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Journal of Economic Entomology, XX(XX), 2019, 1–6

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doi: 10.1093/jee/toz020
Household and Structural Insects Research

Timing of Lambda-Cyhalothrin and Pyriproxyfen Barrier


Treatments for Aedes albopictus (Diptera: Culicidae)
Management
Gregory M. Williams,1,2,4, Isik Unlu,1,3 Ilia Rochlin,1 Yi Wang,1 and Randy Gaugler1

1
Center for Vector Biology, Rutgers University, 180 Jones Avenue, New Brunswick, NJ 08901, 2Hudson Regional Health Commission,
595 County Avenue, Secaucus, NJ 07094, 3Highway Department, Mercer County Mosquito Control, 300 Scotch Road, West Trenton,
NJ 08628 and 4Corresponding author, e-mail: gwilliams@hudsonregionalhealth.org

Subject Editor: Michael Rust

Received 1 November 2018; Editorial decision 13 January 2019

Abstract
Barrier applications, treating vegetation and other potential mosquito resting areas with residual pesticides,
have become standard practice for commercial pest management professionals offering mosquito control ser-
vices. These treatments are generally effective in reducing numbers of the Asian tiger mosquito, Aedes albop-
ictus (Skuse). In the temperate climates, adult Ae. albopictus populations are naturally eliminated each winter
and must be grown from diapausing eggs the following spring. Therefore, early-season control interventions
timed before populations rebound may further reduce population growth compared with interventions that
take place after the population has peaked. We compared Early (1 June) barrier applications of lambda-cyhalo-
thrin (Demand CS) mixed with the insect growth regulator pyriproxyfen (Archer IGR) to Late applications (31
July) in urban and suburban residential parcels in New Jersey. These applications resulted in 43 and 51%
reductions in adult Ae. albopictus populations in the Early and Late intervention study parcels, respectively,
when compared with the untreated Controls. Indirect applications of pyriproxyfen (i.e., rainwater runoff trans-
ferring pesticide) to potential larval habitat did not cause mortality in laboratory larval bioassays but direct
mist applications of the Archer and Demand combination to larval habitats led to elevated larval mortality over
a 6-wk period. The Early-season intervention offered no advantage in efficacy on adult populations compared
with the Late-season intervention, which targeted peak mosquito populations. Our study provides support for
the efficacy of barrier applications and illustrates the importance of timing barrier treatments to coincide with
established Ae. albopictus action thresholds.

Key words: Aedes albopictus, barrier spray, lambda-cyhalothrin, pyriproxyfen

Arbovirus outbreaks such as West Nile virus, chikungunya, and services, their efficacies have not been well documented in the peer-
Zika virus (Kendrick et al. 2014, Likos et al. 2016) have illuminated reviewed literature. Several barrier treatment studies are limited to
the need for mosquito control in the absence of vaccines. However, forced contact bioassays (Xue 2008, Doyle et al. 2009) or semifield
many areas lack public mosquito abatement programs and, if such conditions (Cilek and Hallmon 2006, 2008). Other studies focused
programs exist, they typically lack the resources to routinely service on species not found in the temperate United States (Britch et  al.
private property. Therefore, homeowners are often responsible for 2009, Muzari et al. 2014) or were conducted under the more sub-
managing mosquito problems on their property, but lack the exper- tropical and wet conditions of the southeastern United States (Trout
tise to do so effectively. Private pest managements satisfy this need et  al. 2007). While these studies demonstrated acceptable efficacy,
by offering mosquito control services to their customers, generating more work is needed to determine the most appropriate products
over $157 million in revenue in 2016 alone (Specialty Consultants and best management practices for optimal results under different
2017). More than half of all private pest management companies geographic areas.
surveyed (n  =  224) offer mosquito control services with 74% of We conducted a study in 2016 to evaluate the efficacy of residen-
those relying on the targeted application of mosquito adulticides as tial barrier treatments with lambda-cyhalothrin alone or mixed with
barrier treatments (MGK 2017). Despite the proliferation of these pyriproxyfen against Aedes albopictus (Skuse; Diptera: Culicidae)

© The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. 1
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2 Journal of Economic Entomology, 2019, Vol. XX, No. XX

(Unlu et al. 2018). We reported adult population reductions up to parcel was treated two times (1 June 31 July), Late parcels were only

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78% compared with Controls. No attempt was made to directly treated one time (31 July). No other forms of mosquito management
measure pupal mortality, but the concurrent or exclusive applica- such as source reduction, sanitation, water management, etc. were
tion of pyriproxyfen had no measureable effect on the adult popu- implemented.
lations. The present study expands the previous investigation with To assess pupal mortality, a 19-liter polyethylene bucket was
two objectives. First, we quantifed and compared the efficacy and placed in a shaded area of each treatment and Control parcel.
persistence of Early versus Late-season barrier treatments against The buckets were half-filled with oak leaf infusion (Trexler et  al.
adult Ae. albopictus populations. Secondly, we evaluated the effect 1998) then covered with fine mesh window screen to prevent mos-
of adding pyriproxyfen to the barrier applications on immature Ae. quitoes from utilizing the buckets while allowing runoff to collect
albopictus. weathering to occur. Immediately following the Early barrier appli-
cation (1 June), after the spray had dried, five buckets were placed
below treated vegetation to collect any runoff from rain that might
Materials and Methods wash pyriproxyfen from the leaves into the bucket. During the Late
Study Location, Design, and Mosquito Surveillance application on 31 July, all 10 treatment buckets were sprayed dir-
Residential neighborhoods in Hudson and Mercer counties, New ectly with backpack mist blowers in the same manner as the vege-
Jersey, were selected based on the history of established Ae. albop- tation to measure direct pupal mortality. The screens were removed
ictus populations from mosquito surveillance records (Unlu et  al. during this treatment and then replaced. Five untreated buckets re-
2011, 2018). The potential study sites were identified through mained in the Control parcels. Every 2 wk, 250 ml water samples
neighborhood canvasing. Thirty parcels (15 in each county) were were collected from the buckets in polypropylene containers and
selected and assigned to one of three groups (Early treatment, Late returned to the laboratory for bioassay. The buckets were not re-
treatment, Control) for a total of 10 parcels per group. All parcels filled but rainwater was allowed to collect in the buckets. For each
consisted of single-family houses on grass lots ranging in size from water sample, third instar Ae. albopictus larvae from a laboratory
200 to 500 m2. The Hudson County parcels were generally well colony (n = 20) (Unlu et al. 2018) were added directly into the con-
maintained but several were adjacent to a decommissioned railway tainers and the covers were affixed. Test larvae were reared from
line with overgrown vegetation, temporary pools of rainwater, and eggs previously collected on seed germination paper and stored at
trash. The Mercer County parcels ranged from well-maintained 26 ± 1°C. Larvae were hatched and fed brewer’s yeast (30 mg/liter)
properties to abandoned homes with overgrown vegetation and at 3 d intervals. Five slots (4–5  cm) were cut through the covers
water-filled trash. Control parcels were interspersed among the randomly for aeration. The cups were incubated at 26°C and 16:8
treatment parcels. The distance between the parcels ranged from (L:D) h photoperiod. Dead larvae, dead pupae, and emerged individ-
approximately 0.2 km (0.01–0.6 km) in Hudson County to 2.6 km uals were removed and recorded until all individuals had emerged
(0.1–6.6 km) in Mercer County. or died. Incomplete emergence of adults with attached exuvia was
Adult mosquito populations were monitored with one Biogents recorded as dead pupae. Three untreated cups containing 250 ml of
Sentinel (BGS) trapper parcel (n = 30) baited with a Biogents-Lure aged tap water were used as laboratory controls for each collection.
(Biogents AG, Regensburg, Germany). Traps were deployed in The results are presented by epidemiological week as defined by the
shaded areas on each parcel weekly for a 24  h period. The traps Centers for Disease Control (2016).
were placed in the same locations to minimize variation (Crepeau
et al. 2013). Trapping began 2 wk prior to the barrier treatments Statistical Analysis
(23 May) and continued for 19  wk postapplication until 12 The statistical methods were described previously (Unlu et al. 2018).
October 2017. Briefly, data from both counties were pooled and before-after-
control-impact (BACI) design was employed (Stewart-Oaten et  al.
Pesticide Barrier Treatments and Larval Bioassays 1986) for efficacy analysis. Mixed effects models containing fixed
All field work and pesticide applications were conducted by the re- treatment effects and random time effects were used to determine
spective county mosquito control programs under the authority of overall significance. Post hoc tests were performed by planned con-
Title 26, Chapter 9 of the New Jersey administrative code. The Early trasts with adjusted P-values, or by Tukey’s range test. Henderson
barrier treatments were performed on 1 June according to the label and Tilton (1955) correction was used to calculate control efficacy.
directions. Demand CS (6.34  ml/liter, 0.06% AI) and Archer IGR To check whether the effects differed by county or in males versus
(7.4 ml/liter, 0.01% AI) (Syngenta Crop Protection Inc., Greensboro, females, these variables were introduced in the model containing
NC) were premixed in a 227-liter tank and dispensed directly into the interaction term. For laboratory bioassays, combined pupal and
backpack mist blowers (model SR-450, Stihl Corporation, Virginia larval mortalities were calculated and compared for each sampling
Beach, VA). The mix was applied to all vegetation, leaf litter, and date. All statistical analyses used R v. 3.2.3 (R Core Team 2015) and
potential resting sites on the parcel up to a height of 3 m. For dense the packages lme4 v. 1.1–10 for mixed effects models (Bates et al.
vegetation, the blower nozzle was inserted into vegetation for thor- 2015) and multcomp v.1.4–8 for multiple comparisons. Means are
ough coverage (Trout et  al. 2007), treating leaves just below the followed by the standard error.
point of runoff. Water sensitive cards (Syngenta International AG,
Basel, Switzerland) were placed 1–2 m off the ground on the outer
Results and Discussion
layer of vegetation and deep within the vegetation blind to measure
the thoroughness of the applications. Mist blowers were weighed In Hudson County, 1,688 Ae. albopictus (1,214 females and 474
before and after applications to determine the amount of product males) were captured in 315 BGS collections. In Mercer County,
applied and each application was timed. The Late applications were 1,519 mosquitoes (1,237 females and 282 males) were collected over
made on 31 July to all of the Early and Late treatment parcels fol- the same period. Other mosquitoes such as Aedes triseriatus (Say)
lowing the same methods as the first application. In total, each Early (Diptera: Culicidae) were collected in negligible numbers and were
Journal of Economic Entomology, 2019, Vol. XX, No. XX 3

not included in the analyses. All data were pooled for BACI analysis of 69% 3 wk postspray (Fig. 1C). Efficacy started to decline 7 wk

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as there were no differences in treatment effects between counties or postspray. Average mosquito counts from treated parcels remained
male and female mosquitoes (all P > 0.5). below the controls for 7 of 8 wk (Fig. 1B). This difference was not
During the Early treatment on 1 June, 10.0 l ± 0.9 of material significant (Fig. 1A) likely due to the low populations at the start of
was applied in 12.8 min ± 1.7 per parcel on average. Over the Early the period and drop in efficacy at the end of the period. During the
period, there was a 46% reduction in the treated parcels (Early treat- Early period (1 June–30 July), the adult mosquito populations in
ment) compared with the Controls (Fig. 1A), although the results the untreated Late treatment parcels followed the same trend as the
were not significant relative to the Controls. Following the applica- Control parcels (Fig. 1A and B).
tion (7 June to 26 July) there was limited reduction 1 wk postspray During the application on 31 July, an average of 10.5 l ± 0.9 of
due to low Ae. albopictus populations followed by a peak reduction material was applied in 11.4 min ± 1.0 per parcel to all of the Early

Fig. 1.  Adult Aedes albopictus collections from BGS traps (n = 30) at three different treatments over time. (A) Interaction plot of trap averages (total collected) at
the Control and treatment parcels before treatment, after Early treatment (week 22, 1 June) and after Late treatment (week 30, 31 July). Overall present reduction
by Henderson–Tilton formula relative to the Control parcels are shown, with statistical significance (P < 0.05) indicated with an asterisk. (B) Trap averages for
each week, 21 May–14 October 2017. Thick vertical lines indicate the dates of pesticide applications and separate before, Early, and Late treatment time periods
indicated in (A). (C) Percent reduction in the total number of Ae. albopictus mosquitoes collected per BGS trap for each week post treatment. Each group was
compared with the Control group with Henderson–Tilton’s correction. The horizontal line represents 70% reduction threshold considered as effective.
4 Journal of Economic Entomology, 2019, Vol. XX, No. XX

and Late parcels. Following that application there was an overall non- 6  wk following lambda-cyhalothrin treatments, this was in caged

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significant reduction of 43% in the Early treatment parcels and a sig- trials where mosquitoes had nowhere to rest but on treated vegeta-
nificant 51% reduction in Ae. albopictus adults in the Late treatment tion. Trout et al. (2007) achieved an average of 67% mortality over
parcels relative to the Controls (Fig. 1A). Average mosquito counts 4  wk against Ae. albopictus following residential applications of
remained below the Control parcels for 9 of 11 wk with a 44–51% lambda-cyhalothrin. In the current study, we recorded an average
reduction for the first 3 wk postapplication in the Early parcels. In the of 64% mortality in the Early treatment 2–4  wk postspray, omit-
Late parcels, average mosquito counts remained below the Control ting week 1 due to exceedingly low mosquito populations. In the
parcels for the duration of the study with a 60–64% reduction for the Late treatment, we found a similar 65% reduction 1–3 wk postspray.
first 3 wk postapplication in the Late parcels. Over the duration of the Our overall results are nearly identical to Skiles (2017) who found
study, Control parcels had over two times more mosquitoes than Late a 51–42% reduction in Aedes mosquitoes over a 9 wk period using
parcels (Fig. 1A). Efficacy was relatively consistent 5  wk postspray the same pesticides and application technique. Despite the relatively
until below average temperatures (ONJSC 2017) in the first week of low population reduction, Skiles still achieved a high level of per-
September (week 36) led to low Ae. albopictus trap counts (Fig. 1B). ceived suppression with 83% of homeowners reporting a reduction
For both applications, water sensitive cards confirmed thorough cov- in mosquitoes, 84% spending more time outside, and 100% report-
erage throughout the treated vegetation. ing a reduction in mosquito bites following lambda-cyhalothrin and
The purpose of the Early treatment was to reduce Ae. albopic- pyriproxyfen applications. This illustrates that even low levels of
tus abundance when populations were very low, in an effort to operational control can lead to a significant reduction in mosquito
delay exponential population growth resulting in a lower number of presence and biting frequency.
adults toward the end of the season. Fewer adult mosquitoes laying In the previous study, pyriproxyfen had no measureable effect on
eggs in June should lead to lower mosquito populations in August. adult mortality (Unlu et al. 2018). Pyriproxyfen was deployed in the
Conversely, we saw no advantage to this Early treatment as it was less current study to determine its impact on larval populations. During
effective than the Late treatment. Mosquito abundance did not start the Early treatment period, we investigated indirect pupal mortality
to increase significantly until mid-July (week 28, Fig. 1B). By that time, due to runoff from treated vegetation. Even after 6 wk with 20 rain
the first application was 5 wk old and had likely lost some efficacy as events, there was no significant pupal mortality in any of the buckets
demonstrated previously (Unlu et al. 2018). These results suggest that (data not shown). The reason is unclear but could be the result of
one carefully timed application can be just as effective as two applica- insufficient amounts of pyriproxyfen being washed into the buckets,
tions. Further, postponing the application until mosquito populations or subsequent rainfall diluting the pyriproxyfen to sublethal levels
approach nuisance levels will expose mosquitoes to pesticides before or flushing it from the buckets. During the Late study period, all of
they start to degrade, providing a longer effective period. Nightly trap the treatment buckets (n  =  10) were treated directly. This resulted
counts greater than five Ae. albopictus have been used as a standard
action threshold and appear to coincide with homeowner complaints
(Unlu et al. 2016). In this study, this threshold was reached at the end
of June roughly corresponding to the Late treatment period.
Adult population reductions >70% normally result in reduced
biting frequency and can be considered effective for Ae. albopictus
management (Farajollahi et al. 2012). While we did not achieve that
threshold in 2017 with efficacies varying from 40 to 65% in the Late
treatments (Fig. 1), reductions of 73–75% were observed in 2016
(Unlu et al. 2018). Compared with 2016 we used the same teams,
equipment, neighborhoods (but with some different parcels) and
applied nearly twice as much active ingredient on average to each
parcel in Hudson County. Timing was also similar, as the 2016 appli-
cations were made within 7 d of the Late applications in 2017. One
possible explanation for the reduced efficacy is rainfall. Over 9.9 cm
more rain fell in Hudson County and 6.9 cm in Mercer County from
June through August compared with 2016 (ONJSC 2017). This
heavy precipitation likely eroded the material and led to a reduc-
tion in efficacy as demonstrated for other pyrethroids (Mulrooney
and Elmore 2000, Allan et al. 2009). Pesticide resistance tests were
not performed on the mosquito populations from these study sites
and, therefore, pyrethroid resistance cannot be completely ruled out.
However, testing has been repeatedly performed by both mosquito
control programs on other Ae. albopictus populations with no evi-
dence of pyrethroid resistance found. Marcombe et al. (2014) found
no evidence of pyrethroid or pyriproxyfen resistance among five
New Jersey Ae. albopictus populations studied. Fig. 2.  Laboratory bioassay results (n = 180) of Aedes albopictus pupal and
Our results are similar to previous barrier treatment studies. larval mortality resulting from direct backpack mist applications of lambda-
cyhalothrin (Demand CS) and pyriproxyfen (Archer IGR) to potential larval
Britch et  al. (2009) found 80% mortality against Culex tarsalis
habitat. The Early application was performed on week 22 (data not shown)
Coquillett (Diptera: Culicidae) immediately following field applica-
and only runoff mortality in the sentinel container was measured. The Late
tions of bifenthrin, but efficacy quickly fell to 60% and <40% 1 application was done on week 30 (thick line) and included direct treatments
and 2  wk post application, respectively. While Cilek and Hallmon of the sentinel containers. Statistically significant differences at P  <  0.05
(2008) demonstrated nearly 80% efficacy against Ae. albopictus for between the treatment and the Controls are denoted by asterisk.
Journal of Economic Entomology, 2019, Vol. XX, No. XX 5

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6 Journal of Economic Entomology, 2019, Vol. XX, No. XX

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