Effect of emamectin benzoate on life history traits and relativefitness of Spodoptera litura (Lepidoptera: Noctuidae)

Syed Muhammad Zaka & Naeem Abbas &Sarfraz Ali Shad & Rizwan Mustafa Shah

Received: 6 July 2013 /Accepted: 12 January 2014# Springer Science+Business Media Dordrecht 2014

Abstract Emamectin benzoate, a semisyntheticbioinsecticide, has been used frequently for the manage-ment of lepidopteran pests of cotton worldwide. Toassess the resistance risk and design strategy for resis-tance management, life history traits were establishedfor emamectin benzoate-resistant, unselected and sus-ceptible S. litura strains based on the laboratory obser-vations. Bioassay results showed that the emamectinbenzoate-selected strain developed a resistance ratio of911-fold compared with that of the susceptible strain.The emamectin-selected strain had a relative fitness of0.37 and lower prepupal and pupal weights, prolongedlarval duration and development time, lower fecundityand hatchability compared with the susceptible strain.Mean population growth rates, such as intrinsic rate ofpopulation increase and biotic potential, were lower forthe emamectin-selected strain compared with the sus-ceptible strain. Development of resistance can cost con-siderable fitness for the emamectin-selected strain. Thepresent study provided useful information for determin-ing potential management strategies to overcome devel-opment of resistance.

Keywords Armyworm . Biotic potential . Fitness cost .

Intrinsic rate of population increase . Resistance

Introduction

The armyworm, Spodoptera litura (Fabricius)(Noctuidae: Lepidoptera), is a highly polyphagous pestwith a wide range of hosts including 40 plant families(Brown & Dewhurst 1975; Holloway 1989). The majorcrops attacked by this pest in Pakistan are cotton, chick-pea, tobacco, berseem, alfalfa, groundnut and vegetableslike brinjal, potato and cucurbits (Ahmad 2009). Underfavorable conditions, the population increases in greatnumbers and extensive insecticidal applications are re-quired to save the infested crops. Outbreaks have beenmore common in South Asia, including Pakistan, mostlydue to the development of insecticide resistance andsubsequent control failures (Ahmad 2009; Kranthi et al.2001, 2002). Resistance to carbamates, organophos-phates and pyrethroids (Ahmad et al. 2007) andindoxacarb, spinosad, fipronil, avermectins, acetamipridand insect growth regulators have been reported for thispest in Pakistan (Ahmad et al. 2008; Shad et al. 2010).Resistance to various insecticides is a worldwide problemand even the most effective insecticides have failed tocontrol this pest. High levels of resistance to syntheticinsecticides have caused sporadic outbreaks of S. litura inmany countries, including Pakistan (Saleem et al. 2008).

Emamectin benzoate is a semisynthetic bioinsecticidecomposed of a naturally occurring compound,avermectin, extracted from the soil microorganismStreptomyces avermitilis (Burg et al. 1979). The hydro-chloride salt of emamectin was discovered fromavermectin derivatives in laboratory screenings usingthe southern armyworm, Spodoptera eridania (Cramer),

PhytoparasiticaDOI 10.1007/s12600-014-0386-5

S. M. Zaka :N. Abbas (*) : S. A. Shad (*) : R. M. ShahDepartment of Entomology, Faculty of Agricultural Sciencesand Technology, Bahauddin Zakariya University,Multan, Pakistane-mail: naeemsurbana@gmail.come-mail: sarfrazshad@bzu.edu.pk

and the tobacco budworm, Heliothis virescens (Guenee)(Ishaaya et al. 2002; Mrozik 1994). Emamectin benzoateis a chloride channel activator effect causing pre-vention of muscle contraction, cessation of feeding andfinally death (Ishaaya 2002). It is used at low rates forthe control of lepidopteran pests in different crops(Ishaaya et al. 2002).

Fitness costs related to insecticide resistance arewhere development of resistance to an insecticide isaccompanied by high energy cost or significant disad-vantage that diminishes the insect's fitness comparedwith its susceptible counterparts in the population(Kliot & Ghanim 2012). When relative fitness in resis-tant insect pests is reduced, the rotational ordiscontinuing use of insecticides may decrease the oc-currence of resistant genes and return their susceptibilityto that insecticide (Georghiou & Saito 1983; Roush &McKenzie 1987). When the relative fitness of resistantpests is not influenced by resistance, this can delay thedevelopment of resistance and it is difficult to restoresusceptibility to that insecticide (Plapp et al. 1989). Ahigh dose refuge is the most commonly used strategy fordelaying the development of resistance, in which aninsecticide-free refuge harbors the susceptible geno-types. However, this strategy depends on the recessiveinheritance of resistance in heterozygotes which areproduced by crosses of resistant and susceptible insects(Georghiou & Taylor 1977). Consequently, refuges thatmagnify costs or make them less recessive could en-hance resistance management (Carriere et al. 2010;Crowder & Carriere 2009). Fitness costs are modulateddue to changes in environmental conditions, such ashost plants, overwintering, competition and natural en-emies (Gassmann et al. 2009). The pleiotropic effectsrelated to resistant alleles can occur due to changes insurvival rates, pupal weights, development time,fecundity/female and percent egg hatching (Brewer &Trumble 1991; Groeters et al. 1994). Compared withsusceptible females, resistant females generally havelower fecundity (Georghiou 1972).

Fitness cost associated with insecticide resistance iswell documented in S. litura resistance to imidacloprid(Abbas et al. 2012) and also in many other insects suchas Plutella xylostella to tebufenozide (Cao & Han2006), Nilaparvata lugens to imidacloprid (Liu & Han2006), Heliothis virescens to indoxacarb and deltameth-rin (Sayyed et al. 2008a), Spodoptera exigua totebufenozide (Jia et al. 2009) and P. xylostella tofufenozide (Sun et al. 2012). Understanding life history

parameters changed by fitness costs, degree of domi-nance of these costs and environmental factors whichaffect these fitness costs can be helpful in developingresistance management strategies. The present experi-ment was planned to study the life history traits ofSusceptible, UNSEL and Ema-SEL populations and todetermine the fate of fitness.

Materials and methods

Populations and rearing of S. litura The susceptiblepopulation of S. litura was obtained from the Instituteof Entomology, Guangzhou, China, and designated asSusceptible population (previously Lab-PK). This pop-ulation was collected from a field of cauliflower in 1997and since then has been reared on an artificial diet in alaboratory without exposure to insecticides (Shad et al.2012). The field population of S. litura was collectedfrom a cotton (Gossypium hirsutum L.) field located inPunjab, Pakistan, where different insecticides have beenused for the management of variouw insect pests (Shadet al. 2010). The field-collected population was separat-ed into two populations in the first generation. Onepopulation was not exposed to insecticide and designat-ed as UNSEL, while the other population was exposedto emamectin benzoate for three generations and desig-nated as Ema-SEL (published data; Shad et al. 2010).The UNSEL population was reared for 11 generationswithout exposure to insecticides. The populations werereared on artificial diet (Gupta et al. 2005) at standardlaboratory conditions as described previously by Abbaset al. (2012).

I n s e c t i c i d e a n d c o n c e n t r a t i o n re s p o n s ebioassays Concentration response bioassays ofemamectin benzoate (Proclaim® 019 EC, Syngenta;Pakistan) were done on second instar larvae by usingthe Jia et al. (2009) diet incorporation method. Fiveconcentrations of insecticides, and distilled water onlyas a control, were mixed into a semi-synthetic diet asdescribed by Gupta et al. (2005). The range of concen-trations of emamectin benzoate was 0.0156–0.25μgml−1 for Susceptible, 0.0625–1μg ml−1 for UNSEL,and μg ml−1 for Ema-SEL populations. After setting,the diet was cut into small cubes (3×3×3cm) and trans-ferred to 5-cm-diam petri dishes, with five petri dishesused for each concentration. A total of 180–480 secondinstar larvae were used for each bioassay, including

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control (30 larvae), with 30–50 larvae utilized per con-centration. The bioassays were kept under the condi-tions mentioned above. Mortality was assessed 72 hafter exposure. Larvae were considered dead if theydid not make coordinated movements when proddedwith a probe.

Life history traits Fifty 1st instar larvae were randomlycollected from each of the Susceptible, UNSEL andEma-SEL populations for determination of fitness pa-rameters. These larvae were weighed and separated intoone larva placed individually in glass vials having arti-ficial diet for rearing. All stages of populations weremaintained under standard laboratory conditions(Abbas et al. 2012). Three replications were usedfor each population. The prepupal weight was taken fora final time.

Pupal weight and pupal duration were recorded aswere emergence rate of healthy adults and female ratio.The newly emerged adults were paired and maintained

together. Three pairs were used as one replication andthree replications were used for each population. Everypair was maintained in a plastic jar (11×8cm) havingtissue papers hung vertically for oviposition. The eggswere collected daily and the number of eggs was record-ed. Each day’s total oviposition was marked to eliminatethe confusion with previous batches. Hatchability wasrecorded according to Liu & Han (2006) as follows:

Hatchability ¼ All neonates=All eggs

The net replacement rate (R0) was calculated accord-ing to Jia et al. (2009) as follows:

R0 ¼ Nnþ1=Nn

where Nn means the population quantity of the parentgeneration and Nn+1 means the numbers of the nextgeneration larvae. The relative fitness of the Ema-SELstrain was calculated according to Jia et al. (2009) asfollows:

Relative fitness ¼ R0 of the Ema−SEL strain=R0 of the UNSEL strain

The mean relative growth rate (MRGR) was calcu-lated according to Radford (1967) by the followingformula:

MRGR ¼ ln W2 mgð Þ−ln W1 mgð Þ½ �=T

Where W1 is initial larval weight, W2 is the prepupalweight and T is the time (days) from initial larval toprepupal stage.

The intrinsic rate of population increase (rm) wasdetermined according to Birch (1948) and Alyokhin &Ferro (1999) as follow:

rm ¼ ln R0=T

where T means development time (egg to adultemergence).

Biotic potential (BP) was determined according toRoush & Plapp (1982) as follows:

BP ¼ ln F=DTr

where F means the fecundity (mean number of larvae/female) and DTr is the ratio between development timeof the considered strain and Susceptible strain.

Statistical analysis The concentration response datawas analyzed by using probit analysis (Finney 1971)with POLO software (LeOra Software) to determine theLC50 values, their standard errors, slopes and 95% fidu-cial limits (FL). Mortality was corrected using Abbott’sformula (1925), if necessary. Resistance ratio (RR) wasdetermined as the LC50 of Ema-SEL population dividedby the LC50 of the Susceptible population. LC50 valuesdid not differ significantly (P>0.05) when their 95% FLoverlapped (Litchfield & Wilcoxon, 1949).

Data of larval and pupal duration, prepupal and pupalweight, development time, female ratio, fecundity,hatchability, MRGR, biotic potential and intrinsic rateof increase were analyzed using the General LinearModel Procedure (GLM) at 5% level of significance tocheck the effects of population on different variables;the fixed effect model was employed as follows:

Yij ¼ μþ Pi þ eij:

where Yij is the response variable, μ is the populationaverage, Pi represents ith population (i =1, 2, 3) and eij isthe random error associated with each observation and issupposed to be normally distributed with mean μ andvariance σ2. The means were compared by Least

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Significant Difference (LSD) test at P≤0.05 byusing Statistix version 8.1, analytical software(Anon. 2005).

Results

Emamectin benzoate effect on the Susceptible, UNSELand Ema-SEL populations of S. litura The LC50 valuesof the Susceptible, UNSEL and Ema-SEL populationsof S. litura were significantly different from each otheras their 95% fiducial limits did not overlap.Susceptibility to emamectin benzoate of the UNSELwas significantly less than that of the Susceptible, witha resistance ratio of 20.62-fold (Table 1). After threegenerations of selection with emamectin benzoate, theEma-SEL population of S. litura developed 911.25-foldresistance compared with the Susceptible population(Table 1).

Fitness parameters for the Susceptible, UNSEL andEma-SEL populations of S. litura Comparison of dif-ferent life traits among the Ema-SEL, UNSEL andSusceptible S. litura populations showed significantdifferences that can be correlated with fitness costs.The fitness parameter means are given in Table 2.Male larval duration of Ema-SEL population was sig-nificantly longer than the Susceptible and UNSEL pop-ulations (F=5.94, df =2, 6, P=0.038). However, malelarval duration of Susceptible and UNSEL populationswas similar. The female larval duration of the Ema-SELpopulation was significantly longer than the Susceptiblepopulation (F=52.9, df =2, 6,P<0.001) but similar to theUNSEL population. Male prepupal weight (F=17.1,df =2, 6, P=0.003) and female prepupal weight(F=10.8, df =2, 6, P=0.01) of the Ema-SEL were

significantly lower than the Susceptible and UNSELpopulations. Male pupal weight (F=11.1, df =2, 6,P=0.009) and female pupal weight (F=14.2, df =2, 6,P=0.005) of the Ema-SEL population were significantlylower compared with the Susceptible population. Themale pupal duration (F=2.00, df =2, 6, P=0.215) andfemale pupal duration (F =2.03, df =2, 6, P =0.212) didnot differ significantly among the tested populations.

Male development time (egg to adult) of the Ema-SEL population was significantly longer (F=9.34, df =2,6, P=0.014) than that of the UNSEL population. Femaledevelopment time (egg to adult) of the Ema-SEL popu-lation was significantly longer (F=4.73, df =2, 6,P=0.058) than that of the Susceptible population.There was no significant difference in female ratioamong the populations examined (F=2.43, df =2, 6,P=0.169). The average number of eggs laid by theEma-SEL females was significantly lower (F =22.3,df =2, 6, P=0.002) than the UNSEL and Susceptiblefemales (Table 2). The percentage of eggs hatching inthe Ema-SEL population was significantly lower(F=134, df =2, 6, P<0.001) than that of the UNSELand Susceptible populations although percentage eggshatching between the UNSEL and Susceptible also dif-fered significantly. The number of next generation lar-vae of the Ema-SEL, UNSEL and Susceptible popula-tions was 2699, 7318 and 9273, respectively. The netreplacement rate of the Ema-SEL, UNSEL andSusceptible populations was 53.75, 146.60 and185.46, respectively. The relative fitness of the Ema-SEL population was 0.37 compared with the UNSELpopulation.

Mean relative growth rates of larvae (MRGR), intrinsicrate of population increase (rm), and biotic potential(Bp) of the Ema-SEL, UNSEL and Susceptible

Table 1 Resistance to emamectin benzoate of the Susceptible, UNSEL and Ema-SEL populations

Population na LC50 μg/ml (95%FLb) Slope (SE) χ2 df p RRc

Susceptible 480 0.016 (0.012-0.021) 1.22 ±0.13 0.33 5 0.99 1

UNSEL (G11) 180 0.33 (0.22-0.45) 1.75 ±0.29 2.86 4 0.58 20.62

Ema-SEL (G4) 180 14.58 (8.41-18.08)* 2.88 (±0.29) 1.60 4 0.81 911.25

a Number of larvae used in bioassay including controlb Fiducial limitsc Resistance ratio, calculated as (LC50 of UNSEL and Ema-SEL population) / (LC50 of Susceptible population)

*Published data (Shad et al. 2010)

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populations Mean initial weights of larvae of the Ema-SEL, UNSEL and Susceptible populations were 0.02,0.04 and 0.004, respectively. Mean male relative growthrates of the Ema-SEL, UNSEL and Susceptible popula-tions were 0.76, 0.78 and 0.96, respectively. Mean fe-male relative growth rates of the Ema-SEL, UNSEL andSusceptible populations were 0.78, 0.76 and 1.06, re-spectively. Mean male relative growth rate of the Ema-SEL population was significantly lower (F=99.0, df =2,6, P<0.001) than that of the Susceptible population.Mean female relative growth rate of the Ema-SEL pop-ulation was also significantly lower (F=38.4, df =2, 6,P<0.001) than the Susceptible population but similar tothe UNSEL population (Fig. 1). Mean intrinsic rate ofpopulation increase of the Ema-SEL, UNSEL andSusceptible populations was 0.16, 0.21 and 0.25 (d-1),respectively. Biotic potential of the Ema-SEL, UNSELand Susceptible populations was 4.84, 5.93 and 6.93,respectively. The intrinsic rate of population increaseand biotic potential of the Ema-SEL population wassignificantly reduced compared with the UNSEL andSusceptible populations. There was a significant differ-ence in intrinsic rate of population increase among allthe populations tested (F=51.1, df =2, 6, P<0.001)(Fig. 2). Similarly, there was a significant difference inthe biotic potential among all the populations examined(F=53.1, df =2, 6, P<0.001) (Fig. 3).

Discussion

After continuous selection of the field population withemamectin benzoate, a significant increase in RR value(911-fold) was observed when compared with the sus-ceptible population, suggesting that the selectionprocess had a significant influence on the developmentof resistance.

Fitness costs associated with emamectin benzoateresistance in S. litura are given in Table 1. Insecticidescan change the biology of resistant organisms. Severalreports are available on resistant organisms showingfitness costs or stimulate their abundance (He et al.2007; Yao et al. 2002). The insect biology variationsare closely related to different insecticides (Zhang et al.2009). Relative fitness is the ability of survival andreproduction of a resistant population compared withthe susceptible population. Studying the relative fitnessof resistant populations is essential for understandingandmanaging resistance problems (Georghiou & Taylor1977). It is usually believed that the biological charac-teristics (prolonged growth period and reduced fecundi-ty) change the relative fitness cost. These results showedthat under continuous selection pressure, the Ema-SELpopulation had significantly longer larval duration anddevelopmental time, reduced oviposition, reducedhatching, and lower pupal and prepupal weights.

Table 2 Mean life traits of theEma-SEL, UNSEL andSusceptible populations ofSpodoptera litura(all data are ± SE)

zWithin rows, values followed bya common letter do not differsignificantly (P>0.05)yDT, development time

Life-history trait Ema-SEL UNSEL Susceptible

Larval duration male (days) 13.67 ±0.17 Az 12.94 ±0.20 B 12.87 ±0.18 B

Larval duration female (days) 13.41 ±0.05 A 13.19 ±0.05 A 11.13 ±0.29 B

Prepupal weight male (mg) 799.47 ±55.29 B 956.55 ±3.91 A 1064.80 ±6.76 A

Prepupal weight female (mg) 823.46 ±7.73 A 1015.2 ±28.49B 990.40 ±46.48B

Pupal weight male (mg) 317.83 ±13.26 B 322.29 ±10.71B 386.33 ±10.41A

Pupal weight female (mg) 325.55 ±9.64 B 351.84 ±9.17B 390.93 ±7.16A

Pupal duration male (days) 9.08 ±0.08 A 8.62 ±0.15A 9.33 ±0.41A

Pupal duration female (days) 9.29 ±0.11 A 8.71 ±0.08A 8.33 ±0.57A

DT egg to adult male (days)y 24.75 ±0.14 A 23.53 ±0.07 B 24.20 ±0.31AB

DT egg to adult female (days) 24.70 ±0.07 A 23.91 ±0.26 AB 22.00 ±1.10B

Female ratio 58.52 ±2.31A 52.57 ±2.35A 57.33 ±2.91A

No. of eggs per female 423.33 ±131.27B 895.00 ±150.66A 1121.10 ±14.25A

Hatchability (%) 70.67 ±1.14C 88.49 ±0.98B 92.07 ±0.76A

Next generation larvae 2699 7318 9273

Mean number of larvae/female 299.89 813.11 1030.33

Net reproductive rate (Ro) 53.75 146.6 185.46

Relative fitness 0.37 0.79 1

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Therefore, emamectin resistance in the S. litura popula-tion corresponded with a significant decrease in most ofthe life history traits and these results indicate the pres-ence of a trade-off in resource distribution among resis-tance and fitness costs.

Fitness costs and dominance of fitness costs associ-ated with resistance determine the rate of resistancedevelopment (Carriere et al. 1994). The developmentof insecticide resistance depends on the level of insecti-cide applications and relative fitness of a heterozygouspopulation compared with that of the susceptible

genotype when the resistant genes are rare (Roush &McKenzie 1987). Resistant genes are present mainly inheterozygote insects at lower frequency and when fit-ness costs are dominant, resistance could be increasedslowly in the population, for example, small fitness cost(1%) in heterozygotes compared with the susceptiblehomozygotes can delay the increase of resistant alleles(Carriere & Tabashnik 2001). Although we have notmeasured the fitness cost of hybrid progeny(resistant×UNSEL), the life-history parameters in thepresent study suggest that the fitness costs were domi-nant due to significant differences in life history param-eters of the Ema-SEL compared with the UNSEL and

Fig. 1 Comparison of meanrelative growth rate (MRGR)among the Susceptible, UNSELand Ema-SEL populations ofSpodoptera litura. Error barsshow standard errors. Within eachpopulation, bars having the sameletters do not differ significantly(LSD test, P≤0.05)

Fig. 2 Comparison of Intrinsic rate of population increase amongthe Susceptible, UNSEL and Ema-SEL populations of Spodopteralitura. Error bars show standard errors. Values of different popu-lations differ significantly (LSD test, P≤0.05)

Fig. 3 Comparison of biotic potential (Bp) among the Suscepti-ble, UNSEL and Ema-SEL populations of Spodoptera litura.Error bars show standard errors. Values of different populationsdiffer significantly (LSD test, P≤0.05)

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Susceptible populations. Similarly, the fitness costs oforganophosphate resistance in Culex pipiens L. weredominant (Chevillon et al. 1997) and fitness costs ofdieldrin resistance were additive to co-dominance inLucilia cuprina (Wiedemann) (McKenzie 1990).

Fitness costs associated with insecticide resistanceoccur where the development of resistance to an insec-ticide is accompanied by high energetic cost or othersignificant disadvantages that diminish the insect's fit-ness compared with its susceptible counterparts in thepopulation (Kliot & Ghanim 2012). Decrease of relativefitness associated with insecticide resistance has beendemonstrated for many insects including Nilaparvatalugens (Liu & Han 2006), S. exigua (Jia et al. 2009),Bemisia tabaci (Feng et al. 2009), Bactrocera dorsalis(Zhang et al. 2010) and P. xylostella (Cao & Han 2006;Sun et al. 2012). Fitness costs associated withimidacloprid resistance in S. litura were also studiedrecently by Abbas et al. (2012). The present study alsoindicates that the emamectin resistance could decreaserelative fitness in S. litura. To the best of our knowledge,this is the first report of fitness cost to emamectin inS. litura, worldwide. Consequently, rotation of insecti-cides should be implemented in resistance managementstrategies.

The natural intrinsic rate of population increase pro-vides an estimate of potential growth of insect populations(Rabinovich 1972), which provides considerable insightaside from organism life history traits. The net replace-ment rate (Ro) is not the major component to assess thepotential of a population’s growth because intrinsic rate ofpopulation increase depends on fecundity, percentage ofegg hatching, growth and adult emergence (Khan et al.2012; Saeed et al. 2010). Therefore, variations in theselife history traits might affect the rate of population in-crease of S. litura. The Ema-SEL strain showed a signif-icantly lower intrinsic rate of population increase (rm) thanthe UNSEL and Susceptible populations (Fig. 2). Intrinsicrate of population increase is positively related to themean relative growth rate (Pathan et al. 2010; Sayyed &Wright 2001; Sayyed et al. 2005, 2008a, 2008b).Previously, the intrinsic rate of population increase hasbeen reported in many insects, for example, spinosad andBt toxin Cry1Ac-resistant P. xylostella (Sayyed &Wright2001; Sayyed et al. 2008b), deltamethrin and indoxacarbresistant H. virescens (Sayyed et al. 2008a), pyrethroid-and organophosphate-resistant C. carnea (Pathan et al.2010) and imidacloprid-resistant S. litura (Abbas et al.2012).

Management of insecticide resistance depends on thefitness costs such that the numbers of resistance control-ling factors would be reduced when selection pressure isstopped (Ferre & Van Rie 2002). Analysis of modelsrecommends that incomplete resistance and fitness costsmay delay the development of insecticide resistancewithin pest populations (Tabashnik et al. 2003).Resistant populations suffer disadvantages in the pres-ence of insecticide beyond their performances in theabsence of insecticide, if resistance is incomplete(Sayyed et al. 2005). In the present study, the Selectedpopulation has a greater disadvantage than the UNSELand Susceptible populations, showing that the develop-ment of resistance against emamectin benzoate wouldbe delayed.

Acknowledgments We are highly thankful to Dr. Robert J. (Jeff)Whitworth, Associate Professor, Department of Entomology,Kansas State University, USA, for sparing his precious time tocheck this manuscript for improvement of the English grammar.

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