Dispersion and oviposition of Aedes albopictus in a Brazilian slum: Initial evidence of Asian tiger mosquito domiciliation in urban environments
Dispersion and oviposition of Aedes albopictus in a Brazilian slum: Initial evidence of Asian tiger mosquito domiciliation in urban environments
Tania AylloÂ n 0 1
Daniel Cardoso Portela CaÃ mara 1
Fernanda Cristina Morone 1
Larissa da Silva GoncË alves 1
FaÂ bio Saito Monteiro de Barros 1
PatrÂõcia Brasil 0 1
Marilia SaÂ Carvalho 1 2
Nildimar Alves HonoÂ rio 1
0 LaboratoÂrio de DoencËas Febris Agudas, Instituto Nacional de Infectologia Evandro Chagas/Fiocruz , Rio de Janeiro , Brasil , 2 NuÂcleo Operacional Sentinela de Mosquitos Vetores-Nosmove/Fiocruz , Rio de Janeiro, Brasil, 3 LaboratoÂrio de Mosquitos Transmissores de HematozoaÂrios , Instituto Oswaldo Cruz , Rio de Janeiro , Brasil , 4 Departamento de Zoologia, Universidade Federal de Pernambuco , Recife-PE , Brasil
1 Editor: Amy C. Morrison, University of California , Davis , UNITED STATES
2 Programa de ComputacËão CientÂõfica PROCC/Fiocruz , Rio de Janeiro , Brasil
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: This work was supported by grants from:
Conselho Nacional de Desenvolvimento CientÂõfico e
TecnoloÂgico-CNPq (grant nr. 157464/2015-6),
Programa EstrateÂgico de Apoio aÂ Pesquisa em
SauÂde-PAPES VI (grant nr. 407744/2012-6),
FundacËão Carlos Chagas Filho de Amparo à
Pesquisa do Estado do Rio de Janeiro-FAPERJ
Aedes albopictus, originally considered as a secondary vector for arbovirus transmission,
especially in areas where this species co-exist with Aedes aegypti, has been described in
most regions of the world. Dispersion and domiciliation of Ae. albopictus in a complex of
densely urbanized slums in Rio de Janeiro, Southeastern Brazil, was evidenced. In this
study, we tested the hypotheses that 1) Ae. albopictus distribution in urban slums is
negatively related to distance from vegetation, and 2) these vectors have taken on a domestic
life style with a portion of the population feeding, ovipositing, and resting indoors. To do
this, we developed an integrated surveillance proposal, aiming to detect the presence
and abundance of Aedes mosquitoes. The study, based on a febrile syndrome
surveillance system in a cohort of infants living in the slum complex, was performed on a weekly
basis between February 2014 and April 2017. A total of 8,418 adult mosquitoes (3,052
Ae. aegypti, 44 Ae. albopictus, 16 Ae. scapularis, 4 Ae. fluviatilis and 5,302 Culex
quinquefasciatus) were collected by direct aspiration and 46,047 Aedes spp. eggs were
collected by oviposition traps. The Asian tiger mosquito, Ae. albopictus, was aspirated in its
adult form (n = 44), and immature forms of this species (n = 12) were identified from the
eggs collected by the ovitraps. In most collection sites, co-occurrence of Ae. aegypti and
Ae. albopictus was observed. Key-sites, such as junkyards, thrift stores, factories, tire
repair shops and garages, had the higher abundance of Ae. albopictus, followed by
schools and households. We collected Ae. albopictus at up to 400 meters to the nearest
vegetation cover. The log transformed (n+1) number of females Ae. albopictus captured
at each collection point was inversely related to the distance to the nearest vegetation
border. These results show that Ae. albopictus, a competent vector for important
arboviruses and more commonly found in areas with higher vegetation coverage, is present and
spread in neglected and densely urbanized areas, being collected at a long distance from
(grant nr. E-26 010.001610/2016) and Fundo
Nacional de SauÂde-FNS (grant nr. TED 90/2016).
The funders had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
Competing interests: The authors have declared
that no competing interest exists.
the typical encounter areas for this species. Besides, as Ae. albopictus can easily move
between sylvatic and urban environment, the entomological monitoring of Ae. albopictus
should be an integral part of mosquito surveillance and control. Finally, key-sites,
characterized by high human influx and presence of potential Aedes breeding sites, should be
included in entomological monitoring.
Different arboviruses, such as dengue, chikungunya, Zika and yellow fever are transmitted to
humans by mosquitoes of the genus Aedes (Meigen 1818), particularly Ae. aegypti (Linnaeus,
1762) and Ae. albopictus (Skuse, 1894), two invasive and frequently sympatric species. Although
Ae. albopictus is considered to have a low capacity to transmit pathogens (as arboviruses) to
humans, it has been demonstrated the potential role of this species in dengue, chikungunya and
Zika virus transmission and outbreaks [
]. The domestic form of Ae. aegypti is highly
anthropophilic, predominating in urban and suburban areas, where households and humans are
abundant. However, Ae. aegypti is often found in transition areas between highly urbanized and
urban forest, which might serve somehow as a refuge [
]. Furthermore, Ae. albopictus is
typically more common in areas with higher vegetation coverage and more scattered human
populations, but it has also been described in transitional environments with relatively low
vegetation cover and frequently coexisting with Ae. aegypti [
]. Knowledge of the species
habitat and environmental determinants is essential for predicting Ae. aegypti and Ae. albopictus
presence and abundance in an area, which might impact arboviruses transmission. In this
study, we tested the hypotheses that 1) Ae. albopictus distribution in urban slums is negatively
related to distance from vegetation, and 2) Ae. albopictus has taken on a domestic life style with
a portion of the population feeding, ovipositing, and resting indoors.
Materials and methods
The study was conducted in Manguinhos (22Ê 52' 44,2 S 43Ê 14' 42,0 W), a low income urban
slum complex comprised by 16 different densely urbanized communities. Within an area of 261
square kilometers, a population of 36,160 inhabitants (138 inhabitants per km2) live in 10,816
], characterized by a crowded housing, narrow alleys, inadequate sanitation,
irregular domestic water supplies and haphazard waste management. Violence and constant police
incursions make Manguinhos a difficult neighborhood for research activities and entomological
monitoring. Low vegetation is common in Manguinhos, although there are some green delimited
areas in the community, such as the Fiocruz campus (Fig 1), a river, and other waterways.
A mosquito surveillance integrating a large-scale dengue infant cohort study  was con
ducted from February 2014 to April 2017 in the study area. Ethical clearance was obtained from
the Ethical Committee in Research (CAAE: 13202113.1.0000.5240) from the National School of
Public Health, Oswaldo Cruz Foundation, Ministry of Health, Brazil. Each participant signed
informed consent. Adult mosquito collections were performed weekly integrated to the cohort
study. We used portable backpack aspirators in several collection sites: households, schools and
key-sites (such as junkyards, thrift stores, factories, tire repair shops and garages), the last two
defined as non-residential properties suitable for the maintenance of vector infestation.
Households were visited after the report of fever in any children followed-up in the cohort study.
Schools and key-sites, selected in strategic areas in the vicinity of the fever cases, were character
ized by high human influx and presence of potential Aedes breeding sites. Adult mosquito
sampling was performed for 15±20 minutes in each collection site. All sampling was performed by
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Fig 1. Spatial distribution of collections of Aedes albopictus adults in Manguinhos, Rio de Janeiro. Yellow triangles, circles, and stars represent the households,
keysites and schools, respectively, where Ae. albopictus adults were collected.
the same technicians throughout the whole study period. Aspirations were positive when at
least one mosquito was collected. Adult mosquitoes were counted, sexed and identified to
species level using the taxonomic key of Consoli and LourencËo-de-Oliveira [
] and stored in
freezer (-80ÊC). Oviposition was monitored placing 45 ovitraps weekly in the schools from
October 2015 to May 2016, totaling 806 observations. Wooden paddles were collected weekly
and inspected for the presence of eggs, which were counted and hatched to identify larvae
species. Collection points were geo-referenced, and distance to the nearest vegetation cover was
measured using QGIS 2.18. Shape files are publicly available and free to use at Rio de Janeiro's
Municipal Data Repository (http://www.armazemdedados.rio.rj.gov.br/). We modeled the log
transformed (n+1) abundance of collected Aedes female mosquitoes and the distance from each
collection point to the nearest vegetation patch in the study area using a simple linear model.
Analyses were carried out in R and RStudio [12,13].
The mean daily temperature during the study period was 25.8ÊC (SD = 3.31ÊC, min = 14.3ÊC,
max = 40.7ÊC). Rainfall was observed in 380 days (32.25% of the study period). The mean daily
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precipitation was 5.89mm (SD = 34.76mm, max = 514.60mm). Relative air humidity was
67.66% (SD = 8.99%, min = 41.85%, max = 91.58%). During the three-year period, a total of 244
households, 22 key-sites and nine schools were visited. During the study period, house index
] was routinely evaluated by health department personnel and ranged from 0.19 to 2.16 in
Manguinhos . In the 1,214 visits performed, we identified 5,302 Cx. quinquefasciatus and
3,116 adult Aedes spp. among which 3,052 were Ae. aegypti (68% engorged), 44 were Ae. albopic
tus (58% engorged), 16 (0% engorged) were Ae. scapularis and 4 (0% engorged) were Ae.
fluviatilis (Table 1). In the thirteen locations where Ae. albopictus was observed it co-occurred with
Ae. aegypti in eleven locations (84.6%, Table 2). Thirty-eight Ae. albopictus adults (86.4%) were
collected from seven of 22 key-sites, four (9.1%) from two of nine schools and two (4.5%) from
two of 243 households surveyed (Table 2). Additionally, from 46,047 eggs collected from the
nine schools (eclosion rate: 0.42%), 12 Ae. albopictus and 183 Ae. aegypti larvae were identified.
The mean eggs/week per school varied between 13.2 and 233.8.
Both species were collected during all seasons. Aedes aegypti was more abundant during the
wet season, peaking in December with abundance declining abruptly in May. Aedes albopictus
peaked in June declining afterwards. For both species, more specimens were collected in the
key-sites and schools. Throughout the study period Ae. aegypti was present in all three
different collection sites, while Ae. albopictus maintained a positive mean only in key-sites. In
schools and households, Ae. albopictus was less often found (Fig 2). Both Ae. aegypti and Ae.
albopictus were strongly correlated (R = 0.87, p < 0.05).
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The number of Ae. albopictus adult females retrieved in the urbanized area fitted an exponen
tial regression curve with the distance to the nearest vegetation border (R = 0.65; p < 0.0001).
The log transformed (n+1) number of females Ae. albopictus captured at each collection point
was inversely related to the distance to the nearest vegetation border (Fig 3). The regression
curve parameters estimated were: y = 260.5629 exp (-0.2545 x), where y represents the distance
to the nearest vegetation border and x the number of female Ae. albopictus retrieved. Regression
curve parameters estimated for the linear regression curve: y = a+bx, were a = 253.3969 and
b = -43.4897. The number of Ae. aegypti adult females retrieved near the vegetated areas also
fitted an exponential regression curve, with the number of females decreasing exponentially with
the distance to the nearest vegetation border (p < 0.0001). The number of females of Ae. aegypti
captured at each collection point weighted according to the number of collections performed at
each site, was inversely related to the distance to the nearest vegetation border (Fig 3). The
regression curve parameters estimated were: y = 307.6928 exp (-0.2368 x), where y represents
the distance to the nearest vegetation border and x the number of female Ae. aegypti retrieved
In our study, the entomological survey followed reports of febrile children, in a routine
entomological surveillance. Both Ae. aegypti and Ae. albopictus were collected indoors in an urban
endemic area for dengue, Zika and chikungunya, with the number of females of similar
magnitude (Table 2). Although Ae. albopictus is typically not commonly found in densely urbanized
], we identified 44 adults and 12 immature forms of this species during the three-year
survey in Manguinhos. Aedes albopictus has adapted well to suburban and urban
environments, and has been described as the sole vector in urban areas in China and Italy [
Moreover, there is evidence of a geographical variation in the behavior of this species, with
gravid females captured indoors in Italy [
]. The collection of Ae. albopictus adults in densely
urbanized slums as Manguinhos complex seems to emphasize the dispersion (a statistical term
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Fig 2. Monthly mean abundance of Ae. aegypti and Ae. albopictus during the three-year study period in Manguinhos, Rio de Janeiro. The figure shows the mean
number of Ae. aegypti and Ae. albopictus mosquitoes collected per month during the study.
that describes the distribution of organisms over a landscape) [
] of this species, and could be
indicative of an increased establishment of this species in anthropogenic-influenced
environments, as occurred for Ae. aegypti [
]. In addition, our results support the evidence of an
initial domiciliation by Ae. albopictus, defined as the process by which a species occupy niches
in the anthropic environment (feeding, resting, and perhaps mating indoors) .
Most of the Ae. albopictus adults were collected from key-sites, typically described as highly
favorable to Ae. aegypti infestation as shown by the positive and strong correlation between
both species [
]. The surveillance and monitoring of such areas are essential to inform vector
control strategies [
]. The fragile infrastructure of key-sites favors Ae. aegypti
], but has not yet been linked to Ae. albopictus production. In fact, Manguinhos complex
promotes high vector infestation levels through poor sanitation, interrupted water supply and
high human population density. In locations where Ae. albopictus was collected (5.1% of sites
surveyed), Ae. aegypti was also present in 84.6% (11 of 13) of the locations, showing a clear
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Fig 3. Model of the log-transformed (n+1) abundance of Ae. aegypti and Ae. albopictus females collected in the
study area as related to the distance to the nearest vegetation patch, in meters. The figure shows the abundance of
these species according to the distance, in meters, to the nearest vegetation border.
pattern of co-occurrence, i.e. Ae. aegypti was present in most of the sites where Ae. albopictus
was collected. In a previous entomological survey in the same area, both species co-occurred at
the transition zone between the forest and the densely populated region [
In another entomological survey, low numbers of immature Ae. albopictus were found in
Favela do Amorim, one of the 16 slums that composes Manguinhos complex and which also
surrounds the forested area in the Fiocruz campus [
]. In our study, the presence of Ae.
albopictus adult females and males, together with eggs and larvae, led us to conclude that this
species may be establishing itself in the slums of Manguinhos.
The finding of Ae. albopictus inside the households, where febrile cases were reported,
clearly indicates that this species has a tendency toward domesticity that may not be as strong
as that of Ae. aegypti, but that nevertheless could be of epidemiological importance. Indoor
residence of this species highlights the need of maintaining entomological and epidemiological
surveillance in vulnerable areas. This is of utmost importance, since we demonstrated the
presence of Zika virus in engorged Ae. aegypti mosquitoes in a key-site where Ae. albopictus was
found, in the same densely urbanized slum, before the first case of autochthonous Zika virus
disease was diagnosed in Rio de Janeiro city [
Since both Ae. aegypti and Ae albopictus share the same larval habitats, it has been suggested
that their coexistence may be a transient phenomenon, that should be followed by the
reduction or displacement of one of the two species through interspecific competition during larval
] or through asymmetric reproductive interference via interspecific mating.
This last circumstance is also known as satyrization, that is a form of reproductive interference
where males of Ae. albopictus mate with females of Ae. aegypti resulting in no offspring and
permanent sterilization of the cross-mated females [
]. However, our monitoring of the
current study areas during the last 15 years suggests that the two species may have reached a
relative steady state of coexistence in urban areas of Manguinhos, Rio de Janeiro. In addition,
we recently showed the lack of major competitive displacement of Brazilian Ae. albopictus
males (including Manguinhos strain) to satirize Ae. aegypti females, suggesting that the low
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satyrization potential of Brazilian Ae. albopictus males may account for the lack of
displacements of Ae. aegypti . A previous study showed that this coexistence shows large seasonal
fluctuations in both pupal productivity and interspecific competition in the study area,
favoring Ae. albopictus over Ae. aegypti. Even though the study shows a clear advantage for Ae.
albopictus, seasonal fluctuation of the interspecific competition effects over Ae. aegypti are not
sufficient to displace this species in the study area [
]. It has been shown that A. albopictus is
superior to Ae. aegypti in resource competition, maintaining greater population growth at
higher combined densities [
], as well as producing greater survivorship during periods
of low food availability [
In the present paper, we have found a similar pattern for spatial distribution of Ae. albopictus
females within the urban area, with mosquitoes collected at almost 400 meters to the nearest
vegetation area. Previous studies showed that gravid Ae. albopictus are capable of dispersing at
least 800 m in urban areas [
], and that their larvae showed competitive advantages over Ae.
]. Our results suggest that Ae. albopictus, a competent vector for important
arboviruses, including dengue (DENV), chikungunya (CHIKV), Zika (ZIKV) and yellow fever (YFV)
], may spread into neglected and densely urbanized areas, if close to vegetated areas.
In addition, as this species tends to shelter outside houses , are capable of dispersing great distances inside forests near human dwellings and can easily move between sylvatic and urban environments , there is an urgent need to establish entomological surveillance protocols targeting this species.
The results obtained in this study show the global importance of maintaining entomological
monitoring of Ae. albopictus as a part of surveillance and control programs. This is especially
true in Brazil and elsewhere in the Americas where Ae. albopictus might participate in the
spillback of arboviruses to enzootic cycles much in the same way as happened to YFV in the last
few centuries [
]. In fact, preliminary evidence shows that ZIKV might be already
circulating among neotropical nonhuman primates in Brazil [
]. Besides, this arbovirus has
already been detected in wild-caught Ae. albopictus from Bahia, Brazil [
entomological surveillance studies integrate with host-seeking behavior of Ae. albopictus should be
investigated inside densely urbanized slums in order to determine whether the presence of Ae.
albopictus in slums near vegetated border has an epidemiological importance in the
transmission dynamics of these arboviruses.
Densely urbanized slums favor the permanent circulation of mosquitoes, humans and viruses.
Continuous longitudinal monitoring is essential in these vulnerable areas in spite of all
challenges such as limited access, violence and floodings. Moreover, key-sites, with high human
concentration, mobility, and presence of potential Aedes breeding sites, should be included in
entomological monitoring. Concomitantly, due to the increasing evidence confirming Ae.
albopictus as an efficient viral vector, it would be necessary to extend the entomological
monitoring for Ae. albopictus mosquito species. This species has been shown to be a primary vector
for arboviruses in different countries and has progressively established in urban areas.
However, it has not been a target of surveillance programs in Brazil yet. Finally, this study points
out the great importance of integrated studies, since they reinforce the virological,
entomological and epidemiological approaches.
S1 Table. Excel file containing the original data used for Tables 1 and 2. The table contains
the number of Aedes aegypti and Ae. albopictus mosquitoes collected during the study period
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and the distances, in meters, to the nearest green border.
We thank Gerusa Gibson and Izabel Reis for their assistance in the project. We are very grate
ful to Phil Lounibos and Steven Juliano for their valuable comments on the manuscript. We
would also like to thank the anonymous referees and associate editors who gave many valuable
suggestions, which greatly helped improving the present manuscript.
This work was supported by grants from: Conselho Nacional de Desenvolvimento CientÂõ
fico e TecnoloÂgico-CNPq (grant nr. 157464/2015-6), Programa EstrateÂgico de Apoio aÂ
Pesquisa em SauÂde-PAPES VI (grant nr. 407744/2012-6), FundacËão Carlos Chagas Filho de
Amparo à Pesquisa do Estado do Rio de Janeiro-FAPERJ (grant nr. E-26 010.001610/2016)
and Fundo Nacional de SauÂde-FNS (grant nr. TED 90/2016).
Saito Monteiro de Barros.
Conceptualization: PatrÂõcia Brasil, Marilia SaÂ Carvalho, Nildimar Alves HonoÂrio.
Data curation: Tania AylloÂn, Marilia SaÂ Carvalho, Nildimar Alves HonoÂrio.
Formal analysis: Tania AylloÂn, Daniel Cardoso Portela CaÃmara, FaÂbio Saito Monteiro de
Funding acquisition: PatrÂõcia Brasil, Nildimar Alves HonoÂrio.
Investigation: Tania AylloÂn, Fernanda Cristina Morone, Larissa da Silva GoncËalves, FaÂbio
Methodology: Tania AylloÂn, Daniel Cardoso Portela CaÃmara, Fernanda Cristina Morone,
Larissa da Silva GoncËalves, FaÂbio Saito Monteiro de Barros, Nildimar Alves HonoÂrio.
Project administration: PatrÂõcia Brasil, Nildimar Alves HonoÂrio.
Resources: PatrÂõcia Brasil, Nildimar Alves HonoÂrio.
Supervision: Nildimar Alves HonoÂrio.
Visualization: Daniel Cardoso Portela CaÃmara.
Writing ± original draft: Tania AylloÂn, Nildimar Alves HonoÂrio.
Writing ± review & editing: Tania AylloÂn, Daniel Cardoso Portela CaÃmara, Fernanda Cristina
Morone, Larissa da Silva GoncËalves, FaÂbio Saito Monteiro de Barros, PatrÂõcia Brasil, Marilia
SaÂ Carvalho, Nildimar Alves HonoÂrio.
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