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R E S E A R C H Open Access
New adhesive traps to monitor urban mosquitoes
with a case study to assess the efficacy of
insecticide control strategies in temperate areas
Beniamino Caputo
1*
, Annamaria Ienco
1
, Mattia Manica
1
, Vincenzo Petrarca
2
,RobertoRosà
3
and Alessandra della Torre
1
Abstract
Background: Urban mosquitoes in temperate regions may represent a high nuisance and are associated with the risk of
arbovirus transmission. Common practices to reduce this burden, at least in Italian highly infested urban areas, imply
calendar-based larvicide treatments of street catch basins –which represent the main non-removable urban breeding site
–and/or insecticide ground spraying. The planning of these interventions, as well as the evaluation of their effectiveness,
rarely benefit of adequate monitoring of the mosquito abundance and dynamics. We propose the use of adhesive traps
to monitor Aedes albopictus and Culex pipiens adults and to evaluate the efficacy of insecticide-based control strategies.
Methods: We designed two novel types of adhesive traps to collect adult mosquitoes visiting and/or emerging from
catch basins. The Mosquito Emerging Trap (MET) was exploited to assess the efficacy of larvicide treatments. The Catch
Basin Trap (CBT) was exploited together with the Sticky Trap (ST, commonly used to collect ovipositing/resting females) to
monitor adults abundance in the campus of the University of Rome “Sapienza”- where catch basins were treated
with Insect Growth Regulators (IGR) bi-monthly and Low-Volume insecticide spraying were carried out before
sunset - and in a nearby control area.
Results: Results obtained by MET showed that, although all monitored diflubenzuron-treated catch basins were repeatedly
visited by Ae. albopictus and Cx. pipiens, adult emergence was inhibited in most basins. Results obtained by ST
and CBT showed a significant lower adult abundance in the treated area than in the untreated one after the second
adulticide spraying, which was carried out during the major phase of Ae. albopictus population expansion in Rome.
Spatial heterogeneities in the effect of the treatments were also revealed.
Conclusions: The results support the potential of the three adhesive traps tested in passively monitoring urban
mosquito adult abundance and seasonal dynamics and in assessing the efficacy of control measures. ST showed
higher specificity for Ae. albopictus and CBT for Cx. pipiens. The results also provide a preliminary indication on the
effectiveness of common mosquito control strategies carried out against urban mosquito in European urban areas.
Keywords: Ae. albopictus, Sticky trap, Vector control, Catch basins, Larvicide, Insecticide spraying
Background
In its native range, the mosquito species Aedes albopic-
tus [Stegomyia albopicta] is present throughout much of
the Oriental region from the tropics to northern China
and North Korea. In recent decades, modern transporta-
tion has globalized the species most notably to much of
the New World and several European countries [1,2].
Apart from Albania [3] where it was present since the
mid-1970s (and possibly earlier), Italy was the first coun-
try in Europe (1990) with widespread infestation and
where the densities in urban areas became a serious
nuisance, especially due to the species aggressive day-
time biting behaviour [4-8]. Moreover, Italy was the first
European country to experience an outbreak of Chikun-
gunya virus (CHIK) entirely sustained by Ae. albopictus
[9]. In fact, the species is a competent vector of several
arboviruses [10-12] and has been responsible for major
epidemics of CHIK in islands of Indian ocean and in
* Correspondence: beniamino.caputo@uniroma1.it
1
Dipartimento di Sanità Pubblica e Malattie Infettive, Università di Roma
“Sapienza”, Piazzale Aldo Moro 5, 00185 Rome, Italy
Full list of author information is available at the end of the article
© 2015 Caputo et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,
unless otherwise stated.
Caputo et al. Parasites & Vectors (2015) 8:134
DOI 10.1186/s13071-015-0734-4
India in 2005–2006 [13,14], as well as of the indigenous
transmission of Dengue virus in Japan during the World
War II [15,16] and, more recently, in the south of France
[17,18] and Croatia [19]. These latest events highlighted
the necessity to elaborate preparedness for response to
autochthonous virus transmission in Europe [20]. In fact,
due to the absence of commercially available vaccines
against these arboviroses, vector control is the only ef-
fective measure presently available to stop an epidemic.
In case of arboviral outbreaks in Europe, guidelines by
the European Centre for Disease Prevention and Con-
trol, as well from the Italian National Health Institute
(Istituto Superiore di Sanità, ISS), suggest integration of
different strategies (e.g. public health education, larval
breeding places reduction, biological control of non-
removable potential larval sites such as catch basins, and
insecticide treatments against adults mosquitoes) to re-
duce Ae. albopictus densities and control pathogen trans-
mission [20,21]. A similar integrated approach, based on
the use of adulticides restricted to specific areas (e.g.
cemeteries, school yards and hospitals) or situations of
high concentration of hosts (e.g. fairs, etc.), is also sug-
gested by ISS to prevent the settlement of high Ae. albo-
pictus densities. However, despite the ISS indications,
adulticide treatments are largely implemented in Italian
urban areas by both public and private companies with
the sole aim to reduce the very high biting nuisance to the
citizens. Main control measures usually involve treatments
of catch-basins (considered as the main non-removable
urban larval sites for Ae. albopictus and Culex pipiens
[21-23]) with Insect-Growth-Regulators (IGR, which
interfere with larval development and inhibit adult emer-
gence) and spraying of pyrethroid and/or pyrethrum-
based adulticides by truck-mounted cannon spray
atomizers or portable thermal foggers.
Currently, the most widely used method to detect and
monitor Ae. albopictus populations is the counting of
eggs collected by ovitraps, which are small black con-
tainers resembling typical oviposition sites [24,25]. Ovi-
traps have been sometimes also used to carry out
evaluations of the efficacy of treatments against Ae. albo-
pictus in urban areas [26,27]. The advantages of ovitraps
are that they are inexpensive and sensitive for the detec-
tion of Ae. albopictus, thus allowing large scale surveil-
lance and monitoring schemes. However, ovitraps have
also important constraints. First, there are theoretical
controversies about the use of ovitrap data for assessing
adult populations, particularly at high adult densities
[28]. Second, in areas where species with similar egg/lar-
val morphology are present (e.g. Ae. albopictus and Ae.
aegypti), eggs and larvae need to be maintained until
adult emergence for species identification [29]. These
constraints are overcome by BG-Sentinel traps (BG-
traps; Biogents, Regensburg, Germany), which have been
specifically designed to actively collect host-seeking Ae.
albopictus females (but also collect associated males,
[30,31]) and are being increasingly used to determine
the species abundance [31-33]. Recently, BG-traps have
been also successfully exploited to evaluate the efficacy of
integrated Ae. albopictus control activities in New Jersey,
USA [27,34]. However, BG-traps have several limiting op-
erational constraints (e.g. need of a power-supply, of CO
2
/
lure release and of daily activation/maintenance, large size
and high individual cost), which make their large scale ex-
ploitation very laborious and expensive. Finally, alternative
to ovitraps and BG-traps, adhesive traps have been
exploited to monitor ovipositing Ae. albopictus females
attracted by a small water-container similar to an ovitrap.
Adhesive traps overcome the limits of both ovitraps and
BG-traps, but are less sensitive than ovitraps at very low
densities [35] and collected adults, contrary to those col-
lected by BG-traps, are difficult to be freed from glue in
order to keep them for further analyses (e.g. molecular
genetics analyses) and are not suitable for arbovirus
search. Moreover, several designs of adhesive traps have
been proposed [36-38] and so far used exclusively for re-
search, and a standardized model is not yet accepted for
routine monitoring activities.
The objective of the present study was to propose the
use of adhesive traps not only to monitor urban mosquito
abundance, but also to evaluate the efficacy of insecticide-
based control strategies, such as those typically imple-
mented in Italian urban areas infested by Ae. albopictus
(and Culex pipiens s.l., hereafter Cx. pipiens). To this aim
we tested: i) a newly designed Mosquito Emerging Trap to
assess adult emergence from catch basins treated with
IGR-analogs, and ii) two adhesive trap designs to monitor
adults abundance in relation to insecticide spraying in a
study area in Rome: a) the Sticky Trap, already shown to
provide estimates of species abundance correlated with
those obtained by ovitraps [35] and exploited to study its
behaviour in urban areas [39,40], and b) the Catch Basin
Trap, ad hoc designed for large scale passive monitoring
of urban mosquitoes associated to catch basins.
Methods
Trap design
Three types of adhesive traps have been used in the
present study:
–the Mosquito Emergence Trap (MET; Figure 1b),
consisting of a net panel coated with commercially
marketed rat-glue (DeBello, Zapi Chemical Indus-
tries SpA) on both faces and fixed with ‘velcro’to an
aluminium-frame positioned under the drain-grid.
MET of three sizes (40×40 cm, 44×44 cm, 55×55
cm) were used in relation to the sizes of the specific
catch basin to be surveyed.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 2 of 12
–the Sticky-Trap (ST, [35]; Figure 1c); the Catch
Basin Trap (CBT; Figure 1d) consisting of a black
panel (17×10 cm) set in an aluminium frame
equipped with a top (18×5 cm) to maintain the
frame perpendicular to the drain-grid. A transparent
sheet manually coated with rat-glue at both sides is
fixed at each side of the panel; the area of surface
coated with glue was equal to that of the four adhe-
sive panels in the ST.
Insecticide treatments
Insecticide treatments against mosquito larvae and adults
were carried out during summer 2012 on the campus of
the University of Rome “Sapienza”(~22 hectares; hereafter
“treated area”), which represents a highly urbanized area
in Rome [39]. The campus is mostly characterized by
buildings, roads, car parks and small green areas with
trees and/or hedges and, at its eastern extremity, by a
small botanical garden (Figure 1a).
Catch basins in the campus were treated with a larvi-
cidal IGR (Flubex, 2 g tablets with 2% of diflubenzuron,
I.N.D.I.A.. Industrie Chimiche SRL). One tablet was ap-
plied every second week (starting May 2012) to each of
the 166 catch basins in the treated area, including those
that were dry to avoid risk of production of larvae in
case of rain.
A water-based 0.5% TERBUTIN formulation (ZEP
ITALIA SRL .: 1.5 g pyrethrum 50% extract; 8 g per-
methrin, 2.64 g piperonyl butoxide for 100 g of product)
was sprayed on July 26th and on August 23rd 2012. Cold
Low-Volume (LV) spraying (droplet size < 50 μm) was
carried out by a cannon spray atomizer (series “ELITE”
Spray Team snc) mounted on a flatbed truck, with the
boom angled at 45-70°. The vehicle was driven along all
major roads in the campus (light-brown in Figure 1a) at
an average speed of 15 km/h. Spraying was carried out
60–90 minutes before sunset and was concluded at dusk.
All treatments were carried out by qualified technicians
of a private company (SOGEA s.r.l.).
Figure 1 Map of the campus of University of Rome “Sapienza”.Sketch map (1:3800 scale, a) of the area treated with insecticides, including the
operational subdivision into a 18-cell grid and the location of 8 Mosquito Emerging Traps (MET, b) 36 Sticky Traps (ST, c) and 36 Catch Basin Traps
(CBT, d). The map was obtained by manual digitizing via the software Quantum GIS (QGIS Development Team, 2013. QGIS Geographic Information
System. Open Source Geospatial Foundation Project).).
Caputo et al. Parasites & Vectors (2015) 8:134 Page 3 of 12
Evaluation of insecticide treatments
The MET was used to assess the number of adults visit-
ing and emerging from catch basins. Each week (from
August 1th to September 28th), eight METs were posi-
tioned for 48 hours in two catch basins in each of the
quadrants (North, N; East, E; South, S; West, W) of the
treated area (Figure 1a) and in two basins in the untreated
area (UN). This corresponds to the enclosed garden (the
Institute of Anatomy, ~1 hectare at ~300 m from the
treated area see [41] for details), where no treatments
were performed. Before positioning the METs, mosquitoes
possibly resting on the walls of the catch basin were
chased away by a stick, to be sure that mosquitoes glued
to MET’s inner face were freshly emerged ones. The adhe-
sive panels were brought to the laboratory and glued mos-
quitoes were morphologically identified and counted
under a stereo-microscope.
The CBT and the ST were used to assess the com-
bined effect of larvicidal and adulticidal treatments. The
treated area was sub-divided into a grid of eighteen
100×100m-cells and 2 STs and 2 CBTs were positioned
in each cell, for a total of 72 traps (Figure 1a). Ten STs
and ten CBTs were positioned in the untreated area.
Sticky panels in ST and CBT were replaced on a weekly
basis. Glued mosquitoes were brought to the laboratory
and glued mosquitoes were morphologically identified
and counted under a stereo-microscope [42]. Monitoring
was carried out for 10 weeks (from July 12th to September
20th 2012). Monthly mean temperatures were 27.3°C,
30.2°C and 20.9°C in July, August and September, respect-
ively. Rainfall was negligible in July and August, while nine
days of rain were recorded in September.
To assess the impact of the adulticides and compare this
to published data, an algebraic variation of Henderson’s
method [43] was employed using the formula: Percent-
age control = [100 −(T/U)100]whereTisthepost-
application weekly mean of mosquito counts divided by
the pre-application weekly mean in the treatment site,
and U is the post-application weekly mean divided by
the pre-application weekly mean in the untreated site.
Statistical analysis
A generalized linear mixed model (GLMM) with nega-
tive binomial error term was carried out to compare the
number of adult mosquitoes visiting the catch basins (i.e.
glued in the outer side of METs) between treated and un-
treated sites. The response variables were the number of
males, females and total Ae. albopictus and Cx. pipiens.
Site of trapping (four sites for treated area, corresponding
to the N, E, S and W quarters, and one for untreated area)
was the explanatory variable and date of collection was in-
cluded into models as random effect.
The impact of larvicides on the emergence of Ae. albo-
pictus and Cx. pipiens was assessed by exact Fisher’s
tests, comparing presence/absence of mosquitoes (glued
to the inner side of METs) between treated and untreated
sites. Differences were considered significant when α<
0.05 and all tests were two tailed. In this case, a Fisher’s
test were preferred to a Generalized Linear Model (GLM)
with binomial error as presence/absence of mosquitoes
glued in the inner side of METs perfectly separates zeroes
and ones among treated and untreated sites.
A GLM with negative binomial error term was carried
out to investigate the relationship between ST- and CBT-
counts in the overall sample, as well as in treated and in
untreated sites. In this case, ST-counts were chosen as the
response variable and CBT-counts as explanatory variable.
Four GLMMs with negative binomial error term were
carried out to investigate the effect of treatments (treated
vs. untreated site) and collection method (ST vs. CBT) on
adult mosquito abundance. The response variables were
mosquito counts for Ae. albopictus and Cx. pipiens separ-
ately considering specific models for male and female
mosquitoes. Explanatory variables were treatments, collec-
tion method and their interaction. To account for possible
temporal autocorrelation, date of collection was included
into models as a random effect. In addition, a geostatistical
variogram was applied to model residuals to evaluate if
there was any spatial autocorrelation. In order to evaluate
the temporal effect of adulticide treatments we carried out
GLMMs using three different datasets corresponding to: i)
Table 1 Descriptive statistics of Aedes albopictus and Culex pipiens collected by Mosquito Emerging Trap
Aedes albopictus Culex pipiens
Females Males Females Males
Outer face Inner face Outer face Inner face Outer face Inner face Outer face Inner face
N1.9 (±0.3) 0 2.1 (±0.4) 0 1.3 (±0.3) 0 0.4 (±0.1) 0.1 (±0.1)
E3.9 (±0.5) 1.6 (±0.3) 2.5 (±0.4) 2.5 (±0.4) 2.0 (±0.2) 1.4 (±0.3) 1.1 (±0.3) 2.2 (±0.4)
S2.0 (±0.4) 0 1.6 (±0.4) 0 1.4 (±0.3) 0 0.7 (±0.2) 0.1 (±0.1)
W3.4 (±0.4) 0 2.6 (±0.5) 0 1.5 (±0.3) 0 0.7 (±0.2) 0.1 (±0.1)
UN 5.8 (±0.6) 2.9 (±0.3), 4.1 (±0.6) 5.1 (±0.6) 3.4 (±0.5) 2.1 (±0.3) 2.1 (±0.4) 3.7 (±0.5)
Mean counts /trap/48 hours (±standard error) in Mosquito Emerging Trap in two Diflubenzuron-treated catch basins located in each of quarters (N, E, S, W) of the
treated area and two catch basins in the untreated area (UN) during N = 15 samplings in 2012.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 4 of 12
the first two weeks of the trapping period that did not
include adulticide treatments; (ii) the first six weeks of
trapping that include the first adulticide treatment; (iii)
the whole trapping period (ten weeks) that included both
adulticide treatments. On the other hand, larvicidal-
treatments were applied continuously throughout the trap-
ping season, as explained in the previous section.
Four additional GLMMs with negative binomial error
term were performed to assess the effect of spatial het-
erogeneity and collection method in the treated site. As
above, the response variables were mosquito counts of
the two species (Ae. albopictus and Cx. pipiens) and gen-
der, while fixed effects were the sampling location (cell),
trap types (ST and CBT) and their interaction. Date of
collection was included as a random effect to account
for temporal autocorrelation. In addition, a geostatistical
variogram was applied to model residuals to evaluate if
there was any spatial autocorrelation. In this case, the
GLMMs were carried out only in the overall 10-week
dataset.
Analysis were performed using R 3.0.3 [44] using the
glmmADMB package [45,46].
Results
The two novel adhesive traps designed to collect adult
mosquito visiting and/or emerging from catch-basins (i.e.
the MET, Figure 1b, and the CBT, Figure 1d) were both
shown to collect females and males of the two mos-
quito species know to be associated with street catch
basins in Italian urban areas, i.e. Ae albopictus and Cx.
pipiens (Tables 1 and 2). Comparison of CBT vs ST per-
formance in the untreated area showed that the ratio
between Ae. albopictus and Cx. pipiens was slightly
over 1 in CBT, and ca. 5 in ST (Table 2; Fisher’s Exact
Test, p < 0.001).
Evaluation of the efficacy of IGR-treatments on mosquito
emergence from street catch basins using the Mosquito
Emerging Trap (MET)
Two Diflubenzuron-treated catch basins located at each
of N, E, S and W quarters of the treated area and two
catch basins in the untreated area (UN) were monitored
using the MET. All METs were visited by mosquitoes
(Table 1, “outer face”column). METs located in the E and
W quarters collected a significant higher number of Ae.
albopictus females than those in N and S ones, while no
differences were observed for Cx. pipiens (Additional file 1:
Table S1). A lower mean number of females of both species
was collected in the outer side of the MET in the treated
area compared to the untreated one (GLMM; p < 0.05,
Additional file 1: Table S1).
Virtually no mosquito emergence was observed in the
N-, S- and W-quarters of the treated area (Table 1, “inner
face”and Table 3), while Ae. albopictus and Cx. pipiens
emergence events in the two METs in the E-quarter (in
the botanical garden) were comparable to those in the un-
treated area (E vs UN, Fisher exact test, p-value > 0.05;
mean number of mosquito/trap in 48 hours (SE) = 4.1
(±0.6) and 8 (±0.8) Ae. albopictus and 3.6 (±0.7) and 5.8
(±0.7) Cx. pipiens in sites E and UN, respectively).
Evaluation of the efficacy of insecticide treatments on
mosquito adult densities using Sticky Traps (ST) and
Catch-Basin trap (CBT)
The ratio between Ae. albopictus and Cx. pipiens was
higher in ST than in CBT in both areas (Table 2; Fisher’s
Exact Test, p < 0.001 for all tests), as expected due to the
high specificity of ST for Ae. albopictus [35].
The population dynamics of adult females and males of
Ae. albopictus and Cx. pipiens in the two areas, as de-
termined by ST and CBT collections, are summarized
in Figure 2. The estimated percentage of control after
the second application of adulticides (by Henderson’s
method) was 80% and 87% for Ae. albopictus collec-
tions by ST and CBT, respectively, and 24% and 69% for
Cx. pipiens.
The results of the GLMM models performed to assess
differences in overall abundance of mosquitoes between
traps (ST vs. CBT) and between treated and untreated
areas over the 10-week trapping period are given in
Table 4 for females and Additional file 1: Table S2 for
males: i) ST-counts were significantly higher than CBT-
counts in each area for both Ae. albopictus females and
males, corresponding to an overall difference of 58% and
48%, respectively (Figure 3); ii) CBT-counts were signifi-
cantly higher than ST-counts in the untreated area for
Table 2 Descriptive statistics of Aedes albopictus and Culex pipiens collected by Sticky trap and Catch Basin Trap
Aedes albopictus Culex pipens Aedes albopictus/Culex pipiens ratio
Site Traps (N/area) Females Males Females Males Females Males
Treated ST (36) 4.5 (±0.2) 2.4 (±0.1) 1.6 (±0.1) 0.9 (±0.1) 2.7 2.6
CBT (36) 1.8 (±0.1) 1.1 (±0.1) 1.2 (±0.1) 0.7 (±0.1) 1.5 1.6
Untreated ST (10) 10.9 (±0.9) 6.1 (±0.5) 2.3 (±0.2) 1.1 (±0.1) 4.7 5.3
CBT (10) 4.3 (±0.5) 3.0 (±0.5) 3.7 (±0.3) 2.1 (±0.2) 1.2 1.4
Mean counts/trap (±standard error) collected by 36 Sticky Traps (ST) and 36 Catch Basin Traps (CBT) in the treated area and in 10 STs and 10 CBTs in the
untreated one during the overall 10-week sampling in 2012.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 5 of 12
both Cx. pipens females and males, corresponding to an
overall difference of 60% and 44.5% (Figure 3); iii) ST
and CBT Ae. albopictus counts were significantly lower in
the insecticide-treated than the untreated one (corre-
sponding to a 60% and a 62% catch-difference for females
and males, respectively) (Figure 2). iv) CBT Cx. pipiens
counts were significantly lower in the insecticide-treated
than in the untreated area (corresponding to a 68% and a
57% catch- difference for females and males, respectively)
(Figure 2).
However, no statistical differences in Ae. albopictus and
Cx. pipiens females and males counts between treated and
untreated area were observed when considering collec-
tions carried out in the 2 weeks before the first adulticide
treatment (Additional file 1: Tables S3 and S4), nor
those carried out in the 6 weeks before the second one
(Additional file 1: Tables S5 and S6). In all GLMMs no
spatial autocorrelation was observed (i.e. the variogram
did not show any clear violation of independence).
A positive relationship was observed between ST- and
CBT-counts both for Ae. albopictus (GLM output: Chi-
square = 20.85, df = 1, P < 0.001) and for Cx. pipiens
(Chi-square = 29.86, df = 1, P < 0.001) females within the
treated area only.
Finally, the results of the GLMMs carried out to as-
sess possible spatial differences in mosquitoes counts
among the 18 cells within the treated area in the entire
10-week sampling period (Figure 4; Table 5; Additional
file 1: Table S7) showed: i) significantly higher mosquito
counts in cell-17 and −18; ii) significantly higher Ae.
albopictus counts in ST than in CBT in all cells, except
cell-18; iii) no difference in Cx. pipiens counts between
the two traps in all the cells. Again, in all GLMMs no
spatial autocorrelation was observed.
Discussion
The present results support the exploitation of adhesive
traps to monitor adult mosquitoes in an urban environ-
ment and to assess the efficacy of insecticide treatments
against them.This latter aspect is particularly relevant,
as the efficacy of insecticide control activities is rarely, if
ever, evaluated in European urban areas where these ac-
tivities are carried out to reduce mosquito nuisance
Table 3 Aedes albopictus and Culex pipiens emergence
events from larvicide-treated and untreated street catch
basins
Aedes albopictus Culex pipiens
Site Females Males Females Males
Treated-N 0 0 0 1
Treated-E 11 15 11 14
Treated-S 0 0 0 2
Treated-W 0 0 0 1
Untreated 15 15 14 15
Adult female and male emergence events from two larvicide-treated catch
basins in each of the four quadrants in the treated area and from two untreated
catch basins during N =15 (48-hour) sampling collections by Mosquito
Emerging Trap.
Figure 2 Mosquito population dynamics in the insecticide treated area and in the untreated one. Mean counts/trap/week of Aedes
albopictus and Culex pipiens females (full lines) and males (dotted lines) collected by Sticky (ST) and Catch Basin (CBT) traps in insecticide-treated
(blue line) and untreated (red line) areas. STs and CBTs were 36 in the treated area and 10 in the untreated one. X-axis: sampling dates in summer
2012; asterisks: dates of the two adulticide spraying in the treated area; vertical bars: standard errors.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 6 of 12
rather than to reduce the risk of pathogen transmission.
This is due to a lack of standardized and simple devices
to collect adults urban mosquitoes and of standardized
easy-to-use procedures to take into account all possible
interacting variables (e.g. climatic factors, insecticide
characteristics, spraying methods, etc.), as well as of ap-
propriate motivation and resources.
The newly designed MET allows to discriminate be-
tween mosquitoes freshly emerged from catch basins
and those visiting the basins either for laying eggs or for
resting. Thus MET could be exploited to assess the per-
centage of positive catch basins, thus providing an index
similar to those commonly utilized to evaluate the posi-
tivity of other types of water containers (e.g. Container
Index = percentage of inspected water-holding con-
tainers infested with larvae or pupae). MET has the ad-
vantage to directly assess the presence of emerging
adults (as opposed to larvae or pupae) without the need
of high numbers of larval dips inside the catch basins
(which are needed to collect a representative number of
larvae/pupae [47]), thus also eliminating the need of
rearing larvae to the adult stage, when species with simi-
lar larval morphology are present [48]. Moreover, MET
can be exploited to assess the lethal effect of larvicide-
Table 4 Results of generalized linear mixed model of female mosquito sampling in insecticide-treated versus untreated
areas
Aedes albopictus Culex pipiens
Parameter Estimate SE z-value Pr(>|z|) Estimate SE z alue Pr(>|z|)
Intercept 2.33 0.12 18.46 <0.0001 0.82 0.12 7.09 <0.0001
Site (Treated) −0.91 0.08 −10.74 <0.0001 −0.35 0.11 −3.06 0.0022
Trap (CBT) −0.86 0.11 −7.99 <0.0001 0.47 0.13 3.54 0.0004
Site*Trap −0.08 0.13 −0.62 0.53 −0.80 0.16 −4.99 <0.0001
Number of observation: 862, number of weeks: 10, SE: standard error of parameter estimate, z-value: estimate to standard error ratio, Pr(>|z|): statistic for z-value.
Untreated area and Sticky Trap as reference level (CBT =Catch Basin Traps).
Figure 3 Aedes albopictus and Culex pipiens counts in the insecticide-treated and in the untreated areas. Box-plots of adult female and male
counts in 36 STs and 36 CBTs in the treated area and in 10 STs and 10 CBTs in the untreated one during the 10 weeks sampling in 2012. ST =Sticky
Trap (light grey); CBT =Catch Basin trap (dark grey). The boxes identify the first and third quartiles (the 25th and 75th percentiles). The upper whisker
extends from the boxes to the highest value that is within 1.5 * IQR (inter-quartile range: the distance between the first and third quartiles, so the
height of the boxes). The lower whisker extends to the lowest value within 1.5 * IQR. Points beyond the end of the whiskers are outliers.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 7 of 12
treatments in catch basins, which represent a fundamen-
tal component in the control of the abundance of urban
mosquitoes [49] and are very commonly carried out in
infested municipalities in Italy [21]. Results obtained
showed that, although all monitored catch basins were
shown to be visited by Ae. albopictus and Cx. pipiens,
adult emergence was completely inhibited in most
diflubenzuron-treated basins (the few exceptions are dis-
cussed below). It should be stressed that results obtained
by this approach do not allow an assessment of mortality
rates, which requires collection of larvae/pupae in
treated catch basins followed by laboratory observations,
particularly needed when IGR-analogs, which acts not
only on larvae but also on pupae, are used. MET can
thus be proposed to more easily assess directly in the
field whether the treatments are actually achieving the
expected goal, i.e. the “sterilization”of the catch basins.
Moreover, MET could simultaneously allow an evalu-
ation of the effect of larvicide on adults abundance
based on mosquito collected on its outer side. Possible
limitations for MET exploitation may be represented by
heavy rains and presence of abundant debris which
could reduce the adhesive properties of the trap and the
morphological qualities of collected specimens. Under
Figure 4 Aedes albopictus and Culex pipiens counts in each of the 18 cells of the insecticide-treated area. Box-plots of adult female and male
counts in 2 Sticky-Traps (STs; light grey) and 2 Catch Basin Traps (CBTs; dark grey) in each of the 18 cells of the insecticide-treated area during the 10-
week sampling in 2012. The boxes identify the first and third quartiles (the 25th and 75th percentiles). The upper whisker extends from the boxes to
the highest value that is within 1.5 * IQR (inter-quartile range: the distance between the first and third quartiles, so the height of the boxes). The lower
whisker extends to the lowest value within 1.5 * IQR. Points beyond the end of the whiskers are outliers.
Table 5 Results of generalized linear mixed model of female mosquito sampling in 18-cells within the insecticide-
treated area
Aedes albopictus Culex pipiens
Parameter Estimate SE z value Pr(>|z|) Estimate SE z value Pr(>|z|)
Intercept 1.26 0.18 6.93 <0.0001 0.27 0.22 1.25 0.21
Trap (CBT) −0.80 0.22 −3.64 0.0002 −0.11 0.30 −0.37 0.71
Cell 17 0.67 0.16 4.29 <0.0001 1.04 0.24 4.30 <0.0001
Cell 18 0.62 0.16 3.92 <0.0001 1.10 0.24 4.60 <0.0001
CBT* Cell 17 0.38 0.27 1.43 0.15 0.22 0.35 0.62 0.54
CBT* Cell 18 0.62 0.27 2.34 0.02 0.10 0.35 0.30 0.76
Number of observation: 662, number of weeks: 10, SE: standard error of parameter estimate, z-value: estimate to standard error ratio, Pr(>|z|): statistic for z-value.
Cell 1 and Sticky Trap as reference level. (CBT = Catch Basin Traps).
Caputo et al. Parasites & Vectors (2015) 8:134 Page 8 of 12
our climatic conditions and with the experimental proto-
col applied neither limitations represented a major prob-
lem in the present study.
In contrast to MET, CBT does not allow to discrimin-
ate between freshly emerged specimens and those visit-
ing the catch basins for resting/ovipositing, and thus is
not a good tool to assess efficacy of larvicide treatments
in the catch basin. However, since CBT is easily in-
stalled perpendicular to the drain-grid (and does not
require the lift of the grid needed to locate MET), CBT
can be exploited for large scale monitoring of urban
mosquitoes associated with catch basins. Results from
the untreated area indicated that CBT collected higher
numbers of Cx. pipiens and lower numbers of Ae. albo-
pictus when compared to ST. This suggests that CBT
has the potential to be successfully exploited to pas-
sively monitor Cx. pipiens abundance and dynamics in
urban areas. In fact, monitoring of this species - which
represents a major vector of zoonotic pathogens such
as West Nile Virus [50] and Dirofilaria worms [51] - al-
most exclusively relies on traps requiring a fan driven
by an electric motor and more complicate logistics (e.g.
CDC-light traps, CDC gravid trap). On the other hand,
STisconfirmedtobeaneffectivedeviceformonitor-
ing Ae. albopictus [35]. In fact, although it only targets
ovipositing and resting adults, it collected more individ-
uals than CBT, which also targets freshly emerged adults.
This suggests that in the urban environment Ae. albo-
pictus is less attracted to catch basins than to smaller
oviposition/resting sites, which more closely resemble
its original sylvatic larval habitats (e.g. tree-holes, rock-
holes and fruit husks [8]).
Results also showed that ST and CBT are effective
tools for assessing abundance and population dynamics
of adult Ae. albopictus (and Cx. pipiens) in an area
where catch basins were treated by IGR-analogs and two
insecticide Low Volume sprayings were carried out be-
fore sunsets. Both ST and CBT have major advantages
compared to other tools usually used to evaluate the effect
of control activities against Ae. albopictus, e.g. BG-sentinel
traps or ovitraps [27,34], both of which have major con-
ceptual and operational constraints. BG-sentinel traps are
expensive, require power supply and release of CO
2
and
synthetic lures to attract and collect mosquito adults. Ovi-
traps provide only indirect estimates of adult abundance
based on numbers of eggs collected. In addition, in re-
gions where species with similar egg/larval morphology (e.
g. Aedes aegypti, Ochlerotatus geniculatus) coexist, larvae
must be reared to late instar or adults for reliable identifi-
cation. On the other hand, ST and CBT are cheap, easy to
manage (and can thus be deployed in larger numbers) and
allow easy identification of gender and species. During the
testing in Rome, we found ST to be much more efficient
than CBT for monitoring the impact of control measures
on Ae. albopictus, while the opposite was true for Cx.
pipiens. Moreover, the concomitant use of ST and CBT
provided result in agreement with the lethal effect of diflu-
benzuron treatments in catch basins (already revealed by
MET, see above). In fact, GLM analysis demonstrated a
direct relationship between Ae. albopictus and Cx. pipiens
counts by ST and CBT in the treated area, but not in the
untreated one. The lack of a direct relationship between
CBT- and ST-counts in the untreated area is likely due to
the fact that ST only collects mosquitoes visiting the catch
basin, either for resting or ovipositing, whereas CBT also
collects freshly emerged adults. On the other hand, the
direct relationship between CBT- and ST-counts in the
treated area is likely due to lack of emergent adults in an
area were catch basins are regularly treated with IGR-
analogs.
The abundance of Ae. albopictus and Cx. pipiens was
shown to be significantly lower in the treated vs un-
treated area only after the second adulticide spraying.
This may be due to our sampling effort which could not
have had a high enough resolution to detect the impact
of the first treatment. In fact, this treatment was carried
out in late July when adult densities of Ae. albopictus
were low, whereas the second was carried out four weeks
later when the Ae. albopictus population was growing
[52]. However, it is possible that the results obtained
highlighted an actual different impact of the two treat-
ments on the mosquito adult population. Interestingly, the
mosquito population expansion was evident in the un-
treated site in August but was completely absent in the
treated site for both females and males (Figure 2). Note-
worthy, the estimated percentage of control observed after
the second spraying (i.e. 80% and 87%, as estimated by ST
and CBT collections, respectively) is similar to that ob-
tained after a single night-time ultra-low volume (ULV)
treatment with DUET™Dual-action Adulticide (Clarke H,
Roselle, IL, USA) in New Jersey (USA) (i.e. 73% as esti-
mated by BG-trap collections; [34]). To our knowledge,
our results represent the first preliminary indication of the
effectiveness of LV spraying against Ae. albopictus in
urban areas, which is relevant, as ULV spraying is exten-
sively applied in the US and some European Countries
[53], but not in Italy. The high impact observed in Rome
may have been due to the timing (before sunset rather
than at night as in New Jersey) which corresponds to the
peak of flight activity of Ae. albopictus), when the treat-
ments are supposed to be most effective [54]. Moreover,
the effect of treatment may have been enhanced and pro-
tracted by the fact that the study area, although limited in
size, is surrounded by a ∼3 m-high wall which, based on
the relatively low flight height of Aedes albopictus [8], may
have acted as a barrier to re-introduction of large numbers
of adults from neighbouring areas, thus maximizing the
effect of the spraying.
Caputo et al. Parasites & Vectors (2015) 8:134 Page 9 of 12
The accurate monitoring of the treated area with high
numbers of STs and CBTs revealed spatial heterogene-
ities in the treatment efficacy, which was shown to be
lower in the botanical garden than in the rest of the
treated area (Figure 1a). This may be due to several fac-
tors. First, insecticide spraying was restricted to the per-
imeter of the garden where the dense vegetation may
have blocked movement of the insecticide aerosol (as re-
ported by [54]). Moreover, the regular and abundant
watering of the plants may have diluted larvicide con-
centration in the catch basins. In fact, MET revealed
that the only adult emergence was in the two catch ba-
sins in the botanical garden, where it was comparable to
that in the untreated sites. These results indicate the
need to identify hot-spots of mosquito production (e.g.
small public or private gardens)—as well as of resting
sites—in order to maximize the impact of mosquito con-
trol activities and to achieve an overall successful reduc-
tion of mosquito abundance and nuisance.
Conclusions
The results support the potential of the three adhesive
traps tested in passively monitoring urban mosquito
adult abundance and seasonal dynamics and in assessing
the efficacy of control measures. The results also provide
a preliminary indication on the effectiveness of IGR-
treatments in catch basins carried out during the whole
Ae. albopictus reproductive season in association with
LV insecticide spraying carried out during the beginning
of the major population expansion in reducing adult
abundance. It is important to remind that in this study
adulticide treatments were carried out before sunset,
when they are expected to be most effective, while in
most urban areas for safety reasons the treatments can
be carried out only during night-time or very early in
the morning [20,21]. More data are needed to: a) con-
firm the impact of adulticide treatments carried out i)
during the night, ii) at different phases of the mosquito
seasonal dynamics; iii) under different ecological condi-
tions, and b) to assess the relative role of larvicide and
adulticide treatments. Anyhow, the present results stress
the potential benefits of adulticide treatments conse-
quent to an accurate monitoring of adult densities. The
latter would also have the benefit to identify hot-spots of
larval/resting sites, which need to be specifically targeted
in order to maximize the impact of the control cam-
paign. It is however important to stress that insecticide
spraying should represent a method reserved for emer-
gency response and that a preferred strategy to control
Ae. albopictus should include other integrated activities
[26] - such as larval source reduction [55,56], biological
control [57], education and public awareness, as well as
personal protection [58]–which are often neglected by
the competent authorities.
Finally, it would also be interesting to correlate collec-
tions by ST and/or CBT with levels of mosquitoes nuis-
ance to establish a “threshold of nuisance”(as it has been
done for ovitraps [59], and BG-sentinel traps [27]) over
which adulticide treatments could be recommended not
only to reduce the burden of this aggressive mosquito
biter to the citizens, but also to prevent the establishment
of densities which would represent a high risk in the case
of migrant humans infected by arboviruses, as it occurred
in 2007 with Chikungunya virus in Italy [9].
Additional file
Additional file 1: Table S1. P-values of Generalized Linear Mixed Model
analysis of mosquitoes visiting METs in larvicide-treated and untreated areas.
Table S2. Results of Generalized Linear Mixed Model of male mosquito
sampling in insecticide-treated versus untreated areas. Table S3. Results
of Generalized Linear Mixed Model analysis of female mosquito sampling in
insecticide-treated versus untreated areas before the first insecticide-spraying.
Table S4. Results of Generalized Linear Mixed Model analysis of male
mosquito sampling in insecticide-treated versus untreated areas before the
first insecticide-spraying. Table S5. Results of Generalized Linear Mixed
Model analysis of female mosquito sampling in insecticide-treated versus
untreated areas before the second insecticide-spraying. Table S6. Results of
Generalized Linear Mixed Model analysis of male mosquito sampling in
insecticide-treated versus untreated areas before the second insecticide-
spraying. Table S7. Results of Generalized Linear Mixed Model of male
mosquito sampling in 18-cells within the insecticide-treated area.
Competing interests
The authors declare that they have no competing interests.
Authors’contributions
Designed the study: BC, AdT. Performed the data collection: BC, AI. Analyzed
the data: BC, MM, AI, RR. Wrote the paper: BC, MM, RR, VP, AdT. All authors
read and approved the final version of the manuscript.
Acknowledgements
We are grateful to the Department of Environmental Biology, to the Unit of
Comparative Anatomy of the Department of Biology and Biotechnology and to
Technical Services of Sapienza University for hosting our experiments and for
helping with the logistics. We thank Paul Reiter (Institute Pasteur Paris) for
encouraging us to perform the study and for helpful suggestions to the
manuscript and Alberto and Vito Bruni Ercole and Emanuele Fascetti of SOGEA
srl for helpful interactions during and after the insecticide treatments. This work
has been funded by EU grant FP7-261504 EDENext, and is catalogued by the
EDENext Steering Committee as EDENext291 (http://www.edenext.eu). The
contents of this publication are the sole responsibility of the authors and
do not necessarily reflect the views of the Ministry nor of European Commission.
RR was partially funded by the Autonomous Province of Trento (Italy), Research
funds for Grandi Progetti, Project LExEM (Laboratory of excellence for
epidemiology and modelling, http://www.lexem.eu).
Author details
1
Dipartimento di Sanità Pubblica e Malattie Infettive, Università di Roma
“Sapienza”, Piazzale Aldo Moro 5, 00185 Rome, Italy.
2
Dipartimento di
Biologia e Biotecnologie, Università di Roma “Sapienza”, Piazzale Aldo Moro
5, 00185 Rome, Italy.
3
Dipartimento di Biodiversità ed Ecologia Molecolare,
Centro Ricerca e Innovazione, Fondazione Edmund Mach, San Michele
all’Adige, TN, Italia.
Received: 26 January 2015 Accepted: 12 February 2015
Caputo et al. Parasites & Vectors (2015) 8:134 Page 10 of 12
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