Assessment of Toxicity Risk of Insecticides used in Rice

Ecosystem on Trichogramma japonicum, an Egg Parasitoid of Rice

Lepidopterans
Author(s): Xueping Zhao , Changxing Wu , Yanhua Wang , Tao Cang , Liping
Chen , Ruixian Yu and Qiang Wang
Source: Journal of Economic Entomology, 105(1):92-101. 2012.
Published By: Entomological Society of America
DOI: http://dx.doi.org/10.1603/EC11259
URL: http://www.bioone.org/doi/full/10.1603/EC11259

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 ECOTOXICOLOGY

Assessment of Toxicity Risk of Insecticides Used in Rice Ecosystem on

Trichogramma japonicum, an Egg Parasitoid of Rice Lepidopterans
XUEPING ZHAO, CHANGXING WU, YANHUA WANG,1 TAO CANG, LIPING CHEN, RUIXIAN YU,
AND QIANG WANG

State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control/Key Laboratory for Pesticide
Residue detection of Ministry of Agriculture, Institute of Quality and Standard for Agro-products, Zhejiang Academy of
Agricultural Sciences, Hangzhou 310021, China

J. Econ. Entomol. 105(1): 92Ð101 (2012); DOI: http://dx.doi.org/10.1603/EC11259

ABSTRACT Both chemical and biological methods are essential for control of insects, for example,
lepidopterans, on rice. Thus, it is important to know the effect of chemicals on the biological control
agents. In this study, we assessed the toxicity of commonly used insecticides on a biological control agent,
Trichogramma japonicum Ahmead (an egg parasitoid of rice lepidopterans) by using a dry Þlm residue
method. Results showed that thirty insecticides from seven chemical classes exhibited various degree of
toxicity to this parasitoid. Among the seven classes of chemicals tested, organophosphates (chlorpyrifos,
fenitrothion, phoxim, profenofos, and triazophos) and carbamates (carbaryl, carbsulfan, isoprocarb, me-
tolcarb, and promecarb) exhibited the highest intrinsic toxicity to T. japponicum, with an LC50 of 0.035
(0.029Ð0.044) to 0.49 (0.34Ð0.87) mg active ingredient (a.i.) L⫺1, followed by antibiotics (abamectin,
emamectin benzoate, and ivermectin), phenylpyrazoles (butane-Þpronil, ethiprole, and Þpronil), pyre-
throids (cyhalthrin, cypermethrin, fenpropathrin, and lambda-cyhaothrin), and neonicotinoids (acet-
amiprid, imidacloprid, imidaclothiz, nitenpyram, thiacloprid, and thiamethoxam). Moreover, the insect
growth regulator insecticides (chlorßuazuron, fufenozide, hexaßumuron and tebufenozide) exhibited the
lowest toxicity to the wasps with an LC50 of 3,383 (2406Ð5499) to 30206 (23107Ð41008) mg a.i. L⫺1. Risk
quotient analysis showed that phenylpyrazoles, pyrethroids, insect growth regulators, neonicotinoids (with
the exception of thiamethoxam), and antibiotics (with the exception of abamectin) are classiÞed as safe
agents to the parasitoid, while organophosphates and carbamates are classiÞed as slightly, moderately, or
highly toxic agents to the parasitoid. The data presented in this paper provided useful information on the
selection of compatible insecticides with T. japonicum.

KEY WORDS Trichogramma japonicum, chemical control, biological control, egg parasitoid

Rice, Oryza sativa L. is an important crop in the world,
and some lepidopterans have adversely affected its
yields (Matteson 2000, Oza et al. 2008). For example,
striped stem borer, Chilo suppressalis Walker, yellow
stem borer, Scirpophaga incertulas Walker, and rice
leaf folder, Cnaphalocrocis medinalis Guenee are now
considered as the key pests of rice in many countries,
especially in Asia (Rahman et al. 2004, Cheng et al.
2010, Xu et al. 2010, Zheng et al. 2011). In addition to
insecticide controls, biological controls may offer an
alternative approach, that is both economically and
ecologically feasible, to control arthropod pests found
in rice crop systems (Settle et al. 1996, Van Driesche
et al. 2010). Additionally, biological controls may re-
duce negative impacts of chemical insecticides on the
environment (Landis et al. 2000, Frank 2010). Among
various biological control agents, the species Tricho-
gramma japonicum Ashmead (Homenoptera: Tricho-
grammatidae) is an important egg parasitoid and the
1 Corresponding author, e-mail: wangyanh79@hotmail.com.
most promising natural enemy of lepidopterans in rice
crop (Rani et al. 2007). Although each T. japonicum
female produces ⬇45 offspring, superparasitism is
rare. T. japonicum has been successfully used to con-
trol C. suppresslis and C. medinalis under the Þeld
conditions in China and India (Bentur et al. 1994,
Chen et al. 2010).
Despite of the importance of biological methods for
insect control, the use of insecticides is still necessary
within the current agricultural system because it is
quick, efÞcient, easy to use, and cost effective (Urech
2000, Khan et al. 2008). In this context, multiple tactics
have been applied within the integrated pest manage-
ment (IPM) concept, demonstrating that when insec-
ticides are used in a compatible manner, the effec-
tiveness of biological control may be improved (Wang
et al. 2008b, Preetha et al. 2009). Ideal insecticides
should have minimal side-effects on natural enemies
of the insect pests (MÕhamed and Chemseddine 2002,
Brugger et al. 2010). Therefore, knowledge of com-
patibility and impact of insecticides on natural ene-

0022-0493/12/0092Ð0101$04.00/0 䉷 2012 Entomological Society of America

February 2012 ZHAO ET AL.: RISK OF INSECTICIDES USED IN RICE ECOSYSTEM 93

Table 1. Detailed information (name, manufacturer, stock, and field recommended concn) of insecticides used in this study

Field recommended rate

Insecticide Technical grade (a.i.) Manufacturer
(g a.i. ha⫺1)
Neonicotinoids
Acetamiprid 97% Jiangsu Yangnong Chemical Co., Ltd. 18Ð22.5
Imidacloprid 95.3% Jiangsu Changlong Chemical Co., Ltd. 15Ð30
Imidaclothiz 95% Jiangsu Yangnong Chemical Co., Ltd. 22.5Ð30
Nitenpyram 95% Jiangsu Nantong Agro-chemical Co., Ltd. 15Ð30
Thiacloprid 97.75% Tianjing Xingguang Chemical Co., Ltd. 50.4Ð100.8
Thiamethoxam 97.7% Swiss Syngenta Crop Protection Inc. 15Ð22.5
Antibiotics
Abamectin 93% B1a Hebei Weiyuan Biochemical Co., Ltd. 21.6Ð32.4
Emaectin benzoate 89% B1a Hebei Weiyuan Biochemical Co., Ltd. 1.5Ð1.8
Ivermectin 90.73% B1 Zhejiang Haizheng Chemical Co., Ltd. 3Ð4.5
Phenylpyrazoles
Butene-Þpronil 90% Daliang Ruize Agro-chemical Co., Ltd. 15Ð30
Ethiprole 96% Swiss Syngenta Crop Protection Inc. 45Ð60
Fipronil 87% Hangzhou Bayer Crop Science Ltd. 15Ð22.5
IGRs
Chlorßuazuron 85.7% Jiangsu Yangnong Chemical Co., Ltd. 45Ð60
Fufenozide 97% Jiangsu Changlong Chemical Co., Ltd. 79Ð90
Hexaßumuron 97.1% Daliang Ruize Agro-chemical Co., Ltd. 30Ð56.25
Tebufenozide 92% Jiangsu Baoling Chemical Co., Ltd. 210Ð300
Pyrethroids
Cyhalothrin 95% Jiangsu Yangnong Chemical Co., Ltd. 37.5Ð52.5
Cypermethrin 93.2% Nanjing Red-sun Chemical Co., Ltd. 45Ð90
Fenpropathrin 94% Nanjing Red-sun Chemical Co., Ltd. 90Ð120
Lambda-cyhalthrin 98% Jiangsu Changlong Chemical Co., Ltd. 15Ð30
Organophosphates
Chlorpyrifos 97% Jiangsu Nantong Agro-chemical Co., Ltd. 450Ð600
Fenitrothion 95% Huangyan Yongning Chemical Co., Ltd. 90Ð120
Phoxim 89% Jiangsu Baoling Agro-chemical Co., Ltd. 360Ð540
Profenofos 90.8% Zhejiang Yongnong Chemical Co., Ltd. 480Ð600
Triazophos 80.5% Hubei Xianlong Agro-chemical Co., Ltd. 480Ð600
Carbamates
Carbosulfan 88.89% Suzhou Fumeishi Chemical Co., Ltd. 90Ð180
Carbaryl 94% Hunan Haili Chemical Co., Ltd. 765Ð1,275
Isoprocarb 99.7% Jiangsu Changlong Chemical Co., Ltd. 450Ð600
Metolcarb 96% Nanjing Red-sun Chemical Co., Ltd. 450Ð540
Promecarb 98% Jiangsu Yangnong Chemical Co., Ltd. 200Ð333.3

mies of insects is essential for effective integration of
chemical and biological controls (Moura et al. 2006,
Preetha et al. 2009). However, very little information
and knowledge about the adverse effects of currently
popular insecticides on T. japonicum is available.
Studies of potential toxicity of insecticides used in
the rice ecosystem to natural enemies under labora-
tory conditions are a prerequisite for avoiding the
insecticides that cause high ecological damage (Krish-
naiah and Kalode 1988, Preetha et al. 2010). Currently,
many low toxic organophosphates, carbamates, neo-
nicotinoids, and other novel insecticides are being
considered as potential alternatives to replace highly
toxic organophosphate insecticides in China (He et al.
2008, Wang et al. 2008a). In addition to evaluating
their toxicological effect on the target insects, these
insecticides need to be assessed for their adverse im-
pact on natural enemies of the insects (Brunner et al.
2001, Wang et al. 2008b, Preetha et al. 2009). T. ja-
ponicum is commercially used to control different rice
lepidopterans in paddy Þeld and it is present naturally
in rice ecosystem where many insecticides are fre-
quently used (de Kraker et al. 1999, Hirose 2005).
Therefore, in this study, we determined the toxic ef-
fect of different insecticides on T. japonicum. The
results obtained from this study would provide im-
portant information on the compatibility of biological
and chemical controls.
Materials and Methods
Insect. T. japonicum was maintained on eggs of the
host, Corcyra cephalonica Stainton (Lepidoptera: Pyr-
alidae). The host was obtained from Guangdong En-
tomological Institute (Guangzhou, China) and was
fed corn ßour. The host eggs were glued on paper
cards (6.5 ⫻ 1.5 cm) impregnated with glue and killed
by ultra violet (UV) before being offered to parasi-
toids. After the parasitism period (24 h), parasitized
eggs were transferred to new containers (glass tubes
of dimension 8.0 cm height ⫻ 1.5 cm diameter) and
kept in chambers until the emergence of adults. All the
insects were maintained at 25 ⫾ 1⬚C, RH of 70 ⫾ 10%,
and 14:10 h (L:D) photoperiod. Age of adult parasi-
toids was standardized at 24 Ð 48 h postemergence for
all following experiments.
Insecticides. Insecticides were selected on the basis
of their current and potential use for the management
of insect pests in paddy Þeld. Thirty insecticides from
seven chemical classes were evaluated for the current
study (Table 1). Active ingredients were used instead
of commercial formulations because the aim was to
94 JOURNAL OF ECONOMIC ENTOMOLOGY
document the effects of the neurotoxic molecules on
the mortality without inßuence of adjuvants added in
commercial products. Insecticides of technical grade
were dissolved with analytical grade acetone to obtain
the desired concentrations and were used directly for
contact toxicity studies. A spray volume of 675 L/ha⫺1
was used for the comparison between the Þeld-rec-
ommended concentrations of insecticides and those
with acute toxicity.
Contact Acute Toxicity. A dry Þlm residue method
was used to assess the toxicity of insecticides on T.
japonicum (Desneux et al. 2006). Preliminary studies
were performed to identify the concentration that
causes 10 to 90% mortality to the parasitoid. To es-
tablish the concentration-mortality relationship, adult
parasitoids were exposed to six concentrations in-
creasing with a geometrical ratio of two-fold. Acetone
solutions of insecticide were made in glass tubes
(height: 8.0 cm; diameter: 2.0 cm; internal surface area:
53.38 cm2). Pure acetone was used as control. To
obtain a homogenous deposition, we introduced 500
␮l of solution, which allowed a total coverage of the
internal surface of the tube. The tube was then man-
ually rotated on the palms until no more droplets were
seen on the glass wall. Tubes were left for ⬇1 h at room
temperature to ensure complete evaporation of ace-
tone before introducing the adult parasitoids. Because
the internal surface of tubes and volume of solution
were Þxed, we expressed the quantity of insecticide
residue per unit of surface. Wasps (n ⫽ 80 Ð100) were
placed in each tube containing a small plastic strip
with two drops of honey. The tubes were covered with
Þne nylon mesh to allow air circulation, and were
maintained at 25 ⫾ 1⬚C, 70 ⫾ 10% RH, and 14:10 h
(L:D) photophase. Three replicates were conducted
for each dose and each insecticide. After 1 h of ex-
posure, the wasps were transferred into a clean insec-
ticide-free tube containing honey solution. Parasitoid
mortality was determined at 24 h posttreatment. The
wasps without any movement when prodded were
counted as dead.
Risk Assessment Method. The risk quotient method
was used to assess the risk to nontarget arthropods
from plant protection products and thus the ecological
risk of pesticides (Peterson 2006). It has been used to
assess the safety of predators and parasitoids such as
coccinellids, Cyrtorhinus lividipenis Renter, Bracon he-
betor Say, and Trichogramma cacoeciae Marchal
(Danfa et al. 1998, Peveling and Ely 2006, Preetha et
al. 2009). Risk quotients for the insecticides were cal-
culated from the LC50 values at 24 h after treatment
based on the following formula: risk quotient ⫽ Field
recommended rate (g a.i. ha⫺1)/LC50 of beneÞcial in-
sect (mg a.i. L⫺1). The risk quotient value of ⬍50 for a
pesticide is safe, 50Ð2500 is slightly to moderately toxic
and ⬎2500 is dangerous (Preetha et al. 2010).
Statistical Analysis. The percentage of mortality for
each insecticide to T. japonicum was corrected by
Abott formula (Abott 1925). The data were then sub-
jected to probit analysis as described by Finney using
EPA Probit Analysis Programme Version 1.5 and log
concentration probit mortality line obtained (Finney
Vol. 105, no. 1
1971). SigniÞcant level of mean separation was de-
Þned as nonoverlap between the 95% conÞdence lim-
its (CL) of two LC50 values (Prabhaker et al. 2011).
Results
Contact Toxicity of Insecticides to T. japonicum.
LC50 of the selected insecticides to T. japonicum
ranged from 0.035 (0.029 Ð 0.044) mg a.i. L⫺1 to 30206
(23107Ð 41008) mg a.i. L⫺1 (Table 2). The order of the
toxicity for the 30 insecticides was: metolcarb, chlor-
pyrifos ⬎ phoxim ⬎ promecarb, fenitrothion ⬎ thia-
methoxam, profenofos, triazophos, carbaryl, isopro-
carb abamectin ⱖ nitenpyram ⬎ ivermectin, Þpronil ⱖ
emamectin benzoate ⬎ butane-Þpronil, lambda-cy-
halthrin, carbosulfan ⬎ cyhalothrin ⬎ ethiprole ⬎
cypermethrin, acetamiprid, fenpropathrin ⬎ thiaclo-
prid, imidaclothiz, imidacloprid ⬎ tebufenozide, chlo-
rßuazuron, hexaßumuron ⬎ fufenozide (LC50 value
with overlapping conÞdence intervals were classiÞed
as the same level of toxicity). Overall, organophos-
phates and carbamates showed the highest toxicity,
while IGRs exhibited the lowest toxicity to T. japoni-
cum.
Toxicity of Neonicotinoids to T. japonicum. The
LC50 of neonicotinoids to T. japonicum ranged from
0.40 (0.37Ð 0.45) mg a.i. L⫺1 to 95.48 (86.15Ð106.4) mg
a.i. L⫺1 (Table 2). Among the six neonicotinoids
tested, thiamethoxam showed the highest toxicity to T.
japonicum with an LC50 of 0.40 (0.37Ð 0.45) mg a.i. L⫺1.
Based on the LC50, thiamethoxam is 239- and 202-fold
more toxic than imidacloprid and imidaclothiz, re-
spectively. The order of toxicity for the six neonicoti-
noids was: thiamethoxam ⬎ nitenpyram ⬎ acet-
amiprid ⬎ thiacloprid, imidaclothiz, imidacloprid
(Table 2).
Toxicity of Antibiotics and Phenylpyrazoles to T.
japonicum. The LC50 of antibiotics to T. japonicum
ranged from 0.50 (0.36 Ð 0.81) mg a.i. L⫺1 to 1.11 (1.00 Ð
1.22) mg a.i. L⫺1 (Table 2). Among the three antibi-
otics tested, abamectin had an LC50 of 0.50 (0.36 Ð
0.81) mg a.i. L⫺1, which was higher than ivermectin
and emamectin benzoate, with an LC50 of 0.92 (0.83Ð
1.04) mg a.i. L⫺1 and 1.11 (1.00 Ð1.22) mg a.i. L⫺1,
respectively. The LC50 of phenylpyrazoles ranged
from 0.93 (0.71Ð1.27) mg a.i. L⫺1 to 16.23 (14.66 Ð
18.09) mg a.i. L⫺1. The LC50 of Þpronil and butane-
Þpronil was 0.93 (0.71Ð1.27) mg a.i. L⫺1 and 1.84
(1.46 Ð2.45) mg a.i. L⫺1, respectively, which was lower
than that of ethiprole [16.23 (14.66 Ð18.09) mg a.i.
L⫺1]. Based on the LC50, Þpronil and butane-Þpronil
were 18 and 8.9-fold more toxic than ethiprole.
Toxicity of Insect Growth Rates and Pyrethroids to
T. japonicum. The LC50 of insect growth rates (IGRs)
to T. japonicum ranged from 3,383 (2,406 Ð5,499) mg
a.i. L⫺1 to 30,206 (23,107Ð 41,008) mg a.i. L⫺1. Tebufe-
nozide showed the highest toxicity with an LC50 of
3,383 (2,406 Ð5,499) mg a.i. L⫺1 and chlorßuazuron
showed relatively high toxicity with an LC50 of 4548
(3,310 Ð7,633) mg a.i. L⫺1. The toxicity of tebufenoz-
ide and chlorßuazuron was 8.9- and 6.5-fold, respec-
tively, higher than that of fufenozide. The order (from
February 2012 ZHAO ET AL.: RISK OF INSECTICIDES USED IN RICE ECOSYSTEM 95

Table 2. Median lethal concn of insecticides to T. japonicum

LC50 (95% CI) LC95 (95% CI) Risk

Insecticide Slope (SE) Df (␹2) Categoryb
mg a.i. L⫺1 mg a.i. L⫺1 quotienta
Neonicotinoids
Acetamiprid 1.82 (0.09) 25.39 (21.22Ð31.09) 4 (14.9) 203.6 (136.1Ð356.9) 0.89 1
Imidacloprid 1.58 (0.08) 95.48 (86.15Ð106.4) 4 (7.48) 1056.7 (816.2Ð1440.4) 0.31 1
Imidaclothiz 1.46 (0.07) 80.66 (71.58Ð92.10) 4 (2.82) 1075.7 (783.0Ð1584.2) 0.37 1
Nitenpyram 1.55 (0.08) 0.72 (0.65Ð0.82) 4 (3.99) 8.38 (6.29Ð11.85) 41.7 1
Thiacloprid 1.45 (0.08) 75.26 (65.95Ð87.50) 4 (6.13) 1034.8 (727.5Ð1599.5) 1.34 1
Thiamethoxam 1.78 (0.07) 0.40 (0.37Ð0.45) 4 (3.19) 3.41 (2.82Ð4.27) 54.9 2
Antibiotics
Abamectin 1.63 (0.09) 0.50 (0.36Ð0.81) 4 (30.9) 5.09 (2.36Ð20.54) 64.8 2
Emaectin benzoate 1.68 (0.08) 1.11 (1.00Ð1.22) 4 (9.86) 10.55 (8.56Ð13.51) 1.62 1
Ivermectin 1.61 (0.08) 0.93 (0.83Ð1.04) 4 (7.67) 9.75 (7.39Ð13.65) 4.89 1
Phenylpyrazoles
Butene-Þpronil 1.73 (0.08) 1.84 (1.46Ð2.45) 4 (21.8) 16.51 (9.66Ð37.64) 16.3 1
Ethiprole 1.65 (0.08) 16.23 (14.66Ð18.09) 4 (8.00) 160.6 (124.9Ð216.8) 3.70 1
Fipronil 1.76 (0.09) 0.92 (0.71Ð1.27) 4 (27.4) 7.90 (4.42Ð20.28) 24.5 1
IGRs
Chlorßuazuron 2.08 (0.11) 4548 (3310Ð7633) 4 (32.8) 27994 (14057Ð100008) 0.013 1
Fufenozide 1.82 (0.10) 30206 (23107Ð41008) 4 (11.2) 240315 (143528Ð360246) 1
Hexaßumuron 1.61 (0.10) 5650 (4228Ð8579) 4 (15.1) 59518 (30125Ð173147) 0.010 1
Tebufenozide 1.48 (0.08) 3383 (2406Ð5499) 4 (36.3) 43380 (19064Ð202167) 0.089 1
Pyrethroids
Cyhalothrin 1.90 (0.11) 11.09 (9.76Ð12.88) 4 (8.61) 81.24 (60.17Ð117.7) 4.73 1
Cypermethrin 1.68 (0.09) 21.15 (18.61Ð24.52) 4 (6.25) 201.1 (146.8Ð296.0) 4.26 1
Fenpropathrin 1.70 (0.08) 28.67 (25.85Ð32.10) 4 (10.3) 266.6 (206.0Ð363.4) 4.19 1
Lambda-cyhalthrin 1.95 (0.11) 2.60 (1.93Ð4.10) 4 (30.2) 18.11 (9.28Ð59.38) 11.5 1
Organophosphates
Chlorpyrifos 2.55 (0.13) 0.040 (0.032Ð0.057) 4 (34.2) 0.18 (0.11Ð0.43) 15,000 3
Fenitrothion 1.94 (0.09) 0.25 (0.23Ð0.27) 4 (5.62) 1.77 (1.47Ð2.20) 3,000 3
Phoxim 1.72 (0.09) 0.11 (0.086Ð0.17) 4 (27.3) 1.03 (0.53Ð3.21) 4,909 3
Profenofos 1.94 (0.10) 0.41 (0.33Ð0.53) 4 (18.1) 2.89 (1.80Ð5.82) 1,463 2
Triazophos 1.95 (0.10) 0.42 (0.34Ð0.57) 4 (21.0) 2.93 (1.76Ð6.48) 1,429 2
Carbamates
Carbosulfan 2.27 (0.10) 3.04 (2.12Ð3.58) 4 (14.9) 16.14 (11.93Ð24.33) 59.2 2
Carbaryl 1.69 (0.09) 0.48 (0.36Ð0.69) 4 (22.2) 4.51 (2.39Ð12.64) 2,656 3
Isoprocarb 1.83 (0.10) 0.49 (0.34Ð0.87) 4 (44.1) 3.85 (1.75Ð18.60) 1,224 2
Metolcarb 1.69 (0.08) 0.035 (0.029Ð0.044) 4 (15.7) 0.33 (0.21Ð0.65) 15,429 3
Promecarb 1.75 (0.09) 0.22 (0.18Ð0.29) 4 (15.9) 1.94 (1.16Ð4.09) 1,515 2

a
Risk quotient ⫽ Þeld recommended rate (g a.i. ha⫺1)/LC50 of T. japonicum (mg a.i. L⫺1).
b
Category: 1, safe; 2, slightly to moderately toxic; 3, dangerous.

high to low) of the toxicity for the four tested IGRs
was: tebufenozide, chlorßuazuron, hexaßumuron, and
fufenozide. The LC50 of the four pyrethroids ranged
from 2.60 (1.93Ð 4.10) mg a.i. L⫺1 to 28.67 (25.83Ð
32.10) mg a.i. L⫺1. Lambda-cyhalothrin showed the
highest toxicity to T. japonicum with an LC50 of 2.60
(1.93Ð 4.10) mg a.i. L⫺1, followed by cyhalthrin with
an LC50 of 11.09 (9.76 Ð12.88) mg a.i. L⫺1. In addi-
tion, fenpropathrin and cypermethrin exhibited low
toxicity with an LC50 value of 28.67 (25.85Ð32.10)
mg a.i. L⫺1 and 21.15 (18.61Ð24.52) mg a.i. L⫺1,
respectively.
Toxicity of Organophosphates and Carbamates to T.
japonicum. The LC50 of Þve selected organophos-
phates to T. japonicum ranged from 0.040 (0.032Ð
0.057) mg a.i. L⫺1 to 0.42 (0.34 Ð 0.57) mg a.i. L⫺1.
Chlorpyrifos showed the highest toxicity to T. japoni-
cum with an LC50 of 0.040 (0.032Ð 0.057) mg a.i. L⫺1,
followed by phoxim with an LC50 value of 0.11 (0.086 Ð
0.17) mg a.i. L⫺1. Triazophos and profenofos exhibited
low toxicity to the parasitoid with an LC50 value of 0.42
(0.34 Ð 0.57) mg a.i. L⫺1 and 0.41 (0.33Ð 0.53) mg a.i.
L⫺1, respectively. The LC50 of Þve tested carbamates
to T. japonicum were from 0.035 (0.029 Ð 0.044) mg a.i.
L⫺1 to 3.04 (2.12Ð3.58) mg a.i. L⫺1. Metolcarb showed
the highest toxicity to T. japonicum with an LC50 of
0.035 (0.029 Ð 0.044) mg a.i. L⫺1, followed by prome-
carb with an LC50 value of 0.22 (0.18 Ð 0.29) mg a.i. L⫺1.
Isoprocarb and carbaryl exhibited the similar toxicity
with an LC50 of 0.49 (0.34 Ð 0.87) mg a.i. L⫺1 and 0.48
(0.36 Ð 0.69) mg a.i. L⫺1, respectively. Carbosulfan ex-
hibited the lowest toxicity among the selected car-
bamates with an LC50 of 3.04 (2.12Ð3.58) mg a.i. L⫺1.
Risk Assessment. Risk quotient is an important mea-
sure of risk to beneÞcial insects under Þeld conditions
because it takes into consideration the Þeld recom-
mended dose. In the current study, risk quotient is
used to assess the ecological risk of insecticide sprays
on the parasitoid. All the tested insecticides were
classiÞed into different groups based on risk quotient
values (Table 2). The neonicotinoid thiamethoxam
was lightly to moderately toxic with a risk quotient of
56.25 to T. japonicum, whereas the other neonicoti-
noids (imidacoprid, acetamiprid, nitenpyram, imida-
clothiz, and thiacloprid) were safe with the risk quo-
tients ranging from 0.31 to 41.67. Similar to
thiamethoxam, abamectin was also slightly to moder-
ately toxic with a risk quotient of 66.12, while the other
96 JOURNAL OF ECONOMIC ENTOMOLOGY
two antibiotics (emamectin benzoate and ivermectin)
were safe with risk quotients of 1.65Ð 4.95. The phe-
nylpyrazoles, IGRs, and pyrethroids were also safe to
T. japonicum with risk quotients of 3.71Ð24.73, 0.003Ð
0.089, and 4.20 Ð11.58, respectively. Among organo-
phosphates tested, profenofos, and triazophos (with
the risk quotients of 1,500 and 1,463, respectively)
belonged to the category of slightly to moderately
toxic, while the other three organophosphates (chlor-
pyrifos, phoxim, and fenitrothion) were dangerous
with the risk quotients of 3,000 Ð15,789. Based on the
risk quotients, carbamates carbosulfan, isoprocarb,
and promecarb were classiÞed as slightly to moder-
ately toxic (with the risk quotients of 60.2Ð1515),
whereas metolcarb and carbaryl were ranked as dan-
gerous (with the risk quotients of 2,713Ð133,529) to
the egg parasitoid.
The Þeld recommended concentration should also
be taken into consideration when studying the safety
of insecticides to natural enemies. This is the concen-
tration that nontargets are also subjected to under the
Þeld conditions. A comparison between the LC95 of
the different compounds against T. japonicum and the
Þeld recommended concentration of these tested in-
secticides was shown in Fig. 1. LC95 of Þve organo-
phosphates and Þve carbamates was signiÞcantly
lower than their respective Þeld recommended con-
centration, indicating that these insecticides were
dangerous to wasps (Fig. 1). Neonicotinoids including
nitenpyram and thiamethoxam were also dangerous to
the parasitoid, when comparing the LC95 with their
respective Þeld recommended concentration. Niten-
pyram had an LC95 value of 8.38 (6.29 Ð11.85) mg a.i.
L⫺1, which is signiÞcantly lower than its Þeld recom-
mended concentration of 45 mg a.i. L⫺1. Thiame-
thoxam was also considered as a dangerous chemical
compound with an LC95 value of 3.41 (2.82Ð 4.27) mg
a.i. L⫺1 and Þeld recommended concentration of 33.75
mg a.i. L⫺1. However, the other neonicotinoids are
safe to the wasps. The antibiotic insecticides, abam-
ectin, phenylpyrazoles butane-Þpronil, and Þpronil,
had an LC95 of 5.09 (2.36 Ð20.54) mg a.i. L⫺1, 16.51
(9.66 Ð37.64) mg a.i. L⫺1 and 7.90 (4.42Ð20.28) mg a.i.
L⫺1, respectively, which was signiÞcantly lower than
their respective Þeld recommended concentration
(Fig. 1), indicating they are dangerous to the parasi-
toid. In contrast, the other antibiotics and phenylpyra-
zole were safe as judged by comparing their LC95 and
Þeld recommended concentration. For pyrethroids,
the LC95 of lambda-cyhalthrin was signiÞcantly lower
than its Þeld recommended rate, while the LC95 of
cyhalthrin was almost equal to its Þeld recommended
rate (Fig. 1), suggesting that cyhalthrin is safer than
cyhalthrin. The remaining pyrethroids cyperme-
thrin and fenpropathrin were safe to the wasps. The
LC95 of the four IGRs was substantially higher than
their respective Þeld recommended concentration,
indicating that these IGRs were likely the safest
chemicals (Fig. 1).
Vol. 105, no. 1
Discussion
Our data suggest that some of the tested insecticides
are potential candidates for replacing highly toxic or-
ganophosphate insecticides. These potential candi-
dates include some novel types of insecticides, for
example, neonicotinoids, IGRs, antibiotics, and phe-
nylpyrazoles with high efÞcacy against target insect
pests (He et al. 2008, Wang et al. 2008a, Cloyd and
Bethke 2011).
Ideally, the insecticides used in IPM programs
should be toxic to the target insect pests but not to
their natural enemies (Prabhaker et al. 2007, Bueno et
al. 2011). However, many chemical insecticides that
kill target insect pests may also kill their natural en-
emies because of their common physiology (Cloyd
and Bethke 2011). Thus, selection of appropriate in-
secticides that have less effect on the natural enemies
of the insects is critical in IPM of rice pests (Moura et
al. 2006). Our study demonstrated that different in-
secticides possessed signiÞcantly different risk to T.
japonicum, which in turn might provide more choices
for integration of biological control agents with chem-
ical compounds. For instance, the safe insecticides
may be applied when the parasitoid wasps are in high
density under Þeld conditions.
Adult parasitoids can be exposed directly to insec-
ticide spray droplets or indirectly to the residues re-
mained on the crop foliage when foraging or imbibing
contaminated water droplets, nectar or honeydew
(Longley and Jepson 1996). Immature parasitoids can
be also exposed to insecticides through the bodies of
their hosts (Hsiech and Allen 1986, Longley 1999).
However, several authors have reported that Tricho-
gramma spp. showed higher sensitivity to insecticides
at the adult stage than the egg, larval and pupal stages
because the eggshell of the host protected the imma-
ture stage of parasitoid (Consoli et al. 1998, Suh et al.
2000, Takada et al. 2001b). Therefore, the adult of T.
japonicum was used to evaluate the ecological risk of
insecticides in this study.
Neonicotinoids are among the most effective insec-
ticides for the control of phloem-feeding insect pests,
for example, aphids, whiteßies, planthoppers, and cer-
tain leaf-chewing beetles (Tomizawa and Casida 2003,
Jeschke and Nauen 2008). This extraordinary spec-
trum of efÞcacy, together with full exploitation of the
insect nicotinic acetylcholine receptor, plant system-
icity, long-lasting effect, and versatile applications, has
contributed to the unique success of this chemical
class (Tan et al. 2007, Elbert et al. 2008). However, the
use of neonicotinoids should be evaluated carefully in
IPM programs (Poletti et al. 2007). Results from this
study showed that both nitenpyram and thiame-
thoxam had high acute contact toxicity, and thiame-
thoxam had slightly to moderately toxic risk to T.
japonicum. This high toxicity of neonicotinoids to
Trichogramma spp. has been demonstrated in other
studies. For example, thiamethoxam has been shown
to be toxic to the egg parasitoids of Trichogramma
pretiosum Riley, Trichogramma chilonis Ishii, and
Trichogramma platneri Nagarkatti (Brunner et al.
February 2012 ZHAO ET AL.: RISK OF INSECTICIDES USED IN RICE ECOSYSTEM 97

Fig. 1. Comparison of LC95 of various insecticides to T. japonicum with their Þeld recommended concentrations. Y-axis
represents the recommended concentration and LC95 of each insecticides; X-axis represents each insecticide. (A) Recom-
mended concentration and LC95 of neonicotinoids. (B) Recommended concentration and LC95 of antibiotics and phe-
nylpyrazoles. (C) Recommended concentration and LC95 of IGRs. (D) Recommended concentration and LC95 of pyre-
throids. (E) Recommended concentration and LC95 of organophosphates. (F) Recommended concentration and LC95 of
carbamates.

2001, Williams and Price 2004, Preetha et al. 2009). Our previous studies. Imidacloprid was relatively safe to
results also showed that imidacloprid had relatively Trichogramma nr. Brassicae (Hewa-Kapuge et al.
low toxicity to T. japonicum, which was consistent with 2003). Abamectin, emamectin benzoate, and ivermec-
98 JOURNAL OF ECONOMIC ENTOMOLOGY
tin are a group of macrocyclic lactone antibiotic in-
secticides with broad-spectrum and high efÞciency
against target insect pests (Lastota and Dybas 1991).
Our results showed that all these three antibiotics had
higher acute toxicities (LC50 values) compared with
the neonicotinoids except for nitenpyram and thia-
methoxam. High toxicity of antibiotics to Tricho-
gramma spp. has been observed in other studies, in-
cluding toxicity of abamectin to Trichogramma
evanescens and T. pretiosum (Moura et al. 2006, Vianna
et al. 2009). Our study also indicated that emamectin
benzoate was safe to T. japonicum. Similar results were
reported with regard to the effects of emamectin ben-
zoate on T. chilonis and T. pretiosum, conÞrming its
compatibility with biological control strategies (Gi-
raddi and Gundannavar 2006). Therefore, considering
the high efÞcacy of neonicotinoids and antibiotics
against rice insect pests, thiamethoxam and abamectin
should be used with precaution to avoid direct contact
and minimize contamination of the food source for the
parasitoid.
Phenylpyrazole insecticides (buten-Þpronil, ethip-
role, and Þpronil) disrupt normal nerve function by
blocking the GABA-gated chloride channels, and kill-
ing of insects is dependent on direct contact or in-
gestion (Klis et al. 1991, Cole et al. 1993). Our data
indicated that Þpronil and buten-Þpronil had higher
contact toxicity than ethiprole, but they were safe to
T. japonicum. IGRs (chlorßuazuron, fufenozide,
hexaßumuron, and tebufenozide) inhibit chitin syn-
thesis and kill target insect slowly by disrupting exo-
skeleton formation after molting (Reynolds 1987, Sch-
neider et al. 2008). Because pests and their natural
enemies differ in terms of taxonomic order, IGRs are
generally able to speciÞcally kill the target insect pests
with minimal impact on the natural enemies (Cloyd
and Dickinson 2006, Carmo et al. 2010). Our study
demonstrated the selected IGR insecticides had low
toxicity and were safe for T. japonicum. Low toxicity
of IGRs to other species of Trichogramma spp., for
example, chlorßuazuron, lufenuron, and mild side-
effect of methoxyfenozide on Trichogramma den-
drolimi, T. cacoeciae, and T. pretiosum have been re-
ported previously (Hassan et al. 1998, Takada et al.
2001a, Bueno et al. 2008). Pyrethroids bind to a unique
receptor site and inhibit deactivation and inactivation,
leading to the prolonged opening of sodium channels.
The insecticidal effect of pyrethroids is achieved
through contact and stomach action (Bloomquist
1996, Narahashi 2000). Compared with organophos-
phates and carbamates, pyrethroids had low acute
toxicity and are safe to the adults of T. japonicum.
However, limited studies have been conducted to clar-
ify their toxic effect on the natural enemies (Croft and
Whalon 1982, Sterk et al. 1999). Because phenylpyra-
zoles, IGRs, and pyrethroids have higher efÞcacy
against many rice pests and are relatively safe to the
egg parasitoid, these insecticides are potential candi-
dates for rice IPM (He et al. 2008, Zheng et al. 2011).
However, it is important to bear in mind that our
bioassays evaluated dry-residue effects from contact
exposure. Ingestion of these insecticides by adults of
Vol. 105, no. 1
T. japonicum might occur in Þeld conditions if hon-
eydew or other sources of food are contaminated by
these chemical sprays. Therefore, the possibility and
frequency of food contamination must be further de-
termined.
Organophosphates and carbamates are toxic to in-
sects by virtue of their ability to inactivate acetylcho-
linesterase (Carmo et al. 2010). This type of poisoning
causes loss of the available acetylcholinesterase and
over-stimulations of organs by excessive acetylcholine
at the nerve endings. The affects of organophosphates
and carbamates on pests and natural enemies are sim-
ilar (Fukuto 1990). In this study, we showed that these
two classes of insecticides had high acute toxicity to T.
japonicum. Noxious results of organophosphates and
carbamates on beneÞcial arthropods (e.g., T. pretio-
sum and T. cacoeciae) have been reported in the lit-
erature (Hassan et al. 1988, Bueno et al. 2008). Gen-
erally, the organophosphate and carbamates are
among the cheapest insect-control products available
to the rice growers, thus they are often overused.
However, our results as well as previous studies
showed that these insecticides were not compatible
with natural enemies (Wang et al. 2008b, Carmo et al.
2010). Therefore, organophosphates and carbamates
should be limited or replaced by relatively safe plant
protection products in IPM programs.
A complete evaluation of an insecticide on natural
enemies should include not only its acute toxicity but
also its sublethal effects (Desneux et al. 2004, Hasseeb
et al. 2004). The sublethal effects on natural enemies
are typically chronic and not obvious (Suma et al.
2009, He et al. 2011). Sublethal effect can be expressed
as changes in life-history traits of insects, for example,
parasitism rate, longevity, egg viability, consumption
rate, or behavior (Desneux et al. 2007, Cloyd and
Bethke 2011). It is important to point out that the dry
Þlm residue method does not account for possible
inßuences of the plant surfaces (e.g., absorption) on
insecticide residues. Therefore, in addition to mortal-
ity, an assessment of the impact of an insecticide on
natural enemies together with information on the res-
idue activity of insecticides on plant surfaces under
Þeld conditions as well as their potential sub-lethal
effects are also important (Carmo et al. 2010).
Acknowledgments
The authors are very grateful to Yu Cheng Zhu (USDA-
ARS, Stoneville, MS) and the two anonymous referees for
their constructive and thoughtful comments that have
helped improve the manuscript further. The authors also
appreciate Xiao Hu and Weihua Yu (Zhejiang Academy of
Agricultural Sciences) for technical assistance. The research
was supported by the international cooperation fund and
national high-tech R & D program of Ministry of Science and
Technology of China (S2010GR0905 and 2011AA100806)
and the innovation project of Institute of Quality and Stan-
dard for Agro-products, Zhejiang Academy of Agricultural
Sciences.
February 2012 ZHAO ET AL.: RISK OF INSECTICIDES USED IN RICE ECOSYSTEM
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Received 5 August 2011; accepted 27 October 2011.