Indoor Resting Behavior of Aedes aegypti (Diptera: Culicidae) in Acapulco, Mexico

Abstract

The markedly anthropophilic and endophilic behaviors of Aedes aegypti (L.) make it a very efficient vector of dengue, chikungunya, and Zika viruses. Although a large body of research has investigated the immature habitats and conditions for adult emergence, relatively few studies have focused on the indoor resting behavior and distribution of vectors within houses. We investigated the resting behavior of Ae. aegypti indoors in 979 houses of the city of Acapulco, Mexico, by performing exhaustive indoor mosquito collections to describe the rooms and height at which mosquitoes were found resting. In total, 1,403 adult and 747 female Ae. aegypti were collected, primarily indoors (98% adults and 99% females). Primary resting locations included bedrooms (44%), living rooms (25%), and bathrooms (20%), followed by kitchens (9%). Aedes aegypti significantly rested below 1.5 m of height (82% adults, 83% females, and 87% bloodfed females); the odds of finding adult Ae. aegypti mosquitoes below 1.5 m was 17 times higher than above 1.5 m. Our findings provide relevant information for the design of insecticide-based interventions selectively targeting the adult resting population, such as indoor residual spraying.

Full text

Short Communication
Indoor Resting Behavior of Aedes aegypti
(Diptera: Culicidae) in Acapulco, Mexico
Felipe Dzul-Manzanilla,
1
Je´ sus Ibarra-L
opez,
1
Wilbert Bibiano Mar
ın,
2
Andre´ s Martini-Jaimes,
3
Joel Torres Leyva,
4
Fabi
an Correa-Morales,
1
Her
on Huerta,
5
Pablo Manrique-Saide,
2
and Gonzalo Vazquez M. Prokopec
6,7
1
Centro Nacional de Programas Preventivos y Control de Enfermedades (CENAPRECE), Secretaria de Salud, Eje 4 Sur Benjam

ın
Franklin, Escand
on, Ciudad de Mexico, Mexico (fdzul@me.com; ibarrajosejesus@gmail.com; fabiancorrea@msn.com),
2
Unidad
Colaborativa para Bioensayos Entomol
ogicos, Departamento de Zoolog

ıa, Campus de Ciencias Biol
ogicas y Agropecuarias,
Universidad Aut
onoma de Yucat
an, Carretera Me´rida-Xmatkuil Km. 15.5, Merida, Yucatan, Me´xico (wbm.biol@gmail.com;
pablo_manrique2000@hotmail.com),
3
Servicios Estatales de Salud de Guerrero, Guerrero, Ruffo Figueroa SN, Burocratas, 39090
Chilpancingo de los Bravo, Mexico (entomo_martini@hotmail.com),
4
Unidad Acade´mica de Matem
aticas, Universidad Aut
onoma
de Guerrero, Av. Javier Muˆ`ndez Aponte 1, Fraccionamiento Servidor Agrario, Guerrero, Mexico (joel.torres.leyva@gmail.com),
5
Instituto de Diagn
ostico y Referencia Epidemiol
ogicos (InDRE), Secretaria de Salud, Ciudad de Mexico, Francisco de P.
Miranda 177, Lomas de Plateros, Mexico (cerato_2000@yahoo.com),
6
Department of Environmental Sciences, Emory University,
400 Dowman Dr., Atlanta, GA, 30322 USA (gmvazqu@emory.edu), and
7
Corresponding author, e-mail: gmvazqu@emory.edu
Subject Editor: Jonathan Day
Received 17 August 2016; Editorial decision 24 October 2016
Abstract
The markedly anthropophilic and endophilic behaviors of Aedes aegypti (L.) make it a very efficient vector of
dengue, chikungunya, and Zika viruses. Although a large body of research has investigated the immature habi-
tats and conditions for adult emergence, relatively few studies have focused on the indoor resting behavior and
distribution of vectors within houses. We investigated the resting behavior of Ae. aegypti indoors in 979 houses
of the city of Acapulco, Mexico, by performing exhaustive indoor mosquito collections to describe the rooms
and height at which mosquitoes were found resting. In total, 1,403 adult and 747 female Ae. aegypti were
collected, primarily indoors (98% adults and 99% females). Primary resting locations included bedrooms (44%),
living rooms (25%), and bathrooms (20%), followed by kitchens (9%). Aedes aegypti significantly rested below
1.5 m of height (82% adults, 83% females, and 87% bloodfed females); the odds of finding adult Ae. aegypti
mosquitoes below 1.5 m was 17 times higher than above 1.5 m. Our findings provide relevant information for
the design of insecticide-based interventions selectively targeting the adult resting population, such as indoor
residual spraying.
Key words: mosquito abundance, dengue, indoor residual spraying, vector behavior
Aedes aegypti (L.) is one of the world’s most widely distributed
mosquito species and, as a vector of dengue, yellow fever, chi-
kungunya, and Zika viruses, a major contributor to the global
burden of mosquito-borne illness (Bhatt et al. 2013,Brady et al.
2014). Remarkable behavioral and ecological attributes make
this mosquito an efficient vector. Aedes aegypti is well-adapted
to completing its entire life cycle within urban areas in and
around houses, primarily feeding on humans at a very high fre-
quency (<2 d), a trait that leads to very high human–mosquito
contacts and dengue virus attack rates (Kuno 1995,De
Benedictis et al. 2003,Stoddard et al. 2013,Liebman et al.
2014). Given that Ae. aegypti is primarily found indoors (Perich
et al. 2000,Chadee 2013) and that both males and females
seldom disperse beyond 100 m (Harrington et al. 2005,Russell
et al. 2005), identifying the environmental and behavioral condi-
tions that influence its resting behavior is crucial for devising in-
novative targets for vector control.
Early studies on the resting behavior of Ae. aegypti in Thailand
have shown that the mosquito predominantly rests indoors, primar-
ily on hanging objects (over 90% of all collected specimens; Pant
and Yasuno 1971). In contrast, studies performed in Panama (where
houses are built with concrete and are more enclosed than the
wooden and often elevated houses found in Thailand) have shown
that Ae. aegypti rests both in walls and objects and that 57–64% of
adults rest below 1 m of height and predominantly inside bedrooms
and on surfaces made of cement, wood, and cloth (Perich et al.
V
CThe Authors 2016. Published by Oxford University Press on behalf of Entomological Society of America.
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Journal of Medical Entomology, 2016, 1–4
doi: 10.1093/jme/tjw203
Short Communication
Journal of Medical Entomology Advance Access published December 23, 2016
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2000). Data from Iquitos, Peru, provided further evidence of mos-
quitoes resting at low heights (Vazquez-Prokopec et al. 2009), a pat-
tern also supported by observational studies in experimental huts
performed in Thailand (Tainchum et al. 2013).
During the yellow fever eradication campaign in the Americas,
the perifocal residual spraying of DDT or malathion applied directly
to actual breeding habitats and adjacent resting places was very ef-
fective at controlling Ae. aegypti (Soper 1965). More recently, in
Australia, selective indoor residual spraying (IRS) applications in
known Ae. aegypti resting locations (e.g., under furniture, closets,
lower walls, dark areas) not only reduced intervention costs but also
provided an unparalleled effectiveness against dengue (Ritchie et al.
2002;Vazquez-Prokopec et al. 2010a,b). Before such results could
be translated to existing Ae. aegypti programs in endemic areas
(which may differ from Australia in building construction and avail-
ability of potential resting sites), more research is needed about the
applicability and acceptability of selective IRS. In this study, we
quantified Ae. aegypti indoor resting behavior in the city of
Acapulco (Mexico) and discuss the relevance of our findings for the
adoption of selective IRS, as an alternative to “traditional” IRS for
Anopheles spp. mosquitoes, for the control of Aedes vectors in ur-
ban areas within the Americas.
Material and Methods
Study Area
The study was performed in the city of Acapulco (3243014320
N, 86420118220W), in the State of Guerrero, located in the
Pacific coast of southern Mexico. Acapulco has a population of ap-
proximately 789,971 living in 360,000 households (INEGI, 2014).
From the total households in the city, 10% lacks domestic piped wa-
ter supply, and 60% receives water sporadically within a scheduled
plan. The lack of a reliable water supply promotes the need for wa-
ter storage, leading to the permanent presence of large tanks and
drums. Consequently, Ae. aegypti abundance and productivity are
very high (Che-Mendoza et al. 2015,Manrique-Saide et al. 2015).
Entomologic Surveys
A cross-sectional entomologic study was performed between
February-March and August-September 2013 to collect resting Ae.
aegypti adult mosquitoes within 26 neighborhoods of Acapulco. In
each neighborhood, city blocks were randomly selected, aiming to
obtain a minimum of 10 blocks per neighborhood. Once city blocks
were identified, one house per side of the block was randomly se-
lected for exhaustive entomological surveys. Collections were car-
ried out by four teams composed of three entomologists each from
0800 to 1500 hours using Prokopack aspirators (Vazquez-Prokopec
et al. 2009). Given that our goal was to compare the abundance of
resting Ae. aegypti within houses, we standardized our aspiration
time to not last more than 10 min per house (Getis et al. 2003,
LaCon et al. 2014), with two technicians collecting indoors and a
third one outdoors. Indoors, collections were stratified by height by
having one technician collecting mosquitoes from the bottom (<1.5
m) walls and resting sites and another technician collecting from the
top wall (and any objects or spaces that may serve as resting areas)
and ceiling (>1.5 m) using a telescopic aspirator handle, as previ-
ously described (Vazquez-Prokopec et al. 2009). Prior to the study,
technicians measured the angle of their arm on a wall with a hori-
zontal line marking the 1.5 m threshold. Both technicians collecting
indoors worked simultaneously on each room, with the technician
collecting at <1.5 m starting from the wall located on the right side
of the room’s door and the technician collecting >1.5 m starting
from the wall located on the left (this procedure made collection
time comparable above and below 1.5 m). The same procedure
was followed on each room by using different collection cups per
room (i.e., living-dining room, bedrooms, kitchen, bathroom).
Backyard (patio) collections were also stored on a separate cup,
but not stratified by height. All cups containing at least one mos-
quito were transported to the State Laboratory for further process-
ing, which involved species identification, sex identification, and
determination of level of engorgement (as bloodfed or non-
bloodfed) following the methods described by Vazquez-Prokopec
et al. (2009). We considered the indoor entomological collections
(<1.5 and >1.5 m) within each house as matched pairs and used
conditional logistic regression models to evaluate differences in
collections by height using the function clogit in the R package
Survival (Therneau and Grambsch 2013).
Results and Discussion
From 979 premises accessed and examined, 593 (60.6%) were in-
fested with Ae. aegypti adult mosquitoes and 452 (46.2%) with fe-
male Ae. aegypti. The total number of adult Ae. aegypti collected
was 1,403 (of which 747 were females). More than half of the fe-
males (473, 63.3%) showed evidence of a recent bloodmeal. The av-
erage (SD) number of Ae. aegypti collected per house was 0.72
(1.23), and the average per positive house was 1.87 (1.34,
range ¼1–12 mosquitoes). Most of the collections were obtained in-
doors (98% positive for adult and 99% for female Ae. aegypti)in
comparison with patios. Aedes aegypti adults predominantly rested
in bedrooms (44%), followed by living rooms (25%), bathrooms
(20%), and kitchens (9%). When stratified by height, 82% (1,151/
1,403) of all adults, 83% (626/747) of all females, and 87% (410/
473) of all bloodfed females were found resting below 1.5 m.
Plotting the household abundance also shows that the predominance
of Ae. aegypti below 1.5 m occurred across all indoor abundance
values (Fig. 1). A very low fraction of infested houses (3.9–7.1%)
had Ae. aegypti mosquitoes (adults, females, or bloodfeds) resting
only in the upper wall and ceiling (Table 1). Thus, the sensitivity of
collections (i.e., the percentage of infested houses detected by aspira-
tion) varied dramatically if collections were performed only in the
lower wall (93–96%) or only in the upper wall and ceiling (17–
30%; Table 1). The odds of finding adult Ae. aegypti mosquitoes
resting below 1.5 m was 17 times higher than the odds of finding
mosquitoes resting above 1.5 m (conditional logistic regression
model, odds ratio, OR ¼17.96; 95% CI ¼11.80–27.33; Wald
test ¼181.7; df ¼1; P<0.001). Similar OR values were calculated
for female Ae. aegypti (OR ¼11.0; 95% CI¼7.66–15.80; Wald
test ¼168.7; df¼1; P<0.001) and bloodfed female Ae. aegypti
(OR ¼11.87, 95% CI ¼7.76–18.17; Wald test ¼129.8; df ¼1;
P<0.001).
There is strong consensus in the scientific and public health com-
munities that current vector control tools against Ae. aegypti have
limited entomological efficacy and unknown epidemiological impact
(Bowman et al. 2016). Although several novel methods (Wolbachia,
genetically modified mosquitoes) show a promising outlook (Achee
et al. 2015), more evidence of their epidemiological impact is re-
quired before they are available for widespread implementation
(Reiner et al. 2016). Thus, insecticide-based interventions directed
to the adult resting population represent a relevant approach for Ae.
aegypti control and disease prevention. In Acapulco, where houses
are made of brick and mortar, bedrooms are the key Ae. aegypti
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resting location, and the vast majority of adult mosquitoes rest be-
low 1.5 m. Our observations confirm, with a much larger sample
size, initial findings from Iquitos, Peru, showing that of 56 Ae.
aegypti collected indoors, 82% were found resting below 1.5 m
(Vazquez-Prokopec et al. 2009), and observations from Thailand
(where houses were elevated on wooden poles and had wooden
walls and unscreened windows) showing 57–64% of adults rest be-
low 1 m (Perich et al. 2000).
The “traditional” approach for IRS (used for Anopheles spp. and
other disease vectors) relies on impregnation of the entire wall with in-
secticides (World Health Organization 2006). Such spraying requires
moving all furniture and removing picture frames or other objects
from walls, which increases the time it takes to spray a house (and re-
quires householders to prepare premises before spraying). This is a
major barrier for community acceptance of traditional IRS in urban
areas (Paz-Soldan et al. 2016). The finding of a strong preference by
Ae. aegypti for resting below 1.5 m has important practical implica-
tions for the consideration of “selective” IRS (Ritchie et al. 2002)asa
possible approach for controlling Ae. aegypti in the Americas. Our re-
sults also suggest that not spraying kitchens (a key area where con-
tamination of food items with insecticides is very likely) may not lead
to a dramatic loss of insecticidal coverage to control resting mosqui-
toes. In urban areas such as Acapulco, the selective application of re-
sidual insecticides to which Ae. aegypti is not resistant in resting areas
located below 1.5 m can not only reach the majority of the vector
population but also reduce operational time of spraying a house, the
operators’ exposure to insecticides, and the per-household interven-
tion costs and increase community acceptance. Such increases in effi-
ciency can favor the adoption of this expensive and labor-intensive
vector control method under specific circumstances. Specifically, we
Table 1. House positivity by different Ae. aegypti adult indices, stratified by height of collection indoors (low, <1.5 m; high, >1.5 m and
ceiling)
Adult Index Negative houses Ae. aegypti presence, No. houses (% positive houses) Sensitivity (%)
Low High Both Low High
Adults 386 413 (69.6) 23 (3.9) 157 (26.5) 96.1 30.4
Females 527 352 (77.9) 32 (7.1) 68 (15.0) 92.9 22.1
Bloodfeds 649 273 (82.7) 23 (7.0) 34 (10.3) 93.0 17.3
Sensitivity indicates the percentage of detection of infested houses when collections are done in the lower or only in the higher walls.
Fig. 1. Distribution of paired Ae. aegypti abundances inside houses stratified by collection height. Each symbol indicates an abundance occurrence (e.g., the point
at [x ¼12, y ¼0] shows a house that had 12 Ae. aegypti below 1.5 m and none above 1.5 m). The size of the spheres is proportional to the number of houses with
a given Ae. aegypti abundance above and below 1.5 m (e.g., the largest sphere indicates that 205 houses had the values [1,0], whereas the smallest spheres rep-
resent a single house). The dashed line indicates the point of indifference, where abundance is the same above and below 1.5 m.
Journal of Medical Entomology, 2016, Vol. 0, No. 0 3
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feel that performing selective IRS can be suitable for the emergency
control of Ae. aegypti in homes of pregnant woman (or other high-
risk groups) in areas currently experiencing Zika virus transmission.
Acknowledgments
We thank the Secretaria de Salud from Guerrero State for the operational sup-
port provided to conduct this research and the residents of Acapulco for
kindly allowing us to enter their homes. This research was supported by
Consejo de Ciencia y Tecnolog
ıa and the Government of Guerrero State
(GUE-2008-01-91330, Dzul-Manzanilla, PI) and the National Science
Foundation (NSF/EEID/RAPID: 1640698, Vazquez-Prokopec, PI).
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