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Chlorfenapyr, a potent alternative insecticide of phoxim to control Bradysia odoriphaga (Diptera: Sciaridae) Yunhe Zhao, Qiuhong Wang, Yao Wang, Zhengqun Zhang, Yan Wei, Feng Liu, Chenggang Zhou, and Wei Mu J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b02098 • Publication Date (Web): 03 Jul 2017 Downloaded from http://pubs.acs.org on July 6, 2017

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Journal of Agricultural and Food Chemistry

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Title page

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Chlorfenapyr, a potent alternative insecticide of phoxim to

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control Bradysia odoriphaga (Diptera: Sciaridae)

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Authors: Yunhe Zhao a #, Qiuhong Wang a, d #, Yao Wang a, Zhengqun Zhang b, Yan

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Wei a, Feng Liu a, Chenggang Zhou c, Wei Mu a *

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a

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Diseases and Insect Pests, Shandong Agricultural University, Tai’an, Shandong 271018, P.R.

College of Plant Protection, Shandong Provincial Key Laboratory for Biology of Vegetable

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China

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b

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Shandong 271018, PR China

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c

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P.R. China

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d

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250100, P.R. China

College of Horticultural Science and Engineering, Shandong Agricultural University, Tai'an,

College of Plant Protection, Shandong Agricultural University, Tai’an, Shandong 271018,

Institute of Plant Protection, Shandong Academy of Agricultural Science, Jinan, Shandong

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#

Both authors contributed equally to this work.

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Corresponding authors:

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*Prof. Wei Mu, College of Plant Protection, Shandong Agricultural University,

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61 Daizong Street, Tai’an, Shandong 271018, P.R. China. Tel: +86-538-8242611,

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Email: [email protected] (W. Mu).

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ACS Paragon Plus Environment


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Abstract

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Bradysia odoriphaga is the major pest affecting Chinese chive production and in

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China, it has developed widespread resistance to organophosphorus insecticides.

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Chlorfenapyr is a promising pyrrole insecticide with a unique mechanism of action

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that does not confer cross-resistance to neurotoxic insecticides. However, the effect of

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chlorfenapyr on organophosphate-resistant B. odoriphaga is not well understood. The

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present study evaluated the potential of chlorfenapyr for the control of

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phoxim-resistant B. odoriphaga. The results showed that chlorfenapyr had significant

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insecticidal activity to B. odoriphaga in multiple developmental stages, and there

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were no significant differences in susceptibility between the field (phoxim-resistant)

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and laboratory (phoxim-susceptible) populations. The pot experiment and field trials

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confirmed the results of our laboratory bioassays. In the field trial, chlorfenapyr

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applied at 3.0, 6.0 or 12.0 kg a.i./ha significantly decreased the number of B.

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odoriphaga and improved yield compared with phoxim at 6.0 kg a.i./ha and the

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control condition. Moreover, the final residues of chlorfenapyr on plants were below

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the maximum residue limits (MRLs) due to its non-systemic activity. These results

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demonstrate that chlorfenapyr has potential as a potent alternative to phoxim for

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controlling B. odoriphaga.

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Keywords: chlorfenapyr; Bradysia odoriphaga; insecticide resistance; insecticide

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residue

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INTRODUCTION

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The Chinese chive maggot, Bradysia odoriphaga (Diptera: Sciaridae), is the

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major pest of Chinese chive and also attacks other liliaceous vegetables in Northern

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China.1-3 Its larvae feed on the roots, bulbs, and immature stems of chive plants and

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cause tissue rot and production losses of more than 50% in the absence of insecticide

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treatment.4,5 In the past few decades, the application of chemical insecticides has been

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the most prevalent management practice for controlling B. odoriphaga.4,6 Currently,

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only four insecticides (phoxim, imidacloprid, thiamethoxam and chlorfluazuron) are

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approved to control B. odoriphaga in China. Moreover, phoxim has been the most

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common organophosphorus insecticide used to combat B. odoriphaga in China since

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the 1980s.7 The long-term and extensive use of phoxim has led to widespread

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resistance in B. odoriphaga in China.8,9 Although neonicotinoid insecticides can show

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long-lasting efficacy against this pest when used in the early root-rearing period,6,10

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due to their greater systemic activity, there may be residual risk when used outside the

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root-rearing period. In addition, the speed of toxic action of chlorfluazuron was

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slower to B. odoriphaga larvae.11 Hence, novel alternative insecticides without

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cross-resistance to neurotoxic insecticides and lower residual risk are required for the

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control of B. odoriphaga.

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Chlorfenapyr is a halogenated pyrrole-based pro-insecticide that is currently used to

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control insects and mites on a variety of crops.12-16 It also exhibits good biological

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activity against sanitary pests (Diptera), such as Anopheles funestus and Culex

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quinquefasciatus.17,18 This compound has favorable contact and stomach toxicity on

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the targeted insect pests through the disruption of mitochondrial oxidative

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phosphorylation.19-23 Unlike organophosphorus insecticides, which affect nerve

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function, chlorfenapyr is a promising pyrrole insecticide with a unique mechanism of 3



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action that does not confer cross-resistance to neurotoxic insecticides. Previous

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studies have indicated that chlorfenapyr exhibited significant insecticidal activity

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toward pyrethroid-resistant mosquitoes.17,24,25 Moreover, chlorfenapyr has been

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recommended by WHO for public health use due to its slight toxicity to humans

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(WHO toxicological classification III).25 In addition, chlorfenapyr is a non-systemic

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insecticide possessing lower residual risk to consumers.26 Hence, we speculated that

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chlorfenapyr may be an appropriate alternative to phoxim as an insecticide for

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controlling B. odoriphaga. However, the effect of chlorfenapyr on this pest is not well

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understood.

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Therefore, we conducted laboratory and field tests to illustrate the insecticidal

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activity of chlorfenapyr to Chinese chive maggot and its residues in chive plants. The

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objectives of this study were to evaluate the potency of chlorfenapyr in controlling

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phoxim-resistant B. odoriphaga and to provide data to support its appropriate

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application and reduce pesticide use in Chinese chive planting regions.

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MATERIALS AND METHODS

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Insect Culture and Insecticides. A laboratory colony of B. odoriphaga was

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initiated with larvae and pupae collected from bulbs of Chinese chive plants in

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Liaocheng, Shandong Province, China (36.02°N, 115.30°E) in April 2013. They were

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reared on fresh rhizomes of Chinese chive plants at 25 ± 1 ˚C with 70 ± 5% relative

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humidity (RH) and a photoperiod of 14:10 h (L:D) in a climate controlled chamber.

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The technical-grade chlorfenapyr (96%) and 10% chlorfenapyr suspension

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concentrate (SC) were provided by Shandong Weifang Rainbow Chemical Co., Ltd.

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(Shandong, China). The technical-grade phoxim (91%) and 40% phoxim emulsifiable

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concentrate (EC) were provided by Nanjing Red Sun Co., Ltd. (Jiangsu, China). 4


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Bioassays. Toxicity of chlorfenapyr on eggs. Ten female and ten male newly

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emerged adults (within 12 h) were transferred to plastic oviposition containers (5 cm

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in diameter and 3 cm in height) with a 50-mm-diameter moist filter paper and a fresh

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Chinese chive rhizome. At 48 h after spawning, a moist writing brush was used to

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collect eggs and transfer them to new Petri dishes for bioassays. Bioassays were

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conducted as described by Xue et al.27 The active ingredient of chlorfenapyr was

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dissolved in acetone, and 5 serial dilutions were prepared using 0.1% T-80 water

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solution. Approximately 30 eggs (two days old) were transferred to a 90-mm-diameter

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Petri dish with a piece of filter paper by using a moist brush. Afterwards, 1 mL of

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solution was dropped onto the eggs with a micropipette. The solvent without

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chlorfenapyr was used as a control. Each Petri dish was treated as a single replicate,

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and each treatment included five replicates to determine mortality at each

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concentration. During exposure, eggs were placed in an artificial climate incubator set

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at 25 ± 1 ˚C and 70 ± 5% RH, with a photoperiod of 14:10 h (L:D). The number of

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hatchings was recorded every day after treatment. Eggs were considered dead if they

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failed to hatch within five days.

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Toxicity of chlorfenapyr on larvae. At 48 h after the females had laid eggs, the

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chive rhizomes with eggs were transferred to new Petri dishes (containing filter paper

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and 2.5% agar gel as a bottom layer). After incubation, larvae were used for bioassays

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after they had developed to the first, second and fourth instars. Bioassays were

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conducted using a standard contact-and-stomach method with slight modifications.28

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The stock solution of chlorfenapyr was used to produce 5 serial dilutions with 0.1%

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T-80 water solution. Then, 30 larvae were transferred to a new Petri dish. Afterwards, 5



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1 mL of solution was dropped onto the filter paper and test larvae. Fresh chive

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rhizomes (0.5 cm in length) were dipped into the test solution for 30 s and air dried at

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room temperature, and then four chive rhizomes were transferred to the Petri dish.

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The solvent without chlorfenapyr was used as a control, and five replicates were used

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for each treatment. During exposure, larvae were maintained under the standard

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laboratory conditions described above. Mortality was assessed after 72 h of treatment.

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Larvae were considered dead if their bodies were elongated and they failed to move

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when disturbed with a moist brush.

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Toxicity of chlorfenapyr on pupae. Bioassays were conducted as described by Xue

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et al.27 with slight modifications. The stock solution of chlorfenapyr was diluted into 5

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serial dilutions using 0.1% T-80 water solution. Female and male pupae (2 days old)

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were transferred into new Petri dishes (as described above), respectively. Afterwards,

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1 mL of solution was dropped onto the filter paper and test pupae. The solvent without

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chlorfenapyr was used as a control. Each Petri dish was treated as a single replicate.

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Each replicate contained 25 pupae, with five replicates per treatment. During

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exposure, pupae were maintained under the standard laboratory conditions described

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above. The number of emergences was recorded every day after treatment. Pupae

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were considered dead if they failed to emerge within five days.

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Toxicity of chlorfenapyr on adults. Bioassays were conducted using the residual

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film method described by Mu et al.29 The chlorfenapyr stock solution was made into 5

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serial dilutions using acetone. Then, 300 µL of each solution was added to a glass test

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tube (2.5 cm in diameter, 8 cm in height), and the test tube was rolled back and forth

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until the acetone was evenly distributed over the inner wall and had evaporated. 6


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Afterwards, newly emerged, unmated male and female adults were transferred into

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separate tubes, which were then sealed with pieces of gauze. The solvent without

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chlorfenapyr was used as a control. Each test tube was treated as a single replicate.

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Each treatment included five replicates, and each replicate consisted of 15 adults.

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During exposure, adults were maintained under the standard laboratory conditions

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described above. Mortality was assessed after 24 h of treatment. Adults were

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considered dead if they failed to move after disturbance with a moist brush.

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Temperature Effect of Chlorfenapyr. Bioassays were conducted on fourth-instar

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larvae of B. odoriphaga using the standard contact-and-stomach method described

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above. Six concentrations of chlorfenapyr and one control solvent without

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chlorfenapyr were used to test toxicity at 8±1, 16±1 and 24±1 ˚C, and five replicates

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were included for each treatment. During exposure, larvae were maintained under the

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standard laboratory conditions described above. Mortality was assessed after 72 h of

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treatment.

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Susceptibility of B. odoriphaga to Chlorfenapyr and Phoxim. Seven field

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populations of B. odoriphaga were collected between July and October of 2014 from

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the following seven important Chinese chive planting regions in Shandong, China:

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Jinan, Laiwu, Liaocheng, Dezhou, Tai’an, Weifang, and Linyi (Figure 1). Bioassays

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were conducted on fourth-instar larvae of B. odoriphaga by the standard

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contact-and-stomach method described above. Seven concentrations and one control

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were used to test the toxicities of phoxim and chlorfenapyr to seven field populations

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and the laboratory population, and five replicates were used for each condition.

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During exposure, larvae were maintained under the standard laboratory conditions 7



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described above. Mortality was assessed after 72 h of treatment.

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Pot Experiment. The experiment was carried out in plastic garden pots (12 cm in

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diameter, 10 cm in height) containing 40% sand, 40% clay and 20% organic matter.

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Chinese chive plants were transplanted into the pots and placed in an artificial climate

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incubator set at 25 ± 1 ˚C and 70 ± 5% RH with a photoperiod of 14:10 h (L:D). Five

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days after transplant, thirty third-instar larvae were transferred to the pots near the

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pseudo-stems/bulbs (3 cm from soil surface). After 24 h, 10% chlorfenapyr SC was

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serially diluted to 10, 20, 30, 40, and 50 mg/L with distilled water, 40% phoxim EC

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was diluted to 250 and 1000 mg/L with distilled water, and each pot was irrigated

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with 200 mL of one of those solutions. Equal amounts of distilled water were used as

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a control. Each pot was treated as a single replicate, and each treatment included five

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replicates. Mortality was assessed after 72 h of treatment. Larvae were considered

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dead if their bodies were elongated and they failed to move when disturbed with a

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moist brush.

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Field Experiment. Studies were conducted from October 2015 to March 2016 at

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Tai’an in Shandong, China (36.19°N, 116.88°E). The soil type was Shajiang black soil,

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which was composed of 56% sand, 40% silt and 4% clay, with 1.45% organic matter.

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The Chinese chive plants were sowed directly and cultivated for two years. During the

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period before the experiment, phoxim and chlorpyrifos were frequently used for the

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control of B. odoriphaga, while chlorfenapyr was never used to control this pest. Plots

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were distributed according to a randomized block design with five treatments (three

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replicates each). Each plot was 4.0 m by 20.0 m in area, and Chinese chive was

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soaked with chlorfenapyr (10% SC) at 3.0, 6.0 and 12.0 kg a.i./ha and phoxim (40% 8


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EC) at 6.0 kg a.i./ha (the recommended standard applied dosage in China according to

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the China Pesticide Information Network30) as the plants were irrigated. Control

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plants were treated only with water.

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The effects of chlorfenapyr and phoxim on the growth indices of Chinese chive

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plants were investigated at the first harvest (110 days after treatment). The height and

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stem diameter of Chinese chive plants were measured using the five-spot sampling

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method (1.0 m × 1.0 m for each quadrat). Twenty plants from each quadrat were

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selected at random and measured. Then, all plants in each plot were harvested to

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measure the yield.

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After the plants were treated with chlorfenapyr and phoxim for 120 days, B.

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odoriphaga were counted around the roots and bulbs of randomly selected Chinese

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chive plants (nine locations and a Z-shaped sampling pattern for every plot, 10 cm ×

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10 cm for each location). The larvae were counted by removing the soil, and harm to

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the plants was avoided.

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Residual Determination of Chlorfenapyr and Phoxim in Soils and Chive Plants.

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Soil samples (0-10 cm depth, approximately 500 g) were randomly collected from

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each plot at 1, 3, 5, 7, 14, 21, 30, 45, 60, 75, 90, and 120 days after chlorfenapyr and

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phoxim treatment. To assess the final residues of chlorfenapyr and phoxim in Chinese

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chives, fifty plants were randomly selected from each plot at the first harvest time

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(110 days after treatment). All samples were stored at -20 ˚C until further extraction

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and analysis.

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The extraction and clean-up were performed according to the method of Zhang et

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al.6 The specific procedures are detailed in the supplementary information (File S1).

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The linear standard curves of chlorfenapyr and phoxim were established based on 9



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injections of the standard solutions at concentrations ranging from 0.005 to 2.00

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mg/kg and 0.001 to 0.20 mg/kg, respectively. The recovery tests were carried out at

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three different levels from the soil samples and Chinese chive plants (chlorfenapyr:

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0.01, 0.50 and 10.00 mg/kg; phoxim: 0.01, 0.20 and 5.00 mg/kg). The samples were

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processed as described above, and the experiments were replicated five times for each

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level. The correlation coefficients (R2>0.99) and mean recovery rates (86.87-98.52%)

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for chlorfenapyr and phoxim were within the acceptable range (Tables S1 and S2).

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Statistical Analysis. The data obtained from the toxicity experiments were

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subjected to probit analysis using SPSS (version 13.0; SPSS, Chicago, IL, USA).

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Statistically significantly different mean values were identified using ANOVA, and

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significant differences among the treatments were determined using the LSD test

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(SPSS v. 13.0) (P < 0.05). Before statistical analysis, the hatching rate, emergence

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rate and control eﬀect in pot experiments of chlorfenapyr on the pest were

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transformed using arcsine square-root-transformed percentages.

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RESULTS

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Toxicity of Chlorfenapyr to Different Developmental Stages of B. odoriphaga.

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Eggs. The effects of chlorfenapyr on the hatching rate as described by ANOVA are

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shown in Figure 2a. There were significant differences (P < 0.05) among all

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concentrations (0, 0.25, 0.5, 1, 2, and 4 mg/L). The hatching rate decreased

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significantly as the pesticide concentration increased. In particular, at 1 mg/L, the

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hatching rate after five days was only 52.99%, compared to 94.72% at 0 mg/L.

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Larvae. The toxicity of chlorfenapyr to B. odoriphaga larvae is shown in Table 1.

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Chlorfenapyr caused 50% mortality of first-, second- and fourth-instar B. odoriphaga 10


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larvae after 72 h at concentrations of 3.94, 4.12, and 10.11 mg (a.i.) L-1, respectively.

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Furthermore, the LC50 of this compound for fourth-instar larvae was 2.56 times that

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for first-instar larvae.

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Pupae. Chlorfenapyr strongly inhibits the emergence of both male and female

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pupae (Figure 2b). The concentration of insecticide significantly influenced the

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emergence rate. For male pupae, the emergence rate at each concentration shows

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highly significant effects (P < 0.05). At 2.5 mg/L, the emergence rate was 38.46%,

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versus 100% in the control group. Among female pupae, the emergence rates at

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concentrations of 2.5, 5, 10 and 20 mg/L were significantly different from each other

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and from the control. In addition, at 2.5, 5, and 10 mg/L, male pupae emerged at

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significantly lower rates than did female pupae.

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Adults. The LC50 values of chlorfenapyr for male and female adults at 24 h after

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treatment were 0.80 and 1.06 mg (a.i.) L-1, respectively (Table 1). Our results show

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that the LC50 of chlorfenapyr was greater for female adults than for male adults, but

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this difference was not significant based on the overlapping confidence intervals.

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Temperature Effect of Chlorfenapyr. The toxicity of chlorfenapyr was

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significantly increased at temperatures between 8 and 24 °C. Based on the LC50

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values, the toxicity of chlorfenapyr to B. odoriphaga was significantly greater (3.54-

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and 1.82-fold, respectively) at 16 and 24 °C than at 8 °C (non-overlapping of 95% CL;

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Table 2). In addition, chlorfenapyr showed an overall positive temperature coefficient

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of 6.45-fold for the temperature range tested.

269 270 271

Susceptibility

of

B.

odoriphaga

to

Chlorfenapyr

and

Phoxim.

The

susceptibilities of the fourth-instar B. odoriphaga larvae originating from several field 11



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populations in Shandong Province to chlorfenapyr and phoxim were investigated as

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well. The bioassay results showed that the field populations developed different levels

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of resistance to phoxim. For example, compared to the laboratory population, phoxim

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resistance was 55.68-, 59.61- and 74.32-fold higher in the Dezhou, Tai’an and Linyi

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populations, respectively (Table 3).

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The LC50 of chlorfenapyr in the laboratory population was 10.11 mg/L, while those

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in the Jinan, Laiwu, Liaocheng and Weifang populations were 1.058, 1.076, 1.044 and

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1.043 times that value, respectively, and those of the Dezhou, Tai’an and Linyi

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populations were 0.864, 0.998 and 0.971 times that value, respectively (Table 3).

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Based on the overlapping confidence limits of LC50 values, no significant differences

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in susceptibility to chlorfenapyr were found between the field populations and the

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laboratory population.

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Pot Experiment. The mortality of B. odoriphaga larvae treated with chlorfenapyr

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and phoxim in pot experiments was investigated (Figure 3). The results showed that

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chlorfenapyr at concentrations of 20, 30, 40, 50 mg/L significantly increased the

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mortality of B. odoriphaga compared with the 250 mg/L phoxim treatment and the

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no-insecticide

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concentration-dependent increase in mortality of fourth-instar larvae, and at 50 mg/L,

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there was 88.89% mortality compared to 5.56% mortality among untreated larvae.

control

group

(P

30 ˚C) could suppress the B. odoriphaga population,

361

with the greatest damage usually occurring in the spring and autumn. The average

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temperatures in spring and autumn in Shandong are 4-22 and 6-22 ˚C, respectively.

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Our results thus suggest that chlorfenapyr exhibited increased toxicity with increasing

364

temperature from 8 to 24 ˚C. Hence, growers of Chinese chives should perform

365

chemigation with chlorfenapyr at times of relatively high temperatures in spring and

366

autumn.

of

organophosphates,

carbamates,

pyrethroids

and

neonicotinoid

367

The results of the pot experiment and field trials confirmed the results of our

368

laboratory bioassays; chlorfenapyr is a promising insecticide for the control of B.

369

odoriphaga. When 50 mg/L of chlorfenapyr was used in the pot test, larval mortality

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was approximately 90% (Figure 3). The field results showed that chlorfenapyr applied

371

at 3, 6 or 12 kg a.i./ha could significantly decrease the number of B. odoriphaga 15



372

compared to the numbers observed after treatment with phoxim at 6 kg a.i./ha or in

373

the no-pesticide control group (Figure 4a). In field trials, the yields of Chinese chives

374

were increased when chlorfenapyr was applied at 3, 6 or 12 kg a.i./ha compared to the

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controls and phoxim treatments (Figure 4d) because of the greater protective effects

376

of chlorfenapyr. Moreover, there was a positive relationship between chlorfenapyr

377

dose and yield. Devi et al.39 showed that chlorfenapyr could also increase the yield of

378

okra when the insecticide was used against Earias vittella Fabricius. Meanwhile, there

379

was no phytotoxicity observed in the pot experiment or in the field trial. In addition,

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the final residues of chlorfenapyr and phoxim in chive plants were below the MRLs,

381

due to the light instability of phoxim40,41 and the non-systemic activity of

382

chlorfenapyr.26 Hence, chlorfenapyr has low residual risks and would ensure greater

383

safety for consumers when applied appropriately. All results indicate that chlorfenapyr

384

has great potential as an alternative insecticide against B. odoriphaga. In addition,

385

Zhang et al.42 found that reaching the target area in Chinese chive ecosystems was

386

easier when using the directional spray-washing method than with the chemigation

387

method; hence, the control effect of chlorfenapyr under directional spray-washing

388

method requires further study.

389

In conclusion, this study demonstrated that chlorfenapyr has favorable insecticidal

390

activity against B. odoriphaga at all developmental stages. It can also effectively

391

control B. odoriphaga, which already exhibits high resistance to phoxim. Moreover, it

392

has low residual risk and therefore would improve food safety for consumers. Overall,

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the pyrrole insecticide chlorfenapyr shows great promise against B. odoriphaga and is

394

safe for use in Chinese chives at 3 kg a.i./ha. Although chlorfenapyr is a potent

395

insecticide with a unique mechanism of action, it must still be used at appropriate

396

levels because chlorfenapyr resistance has been observed in other insects.43 Hence, 16


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397

rotating among insecticides and using combinations of different insecticides are

398

important strategies for controlling insect pests and delaying the development of

399

insecticide resistance.

400 401

SUPPORTING INFORMATION

402

The specific procedures for extraction, clean-up and analysis; Calibration curves

403

and recoveries of chlorfenapyr in soils and Chinese chive plants; Calibration curves

404

and recoveries of phoxim in soils and Chinese chive plants.

405 406

ACKNOWLEDGMENTS

407

This study was supported by grants from the Special Fund for Agro-scientific

408

Research in the Public Interest from the Ministry of Agriculture of China

409

(201303027).

410

17



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REFERENCES

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(1) Mei, Z. X.; Wu, Q. J.; Zhang, Y. J.; Hua, L. The biology, ecology and management

413

of Bradysia odoriphaga. Entomol. Knowl. 2003, 40, 396-398.

414

(2) Zhang, P.; Wang, Q. H.; Zhao, Y. H.; Chen, C. Y.; Mu, W.; Liu, F. Investigation of

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crop damage and food preferences of Bradysia odoriphaga Yang et Zhang. Chin.

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J. Appl. Entomol. 2015, 52, 743-749.

417

(3) Feng, F.; Ge, J.; Li, Y.; Cheng, J.; Zhong, J.; Yu, X. Isolation, Colonization, and

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Chlorpyrifos

419

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23



546

Page 24 of 33

Table 1 Toxicity of chlorfenapyr to larvae and adults of Bradysia odoriphaga Stage

LC50 mg/L (95% CL)

Slope ± SE

χ2 (df)

First-instar larvae

3.94 (2.84-4.89)

2.56±0.53

5.3890 (4)

Second-instar larvae

4.12 (2.95-5.09)

3.68±0.60

0.6462 (4)

Fourth-instar larvae

10.11 (9.40-10.66)

11.62±2.94

1.1475 (4)

Female adults

1.06 (0.68-1.56)

1.58±0.32

0.4996 (4)

Male adults

0.80 (0.49-1.22)

2.33±0.61

0.1107 (4)

547

24


Page 25 of 33


548

Table 2 Influence of temperature on the toxicity of chlorfenapyr to fourth-instar

549

larvae of Bradysia odoriphaga Temperature coefficienta Temperature (°C) LC50 mg/L (95% CL)

2

Slope ± SE

χ (df) 8°C

a

8

75.85 (68.62-82.29)

6.64 ± 1.52

1.0985 (5)

16

21.41 (13.46-24.70)

4.56 ± 1.49

0.0897 (5)

3.54

24

11.76 (10.39-12.96)

5.36 ±0.84

0.4786 (5)

1.82

16°C

6.45

Ratio of higher to lower LC50 value for 8 and 16 °C differences in temperature. A positive

coefficient indicates a lower LC50 at the higher temperature.

550

25



Page 26 of 33

551

Table 3 Susceptibilities of several field and laboratory populations of fourth-instar Bradysia odoriphaga larvae in Shandong province to

552

chlorfenapyr and phoxim Phoxim Populations

Chlorfenapyr

LC50 mg/L (95% CL)

Slope ± SE

χ2 (df)

RSIa

LC50 mg/L (95% CL)

Slope ± SE

χ2 (df)

RSI

Jinan

90.43 (65.57-139.96)

1.91 ± 0.43

1.1384 (4)

1.962

10.70 (10.13-11.23)

11.64 ± 2.27

3.7284 (4)

1.058

Laiwu

495.23 (257.28-732.65)

1.55 ± 0.41

0.5189 (4)

10.75

10.88 (10.25-11.54)

9.95 ± 2.19

0.7373 (4)

1.076

Liaocheng

1270.21 (1079.35-1629.00)

6.03 ± 1.20

6.0239 (4)

27.57

10.55 (9.94-11.05)

11.57 ± 2.27

1.1835 (4)

1.044

Dezhou

2565.92 (1748.01-3080.91)

3.29 ± 0.89

0.0571 (4)

55.68

8.73 (6.21-9.67)

5.75 ± 2.05

0.4105 (4)

0.864

Tai’an

2747.03 (1938.08-4194.86)

1.91 ± 0.49

0.0035(4)

59.61

10.09 (8.76-10.68)

14.47 ± 3.70

1.2126 (4)

0.998

Weifang

1813.27 (1012.94-3222.24)

1.89 ± 0.77

0.4441 (4)

39.35

10.54 (9.98-11.02)

12.05 ± 2.21

0.5251 (4)

1.043

Linyi

3424.87 (2338.70-7120.25)

1.79 ± 0.54

0.5589 (4)

74.32

9.82 (8.83-10.37)

10.76 ± 2.98

1.3737 (4)

0.971

Laboratory population

46.08 (24.71-66.06)

1.70 ± 0.42

1.2266 (4)

1.000

10.11 (9.40-10.66)

11.62 ± 2.94

1.1475 (4)

1.000

a

Relative susceptibility index (RSI) was determined by comparing the LC50 value of each population to the LC50 value of the laboratory (reference) population.

553

26


Page 27 of 33


554

Figure captions

555

Figure 1. Points of collection of Bradysia odoriphaga in Shandong, China.

556

Figure 2. Hatching rate (a) and emergence rate (b) of Bradysia odoriphaga after

557

treatment with different concentrations of chlorfenapyr (mean ± SE). Data for

558

same-sex pupae followed by different letters are significantly different at the 0.05

559

level by the LSD test. The asterisk (*) indicates a significant difference at the same

560

concentration between different-sex pupae at the 0.05 level by the t-test (SPSS v.

561

13.0).

562

Figure 3. Mortality of Bradysia odoriphaga larvae after treatment with chlorfenapyr

563

in pot experiments (mean ± SE). Different letters above the bars indicate significant

564

differences at P < 0.05 by the LSD test.

565

Figure 4. Control effect of chlorfenapyr and phoxim against Bradysia odoriphaga

566

and influence on the growth indices of Chinese chive (mean ± SE). (a) The number of

567

B. odoriphaga larvae after 120 days of treatment with chlorfenapyr; (b) The height of

568

Chinese chive plants at the first harvest (110 days after treatment); (c) The stem

569

diameter of Chinese chive plants at the first harvest; (d) The yield of Chinese chive

570

plants at the first harvest. Different letters above the bars indicate significant

571

differences at P < 0.05 by the LSD test.

572

Figure 5. Residual dynamics of chlorfenapyr and phoxim in soil samples. Fitted

573

regression lines were drawn according to the equation y = ae−bx. t1/2: Half-life.

27



Graphical abstract 600x416mm (72 x 72 DPI)


Page 28 of 33

Page 29 of 33


Figure 1. Points of collection of Bradysia odoriphaga in Shandong, China. 172x110mm (150 x 150 DPI)



Figure 2. Hatching rate (a) and emergence rate (b) of Bradysia odoriphaga after treatment with different concentrations of chlorfenapyr (mean ± SE). Data for same-sex pupae followed by different letters are significantly different at the 0.05 level by the LSD test. The asterisk (*) indicates a significant difference at the same concentration between different-sex pupae at the 0.05 level by the t-test (SPSS v. 13.0). 155x223mm (300 x 300 DPI)


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Page 31 of 33


Figure 3. Mortality of Bradysia odoriphaga larvae after treatment with chlorfenapyr in pot experiments (mean ± SE). Different letters above the bars indicate significant differences at P < 0.05 by the LSD test. 63x33mm (300 x 300 DPI)



Figure 4. Control effect of chlorfenapyr and phoxim against Bradysia odoriphaga and influence on the growth indices of Chinese chive (mean ± SE). (a) The number of B. odoriphaga larvae after 120 days of treatment with chlorfenapyr; (b) The height of Chinese chive plants at the first harvest (110 days after treatment); (c) The stem diameter of Chinese chive plants at the first harvest; (d) The yield of Chinese chive plants at the first harvest. Different letters above the bars indicate significant differences at P < 0.05 by the LSD test. 74x55mm (300 x 300 DPI)


Page 32 of 33

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Figure 5. Residual dynamics of chlorfenapyr and phoxim in soils samples. Fitted regression lines were drawn according to the equation y = ae−bx. t1/2: Half-life. 99x74mm (300 x 300 DPI)


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