproduction 12 weeks NOEC 160-400 mg/kg diet
Benomyl
Soil microorganisms Dehydrogenase inhibition 28 days NOEC 6 mg/kg
Worms
Compost worm (Eisena foetida) Acute contact 14 days LC50 10.48 mg/kg
Insects
Hover fly (Syrphus corollae) Reproduction, glass plate, 11 days at 49% reduction
larvae 3 µg/cm2
Ladybird (Coccinella septempunctata) Reproduction, glass plate, 3 weeks at No effect
larvae 0.65 µg/cm2
Predatory mite (Typhlodromus pyri) Reproduction, glass plate, 19 days at 38% reduction
protonymph 0.69 µg/cm2
Honey bee (Apis mellifera) Contact LD50 > 10 µg/bee
Table 2. (cont'd)
Organism Study type Exposure End-point, result (nominal
concentration of active ingredient)
Birds
Japanese quail (Coturnix Dietary 5 days LC50 > 5000 mg/kg feed
coturnix japonica)
Redwing blackbird (Agelaius Oral Acute LD50 100 mg/kg bw
phoeniceus)
Thiophanate-methyl
Soil microorganisms CO2 production 14 days NOEC > 30 mg/kg bw
Nitrification 42 days NOEC > 30 mg/kg bw
Heterotrophic N fixation 7 days NOEC > 5 mg/kg bw
Worms
Compost worm (Eisenia foetida) Acute, artificial soil 14 days LC50 20.8 mg/kg soil
Insects
Honey bee (Apis mellifera) Contact 48 h LD50 > 100 µg/bee
Birds
Bobwhite quail (Colinus virginanus) Dietary 5 days NOEC 4640-> 10 000 mg/kg bw
LC50 > 10 000 mg/kg feed
Mallard duck (Anas platyrhyncos) Acute oral 8 days LD50 > 4640 mg/kg bw
From Van Gestel et al. (1992); Kühner (1992); Pietrzik (1992); Decker (1993)
7. Evaluation of effects on the environment
Benomyl, carbendazim, and thiophanate-methyl are broad-spectrum
systemic fungicides belonging to the benzimidazole group and are used
on a wide variety of crops. Because of the development of resistance,
benzimidazole fungicides are usually alternated with other compounds
with different modes of action. Formulations include wettable powders,
water-dispersible granules, flowable concentrates, dusts, and
granules.
Benomyl and thiophanate-methyl that enter the environment are
converted to carbendazim, which can be regarded as the environmentally
relevant compound. The half-lives are 2-19 h for benomyl and three to
four days for thiophanate-methyl. The carbendazim formed decomposes in
the environment with a half-life of months under aerobic and anaerobic
conditions in soil and water.
Carbendazim partitions from water to soil and sediment. It binds
to the mineral component of the soil, probably through the imidazole
ring. Adsorption is strong and carbendazim does not leach through the
soil profile, despite its low Kow. No contamination of ground-water
can be expected, as confirmed by field monitoring of well-water.
Abiotic degradation is considered to be a minor route of degradation
for carbendazim; microorganisms, predominantly bacteria, represent the
major route of loss. Only moderate bioaccumulation of carbendazim was
seen in laboratory studies at constant concentrations. There is rapid
depuration on transfer to clean water. No significant bioaccumulation
of carbendazim is expected in the field.
Benomyl had no effect on soil bacterial populations in the
laboratory. In studies in greenhouses and the field, application rates
of up to 89.6 kg/ha had little effect on soil microbial populations.
Limited studies suggest that thiophanate-methyl does not adversely
inhibit soil-nitrifying bacteria. Field studies confirm these
findings, even though transient effects on soil fungi have been
observed.
The NOEC for a green algae was 0.5 mg/litre.
Carbendazim is highly to highly acutely toxic to fish, aquatic
invertebrates, and mysid shrimp, with LC50 values of 0.007 mg/litre
for fish, 0.087 mg/litre for aquatic invertebrates, and 0.098 mg/litre
for shrimp. The MATC was 0.019 mg/litre for rainbow trout,
0.004 mg/litre for Daphnia magna, and 0.035 mg/litre for mysid
shrimp.
Field application rates of carbendazim are not expected to pose
an acute hazard to non-target mammalian wildlife species.
Carbendazim, thiophanate-methyl, and benomyl have low acute
toxicity for birds, with dietary LC50 values > 5000 mg/kg. Field
application rates of carbendazim are not expected to pose a hazard to
birds.
Risk assessment
(a) Aquatic environment
A simple screening model (Generic Expected Environmental
Concentration -- Environmental Protection Agency/Office of Pesticide
Products) for worst-case scenarios was used to estimate the predicted
expected concentration (PEC) of carbendazim in aquatic systems after
application of 0.56 kg/ha of carbendazim to vineyards in four
treatments at 14-day intervals. The following parameters are used in
the calculations: Soil Koc, 250; water solubility, 8 ppm; present
spray drift, 5; depth of soil incorporation, 0; soil aerobic metabolic
half-life, 180 days; aquatic aerobic half life, 61 days; longest
hydrolysis half-life, 175 days, and photolysis half-life, stable.
The concentrations found with this model in a water body 2 m deep
were: peak, 56 µg/litre; four-day concentration, 54 µg/litre; 21-day
concentration, 48 µg/litre; and 56-day concentration, 38 µg/litre. The
model is basically the same as that used in the United Kingdom and the
Netherlands. Toxicity exposure ratios (TERs) were calculated, as shown
in Table 3, which indicate that a risk to all aquatic organisms, on
either an acute or a chronic basis, is at least present and often
large. Reduced bioavailability owing to adsorption to sediment would
reduce this apparent risk. Contamination of surface waters by benomyl,
carbendazim, and thiophanate-methyl must be avoided to prevent toxic
effects on aquatic organisms.
(b) Terrestrial environment
The predicted environmental concentration (PEC) used for
evaluating acute effects is based on one application of 0.6 kg/ha, of
which 100% reaches both the canopy and the soil. The soil PEC for
chronic effects is based on four successive applications of 0.6 kg/ha,
as on vines. As the degradation rate of carbendazim in soil is of the
order of months and carbendazim is not mobile, no degradation is
assumed. A further assumption was that the compound is dispersed into
the top 5 cm of a soil with a density of 1.4 g/cm3.
The summary of acute and chronic TERs (Table 4) indicates a
'large' risk to earthworms in the soil. The risk to honey bees is
regarded as low. The large risk to earthworms is confirmed by field
studies; no such studies are available for arthropods.
Table 3. Estimates of acute and chronic risk for aquatic organisms after application of carbendazim to vineyards
Time course Organism PEC Toxicity End-point TER Risk classification
(µg/litre) (µg/litre)
Acute Invertebrate 56 87 LC50 1.55 Present
Acute Fish 56 7 LC50 0.125 Large
Acute Shrimp 56 98 LC50 1.75 Present
Chronic Invertebrate 48 27 NOEC 0.56 Large
Chronic Fish 48 3 NOEC 0.06 Very large
Chronic Shrimp 45 35 NOEC 0.78 Large
PEC, predicted environmental concentration; TER, toxicity:exposure ratio; NOEC, no-observed-effect concentration
Table 4. Estimates of acute and chronic risk for terrestrial organisms after application of carbendazim to vineyards
Time Organism PEC Toxicity End-point TER Risk classification
course
Acute Compost worm 0.86 mg/kg soil 5.7 mg/kg LC50 6.6 Present
(Eisenia foetida)
Acute Honey bee 6 µg/cm3 > 50 µg/bee LC50 12a Low
(Apis mellifera)
Chronic Compost worm 3.43 mg/kg 0.6 mg/kg soil NOEC for 0.17 Large
(Eisenia foetida) reproduction
Chronic Springtail 3.43 mg/kg > 1000 mg/kg Reproduction > 290 Negligible
(Folsomia candida)
Chronic Predatory mite 6 µg/cm3 38% reduction Reproduction - -
(Typhlodromus pyri) at 0.69 µg/cm3
PEC, predicted environmental concentration; TER, toxicity:exposure ratio
a Hazard ratio estimate from toxicity per bee
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