Bionomics of Culex quinquefasciatus within urban areas of Rio de Janeiro, Southeastern Brazil

Bionomía de Culex quinquefasciatus en áreas urbanas en Rio de Janeiro, Brasil

Bionomia de Culex quinquefasciatus em áreas urbanas no Rio de Janeiro, RJ

ARTIGOS ORIGINAIS

Bionomics of Culex quinquefasciatus within urban areas of Rio de Janeiro, Southeastern Brazil

Bionomia de Culex quinquefasciatus em áreas urbanas no Rio de Janeiro, RJ

Bionomía de Culex quinquefasciatus en áreas urbanas en Rio de Janeiro, Brasil

Mariana Rocha David^I; Gabriel Sylvestre Ribeiro^II; Rafael Maciel de Freitas^II

^IPrograma de Pós-Graduação em Biologia Parasitária. Instituto Oswaldo Cruz. Fiocruz. Rio de Janeiro, RJ, Brasil

^IILaboratório de Transmissores de Hematozoários. Instituto Oswaldo Cruz. Fiocruz. Rio de Janeiro, RJ, Brasil

^{Correspondência | Correspondence}

ABSTRACT

OBJECTIVE: To evaluate density, parity rates, daily survival and longevity of natural populations of Culex quinquefasciatus in three neighborhoods with distinct socio-economic and infrastructure profiles.

METHODS: Mosquito collections of the Culex quinquefasciatus species were performed weekly during two four month periods, from August to November 2008 (spring) and March to June 2009 (fall), in a favela (slum), a suburban area and a middle class area of Rio de Janeiro, Southeastern Brazil. Collections were performed with backpack aspirators, in 20 randomly selected houses in each area per week, during 15-20 minutes per house. Ovaries were removed from captured females and classified as initial, intermediary or final stage. Furthermore, females were dissected for determination of parity based on the condition of the tracheal system. Mosquito survival rate and longevity were estimated on a per month basis for each neighborhood.

RESULTS: We collected a total of 2,062 Culex quinquefasciatus, but monthly vector density was not correlated with temperature and rainfall. We dissected the ovaries of 625 Culex quinquefasciatus, and overall, there was a higher proportion of nulliparous females during the dryer months, while gravid females were more frequent in rainy months. In the middle class neighborhood, the parity rate reached up to 93.75% with survivorship of 0.979. Lower parity and survival rates were obtained in the suburban area (as low as 36.4% parity and 0.711 daily survival). Up to 84.7% of Culex quinquefasciatus females could survive the eight day period needed to complete West Nile Virus incubation.

CONCLUSIONS: The survival rate of Culex quinquefasciatus varied significantly between the neighborhoods. This suggests that vectorial capacity and disease transmission risk may vary greatly between different urban areas, which is potentially useful information for vector control programs.

Descriptors: Culex. Parity. Survival. Longevity.

RESUMO

OBJETIVO: Avaliar densidade, taxa de paridade, sobrevivência diária e longevidade de populações naturais de Culex quinquefasciatus de três localidades com diferentes perfis socioeconômicos e de infraestrutura.

MÉTODOS: Mosquitos da espécie Culex quinquefasciatus foram coletados semanalmente em dois períodos de quatro meses, de agosto a novembro de 2008 e de março a junho de 2009, em uma comunidade, uma área de subúrbio e um bairro de classe média no Rio de Janeiro, RJ. As coletas foram realizadas com o auxílio de aspiradores costais em 20 domicílios, aleatoriamente selecionados por semana e por área, durante 15-20 minutos por domicílio. As fêmeas capturadas tiveram os ovários removidos e classificados em estágios inicial, intermediário e final. Adicionalmente, as fêmeas foram dissecadas para determinação da paridade de acordo com as condições do sistema traqueal. A taxa de sobrevivência e a longevidade das fêmeas foram estimadas por mês, para cada localidade.

RESULTADOS: Foram coletados 2.062 Culex quinquefasciatus, porém a densidade mensal deste vetor não apresentou correlação com temperatura e precipitação. Dissecamos os ovários de 625 Culex quinquefasciatus e obtivemos maior proporção de fêmeas nulíparas durante os meses mais secos, enquanto fêmeas grávidas foram mais frequentes nos meses chuvosos. A taxa de paridade foi de até 93,75% no bairro de classe média, com sobrevivência de 0,979. Menores valores de paridade e sobrevivência foram obtidos no subúrbio (começando em 36,4% de paridade e 0,711 de sobrevivência diária). Até 84,7% das fêmeas de Culex quinquefasciatus poderiam sobreviver ao período de oito dias, necessário para completar o período de incubação do vírus da febre do Nilo Ocidental.

CONCLUSÕES: A taxa de sobrevivência de Culex quinquefasciatus variou significativamente entre os bairros, o que sugere que a capacidade vetorial e o risco de transmissão de doenças podem variar entre diferentes áreas urbanas, informação relevante para o planejamento dos programas de controle de vetores.

Descritores: Culex, Paridade. Sobrevivência. Longevidade.

RESUMEN

OBJETIVO: Evaluar densidad, tasa de paridad, sobrevivencia diaria y longevidad de poblaciones naturales de Culex quinquefasciatus de tres localidades con diferentes perfiles socioeconómicos y de infraestructura.

MÉTODOS: Mosquitos de la especie Culex quinquefasciatus fueron colectados semanalmente en dos períodos de cuatro meses, de agosto a noviembre de 2008 y de marzo a junio de 2009, en un barrio, un área de suburbio y una urbanización de clase media en Rio de Janeiro, Litoral Sudeste de Brasil. Las colectas se realizaron con ayuda de aspiradores costales en 20 domicilios, aleatoriamente seleccionados por semana y por área, durante 15-20 minutos por domicilio. A las hembras capturadas se les retiraron los ovarios y clasificaron en fases inicial, intermediario y final. Adicionalmente, las hembras fueron diseccionadas para determinar la paridad de acuerdo con las condiciones del sistema traqueal. La tasa de sobrevivencia y la longevidad de las hembras fueron estimadas por mes para cada localidad.

RESULTADOS: Se colectaron 2.062 Culex quinquefasciatus, sin embargo, la densidad mensual del vector no presentó correlación con la temperatura y precipitación. Se diseccionaron los ovarios de 625 Culex quinquefasciatus y se obtuvo mayor proporción de hembras nulíparas durante los meses más secos, mientras que las hembras grávidas fueron más frecuentes en los meses de lluvia. La tasa de paridad alcanzó el 93,75% en la urbanización de clase media, con sobrevivencia de 0,979. Menores valores de paridad y sobrevivencia se obtuvieron en el suburbio (comenzando en 36,4% de paridad y 0,711 de sobrevivencia diaria). El 84,7% de las hembras de Culex quinquefasciatus podrían sobrevivir al período de ocho días, necesario para completar el período de incubación del virus de la fiebre del Oeste del Nilo.

CONCLUSIONES: La tasa de sobrevivencia de Culex quinquefasciatus varió significativamente entre las urbanizaciones, sugiriendo que la capacidad vectorial y el riesgo de transmisión de enfermedades pueden variar entre diferentes áreas urbanas, información relevante para la planificación de los programas de control de vectores.

Descriptores: Culex, Paridad. Longevidad.

INTRODUCTION

Culex quinquefasciatus Say is a cosmopolitan mosquito with worldwide distribution, more frequent in tropical and subtropical areas in association with human dwellings. The adult females lay eggs preferentially in relatively large, permanent habitats with high concentrations of decomposing organic matter, such as sewage effluents and septic tanks. However, immature stages of this species can be found in artificial containers often filled with polluted or organic-rich water, but rarely co-exist in the same container with the dengue vector Aedes aegypti.

Besides causing nocturnal discomfort and allergic responses, Cx. quinquefasciatus has important medical relevance. This species is established as the main vector of both Wuchereria bancrofti Cobbold in cities of the Northern/Northeastern Brazil, including Salvador, Maceió, Recife and Belém,²⁴ and Dirofilaria immitis Leidy in Brazilian coastal cities such as Florianópolis, Rio de Janeiro, Recife and São Luiz.¹ Moreover, Cx. quinquefasciatus is a competent vector of St. Louis encephalitis (SLE)¹⁸ and West Nile virus (WNV).¹³ Public health authorities from all over the world realized the need to monitor birds, horses and mosquito populations for the prediction of WNV circulation in the end of the 90s, after an outbreak of WNV in New York City was followed by rapid dissemination throughout the country.

WNV plagues the Americas from the North of South America to Canada and its activity is observed in Mexico, countries of Central America, Venezuela, Colombia and Argentina.¹⁴ A recent report has observed the presence of WNV antibodies in horses of the Brazilian Pantanal biome, but all the tested mosquitoes and caimans were negative.²² The vectorial competence of native Cx. quinquefasciatus populations or other species to WNV still remains unknown. Although the surveillance of WNV in mosquitoes, caimans and migratory birds has detected no WNV genome or antibodies up to now, the presence of WNV in horses of the Pantanal suggests this virus has already invaded Brazil. However, no human cases were registered in the country up to August 2011 (Nota Técnica 28/2011).

Little is known about bionomic aspects of Cx. quinquefasciatus in Brazil, especially those parameters governing vectorial capacity. The daily survival probability of adult females is crucial for understanding disease transmission, since small increases in longevity may exponentially augment the vectorial capacity.¹¹ Vectors must survive longer than the pathogen extrinsic incubation period to be able to infect the host by bite. Girard et al¹² have shown that a lifespan of at least eight days is required for WNV transmission. Daily survival rates may be calculated by either a mark-release-recapture experiment or by dissecting the ovaries of wild-caught individuals and assessing their parity rate and gonotrophic cycle length.⁷

This study aimed to assess Cx. quinquefasciatus density, survival rates, longevity and age structure in three neighborhoods with distinct socioeconomic statuses.

METHODS

A field study was performed simultaneously in three urban neighborhoods of Rio de Janeiro, Southeastern Brazil: Tubiacanga (22°47'08" S; 43°13'36" W), Amorim (22°52'30" S; 43°14'53' W) and Vila Valqueire (22°53'17" S; 43°22'20" W). Tubiacanga is an isolated, low middle-class suburban area surrounded in about 70% of its extension by the Guanabara Bay, which has an area of approximately 380 km² and is bordered by eight counties with 7.6 million inhabitants. Tubiacanga has 867 standard houses and 2,902 inhabitants, with human density of 337.4 inhab/hectare, distributed over 14 square blocks. Amorim is a typical overcrowded poverty-stricken Brazilian favela (slum), with narrow alleys and irregular blocks, located in an isolated area surrounded by large highways and an amply vegetated and non-residential area. Amorim lacks regular piped water distribution and garbage collection, and has poor basic sanitation. In Amorim, there are 2,992 people living in 897 premises within ten square blocks, with a population density of 901.2 inhab/ha. Valqueire is a middle-class urban area surrounded by a secondary forest, with paved streets, regular municipal water supply and garbage collection. At a distance of 500 m, an urban polluted stream about 5 m wide flows through part of the study area. Valqueire has 2,962 inhabitants in 895 houses spread over 15 square blocks, with human density of 145.5 inhab/ha. The neighborhoods of Tubiacanga, Amorim and Valqueire were referred to as suburbia, slum and middle-class areas, respectively.

The climate in Rio de Janeiro is characterized by a dry winter (May-August) and a wet summer season (November-March). The sites are approximately 15 km apart from each other in a straight line, which suggests differences in air temperature and precipitation influencing mosquito biology in each area, i.e., development time, survival and competition due to breeding sites availability. All three areas are subject to intense rainfall in the summer (November-March), but the suburbia and slum areas are dryer than the middle-class neighborhood between May-September (Figure 1). Meteorological data were recorded at the nearest meteorological station from each study area to estimate the role of meteorological variations in vector population density and survival.

Mosquito collections were performed in two four- month periods, from August to November 2008 (spring) and from March to June 2009 (fall), preceding and succeeding the winter (the season in which Cx. quinquefasciatus has its peak of density).^20,21 We monitored adult Cx. quinquefasciatus density on a weekly basis by collecting mosquitoes with backpack aspirators in 20 randomly selected houses per area. The backpack aspirator is frequently pointed out as the most effective collection method for adult mosquitoes, since it captures males and females of all physiological statuses, affording adult density estimates. Aspiration was carried out inside and in the peridomestic environments during 15-20 minutes per house. Collected mosquitoes were brought to the laboratory for identification and sequential assays.

All females captured with backpack aspirators had their ovaries removed and preserved in saline solution. The skeins of the ovarian tracheal system were evaluated under a microscope. The irreversible uncoiling of skeins indicates parity.⁸

Ovaries of dissected females were classified according to Christophers,⁵ with stages 1, 1-2, and 2 grouped as initial stages of development, stages 3 and 4 grouped as intermediate and stage 5 classified as final (gravid females). Parity of natural populations of Cx. quinquefasciatus for each season and area was calculated as the number of parous divided by the total number of dissected females. Survival rate was estimated for each neighborhood according to the Davidson⁷ method: S = ^g√ parity rate, where S was the survival rate and g was the duration of the gonotrophic cycle, which was assumed to be three days.^9,15 Mosquito longevity was calculated as 1/-log_e S, and the proportion of females that survived eight days was defined as S.⁶ Eight was the probable duration of the extrinsic incubation period for the WNV virus.¹² We performed parity, survival and longevity analysis on a monthly basis due to the limitations of weekly female collections.

We analyzed the correlation between meteorological variables (minimum, average and maximum temperatures and rainfall) and Cx. quinquefasciatus density by a Spearman correlation test. Data on mosquito density per week were correlated with meteorological variables in the same week as well as in the two weeks prior to field collection.

Parity rates between August-November/2008 and March-June/2009 were compared using a chi-square test to evaluate whether the rates differed regarding the study area and season.

RESULTS

A total of 2,062 Culex quinquefasciatus was collected in the three neighborhoods with a sex ratio remarkably biased to males (Table 1): 851 mosquitoes in the middle-class site (295 females, with a sex ratio of 1:2.88 female:male), 972 in the suburbia (282 females, sex ratio of 1:3.44) and 239 in the slum (103 females, sex ratio of 1:2.32). The percentage of female Cx. quinquefasciatus per area ranged from 29% (in the suburbia district) to 43% (in the slum).

More Cx. quinquefasciatus were collected from August to November/2008 (spring) than during March-June/2009 (fall) (55.9, 80.2 and 65.3% of the collections pertaining to the slum, middle-class and suburbia districts, respectively). The collection of male and female Cx. quinquefasciatus in the three neighborhoods was generally not correlated with minimum, average and maximum temperatures. The exception was that the maximum temperature observed in the week of collection was negatively correlated with the number of Cx. quinquefasciatus females in the three areas (Middle-class: R² = 0.366; Suburbia: R² = 0.61; Slum: R² = 0.60). No correlation was established for mosquito density and rainfall (data not shown).

We dissected ovaries of 88.1%, 96.1% and 91.3% of Cx. quinquefasciatus females collected in the middle-class, suburbia and slum areas, respectively. Cx. quinquefasciatus age structure presented significant variation among the three neighborhoods (Figure 2). Parity rate varied from 64.0% (June/09) to 93.75% (November/08) in the middle-class area, but no significant variation was observed between the two collection periods (χ² = 1.67, p > 0.05). A higher proportion of nulliparous females was observed during the dryer months, but more gravid (stage V) females were collected in rainy months in the middle-class and suburbia neighborhoods.

Parity rates in the suburbia area ranged from 36.4% (May/09) to 78.5% (October/08), while in the slum they varied from 40.0% (May/09) to 73.3% (October/08). There was no evident correlation of the ovarian development stage and parity rates with meteorological data in the slum. There was a higher parity rate in the suburbia site during August-November/08 than in March-June/09 (χ² = 5.28, p > 0.05), but no differences were apparent in the slum (χ² = 3.18, p > 0.05).

Assuming a gonotrophic cycle of three days, there were high values of daily survival, especially for the middle-class neighborhood, which reflected high longevity for females (Table 2). Longevity estimates reinforced the differences in the three neighborhoods. Eight days after a potential infection of WNV, between 30.4 and 84.7% Cx. quinquefasciatus would be alive in the middle-class site. In the suburbia and slum areas the proportion of females surviving eight days after infection would vary between 6.6 and 53.3% and from 7.6 to 48.1%, respectively.

Cx. quinquefasciatus longevity was greater in the middle-class neighborhood, with an average life expectancy ranging from 6.7 to 48.2 days. A lower average life expectancy was obtained in the other two sites, ranging from 2.93 to 12.7 days in the suburbia and from 3.2 to 10.9 in the slum.

DISCUSSION

The variation in vector biology among the areas was remarkable, especially concerning survival and longevity estimates. The results may indicate that Cx. quinquefasciatus biology depends on the urban characteristics of the site where the mosquito is distributed, although we worked in three neighborhoods in a city of around 8 million people. The ecological plasticity of Cx. quinquefasciatus may be useful in the determination of a cost-effective control policy.

There was a moderate negative correlation between mosquito density and maximum temperature in the same week of collection. No significant correlation, positive or negative, was established when the number of mosquitoes was compared with meteorological data one or two weeks before vector collection. However, a higher proportion of nulliparous females was observed during the dryer months, especially in Valqueire and Tubiacanga. There were more gravid (stage V) females in rainy months. This suggests that the larval habitats were close to the capturing points, which might have biased the collection of newly emerged females. Although the collection was homogeneously performed throughout the three study sites, this potential bias must be considered. Mosquito density in the three neighborhoods of Rio de Janeiro was directly influenced neither by temperature nor by rainfall.

Reports indicate the effect of seasonality on mosquito density, but the density peak period seems to vary geographically. In Puerto Rico, Cx. quinquefasciatus was more abundant in the spring than in the fall.²⁵ After modeling mosquito population dynamics, Morin & Comrie¹⁹ reported that Cx. quinquefasciatus populations have a dramatic growth during spring in California, mainly due to the increase in rainfall during January. Mosquitoes were abundant throughout the year because of sufficient precipitation in Florida,¹⁹ but some reports also showed that Cx. quinquefasciatus density peaks occurred during the winter.^{20, 21} More Cx. quinquefasciatus were collected in the winter in India.²⁰ If there is any influence of meteorological variables on mosquito density, it is probably low and caused by the nearby presence of potential breeding sites. Female individuals may have a higher response to microclimatic variations than to outside rainfall and temperature. Cx. quinquefasciatus is well adapted to human dwellings, where the influence of outside temperature is low. All three areas have nearby polluted or sewage water, such as streams, open or leaking sewage systems or the Guanabara Bay. These sites are permanent yearlong, i.e., they support immature mosquito populations continuously throughout the year and, consequently, their availability is not influenced by rainfall. In this particular situation, the effect of meteorological variables on Cx. quinquefasciatus density is masked by the presence of permanent mosquito habitats within the surroundings. Rio de Janeiro has an average winter temperature of 20-22°C, which reduces the potential effects a harsh cold might have on vector density.

The parity rates in Rio de Janeiro were higher than in other regions of Brazil, namely, in the city of Manaus (Northern Brazil)⁴ and in an ecological park located in the State of São Paulo.¹⁵ Collections by Laporta and Sallum¹⁵ were conducted outdoors, which provided several nulliparous specimens. The majority of reports indicate parity rates that are similar to those in our study. Chandra et al³ observed a parity rate of 0.87 in Calcutta, India, while in the study carried out by Garcia-Rejon et al,¹⁰ it varied daily, reaching a maximum value of 0.90. We estimated the monthly instead of the daily parity rate, as Garcia-Rejon et al¹⁰ did. The field strategy of estimating parity rates on a monthly basis may cause a loss in the natural variation of parity rates in field populations. However, due to personal field limitations and to the low number of captured females during some months, we had to assess mosquitoes collected during 3-4 weeks. Estimating the parity rates of a natural population may provide substantial information on its dynamics. When the proportion of nulliparous females in a field population is unexpectedly high, one might assume that this population has suffered a drastic reduction in density for a few weeks, caused by, for example, an insecticide campaign or severe and unfavorable meteorological conditions.¹⁹

Daily vector survival rates may be calculated by either mark-release-recapture (MRR) techniques or by dissection of female insects to assess parity rates,⁸ followed by the application of the Davidson⁷ equation. Discrepancies in survivorship estimations between Davidson's method and linear regression of captures as a function of time in MRR experiments are not known. Theoretically, comparisons between methods are unusual due to sampling bias and population fluctuation over time. To estimate survival rate as the proportion of parous females in a population using Davidson's method, recruitment must be constant throughout the sampling period. The percentage of parous females can be severely reduced by a spike in mosquito emergence, lowering survival estimates.⁹ Estimates based on MRR experiments are strongly influenced by losses due to mosquito death or to emigration from the study site, a crucial difference that is undetectable under conventional MRR procedures.¹⁶ Only one study compared survival estimates based on Davidson's method and linear regression of captures, and it provided similar values for both techniques.²³

Survival estimates calculated by Davidson's method are strongly influenced by the duration of the gonotrophic cycle. Small variations in the length of the gonotrophic cycle can influence survival rates. We assumed a gonotrophic cycle of three days for Cx. quinquefasciatus based on previous reports with very similar estimates.^9,10,15 The high survival rates for Cx. quinquefasciatus may have an important consequence on vectorial capacity and disease transmission, since in a long-lived vector population females have several opportunities to blood feed, which maximizes the contact rate between a potentially infected mosquito and a susceptible human host. High survivorship implicates high longevity. More than 50% of the females would have been able to transmit WNV under field conditions in the middle-class area, with the exception of the month of June/2009. This proportion is higher than that for other arboviruses, such as Ae. aegypti-dengue^6,16 and Aedes camptorhyncus-Ross River virus.² However, before an alarmist scenario is created, one should test the vector competence of Brazilian Cx. quinquefasciatus populations to WNV infections and host-feeding preferences of the native mosquitoes.

The significant differences in survival and longevity estimates in the three neighborhoods are puzzling and may be connected with the availability of artificial containers, socioeconomic levels and human demography. Despite the possible difficulties in disentangling these effects from each other, it is possible to say that the availability of container types is highly correlated with socioeconomic level in Rio de Janeiro.^6,16 Containers used for water storage are abundant in areas with irregular water distribution, such as the slum and suburbia. When piped water distribution is regular, containers such as metal drums and water tanks are almost inexistent, and domestic rains and plastic pots become productive breeding sites.¹⁷ The high abundance of large containers with clean water storage may have influenced the oviposition pattern of Cx. quinquefasciatus in the slum and suburbia areas, strengthening larval competition in containers with high amounts of organic matter. Additionally, districts with lower socioeconomic statuses tend to have higher availability of containers, mainly due to the accumulation of small abandoned objects in the yard and surroundings. Mosquito survival and longevity varied inversely to human demography, i.e., higher survivorship was observed in the middle-class district, where human density is more than six times lower than in the slum. The human defensive behavior may kill mosquitoes during their bite or rest. Thus, the absolute number of mosquitoes being killed by the human defensive behavior would be lower in low human density areas, allowing higher population survival.

We evaluated some aspects of Cx. quinquefasciatus bionomics in three neighborhoods with very distinct socioeconomic and infrastructure statuses in which there were different vector survival rates, an important component of vectorial capacity. Understanding Cx. quinquefasciatus population biology under different urban scenarios may provide an advantage for controlling this potential vector species.

Received: 8/9/2011

Approved: 3/25/2012

The authors declare that there were no conflicts of interest.

• 1. Ahid SM, Vasconcelos PS, Lourenço-de-Oliveira R. Vector competence of Culex quinquefasciatus Say from different regions of Brazil to Dirofilaria immitis. Mem Inst Oswaldo Cruz. 2000;95(6):769-75. DOI:10.1590/S0074-02762000000600004
• 2. Carver S, Spafford H, Storey A, Weinstein P. Dryland salinity and the ecology of Ross River virus: The ecological underpinnings of the potential for transmission. Vector Borne Zoonotic Dis. 2009;9(6):611-22. DOI:10.1089/vbz.2008.0124
• 3. Chandra G, Seal B, Hati AK. Age composition of the filarial vector Culex quinquefasciatus (Diptera: Culicidae) in Calcutta, India. Bull Entomol Res. 1996;86(3):223-6. DOI:10.1017/S0007485300052500
• 4. Charlwood JD. Estudos sobre a biologia e hábitos alimentares de Culex quinquefasciatus Say de Manaus, Amazonas, Brasil. Acta Amazônica 1979;9(2):271-8.
• 5. Christophers SR. Aedes aegypti (L.): The yellow fever mosquito, its life history, bionomics and structure. London: Cambridge University Press; 1960.
• 6. David MR, Lourenço-de-Oliveira R, Maciel-de-Freitas R. Container productivity, daily survival rates and dispersal of Aedes aegypti mosquitoes in a high income dengue epidemic neighborhood of Rio de Janeiro: presumed influence of differential urban structure on mosquito biology. Mem Inst Oswaldo Cruz. 2009;104(6):927-32. DOI:10.1590/S0074-02762009000600019
• 7. Davidson G. Estimation of the survival-rate of anopheline mosquitoes in nature. Nature 1954;174(4434):792-93. DOI:10.1038/174792a0
• 8. Detinova TS. Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr Ser World Health Organ. 1962;47:13-191.
• 9. Elizondo-Quiroga A, Flores-Suarez A, Elizondo-Quiroga D, Ponce-Garcia G, Blitvich BJ, Contreras-Cordero JF, et al. Gonotrophic cycle and survivorship of Culex quinquefasciatus (Diptera: Culicidae) using sticky ovitraps in Monterrey, northeastern Mexico. J Am Mosq Control Assoc. 2006;22(1):10-4. DOI:10.2987/8756-971X(2006)22[10:GCASOC]2.0.CO;2
• 10. García-Rejón JE, Farfan-Ale JA, Ulloa A, Flores-Flores LF, Rosado-Paredes E, Baak-Baak C, et al. Gonotrophic cycle estimate for Culex quinquefasciatus in Mérida, Yucatán, México. J Am Mosq Control Assoc. 2008;24(3):344-8.
• 11. Garret-Jones C, Shidrawi GR. Malaria vectorial capacity of a population of Anopheles gambiae. Bull World Health Organ. 1969;40(4):531-45.
• 12. Girard YA, Klingler KA, Higgs S. West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonotic Dis. 2004;4(2):109-22. DOI:10.1089/1530366041210729
• 13. Goddard LB, Roth AE, Reisen WK, Scott TW. Vector competence of California mosquitoes for West Nile virus. Emerg Infect Dis. 2002;8(12):1385-91. DOI:10.3201/eid0812.020536
• 14. Komar N, Clark GG. West Nile virus activity in Latin America and the Caribbean. Rev Panam Salud Publica. 2006;19(2):112-7. DOI:10.1590/S1020-49892006000200006
• 15. Laporta GZ, Sallum MA. Density and survival rate of Culex quinquefasciatus at Parque Ecológico do Tietê, São Paulo, Brazil. J Am Mosq Control Assoc. 2008;24(1):21-7. DOI:10.2987/5664.1
• 16. Maciel-de-Freitas R, Codeço CT, Lourenço-de-Oliveira R. Daily survival rates and dispersal of Aedes aegypti females in Rio de Janeiro, Brazil. Am J Trop Med Hyg. 2007;76(4):659-65.
• 17. Maciel-de-Freitas R, Lourenço-de-Oliveira R. Does targeting key-containers effectively reduce Aedes aegypti population density? Trop Med Int Health. 2011;16(8):965-73. DOI:10.1111/j.1365-3156.2011.02797.x
• 18. Meyer RP, Hardy JL, Presser SB. Comparative vector competence of Culex tarsalis and Culex quinquefasciatus from the coachella, imperial, and San Joaquin Valleys of California for St. Louis encephalitis virus. Am J Trop Med Hyg. 1983;32(2):305-11.
• 19. Morin CW, Comrie AC. Modeled response of the West Nile virus vector Culex quinquefasciatus to changing climate using the dynamic mosquito simulation model. Int J Biometeorol. 2010;54(5):517-29. DOI:10.1007/s00484-010-0349-6
• 20. Murty US, Sai KS, Kumar DV, Sriram K, Rao KM, Krishna D, et al. Relative abundance of Culex quinquefasciatus (Diptera: Culicidae) with reference to infection and infectivity rate from the rural and urban areas of East and West Godavari districts of Andhra Pradesh, India. Southeast Asian J Trop Med Public Health. 2002;33(4):702-10.
• 21. O'Meara GF, Cutwa-Francis M, Rey JR. Seasonal variation in the abundance of Culex nigripalpus and Culex quinquefasciatus in wastewater ponds at two Florida dairies. J Am Mosq Control Assoc. 2010;26(2):160-6. DOI:10.2987/09-5971.1
• 22. Pauvolid-Corrêa A, Morales MA, Levis S, Figueiredo LT, Couto-Lima D, Campos Z, et al. Neutralising antibodies for West Nile virus in horses from Brazilian Pantanal. Mem Inst Oswaldo Cruz. 2011;106(4):467-74. DOI:10.1590/S0074-02762011000400014
• 23. Reisen WK, Kilby M, Meyer RP, Pfuntner AR, Spoehel J, Hazelrigg JE, et al. Mark-release-recapture studies with Culex mosquitoes (Diptera: Culicidae) in Southern California. J Med Entomol. 1991;28(3):357-71.
• 24. Rocha EMM, Fontes G. Filariose bancroftiana no Brasil. Rev Saude Publica. 1998;32(1):98-105. DOI:10.1590/S0034-89101998000100015
• 25. Smith J, Amador M, Barrera R. Seasonal and habitat effects on dengue and West Nile virus vectors in San Juan, Puerto Rico. J Am Mosq Control Assoc. 2009;25(1):38-46. DOI:10.2987/08-5782.1

Publication Dates

• Publication in this collection
  03 Apr 2013
• Date of issue
  Oct 2012

History

• Received
  08 Sept 2011
• Accepted
  25 Mar 2012