Sublethal effects of hexaflumuron on development and reproduction of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae)

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ORIGINAL ARTICLE

Sublethal effects of hexaflumuron on development and reproduction of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae)

Mohammad Mahmoudvand^1,4, Habib Abbasipour¹, Aziz Sheikhi Garjan² and Ali Reza Bandani³

1Department of Plant Protection, Faculty of Agricultural Sciences, Shahed University, Tehran,²Iranian Research Institute of Plant Protec- tion, Tehran,³Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj,⁴Islamic Azad University, Qom branch, Young Researches Club, Qom, Iran

Abstract Effects of hexaflumuron at 10% lethal concentration (LC10) and LC25 on development and reproduction parameters of the diamondback moth,Plutella xylostella (Linnaeus, 1753) (Lep.: Yponomeutidae) were investigated. Estimated LC₅₀, LC₁₀ and LC₂₅values of leaf dip bioassay of hexaflumuron on the third instar larvae of theP. xy- lostellawere 1.48, 0.59 and 0.91 mg/L, respectively. Hexaflumuron decreased pupal weight in the parent generation at sublethal concentrations but in the offspring generation, this effect was not observed. Sublethal concentrations increased egg, first and second larval instar and pupa developmental time and shortened life span of adults, but did not change the third and fourth larval instars and pre-pupa developmental period. Also fecundity of females reduced significantly but hatchability of treatments and control were similar.

Survival rate of pre-adult stages declined significantly at LC25concentration. Reproduc- tion parameters such as reproductive rate (R0) and intrinsic rate of increase in sublethal concentrations were significantly lower compared with control, but gross reproduction rate (GRR) at the LC10concentration was increased and it could be hormoligosis. Also hexaflumuron significantly increased doubling time (Dt). We conclude that the sublethal effects of hexaflumuron might exhibit significant effects on the population dynamics of P. xylostella.

Key words biological parameters, diamondback moth, hormoligosis, IGR,Plutella xy- lostella, sublethal concentrations

Introduction

The diamondback moth, Plutella xylostella (Linnaeus, 1753) (Lepidoptera: Yponomeutidae) is a major pest of cruciferous plants around the world and in Iran (Mah- moudvand et al., 2009; Talekar & Shelton, 1993). It is an oligophagous pest and feeds on plants that con-

Correspondence: Habib Abbasipour, Department of Plant Protection, Faculty of Agricultural Sciences, Shahed University, Tehran, Iran. Tel:+98 21 51213605; fax:+98 21 51213192;

email: [email protected]

tain mustard oil and glycosides (Thorsteinson, 1953; Ooi, 1986).

Resistance of P. xylostella to all main groups of insecticides has been recorded (Perez et al., 1995) and it is ranked in the 20 most resistant pest species reported up to now (Mota-Sanchez et al., 2002). Insect growth regulators (IGRs) interrupt molting (juvenile hormone or ecdysone mimics) and cuticle formation (chitin synthesis inhibitors) and affect endocrine systems (Dhadiallaet al., 1998). Derivatives of benzoylphenyl ureas (BPUs) are a class of IGRs that inhibit synthesis of chitin in insects and have stomach-poisoning effects (Hajjar & Casida, 1978;

Leonardet al., 1987). BPUs have high specificity, low

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mammalian toxicity and rapid degradation in the environment and they are efficient on immature stages of insects (Moseret al., 1992). Hexaflumuron [N-(((3,5-dichloro-4- (1,1,2,2-tetrafluroethoxy) phenyl)- amino) carbonyl) 2,6 diflurobenzamide] is a chitin synthesis inhibitor and it has been used to control a wide range of agricultural pests (Su & La Fage, 1987; Su, 1994; Nakagawaet al., 1992). Insecticides have lethal and sublethal effects. Sub- lethal doses affect physiological and behavioral proper- ties of insects (Haynes, 1988). Demographic toxicology is an ecotoxicological technique that integrates life table parameters in the background of toxicology. Life table parameters of populations exposed to various concentrations of a poison have been compared with unexposed populations (Stark & Wennergren, 1995). The effect of insecticides can be calculated by estimating life table parameters such asR0,T (response generation time) and rm (Maiaet al., 2000). Some researchers have studied the sublethal effects of IGRs on pupal rate and adult emergence (Marco & Vinuela, 1999), weight of adults (Kellouche & Soltani, 2006; Dallaireet al., 2004), egg hatching (Pineda et al., 2007; Sammour et al., 2008), developmental time (Coppen & Jepson, 1996), fecundity (Biddinger & Hull, 1999), larval weight and adult longevity (Cutleret al., 2005). Since there is no report regarding the effects of hexaflumuron sublethal concentrations on theP. xylostella, this work was undertaken to evaluate such effects.

The objective of this study was to elucidate lethal and sublethal concentrations of hexaflumuron, and then experiments were carried out to study the effects of sublethal doses on egg, larval instars and pupal developmental time and survival rate, fecundity, adult longevity, hatchability and pupal weight. Finally, population growth parameters such as gross reproduction rate (GRR), reproductive rate (R₀), intrinsic rate of increase (r_m) and doubling time (Dt) were evaluated.

Materials and methods Insect rearing

The initialP. xylostellacolony was collected in August of 2008 from cauliflower fields of Shahre-Rey south of Tehran, Iran. For egg laying, about 500 adults ofP. xy- lostellawere placed in a plastic cage (50×30×30 cm) and eggs were transferred to leaves of cauliflower,Bras- sica oleracea var.botrytisas food material to continue their development. Insect stock was maintained at 25± 1^◦C and 65% ± 5% relative humidity under a 16 : 8 (L : D) photoperiod in a growth chamber.

Bioassay

For bioassay experiments, the leaf dip method was used (Tabashnik & Cushing, 1987). Cabbage leaf disks (3 cm in diameter) were dipped in different concentrations of hexaflumuron (Consult^R 10% emulsifiable concentration, DowAgroSciences, Indianapolis, IN, US) solutions containing 0.02% Tween-80 for 30 sec. For control, the leaf disks were dipped in water with 0.02%

Tween-80. The treated leaf disks were permitted to dry at room temperature for 2 h. Then the dry-treated leaf disks were placed in a plastic cup (3 cm depth and 5.5 cm diameter). Ten starved third instars were released on the leaf disks. This test was replicated four times and at least 60 third instars were used for each concentration. Mor- tality was recorded 96 h after treatment (adult emergence stage). The data were analyzed by probit analysis using SAS software (SAS Institute, 1997).

Treatment of sublethal concentrations of hexaflumuron

Cabbage leaf disks treated with 10% lethal concentration (LC₁₀) and LC₂₅ of hexaflumuron and the control were prepared in 0.02% of Tween-80. After drying, 25 individual third larval instars, which had been starved for 2 h, were placed on treated leaves in a plastic cup (3 cm depth and 5.5 cm diameter). For each treatment, eight replicates were considered. After 96 h, surviving larvae were transferred to untreated cabbage leaves and left to continue their development to pupal stage, then the pupae were placed individually in Petri dishes (8 cm diameter) until the adults appeared. Also, 50 individu- als of 2-day-old pupae of each treatment were randomly selected and weighed individually. After the adult emergence, 20 pairs (male and female) of adults in each sublethal concentration and control were selected and then each pair was put in a plastic cage (14 ×11× 5 cm).

For adult feeding, sugar solution (10%) was used. The adults were allowed to lay eggs on cabbage leaves. Leaves were replaced with fresh ones and numbers of eggs laid were recorded daily. This process continued until adults died.

Life history and survival rate

To estimate egg developmental time, in each treatment, 150 eggs were studied daily until hatching. For larval and pupal developmental time, 100 neonate larvae were selected from each treatment and control. Larvae were placed individually on leaves of cabbage in Petri dishes (8 cm diameter) and developmental period was recorded

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Table 1 Toxicity of hexaflumuron on the third instar larvae of diamondback moth.

n^† df LC10(mg/L) LC25(mg/L) LC50(mg/L) Slope±SE χ²

Hexaflumuron 453 5 0.59 (0.38–0.76) 0.91 (0.69–1.08) 1.48 (1.28–1.67) 3.20±0.44 2.57

†Number of subjects.

daily. Also survivorship of different stages was separately recorded.

Data analysis

The data from the experiments were subjected to one- way analysis of variance (ANOVA) (P<0.05) after check- ing for normality. Means were compared by Tukey’s Stu- dentized Range Test, admitting significant differences at P<0.05. Differences in biological parameters were tested through the Jackknife method (Maia et al., 2000). SAS software was used for all analyses (SAS Institute, 1997).

Results

Susceptibility to hexaflumuron

The results of leaf-dip bioassay of hexaflumuron on the third instars of diamondback moth are shown in Table 1.

The values of LC₁₀, LC₂₅and LC₅₀after 96 h were 0.59, 0.91 and 1.48 mg/L, respectively.

Pupal weight, fecundity and hatchability

The results of pupal weight of treatments and control in parent and offspring generations are shown in Fig. 1. Only

Fig. 1 Pupal weight of P. xylostella exposed to hexaflumuron (LC10 and LC25) and control in parent and offspring.

Means marked with different letters are significantly different (P<0.05; Tukey) (parent:F=6.75,P=0.001 6, df=2,147;

offspring:F=0.30,P=0.741 2, df=2,147).

LC₂₅ concentration of hexaflumuron caused decrease in pupal weight in the parent, compared to control (F=6.75, P = 0.001 6, df = 2,147). Pupal weight in LC₁₀ and LC₂₅concentrations and the untreated group in offspring were not significantly different (F=0.30,P=0.741 2, df=2,147).

Table 2 reports the sublethal impacts of hexaflumuron on fecundity and percentage of hatchability of P. xylostella. The fecundity of the diamondback moth treated with hexaflumuron was clearly and significantly lower than control. There was also significant difference between concentrations (F=923.65,P<0.000 1, df=2,57). Sublethal concentrations of hexaflumuron did not affect hatchability (F=1.32,P<0.334 2, df=2,6).

Effects of hexaflumuron on life history and adult longevity

The effects of hexaflumuron at sublethal concentrations on egg, different stages of larva, prepupal and pupal developmental time and adult longevity of the diamondback moth are presented in Table 3. Both sublethal doses significantly increased egg developmental duration ofP.

xylostella (F =94.20, P <0.000 1, df =2,440). Also LC25 concentration extended first and second larval instar developmental periods, but time of developing in the third and fourth larval instar were not longer than control (first instar:F=16.37,P<0.000 1, df=2,233; second

Table 2 Fecundity (mean number of eggs laid by females) and hatchability ofP. xylostellain which third instars were treated with sublethal concentrations of hexaflumuron.

Fecundity Egg hatch (%)

Control 207.29±1.85 a 97.84±1.21 a

LC10 183.64±0.91 b 94.07±2.36 a

LC25 131.13±0.80 c 94.13±1.86 a

P <0.000 1 0.334 2

F 923.65 1.32

df 2,57 2,6

Means marked with different letters within the same column are significantly different (P<0.05; Tukey).

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Table 3 Effect of sublethal concentrations of hexaflumuron on pre-adult developmental period and adult longevity of next generation P. xylostella(third instars of parental populations were treated).

Hexaflumuron

Control P F df

LC10 LC25

Egg 3.26±0.03 c 3.45±0.04 b 3.91±0.02 a <0.000 1 94.20 2,440

First instar 1.61±0.07 b 1.74±0.08 b 2.34±0.11 a <0.000 1 16.37 2,233

Second instar 2.34±0.12 b 2.31±0.10 b 2.90±0.21 a 0.011 1 4.61 2,198

Third instar 2.05±0.10 a 2.15±0.16 a 2.14±0.24 a 0.864 4 0.15 2,174

Fourth instar 2.73±0.09 a 2.96±0.17 a 3.0±0.16 a 0.325 8 1.13 2,155

Total larva 8.71±0.19 b 9.12±0.34 b 9.91±0.44 a 0.038 9 3.32 2,155

Pre-pupa 0.24±0.19 a 0.37±0.06 a 0.30±0.08 a 0.317 8 1.16 2,147

Pupa 3.43±0.09 b 3.91±0.10 a 3.93±0.07 a <0.000 2 9.04 2,139

Male 23.75±0.73 a 21.90±0.52 a 17.90±0.35 b <0.000 1 28.68 2,57

Female 20.65±0.70 a 18.90±0.78 a 16.10±0.75 b <0.000 3 9.38 2,57

Means marked with different letters within the same row are significantly different (P<0.05; Tukey).

instar:F=4.61,P=0.011 1, df=2,198; the third instar:

F=0.15,P=0.864 4, df=2,174; fourth instar:F=1.13, P=0.325 8, df =2,155). Total larval duration only in LC25concentration was significantly longer than control (F=3.32,P=0.038 9, df=2,155). Pre-pupa developmental time remained unaffected (F=1.16,P=0.317 8, df=2,147). The pupa developmental period in the LC25

treatment group was significantly longer than the untreated group (F=2.04,P<0.000 2, df=2,139). The mean life lengths of males and females in the LC₂₅group were significantly shorter than control (male:F=28.68, P<0.000 1, df=2,57; female:F=9.38,P<0.000 3, df=2,57).

Effects of hexaflumuron on survival rate

Survival rates of each life stage ofP. xylostellaexposed to LC10 and LC25 doses of hexaflumuron and control are listed in Table 4. The highest rate of mortality was found during the first and second larval instars. Mortality trend of the first larval instar was increased in treatment groups. Also there was significant difference in the mortality of the second larval instar of diamondback moth;

however, mortality in the third and fourth larval instars, pre-pupa and pupa was similar to controls. Mortality of total larval stages and total pre-adult stages (larva, pre-pupa and pupa) ofP. xylostellaonly in LC₂₅ was significantly

Table 4 Effect of sublethal concentrations of hexaflumuron on survival rate (%) of pre-adult stages of next generationP. xylostella (third instars of parental populations were treated).

Hexaflumuron

Control P F df

LC10 LC25

First instar 90±1.58 a 74±5.78 b 72±5.14 b 0.031 6 4.67 2,12

Second instar 93.19±2.15 a 89.61±3.24 a 68.60±7.57 b 0.008 5 7.29 2,12

Third instar 87.13±4.43 a 94.15±2.45 a 81.52±4.69 a 0.122 1 2.52 2,12

Fourth instar 91.58±2.85 a 87±2.93 a 82.68±9.68 a 0.593 4 0.55 2,12

Total larva 67±4.35 a 55±7.07 ab 36±8.27 b 0.022 0 5.33 2,12

Pre-pupa 98.57±1.43 a 92.35±2.19 a 92±4.89 a 0.301 7 1.33 2,12

Pupa 98.46±1.54 a 92.18±3.72 a 95±50 a 0.506 6 0.72 2,12

Total pre-adult 65±4.72 a 46±4.30 ab 31±7.81 b 0.004 5 8.75 2,12

Means marked with different letters within the same row are significantly different (P<0.05; Tukey).

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Table 5 Comparison of biological parameters ofP. xylostellain which third larvae were treated with sublethal concentrations of hexaflumuron.

GRR (gross reproduction rate) R0(net reproduction rate) rm(per day) (intrinsic rate of increase) Dt (doubling time)

Control 100.12±0.35 b 82.65±0.28 a 0.17±0.0 a 3.89±0.00 c

LC10 101.91±0.53 a 45.66±0.22 b 0.14±0.0 b 4.74±0.00 b

LC25 80.82±0.44 c 22.99±0.13 c 0.10±0.0 c 6.76±0.01 a

P <0.000 1 <0.000 1 <0.000 1 <0.000 1

F 669.46 17 822.40 28 320.97 20 887.43

df 2,57 2,57 2,57 2,57

Means marked with different letters within the same column are significantly different (P<0.05; Tukey).

higher than controls (total larvae:F=5.33,P=0.022 0, df=2,12; pre-pupa:F=1.33,P=0.301 7, df=2,12;

pupa:F=0.72,P=0.506 6, df=2,12; total pre-adult:

F=8.75,P=0.004 5, df=2,12).

Sublethal effects on population growth parameters

Effects of sublethal concentrations of hexaflumuron on reproduction parameters of the diamondback moth were compared between treatments (Table 5). There were significant differences between sublethal concentrations and control. GRR was increased in the LC₁₀ treatment.

In the LC₂₅ concentration, GRR was decreased significantly compared with control (F=669.46,P<0.000 1, df =2,57). Different concentrations had significant effects onR0andrmcompared with control. Also, there were significant differences among two sublethal groups (R0: F=17 822.40,P<0.000 1, df=2,57;rm:F=28 320.97, P<0.000 1, df=2,57). Dt in two sublethal concentrations was significantly increased. Furthermore, doubling time in LC25concentration was significantly longer than LC10(F=20 887.43,P<0.000 1, df=2,57).

Discussion

In this study, hexaflumuron was effective on larvae of P. xylostella through ingestion. Kao and Cheng (1998) examined toxicity of hexaflumuron on four strains of P.

xylostella. Mean of LC₅₀s were 0.242, 3.98, 5.74 and 10.94 mg/L in susceptible and three resistant strains, respectively.

Also hexaflumuron had good impact on biological char- acteristics ofP. xylostella. In general, the effects of hexaflumuron on biological parameters were greater in the LC25group.

In some studies, impacts of IGRs on insects and mites have been investigated. Sublethal effects of hexaflumuron

on insects have been examined (Bakret al., 2009; Abo- Elgharet al., 2003; Kellouche & Soltani, 2006; Coppen &

Jepson, 1996). In our results, fecundity ofP. xylostellawas declined by sublethal doses of hexaflumuron. This clearly shows that ovaries of females were affected by hexaflumuron and it caused reduction in egg laying. Decreasing fecundity is an important factor to success in pest management. Bakret al.(2009) showed that all nymphs ofSchis- tocerca gregaria(Forsk˚al, 1775) when treated with 75 and 100 mg/L of hexaflumuron did not change into adults.

Also duration of nymphal development of S. gregaria were prolonged. In other study, hatchability ofCalloso- bruchus maculatus (Fabricius, 1775) (Col.: Bruchidae) declined significantly in treatments of hexaflumuron and pyriproxyfen (Abo-Elgharet al., 2003). Also, Kellouche and Soltani (2006) studied the effect of hexaflumuron on C. maculatesand found significant decreases in fecundity, adult longevity and increases in developmental time ofC. maculates. Decreasing fecundity and adult longevity and increasing developmental time ofP. xylostellain this study, was similar to results of Kellouche and Soltani (2006) using a different insect. Coppen and Jepson (1996) reported that exposure ofS. gregariato hexaflumuron and teflubezuron prolonged developmental time of nymphal instars. In this study, sublethal doses of hexaflumuron in the parent generation reduced pupal weight of P. xy- lostellabut the offspring generation was not affected by hexaflumuron, indicating that hexaflumuron had a di- rect effect more than an indirect effect. Josan and Singh (2000) stated that a chitin synthesis inhibitor, lufenuron at lethal concentration caused significant decrease in pupal weight of P. xylostella. Also fecundity was diminished in the treatment group but larval and pupal developmental time did not change. According to these results, hexaflumuron had no ability to change hatchability of theP. xylostella. Unlike the present research, Wilson and Cryan (1997) showed that lufenuron, diminished hatchability ofDrosophila melanogaster(Meigen). Consoliet al.

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(2001) reported that survival rate ofTrichigramma galloi (Zucchi) which were treated by lufenuron and triflumuron in the egg–larva and pre-pupal stages were significantly lower than control. In other study, Biddinger and Hull (1999) found that an IGR, diflubenzurun did not affect pupal duration time and pupal survivorship of females of Platynota idaeusalis (Walker, 1859) (Lep.: Tortrici- dae). In this study, survival of larval stages ofP. xylostella was diminished in the offspring generation. Physiologi- cal effects in the parent generation resulted in decreased survival of offspring. S´aenz-De-Cabez´onet al.(2006) re- vealed a decrease in survival trend, gross reproductive rate,net reproduction rate and intrinsic rate of increase of Tetranychus urticae(Koch) (Acari: Tetranychidae) which had been treated with triflumuron, as an IGR. In the study by Yin et al.(2008), LC₂₅ and LC₅₀ concentrations of spinosad decreased intrinsic rate of increase, net reproduction rate, gross reproduction rate and increased doubling time inP. xylostella.Lashkariet al.(2007) indicated that imidacloprid and peymetrozine declinedrm,R₀,λ(finite rate of increase) and increasedTand Dt of cabbage aphid, Brevicoryne brassicae(Linnaeus, 1758) (Hom.: Aphidi- dae). In insecticidal hormoligosis, sublethal doses of insecticides increase fecundity and reproduction parameters of insects. Hormoligosis has been shown in some insects.

Kerns and Stewart (2000) observed that treatingMyzus persicae(Sulzer, 1776) with sublethal doses of bifenthrin increasesed netR0and nymph production. Hormoligosis was seen inP. xylostellain some studies (Sotaet al., 1998;

Fujiwaraet al., 2002; Nemoto, 1993). Sotaet al.(1998) stated that fecundity and rm of P. xylostella with sublethal concentrations of fanvalerate were increased. Mean number of eggs laid by females ofP. xylostellain LC₂₅ groups of fenvalerate was higher than control but it was not significant (Fujiwaraet al., 2002). In this study, GRR, defined as follows [GRR=δ

x=0m_x] (where GRR is gross reproduction rate andm_x is age-specific fertility) was increased in LC10treatment. It can be hormoligosis.

To identify this, more investigation is needed.

In summary, the present results suggest hexaflumuron has an effective role on larval stages of theP. xylostella.

Also sublethal doses of hexaflumuron had effects onP.

xylostella, such as reduction in pupal weight, total survival rate, adult longevity, female fecundity and other biological parameters. Also hexaflumuron caused hormoligosis inP.

xylostella. The mechanism of these effects and resurgence by hexaflumuron may be studied in the future.

Acknowledgments

We thank the Agricultural Entomology section of Iranian Research Institute of Plant Protection, Tehran, Iran and the

Entomology section of the Department of Plant Protection of Shahed University, Tehran, Iran.

References

Abo-Elghar, G.E., El-Sheikh, A.E., El-Sayed, F.M., El- Maghraby, H.M. and El-Zun, H.M. (2003) Persistence and residual activity of an organophosphate, pirimiphos-methyl, and three IGRs, hexaflumuron, teflubenzuron and pyriproxyfen, against the cowpea weevil,Callosobruchus maculatus (Coleoptera: Bruchidae).Pest Management Science, 60, 95–

102.

Bakr, R.F.A., Mohammed, M.I., El-Gammal, A.E.M. and Mahdy, N.M. (2009) Biological effects of chitin-synthesis inhibitor, hexaflumuron compound on the desert locust,Schis- tocerca gregaria(Forsk˚al). Egyptian Academic Journal of Biological Science, 1, 49–57.

Biddinger, D.J. and Hull, L.A. (1999) Sublethal effects of selected insecticides on growth and reproduction of a labora- tory susceptible strain of tufted apple bud moth (Lepidoptera:

Tortricidae). Journal of Economic Entomology, 92, 314–

324.

Consoli, F.L., Botelho, P.S.M. and Parra, J.R.P. (2001) Selectiv- ity of insecticides to the egg parasitoidTrichogramma galloi Zucchi, 1988 (Hym., Trichogrammatidae).Journal of Applied Entomology, 125, 37–43.

Coppen, G.D.A. and Jepson, P.C. (1996) The Effects of the duration of exposure on the toxicity of diflubenzuron, hexaflumuron and teflubenzuron to various stages of II instar Schistocerca gregaria.Pesticide Science, 46, 191–197.

Cutler, G.C., Scott-Dupree, C.D., Tolman, J.H. and Harris, C.R. (2005) Acute and sublethal toxicity of novaluron, a novel chitin synthesis inhibitor, toLeptinotarsa decemlineata (Coleoptera: Chrysomelidae).Pest Management Science, 61, 1060–1068.

Dallaire, R., Labrecque, A., Marcotte, M., Bauce, ´E. and Delisle, J. (2004) The sublethal effects of tebufenozide on the precop- ulatory and copulatory activities ofChoristoneura fumiferana andC. rosaceana.Entomologia Experimentalis et Applicata, 112, 169–181.

Dhadialla, T.S., Carlson, G.R. and Le, D.P. (1998) New insecticides with ecdysteroidal and juvenile hormone activity.An- nual Review of Entomology, 43, 545–569.

Fujiwara, Y.T., Takahashi, T., Yoshioka, T. and Nakasuji, F.

(2002) Changes in egg size of the diamondback moth,Plutella xylostella(Lepidoptera: Yponomeutidae) treated with fenvalerate at sublethal doses and viability of the eggs.Applied Entomology and Zoology, 37, 103–109.

Hajjar, N.P. and Casida, J.E. (1978) Insecticidal benzoylphenyl ureas: structure activity relationships as chitin synthesis inhibitors.Science, 200, 1499–1500.

(7)

Haynes, K.F. (1988) Sublethal effects of neurotoxic insecticides on insect behavior.Annual Review of Entomology, 33, 149–

168.

Josan, A. and Singh, G. (2000) Sublethal effects of lufenuron on the diamondback moth,Plutella xylostella(Linnaeus).Insect Science and Its Application, 20, 303–308.

Kao, C. and Cheng, E.Y. (1998) Validation of a field monitor- ing system for BPU-type IGR resistance in the diamondback moth,Plutella xylostellapresumed working scheme based on IRAC method No. 7 (leaf dipping method).Journal of Agri- cultural Research of China, 47, 142–158.

Kellouche, A. and Soltani, N. (2006) Impact of hexaflumuron, a chitin synthesis inhibitor, on growth, development and reproductive performance of the progeny inCallosobruchus mac- ulatusafter adult treatments.African Journal of Agricultural Research, 1, 57–64.

Kerns, D.L. and Stewart, S.D. (2000) Sublethal effects of insecticides on the intrinsic rate of increase of cotton aphid.

Entomologia Experimentalis et Applicata, 94, 41–49.

Lashkari, M.R., Sahragard, A. and Ghadamyari, M. (2007) Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid,Brevicoryne bras- sicaeon rapeseed,Brassica napusL.Insect Science, 14, 207–

212.

Leonard, P.K., Riches, M.N. and Howard, M. (1987) XRD-473 environmentl pest interaction.Pesticide Science, 20, 157–159.

Mahmoudvand, M., Sheikhi Garjan, A. and Abbasipour, H.

(2009) Toxicity of neurotoxin insecticides on Diamondback moth,Plutella xylostella(Lep.: Plutellidae).Proceeding of the 6th Asia-Pacific Congress of Entomology. pp. 68–69. Beijing, China.

Maia, A.D.H., Alfredo, J.B. and Campanhola, C. (2000) Sta- tistical inference on associated fertility life table parameters using Jackknife technique: Computational aspects.Journal of Economic Entomology, 93, 511–518.

Marco, V. and Vinuela, E. (1999) Efectos del RCI hexaflumuron sobre larvas de la polilla mediterránea de la harinaEphes- tia kuehniellaZeller (Lepidoptera: Pyralidae) en aplicación tópica y por ingestión. Influencia de la edad de las larvas tratadas.Boletin de Sanidad Vegetal Plagas, 25, 59–68.

Moser, B.A., Koehler, P.G. and Patterson, R.S. (1992) Effect of methoprene and diflubenzuron on larval development of the cat flea (Siphonaptera: Pulicidae).Journal of Economic Entomology, 85, 112–116.

Mota-Sanchez, D., Bills, P.S. and Whalon, M.E. (2002) Arthro- pod resistance to pesticides: status and overview.Pesticides in Agriculture and the Environment(ed. W.E. Wheelers), pp.

241–272. Marcel Dekker Incrorporation, New York.

Nakagawa, Y., Matsutani, M., Kurihara, N., Nishimura, K.

and Fujita, T. (1992) Quantitative structure- activity studies of benzoylphenylurea larvides. VIII. Inhibition of N- acetylglucosamine incorporation into the cultured integument

of Chilo suppressalis Walker. Pesticide Biochemistry and Physiology, 43, 141–151.

Nemoto, H. (1993) Mechanism of resurgence of the diamondback moth, Plutella xylostella (L.) (Lepidoptera:

Yponomeutidae).Japan Agriculture Research Quarterly, 27, 27–32.

Ooi, P.A.C. (1986) Diamondback moth in Malaysia.Diamond- back Moth Management(eds. N.S. Talekar & T.D. Griggss), pp. 25–34. The Asian Vegetable Research and Development Center, AVRDC Publication, Shanhua, Tania, Taiwan, China.

Perez, C.J., Shelton, A.M. and Derksen, R.C. (1995) Effects of application technology and Bacillus thuringiensis sub- species on management ofB. thuringiensissubsp.kurstarki- resistant diamondback moth (Lepidoptera: Plutellidae).Jour- nal of Economic Entomology, 88, 1113–1119.

Pineda, S., Schneider, M.S., Smagghe, G., Martinez, A., Estal, P.D., Vinuela, E., Valle, J. and Budia, F. (2007) Lethal and sublethal effects of methoxyfenozide and spinosad onSpodoptera littoralis(Lepidoptera: Noctuidae).Journal of Economic En- tomology, 100, 773–780.

Sáenz-De-Cabezón, F.J., Mart´ınez-Villar, E., Moreno, F., Marco, V. and Pérez-Moreno, I. (2006) Influence of sublethal exposure to triflumuron on the biological performance ofTetrany- chus urticaeKoch (Acari: Tetranychidae).Spanish Journal of Agricultural Research, 4, 167–172.

Sammour, E.A., Kandil, M.A. and Abdel-Aziz, W.F. (2008) The reproductive potential and fate of chlorfluazuron and leufenuron against cotton leafworm Spodoptera littoralis (Boisd.).American-Eurasian Journal of Agricultural & Envi- ronmental Science, 4, 62–67.

SAS Institute (1997)SAS/STAT. Guide for Personal Computers.

Ver. 6.12. SAS Institute, Cary, NC.

Sota, N., Motoyama, N., Fujisaki, K. and Nakasuji, F. (1998) Possible amplification of insecticide hormoligosis from resistance in the diamondback moth,Plutella xylostella(Lepi- doptera: Yponomeutidae).Applied Entomology and Zoology, 33, 435–440.

Stark, J.D. and Wennergren, U. (1995) Can population effects of pesticides be predicted from demographic toxicological studies.Journal of Economic Entomology, 88, 1089–1096.

Su, N.Y. (1994) Field evaluation of a hexaflumuron bait for population suppression of subterranean termites (Isoptera:

Rhinotermitidae).Journal of Economic Entomology, 87, 389–

397.

Su, N.Y. and La Fage, J.P. (1987) Effects of soldier proportion on the wood-consumption rate of the Formosan subterranean termite (Isoptera: Rhinotermitidae).Sociobiology, 13, 145–

151.

Tabashnik, B.E. and Cushing, N.L. (1987) Leaf residue vs. top- ical bioassays for assessing insecticide resistance in the diamondback moth,Plutella xylostellaL.FAO Plant Protection Bulltein, 35, 11–14.

(8)

Talekar, N.S. and Shelton, A.M. (1993) Biology, ecology and management of the diamondback moth. Annual Review of Entomology, 38, 275–301.

Thorsteinson, A.J. (1953) The chemo tactic responses that de- termine host specificity in an oligophagous insect (Plutella maculipennis (Curt.) Lepidoptera). Canadian Journal of Zoology, 31, 52–72.

Wilson, T.G. and Cryan, J.R. (1997) Lufenuron, a chitin-

synthesis inhibitor, interrupts development of Drosophila melanogaster. The Journal of Experimental Zoology, 278, 37–44.

Yin, X.H., Wu, Q.J., Li, X.F., Zhang, Y.J. and Xu, B.Y. (2008) Sublethal effects of spinosad on Plutella xylostella (Lepi- doptera: Yponomeutidae).Crop Protection, 27, 1385–1391.

Accepted November 28, 2010