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Crop Protection 34 (2012) 76e82

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Crop Protection journal homepage: www.elsevier.com/locate/cropro

Susceptibility of adult Trichogramma nubilale (Hymenoptera: Trichogrammatidae) to selected insecticides with different modes of action Yanhua Wang, Ruixian Yu, Xueping Zhao*, Liping Chen, Changxing Wu, Tao Cang, 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, Zhejiang, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 12 September 2011 Received in revised form 13 December 2011 Accepted 15 December 2011

The parasitic wasp Trichogramma nubilale (Hymenoptera: Trichogrammatidae) is one of the most suitable parasitoids for controlling Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae). Although extensive toxicological tests have been carried out to elucidate the toxicities of insecticides to trichogrammatids, the acute toxicity risks of commonly used insecticides to T. nubilale are not well known. Among the 7 classes of tested chemicals, organophosphates and carbamates had the highest intrinsic toxicity to the parasitoid with LC50 values ranging from 0.081 (0.062e0.12) to 2.10 (1.23e3.47) and from 0.12 (0.11e0.14) to 0.95 (0.87e1.05) mg a.i. per liter, respectively. The phenylpyrazoles (with the exception of butene-fipronil), avermectins, neonicotinoids and pyrethroids induced intermediate toxicity responses with LC50 values ranging from 0.29 to 4.67, 2.36 to 11.27, 1.86 to 311.9, and 10.98e150.3 mg a.i. per liter, respectively. In contrast, insect growth regulators (IGRs) exhibited the least toxicity to the parasitoid with LC50 values ranging from 3452 (3114e3877) to 10,168 (8848e12,027) mg a.i. per liter. A risk quotient analysis indicated that neonicotinoids, avermectins, pyrethroids, IGRs and phenylpyrazoles (with the exception of butene-fipronil) were safe, but organophosphates and carbamates were slightly to moderately toxic or highly toxic to T. nubilale. This study provided informative data for implementing both biological and chemical control strategies in integrated pest management (IPM) of corn lepidopterans. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: Insecticide side effects Insecticide selectivity Biological control Integrated pest management

1. Introduction Asian corn borer, Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) is one of the most economically destructive insect pests of corn in Asia and causes substantial yield loss in most cornproducing countries (Nafus and Schreiner, 1991). Estimated average annual losses in China owing to this insect are 6e9 million tons, and the loss can be much greater in an outbreak year (McBeath and McBeath, 2010). Both chemical and biological controls are important for the management of insect pests in corn fields (Musser et al., 2006). However, the intensive use of insecticides has compromised their effectiveness, especially owing to the evolution of O. furnacalis resistance to the main chemicals available in the market (Lin et al., 2008). Consequently, many studies have been conducted to develop alternative biological and integrated control programs (Tipping and Burbutis, 1983; Gardner et al., 2011).

* Corresponding author. State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Quality and Standard for Agroproducts, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, Zhejinag, China. Tel.: þ86 571 86404229; fax: þ86 571 86402186. E-mail address: [email protected] (X. Zhao). 0261-2194/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.12.007

Ideally, integrated pest management (IPM) programs require insecticides to be effective against target species and simultaneously be relatively harmless to natural enemies (Preetha et al., 2010b). However, many natural enemies often exhibit greater susceptibility to insecticides than do their prey or hosts (Bacci et al., 2007; Preetha et al., 2010b). This is caused by a variety of factors, including their active searching behavior, lower detoxification capacity, lower genetic variation and food limitation (Mullin et al., 1982). Selective insecticides are primarily harmful to insect pests but relatively harmless to natural enemies, and their use may increase the effectiveness of biological control (Cônsoli et al., 2001; Bastos et al., 2006). Therefore, the use of selective insecticides enhances the conservation of natural enemies and reduces the frequency of insecticide applications (Musser et al., 2006; Gardner et al., 2011). Trichogramma spp. have potential as biological agents for pestsuppression in corn fields, because these egg parasitoids kill their hosts before they can damage crops (Tipping and Burbutis, 1983; Wang et al., 1999; Gardner et al., 2011). Moreover, mass rearing of Trichogramma spp. is economically feasible (Parra, 2010). Studies show that Trichogramma nubilale Ertle and Davis (Hymenoptera: Trichogrammatidae) is effective at controlling lepidopteran corn pests (Wang et al., 1999). However, the use of insecticides is still

Y. Wang et al. / Crop Protection 34 (2012) 76e82

necessary within the existing agricultural system because it is quick, efficient, easy to use and cost effective (Hassan et al., 1998; Cônsoli et al., 1998). Although extensive toxicological tests have been carried out to elucidate the toxicities of various insecticides to trichogrammatids (Hassan et al., 1998; Varma and Singh, 1987; Cônsoli et al., 1998, 2001; Suh et al., 2000; Grützmacher et al., 2004; Youssef et al., 2004; Bastos et al., 2006; Saber, 2011), little is known about the assessment of toxicity risk of commonly used insecticides against O. furnacalis on the parasitic wasp T. nubilale. The objective of this study was to compare the relative toxicities of selected insecticides with different modes of action to T. nubilale and provide pest managers with specific informations for implementing compatible biological and chemical controls for corn lepidopteran IPM. 2. Materials and methods 2.1. Insects T. nubilale was maintained in the eggs of the rice moth, Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) as host. The host was obtained from the Guangdong Entomological Institute (Guangzhou, China) and was fed corn flour. The host eggs were stuck to gluecovered paper cards (6.5  1.5 cm) and killed with UV radiation before they were exposed to parasitoids. After exposure to adult wasps for 24 h, the parasitized eggs were transferred to new containers (glass tubes; height  diameter, 8.0 cm  1.5 cm) and

77

kept in chambers until the emergence of the adults. All insects were maintained at 25 C  1  C and 70%  10% relative humidity with a 14:10 h (L:D) photoperiod. Adult wasps that emerged from the hosts were maintained in a glass tube containing a small piece of thick paper that had been previously dipped in a 10% honey solution. Adult wasps, 24e48 h after emergence, were used in the experiments. 2.2. Insecticides Thirty insecticides commonly used for corn insect pests control were evaluated in the present study (Table 1). The active ingredients of these insecticides rather than their commercial formulations were used, because the aim of this study was to document the acute effects of the active substances on mortality of T. nubilale while excluding the influence of adjuvants in commercial products. Technical-grade insecticides were dissolved with analytical-grade acetone to obtain the desired concentrations that were directly used for contact toxicity studies. A spray volume of 675 L per ha was used as a comparison between recommended field concentrations of insecticides and acute toxicity. 2.3. Acute contact toxicity A modified slightly dry film residue method was used to assess the toxicities of insecticides on T. nubilale (Wang et al., 2008; Preetha et al., 2009). Preliminary studies were performed to

Table 1 Detailed information of insecticides used in this study. Insecticide Neonicotinoids Acetamiprid Imidacloprid Imidaclothiz Nitenpyram Thiacloprid Thiamethoxam Avermectins Abamectin Emamectin benzoate Ivermectin Phenylpyrazoles Butene-fipronil Ethiprole Fipronil Insect Growth Regulators Chlorfluazuron Fufenozide Hexaflumuron Tebufenozide Pyrethroids Cyhalothrin Cypermethrin Fenpropathrin Lambda-cyhalothrin Organophosphates Chlorpyrifos Fenitrothion Phoxim Profenofos Triazophos Carbamates Carbosulfan Carbaryl Isoprocarb Metolcarb Promecarb HTCa, The highest test concentrations.

Technical grade (a.i.)

Manufacturer

HTCa (mg a.i. per liter)

97% 95.3% 95% 95% 97.75% 97.7%

Jiangsu Yangnong Chemical Co., Ltd. Jiangsu Changlong Chemical Co., Ltd. Jiangsu Yangnong Chemical Co., Ltd. Jiangsu Nantong Agro-chemical Co., Ltd. Tianjing Xingguang Chemical Co., Ltd. Swiss Syngenta Crop Protection Inc.

62.5 1000 250 12.5 200 6.25

93% B1a 89% B1a 90.73% B1

Hebei Weiyuan Biochemical Co., Ltd. Hebei Weiyuan Biochemical Co., Ltd. Zhejiang Haizheng Chemical Co., Ltd.

10.0 25.0 6.25

90% 96% 87%

Daliang Ruize Agro-chemical Co., Ltd. Swiss Syngenta Crop Protection Inc. Hangzhou Bayer Crop Science Ltd.

0.02 20.0 0.78

85.7% 97% 97.1% 92%

Jiangsu Yangnong Chemical Co., Ltd. Jiangsu Changlong Chemical Co., Ltd. Daliang Ruize Agro-chemical Co., Ltd. Jiangsu Baoling Chemical Co., Ltd.

20000 20000 20000 10000

95% 93.2% 94% 98%

Jiangsu Yangnong Chemical Co., Ltd. Nanjing Red-sun Chemical Co., Ltd. Nanjing Red-sun Chemical Co., Ltd. Jiangsu Changlong Chemical Co., Ltd.

31.25 62.5 400 50

97% 95% 89% 90.8% 80.5%

Jiangsu Nantong Agro-chemical Co., Ltd. Huangyan Yongning Chemical Co., Ltd. Jiangsu Baoling Agro-chemical Co., Ltd. Zhejiang Yongnong Chemical Co., Ltd. Hubei Xianlong Agro-chemical Co., Ltd.

0.20 12.5 0.40 0.40 6.25

88.89% 94% 99.7% 96% 98%

Suzhou Fumeishi Chemical Co., Ltd. Hunan Haili Chemical Co., Ltd. Jiangsu Changlong Chemical Co., Ltd. Nanjing Red-sun Chemical Co., Ltd. Jiangsu Yangnong Chemical Co., Ltd.

4.00 25.0 0.40 1.56 0.78

78

Y. Wang et al. / Crop Protection 34 (2012) 76e82

identify the concentrations that caused 10e90% parasitoid mortality. To establish the concentrationemortality relationship, adult parasitoids were exposed to 6 concentrations with 2-fold increases in geometric ratio. Acetone solutions of insecticides were prepared in glass tubes (height  diameter, 8.0 cm  2.0 cm; internal surface area, 53.4 cm2). Pure acetone was used as a control. To obtain a homogeneous deposition, we introduced 500 ml of solution, which completely covered the internal surface of the tube. The tube was then rotated manually until no more droplets were observed on the glass wall. The tubes were allowed to stand for about 1 h at room temperature to ensure the complete evaporation of acetone before the adult parasitoids were introduced. Inasmuch as the internal surface of the tubes and volume of the solution were fixed, we expressed the quantity of the insecticide residue per surface area. Adult wasps (n ¼ 80e100) were placed in each tube, which contained a small plastic strip with 2 drops of honey. The tubes were covered with a fine nylon mesh secured with rubber to allow air circulation; they were maintained at 25 C  1  C and 70%  10% relative humidity with a 14:10 h (L:D) photoperiod. Three replicates were conducted for each dose and each insecticide. After 1 h of exposure, the wasps were transferred into a clean insecticide-free tube that contained a honey solution. After 24 h, dead parasitoids were counted. Wasps, showing no movement after a probing, were counted as dead. 2.4. 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 had also been used to assess the safety of pesticides to the egg parasitoid, Trichogramma chilonis Ishii (Hassan et al., 1998). Risk quotients for the insecticides were calculated from the LC50 values 24 h after treatment according to the following formula: risk quotient ¼ recommended field rate (g a.i. per ha)/LC50 of beneficial insect (mg a.i. per liter). A risk quotient value < 50 for a pesticide was considered safe; 50e2500, slightly to moderately toxic; and >2500, dangerously toxic (Preetha et al., 2010b). 2.5. Statistical analysis The percentage mortality of each insecticide to T. nubilale was corrected using the Abbott’s formula (Abbott, 1925). The data were then subjected to probit analysis using the EPA Probit Analysis Program (version 1.5) and the log concentration probit mortality line (Finney, 1971). A significant level of mean separation (P < 0.05) was based on non-overlap between the 95% confidence intervals of 2 LC50 values. 3. Results 3.1. Contact toxicity of insecticides to T. nubilale The toxicities of 30 insecticides from 7 chemical groups to the parasitoid T. nubilale are summarized in Table 2. The various insecticides exhibited a wide range of contact toxicities. In addition, different insecticides within the same chemical class showed different toxicities to the egg parasitoid. The LC50 values of selected insecticides to T. nubilale ranged from 0.0068 (0.0061e0.0076) to 10,168 (8848e12,027) mg a.i. per liter. The order of toxicity (highelow) for the 30 insecticides was as follows: butenefipronil > chlorpyrifos, isoprocarb  phoxim, profenofos  fipronil, promecarb, metolcarb > carbaryl, carbosulfan > triazophos, thiamethoxam, fenitrothion, ivermectin > abamectin, nitenpyram, ethiprole  cyhalothrin, emamectin benzoate, lambda-cyhalothrin

> acetamiprid, cypermethrin > thiacloprid > imidaclothiz > fenpropathrin > imidacloprid > tebufenozide > chlorfluazuron, hexaflumuron, fufenozide (LC50 values with overlapping the 95% confidence intervals were classified as having the same level of toxicity). Among the tested insecticides, the contact toxicity of phenylpyrazole insecticide butene-fipronil was the highest with a LC50 of only 0.0068 (0.0061e0.0076) mg a.i. per liter; meanwhile, the insect growth regulator (IGR) insecticide fufenozide had the lowest toxicity with a LC50 of 10,168 (8848e12,027) mg a.i. per liter. Therefore, butene-fipronil was found to be 1.50  106 times more toxic than fufenozide to T. nubilale according to their LC50 values. Overall, organophosphates, carbamates and phenylpyrazoles (with the exception of ethiprole) exhibited the highest intrinsic acute toxicities, whereas the IGRs exhibited the lowest intrinsic toxicities toT. nubilale. 3.1.1. Neonicotinoids The LC50 of neonicotinoids to T. nubilale ranged from 1.86 (1.69e2.07) to 311.9 (280.6e350.7) mg a.i. per liter (Table 2). Among the 6 neonicotinoids tested, thiamethoxam showed the highest toxicity to T. nubilale with a LC50 of 1.86 (1.69e2.07) mg a.i. per liter, followed by nitenpyram with a LC50 of 4.37 (3.92e4.94) mg a.i. per liter. Based on LC50 values, thiamethoxam was found to be 168 and 40.5 times more toxic than imidacloprid and thiacloprid, respectively. The order of toxicity (highelow) for the 6 neonicotinoids was as follows: thiamethoxam, nitenpyram > acetamiprid > thiacloprid > imidaclothiz > imidacloprid (Table 2). 3.1.2. Avermectins and phenylpyrazoles The LC50 of avermectins to T. nubilale ranged from 2.36 (2.11e2.68) to 11.27 (9.91e13.09) mg a.i. per liter (Table 2). Among the 3 avermectins tested, ivermectin exhibited the highest intrinsic toxicity with a LC50 of 2.36 (2.11e2.68) mg a.i. per liter, followed by abamectin and emamectin benzoate. The LC50 of phenylpyrazoles ranged from 0.0068 (0.0061e0.0076) to 4.67 (3.03e8.74) mg a.i. per liter. The LC50 values of butene-fipronil and fipronil were 0.0068 (0.0061e0.0076) and 0.29 (0.23e0.39) mg a.i. per liter, respectively, which were lower than the LC50 value of ethiprole (4.67 (3.03e8.74) mg a.i. per liter). Based on their LC50 values, butene-fipronil and fipronil are 687 and 42.6 times more toxic than ethiprole, respectively. The order of LC50 (highelow) for the 3 phenylpyrazole insecticides was as follows: butene-fipronil > fipronil > ethiprole (Table 2). 3.1.3. IGRs and pyrethroids The LC50 of IGRs to T. nubilale ranged from 3452 (3114e3877) to 10,168 (8848e12,027) mg a.i. per liter. Among the 4 IGRs evaluated, tebufenozide had the highest toxicity with a LC50 of 3452 (3114e3877) mg a.i. per liter, followed by chlorfluazuron and hexaflumuron with LC50 values of 7533 (6114e9788) and 9672 (8543e11,086) mg a.i. per liter, respectively; while fufenozide exhibited the lowest toxicity to the parasitoid. The LC50 values of the 4 evaluated pyrethroids ranged from 10.98 (8.33e16.07) to 150.3 (133.8e171.5) mg a.i. per liter. Cyhalothrin and lambdacyhalothrin showed the greatest toxicity to T. nubilale with LC50 values of 10.98 (8.33e16.07) and 13.69 (12.37e15.28) mg a.i. per liter, respectively, followed by cypermethrin with a LC50 of 19.48 (17.52e21.90) mg a.i. per liter. In addition, fenpropathrin exhibited the least toxicity among 4 pyrethroids tested with a LC50 value of 150.3 (133.8e171.5) mg a.i. per liter. The order of toxicity (highelow) of the 4 pyrethroid insecticides was as follows: cyhalothrin, lambda-cyhalothrin > cypermethrin > fenpropathrin. 3.1.4. Organophosphates and carbamates The LC50 of the 5 selected organophosphates to T. nubilale ranged from 0.081 (0.062e0.12) to 2.10 (1.23e3.47) mg a.i. per liter. Chlorpyrifos exhibited the highest toxicity to T. nubilale with a LC50

Y. Wang et al. / Crop Protection 34 (2012) 76e82

79

Table 2 Median lethal concentrations of insecticides to Trichogramma nubilale. Insecticide Neonicotinoids Acetamiprid Imidacloprid Imidaclothiz Nitenpyram Thiacloprid Thiamethoxam Avermectins Abamectin Emamectin benzoate Ivermectin Phenylpyrazoles Butene-fipronil Ethiprole Fipronil Insect Growth Regulators Chlorfluazuron Fufenozide Hexaflumuron Tebufenozide Pyrethroids Cyhalothrin Cypermethrin Fenpropathrin Lambda-cyhalothrin Organophosphates Chlorpyrifos Fenitrothion Phoxim Profenofos Triazophos Carbamates Carbosulfan Carbaryl Isoprocarb Metolcarb Promecarb

Slope (SE)

LC50 (95% CI) mg a.i. per liter

Df (x2)

LC95 (95% CI) mg a.i. per liter

RQa

Categoryb

1.75 1.76 1.77 1.92 1.81 1.92

19.24 (17.31e21.63) 311.9 (280.6e350.7) 75.27 (67.86e84.37) 4.37 (3.92e4.94) 56.73 (51.32e63.27) 1.86 (1.69e2.07)

4 4 4 4 4 4

167.9 (129.3e230.3) 2675 (2059e3670) 636.5 (493.2e865.2) 31.37 (24.23e48.90) 461.2 (362.0e616.3) 13.35 (10.55e37.70)

1.17 0.096 0.40 6.86 1.78 12.1

1 1 1 1 1 1

1.93 (0.10) 1.88 (0.10) 2.04 (0.11)

3.57 (2.90e4.66) 11.27 (9.91e13.09) 2.36 (2.11e2.68)

4 (15.71) 4 (6.94) 4 (9.99)

25.42 (15.77e47.38) 84.54 (62.55e122.50) 15.15 (11.68e20.80)

9.08 0.16 1.91

1 1 1

2.08 (0.10) 2.49 (0.11) 2.05 (0.11)

0.0068 (0.0061e0.0076) 4.67 (3.03e8.74) 0.29 (0.23e0.39)

4 (10.62) 4 (132.3) 4 (20.14)

0.0419 (0.0331e0.0555) 21.35 (10.58e151.23) 1.82 (1.09e4.01)

4412 12.8 77.6

3 1 1

1.41 2.11 1.86 2.06

(0.10) (0.12) (0.11) (0.10)

7533 (6114e9788) 10168 (8848e12027) 9672 (8543e11086) 3452 (3114e3877)

4 4 4 4

(3.29) (12.9) (11.3) (1.79)

111205 (67194e214167) 61154 (44953e89889) 51197 (40846e85741) 21616 (16992e28905)

0.0080 0.0089 0.0058 0.087

1 1 1 1

1.77 1.72 1.74 1.70

(0.09) (0.09) (0.09) (0.08)

10.98 19.48 150.3 13.69

4 4 4 4

(27.60) (8.22) (7.28) (12.8)

93.25 (49.39e270.8) 176.8 (135.9e242.5) 1327.5 (997.5e1877.8) 127.6 (99.2e172.5)

4.78 4.62 0.80 2.19

1 1 1 1

2.19 1.73 1.69 1.69 1.53

(0.12) (0.09) (0.09) (0.09) (0.08)

0.081 (0.062e0.12) 2.10 (1.23e3.47) 0.14 (0.08e0.16) 0.18 (0.13e0.32) 1.81 (1.29e2.85)

4 4 4 4 4

(27.6) (3.73) (8.09) (31.2) (41.6)

0.45 (0.25e1.24) 34.74 (26.73e47.61) 1.35 (1.01e1.94) 1.73 (0.78e7.50) 21.65 (9.86e96.02)

7407 57.1 3857 3333 331.5

3 2 3 3 2

1.85 2.04 1.86 1.66 2.11

(0.09) (0.10) (0.09) (0.09) (0.11)

0.95 0.89 0.12 0.53 0.32

4 4 4 4 4

(4.90) (8.77) (2.17) (20.97) (24.85)

7.40 5.71 0.95 5.20 1.91

189.5 1433 5000 1019 1042

2 2 3 2 2

(0.09) (0.09) (0.09) (0.10) (0.09) (0.09)

(8.33e16.07) (17.52e21.90) (133.8e171.5) (12.37e15.28)

(0.87e1.05) (0.79e1.01) (0.11e0.14) (0.42e0.74) (0.24e0.47)

(1.92) (10.23) (2.06) (4.81) (6.24) (4.31)

(5.97e9.55) (4.60e7.40) (0.74e1.28) (2.87e13.22) (1.07e5.03)

RQa, Risk quotient ¼ recommended field rate (g a.i. per ha)/LC50 of T. nubilale (mg a.i. per liter). Categoryb, 1: safe; 2: slightly to moderately toxic; 3: dangerously toxic.

of 0.081 (0.062e0.12) mg a.i. per liter, followed by phoxim and profenofos with LC50 values of 0.14 (0.08e0.16) and 0.18 (0.13e0.32) mg a.i. per liter, respectively. Triazophos and fenitrothion exhibited the least toxicity to the parasitoid with LC50 values of 1.81 (1.29e2.85) and 2.10 (1.23e3.47) mg a.i. per liter, respectively. The order of toxicity (highelow) to the parasitoid according to LC50 values was as follows: chlorpyrifos > phoxim, profenofos > triazophos, fenitrothion. The LC50 of the 5 tested carbamates to T. nubilale ranged from 0.12 (0.11e0.14) to 0.95 (0.87e1.05) mg a.i. per liter. Isoprocarb exhibited the greatest toxicity with a LC50 of 0.12 (0.11e0.14) mg a.i. per liter, followed by promecarb and metolcarb with LC50 values of 0.32 (0.24e0.47) and 0.53 (0.42e0.74) mg a.i. per liter, respectively; carbaryl and carbosulfan exhibited the least toxicities to T. nubilale among the 4 carbamates tested. The order of toxicity (highelow) of the 5 selected carbamates was as follows: isoprocarb > promecarb, metolcarb > carbaryl, carbosulfan. 3.2. Risk assessment The tested insecticides were classified into different groups on the basis of risk quotient values (Table 2). All tested neonicotinoids, avermectins, IGRs and pyrethroids were safe for T. nubilale with risk quotients of 0.096e12.1, 0.16e9.08, 0.0058e0.087, and 0.80e4.78, respectively. Among the phenylpyrazole insecticides, ethiprole and fipronil were also safe with risk quotients of 12.8 and 77.6, respectively. However, butene-fipronil was considered dangerous

to T. nubilale with a risk quotient of 4412. Among the tested organophosphates, fenitrothion and triazophos (risk quotients, 57.1 and 331.5, respectively) were slightly to moderately toxic, whereas chlorpyrifos, phoxim and profenofos were dangerously toxic to T. nubilale (risk quotients, 3333e7407). Among the carbamate insecticides, isoprocarb was dangerously toxic (risk quotient, 5000), whereas carbosulfan, carbaryl, metolcarb and promecarb were slightly to moderately toxic to the parasitoid (risk quotients, 189.5e1433). The recommended field concentration should also be taken into consideration when studying the safety of insecticides to natural enemies; this is the concentration to which non-targets are subjected to under field conditions (Preetha et al., 2009). A comparison between the LC95 of the different compounds against T. nubilale and the recommended field concentration of these tested insecticides is shown in Fig. 1. The LC95 values of 3 phenylpyrazoles, 5 organophosphates and 5 carbamates were significantly lower than their respective recommended field concentrations, indicating that these insecticides would be harmful to T. nubilale (Fig. 1). In contrast, the LC95 values of the 4 IGRs were distinctly higher than their respective recommended field concentrations, indicating that these IGRs are acutely harmless to the parasitoid. Nitenpyram and thiamethoxam had LC95 values of 31.37 (24.23e48.90) and 13.35 (10.55e37.70) mg a.i.$L1, respectively, which were of the same rank as their respective recommended field concentrations of 45 and 33.75 mg a.i.$L1. Thus, these 2 neonicotinoids are harmful to T. nubilale. Similar to nitenpyram and thiamethoxam, abamectin

Y. Wang et al. / Crop Protection 34 (2012) 76e82

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90

ur

180000 160000 140000 120000 100000 80000 60000 40000 20000 0

D

rin

Field recommended rate

Concentration (mg a.i. per liter)

LC95 of T. nubilale

n

Concentration (mg a.i. per liter)

C

E

Ogranophosphates 1200

LC95 of T. nubilale Field recommended rate

1125

F

1000

900

900

Carbamates

LC95 of T. nubilale Field recommended rate

900

50

600

400

200

LC95 of T. nubilale 40 30 20 10 0 Chlorpyrifos

Fenitrothion

Phoxim

Profenofos

1912.5

2000

1500

900

1000

500

Triazophos

270

Concentration (mg a.i.per liter)

Concentration (mg a.i. per liter)

800

Concentration (mg a.i.per liter)

Concentration (mg a.i.per liter)

2500

810

10 8 6 4 2 0

499.95

LC95 of T. nubilale

Carbosulfan

0

810

Carbaryl

Isoprocarb

Metolcarb

Promecarb

0

Chlorpyrifos

Fenitrothion

Phoxim

Profenofos

Triazophos

Carbosulfan

Carbaryl

Isoprocarb

Fig. 1. Comparison of LC95 values of various insecticides to Trichogramma nubilale with their field recommended rates.

Metolcarb

Promecarb

Y. Wang et al. / Crop Protection 34 (2012) 76e82

was also harmful to T. nubilale with a LC95 value of 25.42 (15.77e47.38) mg a.i.$L1 compared with its recommended field concentration of 48.6 mg a.i.$L1. For the tested pyrethroids, cyhalothrin had a LC95 value of 93.25 (49.39e270.8) mg a.i.$L1, which is of the same rank as its recommended field concentration of 78.75 mg a.i.$L1, indicating that this insecticide is harmful to T. nubilale. In contrast, the other neonicotinoids (acetamiprid, imidacloprid, imidaclothiz and thiacloprid), avermectins (emamectin benzoate and ivermectin) and pyrethroids (cypermethrin, fenpropathrin and lambda-cyhalothrin) were harmless to T. nubilale when their LC95 and recommended field concentrations were compared. 4. Discussion Adult parasitoids can be exposed directly to insecticides in the form of droplets or indirectly to the residues remaining on the crop foliage when foraging or imbibing contaminated water droplets, nectar or dew (Longley and Jepson, 1996). A highly toxic insecticide applied at a low rate may cause less mortality than a less-toxic insecticide applied at a higher rate under field conditions (Youn et al., 2003). For this reason, in addition to determine LC50 values, assessments of the impact of an insecticide on natural enemies should include its recommended field rate (Preetha et al., 2009, 2010b). Therefore, we evaluated the acute toxicity and risk quotients of commonly used insecticides to T. nubilale in the present study. Neonicotinoids were introduced into the market in the early 1990s; today, they are one of the most important chemical groups used to control sucking insects as well as certain leaf-chewing insects (Jeschke and Nauen, 2008). However, the use of neonicotinoids should be evaluated carefully in IPM programs (Cloyd and Bethke, 2011). The results of this study show that thiamethoxam and nitenpyram were harmful to T. nubilale. Similar results are reported for some Trichogramma species in the other literatures, i.e., thiamethoxam has been shown to be toxic to T. chilonis, and Trichogramma platneri Nagarkatti (Brunner et al., 2001; Preetha et al., 2009). In contrast, the other neonicotinoids showed relatively low acute toxicities and were not harmful to the egg parasitoid on the basis of the risk quotients, which are consistent with values obtained in previous studies. Imidacloprid is relatively nontoxic to Trichogramma japonicum Gahan (Zhang et al., 1997). However, some exceptions are reported in the case of Trichogramma spp., such as imidacloprid, which was found to be harmful to T. chilonis, Trichogramma Cacoeciae Marchal, and Trichogramma brassicae Westwood (Preetha et al., 2010a; Saber, 2011). Avermectins are a group of high-efficiency macrocyclic lactones used against target insect pests (Lasota and Dybas, 1991). Abamectin was harmful to T. nubilale, because its LC95 to the egg parasitoid was lower than its recommended field concentration. These results are similar to the results of other studies. For example, abamectin has harmful effects on parasitoids such as Trichogramma cacoeciae and Encarsia sp. (Hassan et al., 1998; Bacci et al., 2007). Our study also indicates that emamectin benzoate and ivermectin are harmless to T. nubilale. Emamectin benzoate is reported to have similar effects on T. chilonis and Trichogramma Pretiosum Riley, confirming its compatibility with biological control agents (Giraddi and Gundannavar, 2006). Therefore, considering the high efficacy of neonicotinoids and avermectins against corn insect pests, nitenpyram, thiamethoxam, and abamectin should be used cautiously to avoid direct contact with the parasitoid and minimize contamination of its food source. Phenylpyrazole insecticides disrupt normal nerve function by blocking gamma-aminobutyric acid-gated chloride channels, and they can kill insects via direct contact or ingestion (Cole et al., 1993). Adult T. nubilale were highly susceptible to phenylpyrazoles through residual exposure,

81

probably reflecting a lower metabolization of these compounds in this parasitoid. The IGRs chlorfluazuron, fufenozide, hexaflumuron, and tebufenozide were selective for adult T. nubilale. The 4 IGRs mentioned above were the safest insecticides and had the least intrinsic acute toxicities to T. nubilale compared with all other insecticides tested in this study. These chemicals inhibit chitin synthesis and kill target insects slowly by disturbing exoskeleton formation after molting (Schneider et al., 2008). IGRs are usually regarded as less harmful to beneficial insects than other chemical groups, although some negative side effects are reported (Cônsoli et al., 1998). In the literature, IGRs selectivity, including the effects of diflubenzuron, chlorfluazuron, lufenuron and methoxyfenozide to Trichogramma dendrolimi Matsumura, T. cacoeciae, and T. Pretiosum, is reported to be harmless or have mild side effects only (Hassan et al., 1998; Takada et al., 2001). Although IGRs were harmless or only slightly harmful to T. nubilale, they may have effects on later stages, because they interfere with the molting mechanism (Wang et al., 2008). In addition, our bioassays evaluated only dry-residue effects from contact exposure, while ingestion of these insecticides by adult T. nubilale might occur under natural conditions if dew or other food sources are contaminated by chemical sprays (Carmo et al., 2010). However, this was not investigated in the present study. Therefore, further testing is needed before the compatibility of IGRs with IPM can be assessed. Moreover, the influence of IGRs on parasitoid physiology and behavior needs also to be investigated. Pyrethroids bind to a unique receptor site and inhibit deactivation and inactivation, resulting in prolonged opening of sodium channels; they are highly insecticidal via contact and stomach action (Bloomquist, 1996). These compounds are largely used for the control of agricultural pests; 40% of their targeted insects are lepidopterans followed by sucking insects and coleopterans (Desneux et al., 2004a, 2004b). However, various insecticides in this group are reported to be harmful to natural enemies (Desneux et al., 2004a; Bayram et al., 2010b). For example, gammacyhalothrin and bifenthrin are harmful to adult Telenomus remus Nixon (Delpuech et al., 2001; Carmo et al., 2010). Despite this, some exceptions are reported in the case of the parasitic wasp Anagrus nilaparvata Pang et Wang (Wang et al., 2008). This is consistent with experimental results reported here in that cypermethrin, fenpropathrin and lambda-cyhalothrin are harmless to adult T. nubilale. Organophosphates and carbamates are toxic to insects because of their ability to inactivate acetylcholinesterase (Fukuto, 1990). The high toxicity of these 2 classes of compounds to natural enemies is possibly associated with their low molecular masses (Bacci et al., 2007). Substances with low molecular masses have higher capacity to penetrate the cuticle of an insect (Stock and Holloway, 1993). Organophosphates and carbamates are two classes of insecticides that are well known for their harmful effects to the agroecosystem (Cônsoli et al., 1998; Delpuech and Meyet, 2003; Youssef et al., 2004; Bastos et al., 2006). Moreover, our results and the results of previous studies show that these insecticides are not compatible with natural enemies (Suh et al., 2000; Brunner et al., 2001; Takada et al., 2001; Preetha et al., 2009). Therefore, organophosphates and carbamates should be replaced with relatively safe plant-protection products in IPM programs where possible. This study yielded important results that will help pest managers to choose the best insecticides to be applied, because products with the lowest impact on biological control agents are the most appropriate for use in IPM programs. In addition to evaluating acute toxicity of an insecticide, the sub-lethal and chronic effects of the insecticide should be evaluated; the latter effects are often ignored, because they are not as distinct as acute toxic effects (Delpuech and Meyet, 2003; Desneux et al., 2004b,

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2007; Bayram et al., 2010a). It is important to point out that the present study was carried out under laboratory conditions in which the parasitoids were subjected to the highest possible insecticide pressure. Insecticides might have less negative impact under field conditions, because biological control agents can take advantage of natural shelters and avoid treated areas. Moreover, sunlight degradation plays an important role in the field by decreasing the impact of insecticides on the parasitoids observed in the laboratory. In addition, the dry film residue method does not account for possible influences that plant surfaces may have on insecticide residues, such as absorption. Therefore, further work is needed to evaluate the residual toxicity of these insecticides on plant surfaces as well as their potential sub-lethal effects. Acknowledgments The authors thank Xiao Hu and Weihua Yu (Zhejiang Academy of Agricultural Sciences) for assistance with the experiments. This research was funded by the International Cooperation Fund and the National High-Tech R&D Program of the Ministry of Science and Technology of China (Grant Nos. S2010GR0905 and 2011AA100806) and by the Innovation Project of the Institute of Quality and Standard for Agro-Products of the Zhejiang Academy of Agricultural Sciences. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265e267. Bacci, L., Crespo, A.L.B., Galvan, T.L., Pereira, E.J.G., Picanco, M.C., Silva, G.A., Chediak, M., 2007. Toxicity of insecticides to the sweetpotato whitefly (Hemiptera: Aleyrodidae) and its natural enemies. Pest Manag. Sci. 63, 699e706. Bastos, C.C., Almeida, R.P., Suinaga, F.A., 2006. Selectivity of pesticides used on cotton (Gossypium hirsutum) to Trichogramma pretiosum reared on two laboratory-reared hosts. Pest Manag. Sci. 62, 91e98. Bayram, A., Salerno, G., Onofri, A., Conti, E., 2010a. Sub-lethal effects of two pyrethroids on biological parameters and behavioral responses to host cues in the egg parasitoid Telenomus busseolae. Biol. Control 53, 153e160. Bayram, A., Salerno, G., Onofri, A., Conti, E., 2010b. Lethal and sublethal effects of preimaginal treatments with two pyrethroids on the life history of the egg parasitoid Telenomus busseolae. BioControl 55, 697e710. Bloomquist, J.R., 1996. Ion channels as targets for insecticides. Annu. Rev. Entomol. 41, 163e190. Brunner, J.F., Dunley, J.E., Doerr, M.D., Beers, E.H., 2001. Effect of pesticides on Colpoclypeus florus (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae), parasitoids of leafrollers in Washington. J. Econ. Entomol. 94, 1075e1084. Carmo, E.L., Bueno, A.F., Bueno, R.C.O.F., 2010. Pesticide selectivity for the insect egg parasitoid Telenomus remus. BioControl 55, 455e464. Cloyd, R.A., Bethke, J.A., 2011. Impact of neonicotinoid insecticides on natural enemies in greenhouse and interior scape environments. Pest Manag. Sci. 67, 3e9. Cole, L.M., Nicholson, R.A., Casida, J.E., 1993. Action of phenylpyrazole insecticides at the GABA-Gated chloride channel. Pestic. Biochem. Physiol. 46, 47e54. Cônsoli, F.L., Botelho, P.S.M., Parra, J.R.P., 2001. Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988, (Hym., Trichogrammatidae). J. Appl. Entomol. 125, 37e43. Cônsoli, F.L., Parra, J.R.P., Hassan, S.A., 1998. Side-effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae). J. Appl. Entomol. 122, 43e47. Delpuech, J.M., Legallet, B., Fouillet, P., 2001. Partial compensation of the sublethal effect of deltamethrin on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 42, 985e991. Delpuech, J.M., Meyet, J., 2003. Reduction in the sex ratio of the progeny of a parasitoid wasp (Trichogramma brassicae) surviving the insecticide chlorpyrifos. Arch. Environ. Contam. Toxicol. 45, 203e208. Desneux, N., Wajnberg, E., Fauvergue, X., Privet, S., Kaiser, L., 2004a. Oviposition behaviour and patch-time allocation in two aphid parasitoids exposed to deltamethrin residues. Entomol. Exp. Appl. 112, 227e235. Desneux, N., Decourtye, A., Delpuech, J.M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81e106. Desneux, N., Pham-Delegue, M.H., Kaiser, L., 2004b. Effect of sub-lethal and lethal dose of lambda-cyhalothrin on oviposition experience and host searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag. Sci. 60, 381e389. Finney, D.J., 1971. Probit Analysis. Cambridge University Press, Cambridge, UK, 333 pp. Fukuto, T.R., 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environ. Health Persp. 87, 245e254.

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