• View in gallery

    Ovarian development stages of dust-marked Ae. aegypti females released in the suburban area (Tubiacanga) and recaptured with backpack aspirators. (A) MRR conducted in the wet season, where 210 females were dissected. (B) MRR performed in the dry season, where 118 females were collected.

  • View in gallery

    Ovarian development stages of dust-marked Ae. aegypti females released in the urban area (Favela do Amorim) and recaptured with backpack aspirators. (A) MRR conducted in the dry season, where 107 females were dissected. (B) MRR performed in the wet season, where 201 females were collected.

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DAILY SURVIVAL RATES AND DISPERSAL OF AEDES AEGYPTI FEMALES IN RIO DE JANEIRO, BRAZIL

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  • 1 Laboratório de Transmissores de Hematozoários, Departamento de Entomologia, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil; Programa de Computação Científica, Fiocruz, Rio de Janiero, Brazil

Daily survival rates, life expectancy, dispersal, and parity are important components of vectorial capacity of Aedes aegypti. These parameters were estimated for mosquito populations from a slum and a suburban district in Rio de Janeiro, during the wet and dry seasons in 2005. In each mark-release-recapture experiment, three cohorts of dust-marked Ae. aegypti females were released. Recaptures were carried out daily in randomly selected houses, using backpack aspirators, adult traps, and sticky ovitraps. Recapture varied between 6.81% and 14.26%. Daily survival was estimated by fitting two alternative models: exponential and nonlinear models with correction for the removal of individuals. Slum area presented higher survival and parity rates (68.5%). Dispersal rates were higher in the suburban area, where a maximum dispersal of 363 m was observed. Results suggest intense risk of dengue epidemic, particularly in the urban area.

INTRODUCTION

A precise estimation of life history parameters of Aedes aegypti is essential for the development of dengue transmission models.1 Among these parameters, the daily survival probability of adult females is one of the most important, because small increases in survival may exponentially increase the vectorial capacity of mosquitoes.2 As a rule, vectors must survive longer than the sum of the initial non-feeding period plus the extrinsic incubation period to be able to infect another human. For dengue transmission, that means a lifespan of least 12 days (2 days of nonfeeding and 10 days of incubation).3,4

Besides survival, another important component of vectorial potential is dispersal. A very mobile infected vector has greater chance of finding susceptible humans than one with low dispersal. Ae. aegypti is not a very mobile species, generally flying 50–300 m during its lifetime5. Reports of longer distance flights exist and suggest that Ae. aegypti is capable of covering considerable distances in few days if necessary.6,7 Variation in mosquito displacement may be explained by heterogeneity in the availability of breeding sites and blood opportunities.810

In Rio de Janeiro city, dengue fever has become endemic since its reintroduction in the 1980s. Ae. aegypti is specially abundant in urbanized and densely populated neighborhoods.1113 To provide parameters for the development of models of dengue transmission in Rio de Janeiro, we used a mark-release-recapture (MRR) study design to evaluate the variation in the probability of daily survival, average life expectancy, and dispersal of Ae. aegypti females in two areas of contrasting urbanization patterns in Rio de Janeiro during the dry and wet seasons. We also evaluated the ovarian development and parity rates of natural populations of Ae. aegypti living in the above conditions. The ultimate goal of this study is to increase the understanding on dengue transmission in Rio de Janeiro.

MATERIALS AND METHODS

Study area.

MRR studies were conducted in two neighborhoods at Rio de Janeiro city—Favela do Amorim and Tubiacanga—characterized by contrasting urbanization patterns and potential isolation from the surroundings, which is expected to minimize mosquito losses by emigration during MRR experiments.

Favela do Amorim (22°52′30″ S; 43°14′53″ W) was chosen to represent a densely populated (901.2 hab/ha) low-income urban area, characterized by disordered human occupation and scarce vegetation coverage (a typical Brazilian slum). There, 2,992 people live in 897 substandard houses, in an estimated area of 2.32 ha. Houses are very small—rarely with more than one room—and without yards or any kind of peri-domestic area. The neighborhood is surrounded by large highways and the Oswaldo Cruz Foundation campus, which is a largely vegetated, non-residential area, which probably does not encourage Ae. aegypti females to emigrate from the slum.

Tubiacanga (22°47′08″ S; 43°13′36″ W) was chosen to represent a planned, suburban area. There, 2,902 residents live in 867 houses, which resulted in a human density of 337.4 hab/ha (an estimated area of 8.6 ha). This neighborhood is located in a lowland coastal area, partially surrounded by the Guanabara Bay shores and a 3-m wall of the Tom Jobim International Airport of Rio de Janeiro and its numerous landing strips. There is a single way to get into Tubiacanga by car: a 2.1-km paved road, which connects the area to the nearest neighborhood. Thus, mosquito emigration is not expected to happen in large scale. The area has extensive unpaved streets and moderate vegetation coverage. Most houses have a large peridomestic environment and at least two bedrooms.

Climate and MRR periodicity.

Climate in Rio de Janeiro is characterized by a dry winter (May–August) and a wet summer season (November–March).14 During the 1930–1990 period, dry and wet seasons in Rio de Janeiro had mean temperatures of 25.1°C and 28.8°C and mean total rainfall of 46.4 and 132 mm, respectively. MRR experiments were performed during both seasons in each area: Tubiacanga in February 2005 (wet) and July 2005 (dry) and Favela do Amorim in June 2005 (dry) and December 2005 (wet season). Air temperature and precipitation data for these months were obtained from a meteorological station located 5 km away from the two study areas.

Mosquitoes.

Aedes aegypti used in MRR experiments came from a laboratory colony that is constantly renewed with eggs collected in Rio de Janeiro. Larvae were fed with fish food (Tetramin, Tetra Sales, Blacksburg, VA) and reared according to Consoli and Lourenço-de-Oliveira.15 After emergence, females were kept together at 25 ± 3°C and 65 ± 5% relative humidity (RH) and fed with sucrose solution until the time to release.

Marking and releasing.

Before each experiment, eggs were split into three groups and allowed to hatch on 3 consecutive days, producing three female adult cohorts. Each cohort was marked with a different color of fluorescent dust (Day-Glo Color Corp., Cleveland, OH) in small cylindrical cups (12 × 10 cm). Mated and unfed females were released outdoor at each area in the morning of their fourth day after emergence (between 8:00 AM and 9:00 AM), ~1 hour after dust marking. One mosquito cohort was released each day for 3 consecutive days in each area, both in dry and in wet seasons, totalizing 12 field experiments. Each cohort was released at different points of the study areas. Around 4–5 months elapsed between releases of the cohorts in each area.

Capturing.

Dust-marked females were captured with CDC backpack aspirators (John W. Hock, Gainesville, FL), BG-Sentinels adult trap (BioSantos GmbH, Rejemsburg, Germany), and sticky ovitraps.1619 Captures started 1 day after the release of the first cohort. Fifteen houses were randomly selected per day for aspiration, which was done in 15–20 minutes per house. The whole house was aspirated, including the peridomestic area. BG-Sentinel traps (BGS-Trap) were installed in 15 houses, and remained there during the whole extension of the MRR study, being daily monitored for the presence of dust-marked females. Occasionally, aspiration was done in the same house where a BGS-Trap was installed. Results concerning species specificity, capture efficiency, and a more suitable description of BGS-Trap can be found elsewhere.17,18 Finally, 20 sticky ovitraps were placed at the perimeter of the study areas, as an attempt to capture emigrating insects from study areas. Sticky ovitraps were placed on the ground, in the peridomestic environment, 30–40 m apart from each other in Tubiacanga and 50–60 m apart in Favela do Amorim. Because we assumed mosquito females would not fly toward the sea, we installed sticky ovitraps in only one half of the perimeter in Tubiacanga, which resulted in a more dense coverage in Tubiacanga than in Favela do Amorim. A prior report attested that oviposition traps (OTs) placed in the peridomestic area were more efficient at capturing Ae. aegypti mosquitoes in comparison with the OTs placed indoors.20 Adhesive papers were applied to the internal section of ovitraps baited with hay infusion, as used in previous reports.10 Sticky ovitraps were checked only once at the end of experimental period. Daily capture stopped when no dust-marked females were collected by any method for 3 consecutive days. Captured mosquitoes were examined under UV light to check for the presence of fluorescent dust.

Survival analysis.

Daily probability of survival (PDS) was estimated by fitting two models: the exponential model21 and the nonlinear model by Buonaccorsi.22 The exponential model has been traditionally used for Ae. aegypti23 but has two fundamental drawbacks. It assumes a priori that mosquito mortality does not vary with increasing age and does not consider removal of individuals by the capturing procedure. Recently, a non-linear survival model was proposed, which allows for the correction of estimates caused by the removal of individuals22:

C(t)=NStc(1c)t1

where C(t) in the number of marked individuals captured on day t; c is the daily capture probability; and S is daily survival probability. Buonaccorsi22 compared the two models using Ae. aegypti data from MRR experiments conducted in Thailand24 and found that the new model had a better fit to the data. We fit both models to our data, using linear and nonlinear least squares standard procedures available in the software R 2.0.25

From the lower and upper 95% limits of the confidence interval for PDS (estimated by the nonlinear model), we derived two quantities: the average life expectancy (ALE), defined as 1/–loge PDS26, and longevity, defined as PDS10, (where 10 is the duration of the extrinsic incubation period for dengue), which gives the expected proportion of mosquitoes surviving long enough to transmit dengue virus.

Dispersal analysis.

The locations of all release and positive capture points were geo-referenced using a Global Position System (GPS; Garmin eTrex personal navigator, Gavmin International, Olathe, KS) to calculate distance between release and capture points. The flight behavior of Ae. aegypti females in the two study areas was summarized by a set of dispersal measures: mean distance traveled (MDT), maximum distance traveled (MAX), and flight ranges (FR).27,28 Frequency distributions of the numbers of marked mosquitoes recaptured that had traveled < 100 and > 200 m from the release point were constructed to further characterize the flight range of Ae. aegypti females.

Ovarian development stage and parity rate.

To evaluate the evolution of ovarian development in marked females, all dust-marked females captured with backpack battery-powered aspirator had their ovaries removed in saline solution, and skeins of the ovarian tracheal system were evaluated under a microscope. Ovarian of dissected females were classified according to Christophers,29 with stages 1, 1–2, and 2 grouped as initial stages of development; stages 3 and 4 grouped as intermediary stages; and stage 5 classified as final stage (gravid females).

All non-marked females captured (i.e., wild individuals) were dissected for determination of parity based on the condition of the tracheal system, as described by Detinova.30 Parity of natural population of Ae. aegypti for each season and area was calculated as the number of parous divided by the total number of females captured.

Comparisons between sites and seasons.

Differences in survival rates between study areas and seasons were evaluated by comparing the point estimates of survival rates by two-sample t test.31 To evaluate the effect of study area (categorical variable: Tubiacanga/Amorim), season (categorical variable: dry/wet season), and days since release (continuous variable) on mosquito dispersal, we used generalized estimating equations (GEEs), which are linear regression models with a correction of variance caused by the blocking design (cohorts). The GEE model was fitted, assuming an exchangeable correlation structure.32 In all analyzes, dispersal distances were log-transformed, because this variable presented non-normal distribution. All model fitting was performed using the R 2.0 program (package geepack, for GEE fitting).25

Parity rates observed in field populations were compared with χ2 tests. The aim was to evaluate whether parity rates observed during MRR experiments were different regarding the study areas and seasons.

Ethical considerations.

MRR experimental protocols were submitted to and approved by Fiocruz Ethical Committee (CEP/Fiocruz protocol no. 11591-2005).

RESULTS

Climate.

In Tubiacanga, during the wet season, temperature varied from 23.3°C to 29.6°C, and month rainfall was 161.9 mm; during the dry season experiment, temperature varied from 18.3°C to 26.5°C, with 44.1 mm of rainfall. In Favela do Amorim, temperatures ranged from 19.8°C to 27.5°C during the dry season and from 23.8°C to 30.1°C during the wet season, and precipitation was 58.3 and 125.9 mm, respectively.

Release and recapture.

During the whole study, 8,792 marked Ae. aegypti females were released. Capturing lasted 8–13 days, and the proportion captured in each experiment varied from 6.81% to 14.26% (Table 1).

Daily survival rates and longevity.

Overall, the Buonaccorsi model provided higher estimates of daily survival (PDS) than the exponential model. This is expected because it corrects for the removal of individuals. Within each site/season, cohorts showed good agreement (Table 2). Mosquitoes released in Tubiacanga showed lower survival than those released in Favela do Amorim. This happened both in the dry and wet seasons (dry season: t = 17.58, P < 0.001; wet season: t = 9.52, P < 0.001). Survival differences between sites were found to be as great as 10% during the wet season and 13% during the dry season. Within each area, survival was higher during the dry season (Tubiacanga: t = 2.28, P < 0.05; Favela do Amorim: t = 17.4, P < 0.001).

Variation in PDS led to large variation in the ALE, which varied from 3 to 12 days in Tubiacanga and 4 to 16 in Amorim (Table 2).

Dispersal.

In Tubiacanga, 60% of females were captured within a radius of 100 m from the releasing point in the wet season (93% in the dry season). The average distance traveled was 81–86 m, depending on the season, and the maximum distance traveled was 363 m. In Favela do Amorim, on the other hand, 96% (dry season) and 100% (wet season) of captured mosquitoes was found within 100 m from their release point, having traveled an average distance of 40 m in the wet summer and 53 m in the dry winter; no female was found beyond 200 m (Table 3). No significant differences were observed between distances traveled in the dry and wet seasons in both areas (t = 0.16, P = 0.87).

In Tubiacanga during the wet season, two marked (0.65% from the total of collections) and five unmarked females were captured, whereas in the dry season no marked and three unmarked females were collected in sticky ovitraps. In Favela do Amorim during the dry season, 5 marked (2.08%) and 1 unmarked females were collected, whereas in the wet season, 12 (4.41%) marked and 6 unmarked females were captured in stick ovitraps. Low numbers of captures in the surroundings of both areas suggests low emigration of mosquitoes. However, this information should be reviewed carefully, because spacing between sticky ovitraps could be considered too high, particularly in the Favela do Amorim area.

When a multivariate linear model was fit to the data (Table 4), “time since release” and “study area” had significant effects on dispersal. In Tubiacanga, marked mosquitoes were found significantly far away from the release point than in Amorim. No significant effect of season was found. Within-cohort correlation was estimated as 0.1, which is marginally non-significant (P = 0.065). Assuming that cohort effect is negligible, we may use R2 to measure goodness-of-fit. We found R2 = 0.34.

Ovarian development stages.

In Tubiacanga, during the wet season, almost 60% of recovered mosquitoes in the first day after release were in stage N. This proportion tended to decrease in the following days (Figure 1A). Stages 3–4 and gravid females started to appear at days 3 and 4 after release, respectively. A similar pattern of ovarian development was observed during the dry season (Figure 1B).

In Favela do Amorim, during the dry season, 40% were at stage N at the first day, and we observed a steep decrease in this frequency in subsequent collections (no females at stage N were found after day 4). Females at stages 3–4 first appeared in the second day after release, whereas gravid females were collected on day 3 (Figure 2A). Similar patterns of ovarian development were observed in the wet season (Figure 2B).

Parity.

In Tubiacanga, parity rates of 53.8% (N = 405) and 48.7% (N = 316) were observed in the captured wild population during the wet and dry seasons, respectively. In Favela do Amorim, during the dry season, the parity rate was 62.6% (N = 297) among unmarked captured females and 68.5% (N = 476) during the wet season. In both areas, parity rate did not vary significantly between seasons (Tubiacanga: χ2 = 2.13, P > 0.05; Amorim:χ2 = 2.51, P > 0.05). Parity rate observed in Favela do Amorim was significantly higher than in Tubiacanga in both seasons (wet season: χ2 = 16.83, P < 0.05; dry season: χ2 = 6.02, P < 0.05).

DISCUSSION

This report provides substantial information about Ae. aegypti ecology and vectorial potential under the natural conditions of Rio de Janeiro city. It was the first time that survival rate of dengue vector was evaluated locally, in a city with intense history of dengue transmission during the last 20 years. Besides survival, longevity, dispersal, ovarian development, and parity of the natural population were studied in two areas in different seasons. Our findings suggest that both localities have appropriate conditions for elevated dengue transmission. In Favela do Amorim, a poor community with extremely high human density and disordered occupation, ecological conditions showed to be more adequate for mosquito survival, and consequently, dengue transmission. High daily survival rates increase the chance of a mosquito to blood feed in a viremic person, become infective, and transmit the virus. Indeed, almost one half of living females could live for periods longer than the extrinsic incubation period of dengue virus in the urban area of Favela do Amorim during the dry season and 33.3% during the wet season. Life expectancy estimated for Favela do Amorim is long enough to allow four or even five gonotrophic cycles. Thus, because Ae. aegypti females usually takes multiple blood feedings during a single gonotrophic cycle and rarely feed on sugar,33,34 pathogen transmission could be enhanced there. Even with a lower life expectancy, Tubiacanga also has suitable conditions for dengue transmission, because ~10% of females could live longer than the extrinsic incubation period (i.e., 10 days). However, because of its higher survival rates, dengue transmission seems to be more feasible in Favela do Amorim. Therefore, everything else been equal, it would be reasonable to expect a higher number of dengue cases in Favela do Amorim than in Tubiacanga.

During 2005, 983 dengue cases were reported in Rio de Janeiro, 7 in Favela do Amorim, and 3 in Tubiacanga. Up to the 18th entomological week of 2006, 9,408 dengue cases were confirmed in Rio de Janeiro city, with 66 cases in Favela do Amorim and 21 in Tubiacanga.35,36 Thus, differences in mosquito survival are concordant with dengue incidence in both areas, although the incidence of a disease in an area is dependent of several factors (e.g., vector and host densities and number of susceptible individuals).

Estimates of daily survival probabilities agree with previous studies, which show values ranging between 0.70 and 0.90.24,37,38 We found a tendency toward longer survival during the dry winter. Possibly, weather conditions during the wet and hot season were less favorable to adult mosquitoes; the mean temperature during tropical summer can be ~30°C and reach a maximum temperature of > 40°C at midday. On the other hand, the dry season generally presents more suitable climatic conditions, with mean temperatures rarely exceeding 28°C in a single day. Therefore, the unfavorable weather conditions during the wet season possibly constrained Ae. aegypti survival rate. The assumption that adult daily survival is constant over the year, despite seasonal trends in rainfall and temperature, was used in simulation models describing vector population dynamics and the epidemiology of dengue viruses in urban environments.3941 The seasonal variation in survival rates observed in this report can add accuracy to current models.3941

Regarding dispersal, we found differences between areas but not seasons. This result agrees with previous studies.5 Females released in Tubiacanga dispersed more than those released in Favela do Amorim. Tubiacanga and Amorim share approximately the same density of water-holding containers (R. Maciel-de-Freitas, unpublished data), but human density in Favela do Amorim is almost three times greater. It is possible that the diversity of obstacles posed by the irregular and dense constructions in Favela do Amorim, associated with high availability of blood sources, constrained mosquito dispersal in this area, where very few or none mosquito flew beyond 100 m from the release site. Because mosquito capturing was performed in houses randomly selected rather than in concentric circles from the release point, dispersal rate estimations may be biased. However, dispersal distances found in this study agrees with similar studies performed by in other countries.5,42

Dispersal has important consequences for dengue control. Usually, the first action after the identification of a new dengue case is the implementation of source reduction activities and larvicides applications within a ring area centered at the identified case. Our results suggest that a ring with radius = 200 m would be appropriate in both Tubiacanga and Favela do Amorim areas. Indeed, a smaller ring could be established in the slum area, because mosquitoes displaced less there.

Data on ovarian development of marked females in Tubiacanga and Favela do Amorim showed important differences. Mainly, the continuous appearance of females at stage N in Tubiacanga and the appearance of gravid females 3 days after release in Favela do Amorim (in Tubiacanga gravid females were collected just 4 days after release) reinforce the idea that females can complete a gonotrophic cycle earlier in more densely human populated areas, where the probability of a blood-seeking female encounter a host is higher.

Parity rate in Favela do Amorim was higher than in Tubiacanga in both dry and wet seasons. However, with the study design reported in this paper, the authors are not confident to state if higher parity was a consequence of higher human density or higher mosquito survivorship, which was also higher in Favela do Amorim.

Recapture rates varied between the MRR experiments. Lower recapture was observed during dry season (mean of 7.88% and 11.23% for Tubiacanga and Favela do Amorim, respectively), when the highest survival rates were observed. Low rates can lead to a bias in results concerning mortality rate and dispersal, although observed recapture rates were similar or even higher than several prior reports.9,37

In summary, this study assesses several aspects of mosquito ecology in two distinct neighbors in Rio de Janeiro, a city where vector density and dengue transmission have shown to be highly heterogeneous1 and mosquito control faces several drawback to be surpassed, such as insecticide resistance and reduced effectiveness in mosquito control because of the inaccessibility to some areas such as slums because of criminality.4345 Other field evaluations concerning daily survival rates, longevity, dispersal, ovarian development, and parity in different areas and seasons would give more light for the understanding of dengue transmission pattern in Rio de Janeiro and improve mosquito control.

Table 1

Number of dust-marked Ae. aegypti females released and captured per day in the two neighbors in Rio de Janeiro, using two capturing methods: backpack battery-power aspirator and BGS-Traps

Tubiacanga wet seasonTubiacanga dry seasonFavela do Amorim dry seasonFavela do Amorim wet season
Days after releaseCohort 1Cohort 2Cohort 3Cohort 1Cohort 2Cohort 3Cohort 1Cohort 2Cohort 3Cohort 1Cohort 2Cohort 3
Released821676893851712619731698707652703729
128253019172015810101312
2191722811101069131010
314142011991381115813
4121216869121169149
59911434895131210
676833511589106
7346333637687
8423111664793
92120246876
101314355
11542
1252
131
Total9890118585361976776939683
Recapture rate (%)11.9313.3113.216.817.449.8513.269.5910.7414.2613.6511.38
Table 2

Survival analysis for three Ae. aegypti female cohorts released in Tubiacanga and Favela do Amorim, Rio de Janeiro city, during wet and dry seasons, and captured with backpack battery-powered aspirators and BGS-Traps

Daily probability survival (95% CI)
Site/seasonCohortExponentialBuonaccorsiALE (days) Buonaccorsi
Daily probability of survival (DPS) was estimated by the exponential and Buonaccorsi models.
ALE, average life expectancy.
Tubiacanga wet season10.730.76 (0.73–0.80)3.2–4.4
20.710.76 (0.73–0.78)3.2–4.1
30.710.75 (0.72–0.79)3.1–4.3
Tubiacanga dry season10.750.77 (0.73–0.80)5.8–9.6
20.720.75 (0.73–0.78)5.8–14
30.720.75 (0.72–0.79)6.6–12
Favela do Amorim wet season10.830.86 (0.81–0.92)4.8–12
20.850.88 (0.83–0.94)5.3–16
30.840.86 (0.82–0.90)5.3–9.4
Favela do Amorim dry season10.850.87 (0.84–0.90)5.8–9.7
20.870.88 (0.84–0.93)5.8–14
30.870.89 (0.86–0.92)6.6–12
Table 3

Distances traveled by dust-marked Ae. aegypti females captured with backpack aspirators and BGS-Traps in a suburban neighbor (Tubiacanga) and a slum in the urban area (Favela do Amorim) in Rio de Janeiro during the dry and wet seasons

Tubiacanga wet seasonTubiacanga dry seasonFavela do Amorim dry seasonFavela do Amorim wet season
MDT (m)86.8780.9453.1539.49
FR50 (m)51.1372.3352.8038.50
FR90 (m)151.09137.8991.4471.33
MAX (m)248.28363.09151.9299.53
Females flying up to 100 m (%)60.1393.3896.45100.00
Females flying beyond 200 m (%)2.288.72
Table 4

Generalized estimating equations (GEE) model for log (dispersal) of marked Ae. aegypti females released in Tubiacanga and Favela do Amorim in both dry and wet seasons and captured with BGS-Traps and backpack aspirators

VariableEffectSEWaldP
* Correlation structure used was the “exchangeable.”
Intercept2.9610.244146.9< 0.0001
Area (Tubiacanga)0.6500.13722.4< 0.0001
Season (wet)0.0290.2170.0190.89
Time after release0.1680.03228.5< 0.001
Correlation*0.100.053.390.06
Figure 1.
Figure 1.

Ovarian development stages of dust-marked Ae. aegypti females released in the suburban area (Tubiacanga) and recaptured with backpack aspirators. (A) MRR conducted in the wet season, where 210 females were dissected. (B) MRR performed in the dry season, where 118 females were collected.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 76, 4; 10.4269/ajtmh.2007.76.659

Figure 2.
Figure 2.

Ovarian development stages of dust-marked Ae. aegypti females released in the urban area (Favela do Amorim) and recaptured with backpack aspirators. (A) MRR conducted in the dry season, where 107 females were dissected. (B) MRR performed in the wet season, where 201 females were collected.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 76, 4; 10.4269/ajtmh.2007.76.659

*

Address correspondence to Rafael Maciel-de-Freitas, Laboratório de Transmissores de Hematozoários, PavilhaóCarlos Chagas, 4° andar sala 04, Departamento de Entomologia, Rio de Janeiro, Brazil 21040-360. E-mail: freitas@ioc.fiocruz.br

Authors’ addresses: R. Maciel-de-Freitas and R. Lourenço-de-Oliveira, Laboratório de Transmissores de Hematozoários, Pav. Carlos Chajas, 4° andar, Sala 04, Departamento de Entomologia. CEP: 21040-360. FundaçaóOswaldo Cruz, Fiocruz, Rio de Janiero, Brazil. E-mails: freitas@ioc.fiocruz.br, lourenco@ioc.fiocruz.br. C. T. Codeço, Programa de ComputacóCientifica, Fundaçao Oswaldo Cruz, Fiocruz, Rio de Janiero, Brazil. CEP: 21040-360. E-mail: codeco@fiocruz.br.

Acknowledgments: We thank Gláuber Rocha, Kleber Soares, Marcelo Celestino dos Santos, Marcelo Quintela Gomes, Mauro Menezes Muniz, Reginaldo Rego, Renato Carvalho, Roberto Costa Peres, and Sérgio Cunha for field assistance. We also thank Dr Álvaro Eiras for allowing the use of BG-Sentinels and the comments of two anonymous referees that improved this manuscript quality.

Financial support: This study was supported by FAPERJ, CNPq, and Fiocruz.

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