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Efficacy of Residual Bifenthrin Applied to LandscapeVegetation Against Aedes albopictusAuthor(s): Melissa A. Doyle, Daniel L. Kline, Sandra A. Allan, and Phillip E.KaufmanSource: Journal of the American Mosquito Control Association, 25(2):179-183.2009.Published By: The American Mosquito Control AssociationDOI: http://dx.doi.org/10.2987/08-5804.1URL: http://www.bioone.org/doi/full/10.2987/08-5804.1

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EFFICACY OF RESIDUAL BIFENTHRIN APPLIED TO LANDSCAPEVEGETATION AGAINST AEDES ALBOPICTUS

MELISSA A. DOYLE,1 DANIEL L. KLINE,1 SANDRA A. ALLAN1AND PHILLIP E. KAUFMAN2

ABSTRACT. The daytime biting mosquito Aedes albopictus is a nuisance pest commonly found insuburban yards. The recommended course of treatment for Ae. albopictus is to keep yards free of water-holding containers; however, infestations may require additional control methods such as residual pesticideapplications to vegetation. Five plants commonly found in yards or in uncultivated areas in Gainesville, FLwere chosen as substrates for evaluation of the effectiveness of residual bifenthrin against 5–7-day-old femaleAe. albopictus. Knockdown of mosquitoes after 1 h of exposure was highest the day of and 7 days aftertreatment. Plant species clearly impacted the effectiveness of residual bifenthrin. One-hour knockdown 7days after treatment remained high (.62%) only on azalea and holly bush vegetation. Knockdown counts24 h after exposure demonstrated that residual efficacy of bifenthrin was highest on azalea, with .77%mortality for up to 35 days. Additional bioassays revealed significant differences in the knockdown rates ofmale, female, gravid, and blood-fed Ae. albopictus exposed to residual bifenthrin treatments, with the highestknockdown observed on the day of and 7 days after treatment.

KEY WORDS Aedes albopictus, bifenthrin, residual pesticide, mosquito control

INTRODUCTION

The Asian tiger mosquito, Aedes albopictus(Skuse), was first detected in the United States inHarris County, Texas in 1985 (Sprenger andWuithiranyagool 1986), and is now established in28 states (Moore, personal communication). Theevaluation of efficacy efforts against Ae. albopic-tus is warranted because of its ability to vectorarboviruses (Shroyer 1986, Mitchell 1991, Gratz2004) and transmit other pathogens (Konishi1989, Mitchell et al. 1998). The diurnal mate- andhost-seeking activity of Ae. albopictus decreasesthe likelihood that adult populations will beimpacted by organized mosquito control efforts,such as broad-spectrum ultralow-volume pesti-cide sprays aimed to control crepuscular mosqui-toes. However, infestations of Ae. albopictus mayrequire more active control methods because Ae.albopictus is a potential vector for arboviruses,including eastern equine encephalitis (Savage etal. 1993). These methods include personal repel-lents, area repellents such as citronella-burningdevices, professional pesticide applications, andtrapping devices.

The use of residual pesticide applications onmosquito resting sites has been shown to beeffective in managing pest mosquito populations(Anderson et al. 1991, Standfast et al. 2003, Cilekand Hallmon 2006, Trout et al. 2007). Landingrates decreased 80–90% in salt marsh areas wherefoliage was treated with permethrin and malathi-on in North Carolina (Anderson et al. 1991).

Cilek and Hallmon (2006) evaluated the efficacyof 3 different pyrethroids applied to southern waxmyrtles, Myriac cerifera L., and found that AquaReslinH, PermanoneH EC, and SuspendH weremost effective for the week following treatment infield cage tests. Residual treatments of bifenthrinand lambda-cyhalothrin were found to be effec-tive against Ae. albopictus for 6 wk posttreatmentin bioassays (Trout et al. 2007).

Residential yards often contain a variety ofplant species with unique physiological makeupsand varying growth rates. The reduced efficacy ofresidual sprays has been attributed to new plantgrowth providing nontreated harborage forresting mosquitoes in previous studies (Cilekand Hallmon 2006). Knockdown of insects hasbeen found to vary on different plant species(Ford and Salt 1987). However, the efficacy ofresidual pesticides sprayed on different plantspecies against Ae. albopictus is unknown andwas the object of this study. Bioassays were alsoconducted to evaluate the longevity of residualsprays in knocking down male, female, gravid,and blood-fed Ae. albopictus.

MATERIALS AND METHODS

Plant-species comparisons: plant selectionand treatment

Five plant species commonly found in yards orin uncultivated areas in Gainesville, FL werechosen to evaluate the effectiveness of residualbifenthrin against Ae. albopictus. These plantsincluded Rhododendron 3 ‘Fashion’ Linnaeus(azalea), Callicarpa americana Loureiro (beautyberry), Ilex cornuta Lindley (holly bush), Spartinabakeri Merrill (sand cord grass), and Magnoliagrandiflora Linnaeus (southern magnolia). The R.

1 United States Department of Agriculture, Agricul-tural Research Service, Center for Medical, Agricultur-al, and Veterinary Entomology, 1600 SW 23rd Drive,Gainesville, FL 32608.

2 University of Florida, Entomology and Nematolo-gy Department, PO Box 110620 Gainesville, FL 32611.

Journal of the American Mosquito Control Association, 25(2):179–183, 2009Copyright E 2009 by The American Mosquito Control Association, Inc.

179

3 ‘Fashion’ and I. cornuta plants were purchasedat Lowe’s Home Improvement store (Gainesville,FL) and the other plants were purchased fromChiappini Nursery (Melrose, FL). Five plants perspecies were treated according to label directionswith TalstarOneH (79.01 ml active ingredient[AI]/liter FMC, Philadelphia, PA) on August 22,2006 until pesticide runoff. Two plants per specieswere left untreated for control bioassays. Leaveswere allowed to dry for 4 h after treatment, keptoutdoors in full sun, and watered with dripirrigation. Bioassays were performed with leavesremoved the day of treatment and weeklythereafter for 5 wk (average temperature 19.0uC,with total 115.8 mm rainfall). The plants re-mained in the field for 3 additional weeks and thesame plants were retreated on October 17, 2006for a 2nd replication. Bioassays were performedwith the use of leaves removed 4 h posttreatmentand weekly thereafter for the following 5 wk.

Sex and physiological-state comparison: plantselection and treatment

Rhododendron simsii Planch (Ericaceae) werechosen for these bioassays and purchased fromHarmony Gate Nursery (Gainesville, FL). Pesti-cide application was made on January 27, 2007with application rate and method as previouslydescribed. The average temperature was 14.1uCwith 195.3 mm of rainfall for the duration of thestudy.

Petri dish preparation

Bioassays were conducted in 100 3 15-mm petridishes (Fisher Scientific, Hampton, NH) preparedwith double-sided, 48-mm-wide indoor/outdoorcarpet tape (Henkel Consumer Adhesives, Inc.,Avon, OH) applied to the inside bottom dish toadhere leaves. Leaves were hand picked, placedinto paper envelopes, and then fastened to thedouble-stick tape so that the upper surface of theleaf was exposed and the entire bottom surface ofthe dish was covered. A recent 7-wk trial indicatedthat mosquito knockdown was similar afterexposure to the top and bottom surfaces ofbifenthrin-treated wax myrtle leaves (Allan, un-published data). Latex gloves were worn during leafremoval and changed between treated and controlplants. Cotton was applied to exposed adhesive toprevent mosquito contact with the adhesive.

Plant-species comparison: bioassays

Nulliparous 5–7-day-old female Ae. albopictuswere obtained from the USDA, ARS, Center forMedical Agricultural, and Veterinary Entomolo-gy rearing laboratory colony that was establishedin 1992 (Hoel et al. 2007). Larvae were fed a 3:2mixture of beef liver powder and yeast. Adults

were provided cotton balls saturated with a 10%sucrose water solution. The colony was keptunder 14:10 (L:D) photoperiod at room temper-ature (27uC to 32uC). Ten adult females were coldanesthetized and placed into the prepared petridishes; 16 dishes were prepared with treatedleaves and 6 were prepared with control untreatedleaves (22 petri dishes total per plant species, 220total mosquitoes). The dishes were stored inrelative humidity between 70% and 85% at 20–22uC. Knockdown was assessed at 1 h and 24 hpostintroduction into the petri dish. Mosquitoeswere considered alive if they were able to flywithin the dish and rated as knocked down if theywere unable to fly.

Sex and physiological-state comparison: bioassays

Bioassays were performed to evaluate theefficacy of bifenthrin against 8–12-day-old Ae.albopictus of differing sex and physiological state.To obtain gravid females, 5-day-old mosquitoeswere blood fed on defibrinated bovine bloodthrough a membrane and held separately for 3–5days until eggs developed; the mosquitoes werenot provided with an oviposition substrate.Mosquitoes for the blood-fed bioassays wereblood fed on the day of the test. Non–blood-fedfemales and males were held in the colony until thetest date. For each sex/physiological state exam-ined, 10 mosquitoes were cold anesthetized andplaced into the prepared petri dishes; 24 disheswere prepared with treated leaves and 8 wereprepared with control untreated leaves. Knock-down was recorded at 1, 4, and 24 h postintro-duction into the petri dish and rated as describedin the plant-species comparison bioassays.

Statistical analyses

Plant-species bioassay data were analyzed formain effects of plant species and time by 2-wayanalysis of variance (ANOVA) with the use of theGeneral Linear Models procedure (GLM) of theStatistical Analysis System (SAS Institute 1985).Knockdown was adjusted for control knockdownwith the use of Abbott’s formula (Abbott 1925);then data were transformed with arcsine trans-formation. Differences between plant species wereevaluated with the use of the Means/Tukey’sstatement within the GLM procedure in separateANOVAs conducted for each time interval aftertreatment. Main effects of sex/physiological stateand time were analyzed as in the plant-speciesbioassay data analysis with the use of arcsine-transformed knockdown data.

RESULTS

Knockdown of Ae. albopictus after 1 h ofexposure to treated leaves was highest on the

180 JOURNAL OF THE AMERICAN MOSQUITO CONTROL ASSOCIATION VOL. 25, NO. 2

day of and 1 wk after pesticide application for R.3 ‘Fashion’, C. americana, I. cornuta, and M.grandiflora (Table 1). Only 15.6% knockdownwas observed on the day of treatment in thebioassays with treated S. bakeri, and knockdownafter 1 h of exposure dropped sharply in thefollowing weeks. In the overall ANOVA, theeffects of plant species (F 5 86.01; df 4, 450; P ,0.001) and time since treatment (F 5 672.09; df 5,450; P , 0.0001) were significant, as was theinteraction between these 2 factors (F 5 45.14; df20, 450; P , 0.0001).

Knockdown in the 24-h bioassays remainedhigh for 3 wk posttreatment in the R. 3‘Fashion’, C. americana, and I. cornuta bioassays.A sharp decrease in knockdown was observedafter 2 wk in the 24-h bioassays of residualpesticide applied to S. bakeri and M. grandiflora.As was seen in the 1-h counts, the overallANOVA at 24 h revealed that the effects of plantspecies (F 5 109.32; df 4, 450; P , 0.0001) andtime since treatment (F 5 323.91; df 5, 450; P ,0.0001) were significant, as was the interactionbetween these 2 factors (F 5 22.94; df 20, 450;P , 0.0001).

Sex and physiological-state comparison bioassays

Knockdown of male, female, gravid, andblood-fed Ae. albopictus after 1 h of exposure toresidual pesticide was highest on the day of and1 wk after treatment (Table 2). The main effectsof sex/physiological state (i.e., male, sugar-fedfemale, gravid female, blood-fed female; F 5372.14; df 3, 644; P , 0.0001) and time since

treatment (F 5 7,185.53; df 6, 644; P , 0.0001)were significant, as was the interaction betweenthese main effects (F 5 173.57; df 18, 644; P ,0.0001). Knockdown of females after 4 h ofexposure dropped sharply after 2 wk, whereasthe male knockdown remained relatively high(60%) in comparison. After 3 wk, knockdownwas not observed in the female groups and lowknockdown was observed in the male bioassays inWeeks 3 and 4.

As with the 1-h bioassays, significant sex/physiological-state (F 5 623.91; df 3, 644; P ,0.0001) and time effects (F 5 8,447.16; df 6, 644;P , 0.0001) were observed with the 4-h counts,and the interaction of these effects was significantas well (F 5 263.12; df 18, 644; P , 0.0001).Knockdown of Ae. albopictus after 24 h ofexposure remained above 50% in all sex/physio-logical-state bioassays for 5 wk posttreatment.Significant sex/physiological-state effects (F 58.36; df 3, 644; P , 0.0001) and time effects (F 5478.95; df 6, 644, P , 0.0001) were observed, andthe interaction of these effects was significant aswell (F 5 3.42; df 18, 644; P , 0.0001). Overall,treatment (sex/physiological) effects in the 24-hcount data were relatively small and knockdownremained .45% in all treatment groups for theduration of the test.

DISCUSSION

Overall, the greatest knockdown of Ae. albo-pictus after 1-h exposure to pesticide-treatedleaves was observed on the day of and 1 wk aftertreatment, with a significant drop in knockdown

Table 1. Mean percent knockdown (SE) of Aedes albopictus observed at 1 and 24 h after exposure toTalstarOneH-treated leaves (active ingredient, bifenthrin 7.9%).

Plant

Days posttreatment

0 7 14 21 28 35

1 h

Rhododendron 3‘Fashion’ 90.0 (4.6)a1 62.5 (5.3)a 4.4 (1.8)ab 1.3 (1.3)a 0 (0.0) 0 (0.0)

Callicarpa americana 97.5 (1.9)a 21.3 (7.1)b 3.1 (1.5)ab 0.0 (0.0)a 0 (0.0) 0 (0.0)Ilex cornuta 100.0 (0.0)a 77.5 (7.9)a 7.5 (2.1)a 0.0 (0.0)a 0 (0.0) 0 (0.0)Spartina bakeri 15.6 (6.3)b 2.5 (1.4)b 0.0 (0.0)b 0.0 (0.0)a 0 (0.0) 0 (0.0)Magnolia grandiflora 96.9 (1.5)a 8.8 (3.1)b 2.5 (1.7)b 1.3 (0.9)a 0 (0.0) 0 (0.0)ANOVA2 F 97.93** 36.80** 2.88* ns ns ns

24 h

Rhododendron 3‘Fashion’ 100.0 (0.0)a 100.0 (0.0)a 98.7 (0.9)a 94.3 (2.3)a 89.4 (2.7)a 77.7 (2.1)a

Callicarpa americana 100.0 (0.0)a 99.3 (0.0)a 91.1 (5.1)ab 90.6 (2.8)a 26.2 (3.7)b 19.4 (2.1)cIlex cornuta 100.0 (0.0)a 100.0 (0.0)a 100.0 (0.0)a 91.7 (3.1)a 44.0 (8.3)b 36.4 (4.7)bSpartina bakeri 99.3 (0.7)a 87.2 (3.5)b 75.0 (7.3)b 25.6 (5.6)b 25.0 (4.7)b 16.3 (1.8)cMagnolia grandiflora 97.9 (1.5)a 100.0 (0.0)a 90.3 (3.1)ab 26.3 (6.0)b 27.6 (6.2)b 16.9 (2.5)cANOVA F ns 12.21** 5.55** 72.56** 24.74** 83.88**

1 Means within each column followed by the same letter are not significantly different. Tukey’s HSD test (P 5 0.05), N 5 24.2 ANOVA, analysis of variance; ns, P . 0.05.* P , 0.05.** P , 0.01.

JUNE 2009 EFFICACY OF RESIDUAL BIFENTHRIN 181

in the following weeks. Anderson et al. (1991) andCilek and Hallmon (2006) also found knockdownto be highest within 1 wk of application ofpermethrin to vegetation. Trout et al. (2007)found that populations of Ae. albopictus inperidomestic yards in Lexington, KY werereduced for 1 mo following treatment of vegeta-tion with bifenthrin and lambda-cyhalothrin.Laboratory bioassays performed with treatedleaves from the field sites supported thesefindings. However, observations of mortalitywere made only after 24-h exposure. In our 24-hbioassays, plant species clearly impacted theefficacy of the residual treatments and uniformcontrol was not observed across the plant speciesas in the Trout et al. (2007) study.

Many species of shrubs and bushes are oftenpresent in suburban yards. Each plant speciesvaries in the abundance of leaves, arrangement ofleaves, and the chemical makeup of the leafcuticular wax. The species of plant treated withresidual pesticide may alter the efficacy of theresidual treatments because of variations of thecuticular wax, which has been shown to affectpesticide transfer to an organism (Ford and Salt1987, Kirkwood 1987). Chowdhury et al. (2001)treated 16 different plant types with varyingcharacteristics and found that the efficacy ofresidual pesticides against Folsomia candida(Willem) varied and that pesticide efficacy wasnot predictable by any obvious pattern. In ourstudy, bifenthrin efficacy against Ae. albopictus

clearly varied among the 5 plant species. Knock-down was observed at high levels on R. 3‘Fashion’ (90.0%) and C. americana (97.5%).On Day 7, the efficacy of the knockdown ofmosquitoes exposed to treated C. americanaleaves dropped to 21.3%, whereas knockdownof mosquitoes on R. 3 ‘Fashion’ leaves remainedrelatively high at 62.5%. The observed differencescould be attributed to the type of cuticle in theleaves or the differing abilities of these plantspecies to adhere and retain pesticide.

In addition to interactions of pesticide withcuticular waxes, the application techniques usedfor pesticides may contribute to the residualefficacy of a pesticide. Knockdown of mosquitoeswith treated leaves of S. bakeri was reduced 1 wkafter treatment at both the 1-h and 24-hpostexposure observations. The differences ob-served with the S. bakeri compared to the otherplants could be attributed to the manner in whichthe pesticide was applied. The comparativethinness, arrangement and narrowness of theblades made it difficult to direct the spray ontothe blades and ensure that the blades were coatedproperly with the pesticide. Another type ofapplicator, such as a backpack mist blowerapplicator as used in the Trout et al. (2007)study, may be more effective than the handheldpump used to apply the pesticide in our study.

Mosquitoes in different physiological stateshave shown varied responses to pesticide treat-ments (Hadaway and Barlow 1956). Bransby-

Table 2. Mean percent knockdown (SE) of different sexes and states of Aedes albopictus observed at 1, 4, and 24 hafter exposure to TalstarOneH-treated Rhododendron simsii leaves (active ingredient, bifenthrin 7.9%).

Days posttreatment

0 7 14 21 28 35 42

1 h

Sugar-fed male 100.0 (0.0)a1 72.1 (3.1)a 7.1 (1.6)a 5.4 (1.5)a 0.0 (0.0) 0.0 (0.0) 0.0 (0.0)Sugar-fed female 100.0 (0.0)a 66.3 (2.2)ab 4.2 (1.5)ab 1.7 (3.8)a 0.0 (0.0) 0.0 (0.0) 0.0 (0.0)Gravid female 100.0 (0.0)a 57.1 (3.0)b 1.7 (1.0)b 0.0 (0.0)b 0.0 (0.0) 0.0 (0.0) 0.0 (0.0)Blood-fed female 100.0 (0.0)a 58.3 (4.0)b 2.9 (1.5)b 1.7 (4.8)a 0.0 (0.0) 0.0 (0.0) 0.0 (0.0)ANOVA2 F ns 5.53** 27.81* 5.17** ns ns ns

4 h

Sugar-fed male 100.0 (0.0)a 100.0 (0.0)a 60.0 (2.7)a 10.0 (0.0)a 0.4 (0.4)a 0.0 (0.0) 0.0 (0.0)Sugar-fed female 100.0 (0.0)a 100.0 (0.0)a 23.8 (2.9)b 0.0 (0.0)b 0.0 (0.0)a 0.0 (0.0) 0.0 (0.0)Gravid female 100.0 (0.0)a 100.0 (0.0)a 25.4 (3.7)b 0.0 (0.0)b 0.0 (0.0)a 0.0 (0.0) 0.0 (0.0)Blood-fed female 100.0 (0.0)a 100.0 (0.0)a 23.3 (2.2)b 0.0 (0.0)b 0.0 (0.0)a 0.0 (0.0) 0.0 (0.0)ANOVA F ns ns 22.66** 1.00** 1.00** ns ns

24 h

Sugar-fed male 100.0 (0.0)a 100.0 (0.0)a 100.0 (0.0)a 98.3 (0.8)a 89.6 (1.9)a 82.9 (2.7)a 79.6 (2.2)aSugar-fed female 100.0 (0.0)a 100.0 (0.0)a 97.1 (5.5)a 95.4 (1.6)a 83.3 (2.1)a 72.5 (3.4)ab 58.3 (2.7)bGravid female 100.0 (0.0)a 100.0 (0.0)a 99.2 (0.6)a 94.6 (1.9)a 73.3 (2.6)b 53.3 (3.0)c 45.4 (1.3)cBlood-fed female 100.0 (0.0)a 100.0 (0.0)a 98.7 (0.9)a 96.6 (1.0)a 84.1 (3.5)a 62.1 (5.3)bc 56.3 (4.1)bANOVA F ns ns ns ns 6.36** 10.73** 26.31**

1 Means within each column followed by the same letter are not significantly different. Tukey’s HSD test (P 5 0.05), N 5 24.2 ANOVA, analysis of variance; ns, P . 0.05.* P , 0.05.** P , 0.01.

182 JOURNAL OF THE AMERICAN MOSQUITO CONTROL ASSOCIATION VOL. 25, NO. 2

Williams and Webley (1965) applied DDT directly toblood-fed Culex pipiens fatigans Wiedemann andobserved higher tolerance to the pesticide than inblood-fed Anopheles gambiae Giles and Ae.aegypti Linnaeus. Halliday and Feyreisen (1987)found that DDT tolerance increased at 24 h inCx. pipiens and postulated that the increasedpesticide tolerance was due to changes in detox-ification pathways activated during blood mealdigestion. Increase in tolerance was not observedin Cx. pipiens treated with cyclodiene andcarbamate pesticides. Previous studies showedhigher tolerance to pesticides in blood-fed mos-quitoes for 48-h post–blood-meal ingestion, atwhich point the LD50 returned to levels shown insugar-fed females (Bransby-Williams and Webley1965, Halliday and Feyreisen 1987). The blood-fed female mosquitoes in our study did not showincreased tolerance to the residual pesticide incomparison to female sugar-fed or gravid mos-quitoes for the 1st 21 days posttreatment. Theseconflicting findings may be due to differences intolerance levels of the species studied.

Residual pesticide application to vegetation is auseful technique in suppressing targeted pestspecies, such as Ae. albopictus, and may beespecially effective during zoonotic disease out-breaks. This technique can also be used with atargeted integrated pest-management approach.A residual pesticide application applied whenpopulations of adult Ae. albopictus are high willprovide relief from the host-seeking adults andallow time for the treatment of water-holdingcontainers. Further study of how physiologicalstate impacts the efficacy of residual pesticidetreatments and the resting behavior of this andother species should be undertaken to improvethe efficacy of this control methodology.

ACKNOWLEDGMENTS

We thank B. Quinn and E. Vrzal, USDA-ARS,Gainesville, FL for their technical assistance inthis study.

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