Contact toxicity of insecticides for attract-and-kill applications against adult Plodia...

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Research ArticleReceived: 9 October 2009 Revised: 13 January 2010 Accepted: 15 January 2010 Published online in Wiley Interscience: 4 March 2010

(www.interscience.wiley.com) DOI 10.1002/ps.1938

Contact toxicity of insecticidesfor attract-and-kill applications against adultPlodia interpunctella (Hubner)(Lepidoptera: Pyralidae)Manuel Camposa,b∗ and Thomas W Phillipsa,c

Abstract

BACKGROUND: The Indian meal moth (IMM), Plodia interpunctella (Hubner), is an important pest of stored food products.Contact toxicities of 13 insecticides applied to different surfaces were evaluated at registered label and a higher dose for killingadult males. The ultimate objective was to develop attract-and-kill technologies for P. interpunctella. Two-day-old adult maleswere exposed to treated surfaces for 2.0 s and then paired with virgin females for mating and oviposition over a 24 h period.

RESULTS: Permethrins and pyrethrins (organic pyrethrin and pyrethrin plus a synergist) caused over 70% mortality to males.Oviposition was impacted by these insecticides, while egg hatch was not. A second experiment tested the 8 week residualtoxicity of cyfluthrin, permethrin and pyrethrin at label and at a higher dose of 20 g AI L−1 on five surfaces: plastic-coated paper,metal, painted plastic, unpainted plastic and wood. Permethrin at 20 g AI L−1 suppressed males at over 80% for up to 8 weeksand retained activity on surfaces made with plastic-coated paper, metal or plastic. Oviposition was variable among treatments.Egg hatch was generally unaffected by treatment.

CONCLUSION: Effective attract-and-kill surfaces can be developed for killing IMM males and thereby potentially lead to reducedreproduction and, ultimately, population suppression.c© 2010 Society of Chemical Industry

Keywords: stored-product insects; residual insecticide; surface sprays; oviposition; pest control; Plodia interpunctella

1 INTRODUCTIONThe Indian meal moth, Plodia interpunctella Hubner (Lepidoptera:Pyralidae), is a common pest in confectionary factories, foodwarehouses, retail stores, food processing facilities, bulk-storedcommodities,1 – 3 flour mills4 and dried vegetable commodities.5

Plodia interpunctella is also reported as a potential pest insoybean meal commodities.6 The infestation and damage byP. interpunctella and similar species of stored-product moths ofthe subfamily Phycitinae are the cause of many complaints fromfood manufacturers, retailers and consumers.7 There have beenseveral methods of pest control for stored-product moths, but theireffectiveness is limited and alternatives are needed. The fumigantmethyl bromide was widely used to control storage insects, butits use has been banned or is currently being curtailed, exceptfor quarantine treatments.7,8 Protective sprays of synergizedpyrethrum mixed with technical oil have been applied to stacksof bagged wheat against Cadra cautella (Wlk.), a related pestspecies, but it caused excessive staining of stored bags.9 Aerosolapplications using pyrethrin in a chocolate-based consumablesfactory against C. cautella reduced the use of other pesticides by asmuch as 80–90%, but there were control failures owing to survivalof non-exposed insect life stages.10

Pheromone-based methods for controlling stored-productinsects have been of interest to researchers and pest managers,

as the use of traditional chemical controls has become limitedowing to regulations or low biological activity. The attract-and-killmethod utilizes an attractant, such as a sex pheromone, to lureinsects of the target species to an insecticidal surface or device formass killing and ultimate population suppression, and can havethe same effect as mass trapping.7,11,12 When a synthetic femalesex pheromone is used to lure male moths in an attract-and-kill strategy, a large number of male moths must be killed overextended periods of time to reduce mating and reproduction, andultimately to suppress the pest population. The attract-and-killapproach may be more practical than mass trapping because notrap servicing or other frequent maintenance would be required.The major sex pheromone of the Indian meal moth is a strongattractant for males, and earlier work has suggested it can be

∗ Correspondence to: Manuel Campos, Texas AgriLife Extension Service, TexasA&M University, 17360 Coit Road, Dallas, TX 75252, USA.E-mail: [email protected]

a Department of Entomology and Plant Pathology, Oklahoma State University,Stillwater, OK, USA

b Texas AgriLife Extension Service, Texas A&M University, Dallas, TX, USA

c Department of Entomology, Kansas State University, Manhattan, KS, USA

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Attract-and-kill insecticides for P. interpunctella www.soci.org

used for population control with attract-and-kill techniques.13,14

A gel-based attract-and-kill formulation that contains syntheticfemale sex pheromone and permethrin was found to be activeagainst adult males of P. interpunctella in simulated field trials.15

This same type of insecticide gel formulation was also effectiveagainst adult males of Grapholita molesta (Busck.)16 with thatspecies’ pheromone. However, the attract-and-kill gel formulationrequired a high-density application rate, and field persistence ofthe attractant in the gel was limited. The efficacy of residual-contactinsecticides for protecting grain and controlling stored-productinsects in structures has been studied and reviewed,17,18 butdevelopment of an attract-and-kill method for storage mothsrequires further research on the residual activity of short-termtime contact of adult males with insecticides.

The objective of the study reported here was to evaluatethe contact toxicities of 13 insecticides with potential for usein attract-and-kill formulations to control P. interpunctella malessubjected to brief contact times. The most active materials werefurther evaluated for their residual toxicity for up to 8 weeksafter application on different surfaces. The reproductive successof treated P. interpunctella males was determined after pairingwith female moths and assessment of eggs laid and larvaeproduced.

2 MATERIALS AND METHODS2.1 InsectsPlodia interpunctella adults from a laboratory culture at OklahomaState University were reared on a diet containing corn meal, chickstarter crumbles, chick laying crumbles and glycerol (4 + 2 + 2 + 1parts by volume) in 450 mL glass jars maintained at 28 ◦C, 60–70%relative humidity and 16 : 8 h light : dark photoperiod. Pupae wereisolated from colonies by placing 1.0 cm wide rolls of single-facedcorrugated cardboard into culture jars that contained wandering-stage larvae, which then pupated inside the corrugations. Pupaewere separated by sex and placed individually into 1.0 dramventilated vials (Fisher Scientific, Pittsburg, PA) and held untilthey emerged as adults.15 Experiments utilized 1–2-day-old virginadults, and each adult was only used once.

2.2 InsecticidesTable 1 lists the 13 commercial insecticides, grouped by type ofactive ingredient, used in the initial toxicity test. Insecticideswere applied at concentrations prescribed on the label (theso-called label dose, LD) on 9.0 cm diameter plastic petridishes (Fisher Scientific, Canada). Further experiments includedcommercial formulations containing cyfluthrin (Bayer, Kansas City,MO), permethrin (FMC Corp., Philadelphia, PA) and pyrethrin(McLaughlin Gormley King Co., Minneapolis, MN) at label dose(Table 1) and a higher dose (HD) at a concentration of 20 g AIL−1 in water mixtures. The mixtures were applied to plastic-coated paper, metal, painted plastic, unpainted plastic and woodsurfaces.

2.3 Contact toxicity experimentThe interior surfaces (lid and bottom) of plastic petri dishes weresprayed with 0.25 mL of a water dispersion with one of the13 insecticides using an artist’s ‘airbrush’ (Paasche Airbrush Co.,Hardwood Heights, IL). Water only was sprayed as the non-treatedcontrols. The petri dishes were allowed to dry in the laboratoryhood for 3 h before use. An adult male was transferred from a

Table 1. Insecticide active ingredients used in the initial test ofcontact toxicity against adult male Plodia interpunctella for attract-and-kill formulations, listed by insecticide classification

Active ingredientg AI L−1 atlabel ratea

Manufactureror supplier

OrganophosphatesMalathion 22.0 Drug and Chemical

Co., Floral Park, NY

Chlorpyrifos-methyl 10.0 Gustafson, McKinney,TX

Dichlorvos 10.0 Biotech Co.,Painesville, OH

Synthetic pyrethroidsCyfluthrin 0.5 Bayer Crop Sciences,

Kansas City, MO

Permethrin 5.0 Gustafson, McKinney,TX

Deltamethrin 0.6 Gustafson, McKinney,TX

PyrazolesFipronil 1.2 Aventis, Montjave, NJ

NeonicotinoidsImidacloprid 1.0 Gustafson, McKinney,

TX

MicrobialsAbamectin 2.0 Novartis, Greensboro,

NC

Spinosad 1.7 Gustafson, McKinney,TX

BotanicalsAzadirachtin 0.1 AMVAC, Los Angeles,

CA

Pyrethrin ‘organic’ 2.0 MGK Co.,Minneapolis, MN

Pyrethrin + PBOb 0.1 Whitmire Micro-Gen,St Louis, MO

a Amount reported is the concentration in the final spray mix derivedfrom product label instructions for mixing and application to surfacesof a given area.b PBO = piperonyl butoxide.

vial and confined inside a treated petri dish (lid and bottom)for 2.0 s. The male moth was then put into a 950 mL glassjar with a single virgin female and 15 g of wheat kernels; thejar was covered with a ventilated paper lid. The wheat kernelswere used as a female oviposition substrate. Jars were placedin a growth chamber held at 28 ◦C, 60–70% relative humidityand 16 : 8 h light : dark photoperiod. After 24 h, the mortality ofthe male and female in each jar was assessed and recorded.Wheat kernels from each jar were sifted with a US No. 14 sieve(Seedburo Equipment Co., USA) to collect and count eggs. Eggswere placed on double-sided tape on a 9 cm diameter black filterpaper (Ahlstrom, Mt Holly Springs, PA) in the bottom of a plasticpetri dish and put into the growth chamber for 5 days at 28 ◦C,60–70% relative humidity and 16 : 8 h light : dark photoperiod,after which the number of hatched eggs was determined. Eachtreated dish was exposed to ten separate males, and there werefour dishes (replicates) of each insecticide, for a total of 40 malestested for each insecticide and the control in the initial contacttoxicity study.

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www.soci.org M Campos, TW Phillips

2.4 Residual toxicity experiment with different surfacesThe following surfaces were treated inside a 9 cm diameter dishbioassay arena with solutions of insecticides: uncoated plastic (thesame petri dishes as used in the initial contact toxicity experiment;Fisher Scientific, Canada); plastic petri dishes coated with a layer ofwhite latex house paint (marketed by Wal-Mart, Bentonville, AR);customized petri dishes (similar in interior diameter and depth tothe plastic petri dish bottoms and lids) made with non-paintedplywood; non-painted metal (sheet of aluminum, 3.0 mm thick);and a circular piece of plastic-coated paper fitted into the plasticpetri bottoms and lids. Insecticide formulations were diluted inwater, and a volume of 0.25 mL was sprayed on the interior surfaceswith an artist’s airbrush (the same as that used in the initial contacttoxicity experiment) and dried in a fume hood for 3 h. Water onlywas sprayed for non-treated control dishes. Tests were carriedout on cyfluthrin, permethrin and organic pyrethrin lacking thesynergist piperonyl butoxide (PBO), based on results of the initialcontact toxicity experiment described in Section 2.3. The firstbioassays began after the dishes had been dried, and this set wasdesignated time 0. Petri dishes were stored at room temperaturebetween bioassay periods. A HOBO data logging unit (OnsetComputer Co., Bourne, MA) was placed with the dishes and usedto monitor the temperature and relative humidity, which werefound to vary between 22 and 25 ◦C and 40 and 60% respectively.This experiment followed the same procedures as in the initialcontact toxicity experiment described in Section 2.3. However,five males were bioassayed separately and consecutively per petridish, with four different dishes as replicates per treatment, or 20males per treatment. Residual toxicity of the insecticides on thedifferent surfaces was evaluated by conducting bioassays with theoriginal petri dishes at 0, 4, and 8 weeks post-treatment.

2.5 Statistical analysisThree response variables were observed in both experiments:percentage mortality of treated adult males (dead females werealso noted), number of eggs laid and percentage of the eggsthat hatched. Proportions (percentages) were transformed by thearcsine square root function prior to analysis. The experimentaldesign used for the initial toxicity test of 13 insecticides was acompletely randomized design with four replicates per treatment.Ten males were observed for each of the four treated petri dishes.A protected least significant difference procedure19 was used forseparating means at the α = 0.05 level. The persistence of theinsecticides on the different surfaces through the 8 week periodwas analysed as a randomized complete block design, with afactorial arrangement (type of surface material and dose of activeingredient as factors), and repeated 4 times. Data were analysedwith the PROC MIXED procedure using the REPEATED option.20

Treatment differences within a week were analysed with pairwiset-tests, and comparisons were protected by examining the SLICEoption within the LSMEANS statement at the α = 0.05 level.

3 RESULTS3.1 Initial contact toxicity experimentCyfluthrin, permethrin, deltamethrin, pyrethrin alone andpyrethrin + PBO were the treatments with the highest percentagemortality and were statistically similar as a group, with averages of73–89% mortality of P. interpunctella adult males following 2.0 sexposures to insecticides and 24 h of recovery time. These weresignificantly different from mortalities caused by the other insec-ticides tested and from the non-treated controls (F13,42 = 21.70,

Figure 1. Mean percentage mortality of P. interpunctella adult males after2.0 s contact with the treated surface of a plastic petri dish. Bars with thesame letter are not significantly different (n = 10, t-test, P > 0.05).

Table 2. Oviposition and the percentage of eggs that hatched perPlodia interpunctella female following pairing with males that had beentreated for 2.0 s in the initial contact toxicity test with 13 insecticides

TreatmentsMean number of eggs laid

(± SE)aMean % egg hatch

(± SE)a

Malathion 31.5(±7.1) b 64.1(±15.3) ab

Chlorpyrifos-methyl 37.7(±3.4) b 59.5(±9.8) b

Dichlorvos 32.5(±13.4) b 45.7(±7.0) b

Cyfluthrin 24.5(±2.9) bc 72.8(±6.5) ab

Permethrin 7.8(±1.3) c 53.5(±9.7) b

Deltamethrin 7.3(±2.1) c 73.7(±4.7) ab

Fipronil 19.9(±6.6) bc 71.0(±13.5) ab

Imidacloprid 22.7(±9.3) bc 66.8(±9.7) ab

Abamectin 24.4(±8.1) bc 57.1(±12.9) b

Spinosad 31.9(±4.9) b 65.9(±7.3) ab

Azadirachtin 33.7(±14.9) b 74.9(±15.7) ab

Pyrethrin ‘organic’ 7.1(±2.7) c 67.3(±11.2) ab

Pyrethrin + PBO 25.3(±10.4) bc 60.2(±10.3) b

Untreated control 76.4(±8.1) a 92.0(±2.3) a

a Means within a column having the same letter are not significantlydifferent (LS means comparison, using protected LSD procedure α

between comparisons = 0.05).

P < 0.0001) (Fig. 1). This initial study revealed that 2.0 s exposuresof males on the insecticide-treated petri dishes had significanteffects on oviposition by females that were paired with thesemales for 24 h (F13,42 = 4.42, P = 0.0001) (Table 2). There was anaverage of more than 76 eggs laid per female paired with malesfrom non-treated control dishes, and this was significantly differentfrom eggs laid following pairings involving males from insecticide-treated dishes. Females paired with permethrin, deltamethrin ororganic pyrethrin (lacking PBO) treated males produced less thaneight eggs per female. These insecticides were statistically similarto each other and considered as the best treatments for sup-pressing reproduction (Table 2 and Fig. 1). However, these threeinsecticides did not differ statistically in their effect on ovipositionfrom females paired with males exposed to cyfluthrin, fipronil, im-idacloprid, abamectin or pyrethrin + PBO, which averaged 20–25eggs laid per female. The remaining five insecticides, malathion,

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Figure 2. Mean percentage (± SE) mortality of P. interpunctella adult males after 2.0 s contact tests with cyfluthrin, permethrin or pyrethrin (no PBO) atlabel dose (LD) and at a higher dose (20 g AI L−1, HD) on plastic-coated paper, metal, painted plastic, unpainted plastic and bare wood surfaces at threetime periods after treatment. Means within a time period on a given surface with the same letter are not significantly different, P > 0.05.

chlorpyrifos, dichlorvos, azadirachtin (neem) and spinosad, hadthe least effects on oviposition and were not significantly differ-ent from each other. This same group of insecticides was alsoleast effective at killing males following 2.0 s exposures (Fig. 1).Statistical analysis for egg hatching (Table 2) showed that therewas a significant treatment effect on egg hatching (F13,42 = 7.22,P < 0.0001). Eggs derived from pairings with males from non-treated petri dishes had the highest percentage of eggs hatched,92%, which was statistically similar to eight of the insecticide treat-ments and different only from chlorpyrifos, dichlorvos, permethrin,abamectin and pyrethrin + PBO.

3.2 Residual toxicity on several surfacesResults for the residual toxicity of insecticides applied to differentsurfaces are presented below within the context of a given surfacetype within a given number of weeks after treatment, times 0, 4and 8 weeks following application of the insecticides.

3.2.1 Mortality

The residual toxicity of the three insecticides at prescribedlabel dose (LD) and at the 20 AI g L−1 high dose (HD) againstP. interpunctella adult males on several surfaces varied substantiallyaccording to surface and active ingredient (Fig. 2). There was asignificant three-way interaction among surface, insecticide andweeks (F48,210 = 3.41, P < 0.0001).

Mortality on the plastic-coated paper surface at time 0 wasabove 95% for the treatments of cyfluthrin HD, permethrin LD andHD and pyrethrin LD and HD, and these differed statistically frommortality on cyfluthrin LD, which was about 60% (Fig. 2). All thesetreatments on the plastic-coated paper were significantly differentfrom the non-treated controls at 0% mortality. Similar levels ofmortality were observed at week 4, except for pyrethrin LD, whichdropped to 5% and was statistically similar to the control. Onlypermethrin HD kept a high level of mortality (90%) at week 8,which was statistically different from the other treatments. Lower


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mortalities (30–50%) were observed for cyfluthrin LD and HD,permethrin LD and pyrethrin HD, which were similar statistically.Furthermore, pyrethrin LD did not kill any adult males at week8, and it was similar statistically to the non-treated control at 0%mortality.

Residual toxicity on the metal surface at week 0 showed thatpermethrin HD and pyrethrin LD and HD were similar statistically,with 100% mortality to adult males. Permethrin LD and cyfluthrinHD were not significantly different and showed lower kill, at85% mortality, compared with the others. Furthermore, thesetreatments elicited significantly higher mortality than cyfluthrin LDand the non-treated control, with 25 and 0% mortality respectively.A similar trend was exhibited at week 4 on metal, except thatthe efficacy of pyrethrin LD dropped to 10% and was similarstatistically to the non-treated control at 0% mortality. Also,permethrin LD, cyfluthrin HD and cyfluthrin LD were similarstatistically and showed lower effectiveness, with 60, 45 and20% mortality respectively. However, cyfluthrin LD also was notdifferent statistically from pyrethrin LD. At 8 weeks the permethrinHD showed the highest effectiveness in killing adult moths, with85% mortality, and this was significantly higher than mortality onall the other treatments.

The residual toxicity of the insecticides on the painted surfacewas overall very poor (Fig. 2). Pyrethrin HD killed 100% of theadult moths at week 0 and was significantly higher in activitythan others tested, which were low and mostly similar to thenon-treated control. Residual toxicity of all the tested compoundson the painted surface was less than 20% on average at the 4 and8 week bioassays.

The adult mortality response for the treated plastic surfaceshowed that pyrethrin HD, permethrin HD and cyfluthrin HD werestatistically similar to each other and killed over 95% of the adultmoths tested at week 0. However, permethrin HD and cyfluthrinHD were similar statistically to permethrin LD and cyfluthrin LD,with 80 and 85% mortality. Pyrethrin LD killed only about 35% ofadult moths tested, but this was significantly greater than the 0%mortality of moths exposed to non-treated plastic. At week 4, thepermethrin HD had 85% mortality, which was similar statisticallyto permethrin LD and pyrethrin HD. However, permethrin LDand pyrethrin HD were not significantly different from cyfluthrinLD and HD at this time period. Pyrethrin LD elicited only 5%mortality at 4 weeks, which did not differ statistically from thenon-treated control. At 8 weeks the Permethrin HD on plastic killedabout 80% of adult moths treated, which was similar statisticallyto cyfluthrin HD at 60% mortality. However, cyfluthrin HD wasnot significantly different from permethrin LD, with about 45%mortality. Furthermore, permethrin LD did not differ statisticallyfrom pyrethrin HD and cyfluthrin LD, at 45% and 20% mortalityrespectively. Additionally, pyrethrin HD on plastic exhibited lowefficacy at 8 weeks and was similar statistically to the rest of thetreatments and to the non-treated control.

Residual activity of insecticides tested on the bare wood surfacewas generally poor (Fig. 2). Permethrin HD killed an average of80% of adult moths at time 0, which was statistically higherthan response to cyfluthrin LD and HD at 35 and 40% mortalityrespectively. These treatments were significantly different fromthe rest of the treatments, and a similar trend was observed atweeks 4 and 8, during which only permethrin HD elicited a highmortality, 75 and 60% respectively, but when the other treatmentshad very low activity.

3.2.2 Egg layingThe mean number of eggs laid per female P. interpunctella (Fig. 3)paired with treated males varied significantly among insecticides(F6,105 = 18.14; P < 0.0001), and there was a significant interactionbetween insecticide and weeks (F12,210 = 1.89, P = 0.0367).However, there were no significant differences among the surfacetypes (F4,105 = 0.68, P = 0.6071), a marginal significance wasdetected among weeks (F2,210 = 2.80, P = 0.0630) and nosignificant interaction between surface and insecticide (F24,105 =0.70, P < 0.8373), surface and weeks (F8,210 = 0.55, P = 0.8182)or surface and insecticide and weeks (F48,210 = 0.77, P < 0.8559).As expected, females paired with males from non-treated controlslaid more eggs throughout the experiment than females pairedwith insecticide-treated males. Generally, those females pairedwith males from treatments that caused high male mortality laidthe lowest numbers of eggs.

The mean number of eggs was over 17 per female for non-treated controls, pyrethrin HD, permethrin LD and HD andcyfluthrin LD on the plastic-coated paper surface at week 0,and these responses were statistically similar to each other(P > 0.05). However, these same treatments, excluding the non-treated control, were not significantly different from the remainingtreatments. At week 4, all treatments were statistically similar toeach other on the plastic-coated paper, except for pyrethrin HD(4.9 eggs laid per female), which was significantly different fromnon-treated and permethrin LD (35 and 35.4 eggs laid per femalerespectively). At week 8 the non-treated, pyrethrin HD, permethrinLD and permethrin HD did not differ statistically. These treatments,except for the non-treated control, were statistically similar topyrethrin LD and cyfluthrin LD (10 and 15.9 eggs laid per femalerespectively). A low and statistically similar mean number of eggswere laid by females paired with males treated with cyfluthrinLD and HD, permethrin HD and pyrethrin LD and HD. However,these treatments were not significantly different from cyfluthrinLD, permethrin HD and pyrethrin LD and HD. These treatmentswere statistically similar to permethrin HD and pyrethrin HD forwhich the females laid higher number of eggs.

The mean number of eggs laid by females paired with malesfrom treated metal surfaces at week 0 was more than 34 eggs perfemale for the non-treated control, pyrethrin HD and permethrinLD and HD, which were not significantly different from eachother. However, pyrethrin HD and permethrin HD were alsostatistically similar to pyrethrin LD, which averaged 15.5 eggs perfemale. Moreover, these treatments, except for pyrethrin HD, werestatistically similar to the rest of the treatments, which averagedfewer than 20 eggs laid per female. A similar trend was observed atweek 4, except for pyrethrin HD, for which the egg laying droppedto an average of 8.5 eggs per female. The egg laying in responseto males treated with permethrin HD was 40.4, which was similarstatistically to pyrethrin LD and cyfluthrin LD and HD. However,these treatments, except permethrin HD, did not differ from therest of the treatments. At week 8, non-treated and permethrinLD showed high averaged egg laying (61.2 and 35.6 respectively).Response to permethrin was significantly higher than to the otherinsecticide treatments.

On the painted surface at week 0, all the insecticide treatmentswere similar statistically. However, pyrethrin LD and HD andpermethrin LD did not differ from the non-treated control whichaveraged the highest number (47.1) eggs laid per female. At week4 there was greater than 22.85 eggs laid per female for the non-treated control, permethrin LD and HD and cyfluthrin HD, whichwere statistically similar to each other. These treatments, except


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Figure 3. Mean number (± SE) of eggs laid per P. interpunctella female after pairing with males from the contact test of active ingredients cyfluthrin,permethrin or pyrethrin (no PBO) at label dose (LD) and at a higher dose (20 g AI L−1, HD) on plastic-coated paper, metal, painted plastic, unpaintedplastic and bare wood surfaces. Means within a time period on a given surface with the same letter are not significantly different within weeks, P > 0.05.

for the non-treated paint surface, did not differ from pyrethrinLD, which averaged 16.8 eggs laid. Moreover, these treatments,except permethrin LD, were not significantly different from therest of the treatments. At week 8, the egg laying was over 17.3eggs per female for all treatments, except cyfluthrin LD, whichelicited an average of 9.35 eggs laid. All treatments were similarstatistically, except non-treated, which was significantly differentfrom cyfluthrin LD.

The plastic surface at week 0 resulted in egg laying that wasgreater than 17 eggs for the non-treated control, pyrethrin H andpermethrin LD and HD. However, permethrin LD and pyrethrinHD were statistically similar to the rest of the treatments. Atweek 4 the non-treated plastic and permethrin LD and HDshowed more than 41.9 eggs per female. These treatmentsdid not differ statistically from each other. However, permethrinHD was statistically similar to cyfluthrin LD and pyrethrin LD(11.4 and 16.1 eggs laid respectively). These treatments, except

permethrin HD, were not significantly different from the rest ofthe treatments. At week 8 there was no substantial variation inegg laying, and all the treatments were statistically similar to eachother.

On the wood surface at week 0, the average egg layingwas greater than 23.5 eggs per female for non-treated control,pyrethrin LD and permethrin LD and HD, which were similarstatistically. These treatments, except for the non-treated woodand permethrin HD, were not significantly different from the restof the treatments. A similar trend was observed at week 4, exceptthat pyrethrin LD, with a mean of 22.5 eggs, was significantlydifferent from non-treated wood and permethrin HD. At week 8,the egg laying was not statistically different among treatments,except for pyrethrin HD and cyfluthrin LD, which elicited averagesof 13.4 and 9.8 eggs respectively, and these were statistically lowerthan eggs laid by females paired with males from non-treatedwood (mean of 52.5 eggs laid).


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3.2.3 Egg hatching

The three insecticides and five surfaces analysed impacted theproportion of P. interpunctella eggs hatching over time (Fig. 4). Theegg hatching differed significantly among insecticides (F6,105 =17.78, P < 0.0001), among the surface types (F4,105 = 29.42,P < 0.0001) and among weeks (F2,210 = 60.79, P < 0.0001).There was significant interaction between surface and insecticide(F24,105 = 5.01, P < 0.0001), surface and weeks (F8,210 = 2.74,P = 0.00668) and insecticide and weeks (F12,210 = 3.21,P = 0.0003), but there was no significant three-way interaction ofsurface, insecticide and weeks (F48,210 = 1.14, P < 0.2679).

On the plastic-coated paper surface at week 0, the averagepercentage of egg hatching was 95% for the non-treated control,which was significantly different from the rest of the treatments.A similar trend was observed at weeks 4 and 8, except for thepyrethrin LD and cyfluthrin LD, which were statistically similar tothe non-treated control.

The metal surface had an average of greater than 95% egghatching for the non-treated control at week 0, which wassignificantly different from the rest of the treatments. At week4, non-treated and cyfluthrin LD were statistically similar (95.1 and52% respectively). However, cyfluthrin LD was not significantlydifferent from pyrethrin LD and HD and permethrin LD. Thesetreatments, except for cyfluthrin LD, were similar statistically tothe rest of the treatments. At week 8, the average percentageegg hatching was greater than 56% for non-treated, pyrethrin LD,permethrin LD and cyfluthrin LD, which did not differ significantly.These treatments, except for non-treated, were not significantlydifferent from pyrethrin HD and cyfluthrin HD, which were 48.8 and46.7% hatch respectively. Additionally, pyrethrin HD and cyfluthrinHD did not differ from the rest of the treatments.

The paint surface at week 0 had a percentage egg hatch rate thatwas greater than 82% for non-treated control and pyrethrin LD,and these were similar statistically. However, pyrethrin LD was alsostatistically similar to permethrin LD (46%). These treatments werestatistically different from the rest of the treatments, except forpermethrin LD, which did not differ from the rest of the treatments.At week 4, the percentage egg hatching was greater than 58% fornon-treated, pyrethrin LD, permethrin HD and cyfluthrin LD, whichwere not significantly different. These treatments, except for thenon-treated metal, did not differ from the rest of the treatments.At week 8, the percentage egg hatching was greater than 74%for non-treated, pyrethrin LD, permethrin HD and cyfluthrin LDand HD, which did not differ statistically. However, pyrethrinLD and cyfluthrin HD, with 74.1 and 85.1% hatch respectively,were also similar statistically to pyrethrin HD (46.2% hatch). Thesetreatments, except pyrethrin HD, were significantly different fromthe rest of the treatments.

The plastic surface showed greater than 96% egg hatchingat week 0 for the non-treated control, which was significantlydifferent from the rest of the treatments. At week 4, non-treated, pyrethrin LD and cyfluthrin LD, at 55.2 and 74.9% hatchrespectively, were similar statistically. These treatments, exceptfor the non-treated plastic, did not differ from cyfluthrin HD at45% hatch. However, pyrethrin LD and cyfluthrin HD were notstatistically different from the rest of the treatments. At week 8,the percentage average egg laying was greater than 66.5% for non-treated, pyrethrin LD and cyfluthrin LD. These treatments, exceptcyfluthrin LD, were not significantly different from pyrethrin HD,permethrin LD and cyfluthrin HD, with 41.6, 28.0 and 33.1% hatchrespectively.

On the wood surface at week 0, the non-treated control (97.8%)and pyrethrin LD (76.8%) averaged the highest percentage ofegg hatch and were statistically similar. These treatments differedfrom the rest of the treatments, except for permethrin LD (46.7%),which was statistically similar to pyrethrin LD. At week 4, thenon-treated wood showed the highest percentage egg hatch(97.7%) and was not significantly different from permethrin LD(67.1%). However, permethrin LD did not differ from the rest ofthe treatments, except for pyrethrin LD (19.9%). At week 8, thepercentage average egg hatching was greater than 95.7% for thenon-treated control and pyrethrin and permethrin both at LD,and did not differ from cyfluthrin and pyrethrin both at HD (85.5and 66.6% respectively). These treatments, except for pyrethrinHD, were significantly different from cyfluthrin LD (41.5%) andpermethrin HD (21.0%).

4 DISCUSSIONResults from 2.0 s contact toxicity tests aimed at preventing adultmale P. interpunctella from mate-finding and reproduction clearlyidentify the types of toxin and the types of surface that wouldperform best in attract-and-kill pest management methods forthis serious pest. Initial screening of a range of active ingredientsidentified synthetic pyrethroids and natural pyrethrin insecticidesas more effective than several other insecticides known to beeffective in other contexts, and 8 week residual toxicity was bestfor higher application rates of permethrin on most surfaces exceptfor the painted plastic surface.

The low activity of compounds other than pyrethroids andpyrethrins may be explained by inherent factors of these com-pounds related to the application method and the mode of action.There were low percentages or no mortality to the organophos-phate (OP) treatments, perhaps owing to the presumed inherent,genetically based resistance to organophosphates in the labora-tory culture of P. interpunctella used in the experiments. OP resis-tance by P. interpunctella is widespread and well documented.8,17

Low mortality was also observed in the treatments with fipronil,imidacloprid, abamectin, spinosad and azadirachtin, and was per-haps due to the brief contact by the males with the treated petridishes or to specific details of the modes of action for thesecompounds. Previous work that demonstrated contact toxicity ofP. interpunctella to these or similar compounds had much longercontact times, usually several days to weeks,21,22 and did notutilize adults. The 2.0 s contact in the bioassays conducted hereclearly limited the types of insecticide that would be effective. Syn-thetic pyrethroids and naturally derived pyrethrins are known forhaving rapid ‘knockdown’ mortality for various insects, includingLepidoptera,16,23,24 so the effectiveness of these active ingredientsagainst P. interpunctella adult males in the present 2.0 s contactbioassays was not unexpected.

Variation in male reproductive success, which was measuredby the number of eggs laid by females paired with treated malesand the percentage of these eggs that hatched, thus the fertilityof the eggs, is noteworthy and can also be explained by thenature of the brief contact bioassay used. Some experimentalunits with dead males at 24 h post-treatment also had deadfemales and few or no eggs (female mortality data not reported),which suggests that insecticide-contaminated males were able totransfer a lethal dose of toxin to a female during courtship andcopulation. Unmated P. interpunctella females are known to layno or only a few unfertilized eggs over several days;25 however,unmated or chemically intoxicated female P. interpunctella were


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Figure 4. Mean percentage (± SE) of eggs hatched from those laid by P. interpunctella following pairing with males in the contact test of active ingredientscyfluthrin, permethrin or pyrethrin (no PBO) at label dose (LD) and at a higher dose (20 g AI L−1, HD) on plastic-coated paper, metal, painted plastic,unpainted plastic and bare wood surfaces. Means with the same letter are not significantly different within weeks, P > 0.05.

observed laying eggs in the laboratory. The highest ovipositionlevels in the experiments reported here were associated with non-treated control males; however, some treatments that resulted inhigh male mortality also had high levels of oviposition. Interactionsof males and females were not observed or recorded during the24 h holding period after treatment of males, but it is likely thatmating occurred in some cases prior to death of the treated male,which then resulted in substantial oviposition by the associatedfemale. Subsequent low levels of egg hatch for some treatments,such as 50–70% hatch for females paired with insecticide-treatedmales as opposed to 92% hatch for females from non-treatedcontrols (Table 2), may have been due to incomplete fertilizationresulting from male intoxication. In some cases the females mayhave laid substantial numbers of unfertilized eggs, which did nothatch, as a spontaneous abortion effect in response to stress frominsecticide intoxication before death.

The type of material comprising the surface treated with agiven insecticide significantly impacted the residual toxicity ofinsecticides at 0, 4 and 8 weeks after application of the toxicants.

Such negative effects on residual activity may be attributed tophysical or chemical reactions of the surface with the insecticidesto cause degradation or loss of material from the surface. It hasbeen demonstrated that pyrethroids and pyrethrins are stable atacid and neutral pH, but they begin to hydrolyze under alkalineconditions.26 This study showed that the painted surface andthe bare wood surface had the lowest performance for residualtoxicity of most test compounds after time 0. Only pyrethrin at thehigh dose had any activity on the painted surface against adultmales at time 0, but this activity was lost in subsequent bioassaytimes. Low toxic activity was also associated with the treatmentson the bare wood surface at all three testing times, except forthe high dose of permethrin, which persisted with greater than50% mortality after 8 weeks. Treatment surfaces have been shownto be important in variation of toxic activity for other insects,27

and this may be attributed to a physical or chemical reaction ofthe substrate with the insecticide that lowers the activity. Furtherresearch is needed to determine the basis for surface effects ontoxicity of these compounds against P. interpunctella males. In any


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case, it is clear that painted or wooden surfaces should be avoidedin developing attract-and-kill technology for P. interpunctella.

The synthetic pyrethroids cyfluthrin and permethrin and thenaturally derived pyrethrins lacking PBO, applied to plastic-coatedpaper, metal or plastic surfaces at various concentrations, had thehighest mortality against adult male Indian meal moths in thesestudies compared with other insecticides. Permethrin applied atthe high dose of 20 g AI L−1 in the final spray suppressed adultmales of P. interpunctella and prevented substantial reproductionfor up to 8 weeks when applied to surfaces of plastic-coatedpaper, bare metal, bare plastic and to a lesser degree bare wood.Residual activity of pyrethroids and pyrethrins was very poorwhen applied to a painted surface, and this maybe was from alipophilic action that can result following addition or mixing of theactive ingredient to plastic, the material under the paint in thisformulation. Pyrethroids can be absorbed up to 50% by plasticcontainers in 24 h, and the toxic effect reduced by 50% in 4 h inCeriodaphnia dubia Richard.28

This study clearly shows that attract-and-kill formulations tocontrol P. interpunctella for up to 8 weeks can be developed usingadequate concentrations of permethrin on a variety of surfaces.The attract-and-kill method is desirable for reduced input ofinsecticides in food storage areas because the specific pest istargeted via the pheromone lure to contact a small amount of aneffective and locally contained killing agent.

5 CONCLUSIONSThe overall conclusions on the contact toxicity experiments with avariety of insecticides found that pyrethroids and naturally derivedpyrethrins, both applied to surfaces at registered label dose, hadthe highest toxicity against adult male Indian meal moths inthese 2.0 s contact toxicity studies compared with other classesof insecticides. Permethrin applied at the high dose of 20 g AIL−1 in the final spray suppressed adult males of P. interpunctellaand prevented reproduction for up to 8 weeks when applied tosurfaces of plastic-coated paper, bare metal, bare plastic and, toa lesser degree, bare wood. Residual activity of pyrethroids andpyrethrins was very poor when applied to a painted surface, andthis may be due to degradation or reaction of the active ingredientwhen in contact with the dry paint. The study clearly showedthat attract-and-kill formulations could control P. interpunctellafor up to 8 weeks and can be developed using an adequateapplication dose of permethrin to a variety of surfaces. The attract-and-kill method is desirable for reduced input of insecticidesin food storage areas because the specific pest is targeted viathe pheromone lure to contact a small amount of an effectiveand locally contained killing agent. Further research will test thelongevity of the attract-and-kill formulations under wind tunnelconditions, in simulated warehouses and ultimately by evaluationin commercial establishments.

ACKNOWLEDGEMENTSThe authors thank Dr Mark Payton for advice on statistical analysesand also Drs Jack Dillwith, Brad and Kard and Mark Payton forcomments on earlier drafts of this manuscript. Technical assistanceand logistical support was provided by Edmond Bonjour and hisstaff for maintenance of insect colonies. Financial support wasprovided by grants from the USDA Risk Avoidance and MitigationProgram, the Oklahoma Agricultural Experiment Station and theKansas Agricultural Experiment Station.

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12 Lanier GN, Principle of attraction–annihilation: mass trappingand other means, in Behavior Modifying Chemicals for InsectManagement, Applications of Pheromones and Other Attractants,ed. by Ridgway RL, Silverstein RM and Inscoe MN. Marcel Dekker,New York, NY, pp. 25–45 (1990).

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20 SAS/STAT User Guide, Version 9.1. SAS Institute, Cary, NC (2003).21 Huang F, Subramanyam B and Toews MD, Susceptibility of laboratory

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23 Amin UK and Knowles CO, Toxicity of pyrethroids and effect ofsynergist to larval and adult Helicoverpa zea, Spodoptera frugiperda,and Agrotis ipsilon (Lepidoptera: Noctuidae). J Econ Entomol94:868–873 (2001).


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28 Wheelock CE, Miller JL, Miller MJ, Phillips BM, Gee SJ, Tjeerdema RS,et al, Influence of container adsorption upon observed pyrethroidtoxicity to Ceriodaphnia dubia and Hyalella azteca. Aquat Toxicol74:47–52 (2005).


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