Presumed unconstrained dispersal of Aedes aegypti in the city of Rio de Janeiro, Brazil

Dispersión ilimitada de Aedes aegypti en la ciudad de Río de Janeiro, Brasil

Dispersão de Aedes aegypti em local presumidamente sem barreira limitante ao vôo na cidade do Rio de Janeiro

ARTIGOS ORIGINAIS ORIGINAL ARTICLES

Presumed unconstrained dispersal of Aedes aegypti in the city of Rio de Janeiro, Brazil

Dispersão de Aedes aegypti em local presumidamente sem barreira limitante ao vôo na cidade do Rio de Janeiro

Dispersión ilimitada de Aedes aegypti en la ciudad de Río de Janeiro, Brasil

Rafael Maciel-de-Freitas; Ricardo Lourenço-de-Oliveira

Laboratório de Transmissores de Hematozoários. Instituto Oswaldo Cruz. Rio de Janeiro, RJ, Brazil

^{Correspondence}

ABSTRACT

OBJECTIVE: To evaluate dispersal of Aedes aegypti females in an area with no container manipulation and no geographic barriers to constrain mosquito flight.

METHODS: A mark-release-recapture experiment was conducted in December 2006, in the dengue endemic urban district of Olaria in Rio de Janeiro, Southeastern Brazil, where there is no evident obstacle to the dispersal of Ae. aegypti females. Mosquito traps were installed in 192 houses (96 Adultraps and 96 MosquiTRAPs).

RESULTS: A total of 725 dust-marked gravid females were released and recapture rate was 6.3%. Ae. aegypti females traveled a mean distance of 288.12 m and their maximum displacement was 690 m; 50% and 90% of females flew up to 350 m and 500.2 m, respectively.

CONCLUSIONS: Dispersal of Ae. aegypti females in Olaria was higher than in areas with physical and geographical barriers. There was no evidence of a preferred direction during mosquito flight, which was considered random or uniform from the release point.

Descriptors: Aedes. Disease Vectors. Mosquito Control. Culicidae. Dengue.

RESUMO

OBJETIVO: Avaliar a dispersão de fêmeas de Aedes aegypti em uma área onde não houve nenhuma interferência quanto à redução de potenciais criadouros e não há barreira geográfica que limite o vôo dos mosquitos.

MÉTODOS: Um experimento de marcação-soltura-recaptura foi realizado em dezembro de 2006, no bairro urbano Olaria, endêmico para dengue na cidade do Rio de Janeiro (RJ), onde não há obstáculos evidentes à dispersão de fêmeas de Ae. aegypti. Armadilhas para captura de mosquitos foram instaladas em 192 residências (96 Adultraps e 96 MosquiTraps).

RESULTADOS: Foram soltas 725 fêmeas grávidas marcadas com pó fluorescente e a taxa de recaptura foi de 6,3%. Fêmeas de Ae. aegypti dispersaram em média 288,12 m do ponto de soltura e o deslocamento máximo foi de 690 m; 50% e 90% das fêmeas voaram até 350 m e 500,2 m respectivamente.

CONCLUSÕES: A dispersão de fêmeas de Ae. aegypti em Olaria foi maior que em áreas com barreiras físicas e/ou geográficas. Não houve evidências de preferência de direção do vôo dos mosquitos, o qual foi considerado randômico ou uniforme a partir do ponto de soltura.

Descritores: Aedes. Vetores de Doenças. Controle de Mosquitos. Culicidae. Dengue.

RESUMEN

OBJETIVO: Evaluar la dispersión de hembras de Aedes aegypti en un área sin manipulación de recipientes y sin barreras geográficas que limiten el vuelo del mosquito.

MÉTODOS: Se realizó un experimento de marcaje y recaptura en diciembre de 2006, en el distrito urbano Olaria, Rio de Janeiro (Sureste de Brasil), área endémica para dengue, donde no hay obstáculo evidente para la dispersión de hembras de Ae. aegypti. Trampas para mosquitos fueron instaladas en 192 casas (96 Adultraps y 96 MosquiTraps).

RESULTADOS: Un total de 725 hembras grávidas marcadas con polvo fueron liberadas y recapturadas siendo la tasa de 6,3%. Las hembras de Ae. Aegypti viajaron una distancia promedio de 288,12 m y su máximo desplazamiento fue de 690 m; 50% y 90% de las hembras volaron hasta los 350 m y 500,2 m, respectivamente.

CONCLUSIONES: Dispersión de las hembras de Ae. aegypti en Olaria fue mayor que en las áreas con barreras físicas y geográficas. No hube evidencia de una dirección preferida durante el vuelo del mosquito, por lo que se considera aleatorio y uniforme desde el punto de liberación.

Descriptores: Aedes. Vectores de Enfermedades. Control de Mosquitos. Culicidae. Dengue.

INTRODUCTION

In the city of Rio de Janeiro, Brazil, the mosquito Aedes aegypti is essentially associated with human density, and is especially abundant in urbanized and densely populated areas.¹Ae. aegypti breeds almost exclusively in artificial large containers located in the peridomestic area, such as water tanks and metal drums¹⁵ and seldom invade the fringe of urban forests, generally not laying eggs or flying through distances exceeding 100 m from houses.^12,14

Dispersal may have several implications on mosquito population genetics, spreading of gene pools, such as insecticide resistance and virus susceptibility, and determination of control strategies by public health authorities. The dispersal ability of Ae. aegypti females have already been studied.²⁰ However, several previous dispersal estimates might be biased. Common sources of bias in dispersal estimates seem to be site manipulation prior to mosquito release or recaptures performed in a limited area, such a small village or a single block, frequently close to the release point.^{9,10,13,14,17,21,22} For example, Honório et al¹⁰ performed a mark-release-recapture experiment in a highly endemic area of dengue with female mosquitoes with amputated proboscis to avoid ethical issues and they also eliminated or removed most small containers from the study area. These interventions may have influenced the dispersal pattern of Ae. aegypti females, which displaced at least 800 m from their release point. Maciel-de-Freitas et al¹³ evaluated dispersal of Ae. aegypti females in two areas with distinct landscape and physical barriers, such as sea and extensive highways, and observed differential displacement from the release site in both areas.

The objective of the present study was to evaluate dispersal of Ae. aegypti females in an area with no container manipulation and no geographic barriers to constrain mosquito flight.

METHODS

The residential district of Olaria (22°50'45''S; 43°15'39''W), located in the city of Rio de Janeiro (Southeastern Brazil), was selected to release dust-marked Ae. aegypti females. It has an estimated population of 62,509 inhabitants in an area of 369 hectare, nearly 169 inh./ha. Olaria is a lowland district with extensive paved streets, moderate traffic and a busy rail station. Houses generally have 2-4 rooms and large peridomestic area, with usually no more than 4-5 persons per house. There is a regular service of garbage collection and water supply. Olaria is in one of the most important dengue endemic zone in the city, which registered 49,266 dengue cases from 1986 to 2001. According to the Health Department of the City of Rio de Janeiro, during the 2001 dengue epidemic, more than 8% (2,165/26,535 cases) of the city's total cases were reported there; in 2007 there were 208 dengue cases. In July 2006, five months prior to experiment start, Olaria had a house index of 8.8.

Released Ae. aegypti females were derived from a laboratory colony that is renewed at least twice a year with eggs collected in ovitraps installed in Rio de Janeiro. Larvae were fed with fish food (Tetramin) and reared according to Consoli & Lourenço-de-Oliveira.² After emergence, females were separated from males and kept together at 25 ± 3°C and 65 ± 3% relative humidity and provided with sucrose solution up to a day before the first blood feeding.

Two blood meals were offered on 3-4 days after emergence in an artificial membrane feeder apparatus.¹⁹ We expected all released females were gravid when released three days after blood meals. A total of 725 Ae. aegypti females with 6-7 days of emergence were marked with fluorescent dust (Day-Glo Color Corp., Cleveland, OH) and released outdoor in the morning (between 08:00 AM and 09:00 AM) of December 2^nd, 2006, approximately one hour after dust marking.

To capture released Ae. aegypti females a total of 192 traps (96 Adultraps⁸ and 96 MosquiTRAPs⁶) were installed in Olaria. Briefly, both traps were originally designed to capture gravid Ae. aegypti females. Adultrap is a black plastic jar with an external plastic screen using only water as attractant.⁸ MosquiTRAP has a glued car inside a black plastic jar, using a commercial mixture as attractant.⁶ Adultrap and MosquiTRAP were installed in the peridomestic area of adjacent houses and were left in the same place until the end of the experiment, covering an area of 3.14 km². Recaptures were carried out for 18 days. All collected mosquitoes were brought to the laboratory to be identified and checked for the presence of fluorescent mark with an UV light.

As for dispersal, the 192 houses where mosquito traps were installed were geo-referenced using a Global Position System (GPS; Garmin eTrex personal navigator) to calculate distance between releasing and capture points. The flight behavior of Ae. aegypti females was summarized by a set of dispersal measures: mean distance traveled (MDT), maximum distance traveled (MAX), and flight ranges of 50% (FR₅₀) and 90% (FR₉₀) of the population.^11,16 Frequency distributions of the marked mosquitoes that had traveled <100 m and >200 m from the release point were also evaluated.

We also used circular statistics to help understanding flight dynamics of Ae. aegypti females and most importantly, if they had an isotropic direction or a uniform distribution from the release point. For that, we calculated the angle formed between the release point and collection sites, forming a circular histogram, which shows the distribution of flight angles (to the south-north axis), with the North direction set as 0°. Flight direction tendencies were visually interpreted based on the histogram shape. The Rayleigh test of uniformity was used to calculate the probability of the null hypothesis that the data have a uniform distribution.²³ Circular histogram and data analysis were performed using Oriana program, v. 2.02.^ª

Mark-release-recapture (MRR) experiment protocols were submitted and approved by Fundação Oswaldo Cruz (Fiocruz) Research Ethics Committee (CEP/Fiocruz protocol no. 11591-2005).

RESULTS

A total of 46 (6.34%) dust-marked females were recaptured, 17 (36.9%) of them collected in Adultraps and 29 (63.1%) in MosquiTRAPs (Table 1). Dust-marked Ae. aegypti mosquitoes were recaptured up to nine days after release; the majority of them were recaptured up to four days (Table 1).

Ae. aegypti females had an average dispersal of 288.1 m from the release point. However, the maximum distance traveled observed was 690 m, corresponding to a single female that flew to the southeast direction. Additionally, 90% of released females flew up to 500.2 m and 69.0% displaced more than 200 m from the release point (Table 2).

Ae. aegypti flight showed an isotropic behavior from the release point, showing no evidence of a preferred direction (z = 0.242; p = 0.787). In fact, a circular histogram constructed with the angles formed by release and recapture points emphasizes the uniform distribution of flight direction (Figure).

DISCUSSION

Recapture rate of Ae. aegypti females were in accordance with other similar studies performed in Rio de Janeiro, even when recapture effort was confined to a smaller area.¹³ As there is no evident physical or geographical obstacle in Olaria, mosquito emigration was expected to be less controlled than in other studies in areas with physical barriers.^{9,13,17,21,22}

Dispersal of Ae. aegypti females in Olaria was higher than that seen in two other districts of the city of Rio de Janeiro and in other areas with physical and geographical barriers. ^{9,13,17,21,22} In Favela do Amorim, an urban area with high human density and container availability, Ae. aegypti females had an MDT of around 50 m and a MAX of 151 m. In Tubiacanga, a suburban area with a human density three times lower than Favela do Amorim, MDT was approximately 80 m with a maximum displacement of 363 m.¹³ Since mosquito flight seems to be associated to the heterogeneity distribution of blood sources⁷ and oviposition sites,⁵ low availability or container elimination during dry season or control campaigns may increase mosquito dispersal rates because females would have to fly longer distances to lay their eggs.^3,4,18 Therefore, the elimination of small containers during the dry season by Honório et al¹⁰ before Ae. aegypti releasing may have stimulated mosquito dispersal. These authors evaluated dispersal by collecting rubidium chloride (RbCl)-marked eggs with ovitraps set along varied distance from the release point. Several positive ovitraps were found at 800 m from the release site, the most distant collection point, suggesting that the displacement of Ae. aegypti females was beyond the most distant collection point.¹⁰ Besides, Honório et al¹⁰ amputated proboscis of released gravid Ae. aegypti females which may have influenced the observed dispersal range.

Dispersal is an important parameter in disease transmission dynamics and vector control. In theory, a disease vector able to displace long distances may spread pathogens to large areas. According to our results, an effective and efficient control is required that can include container elimination and insecticide spraying in a radius of at least 500 m from a reported dengue case.

ACKNOWLEDGEMENTS

To Roberto C. Peres and Reginaldo L.S. Rêgo, from Instituto Oswaldo Cruz, for their technical support and Mauro Brandolini, Fábio Castello and Fernando Alves, from the Dengue Control Campaign of the city of Rio de Janeiro, for field collections; to the Health Department of Paraná and Dr. Álvaro Eiras for providing Adultraps and MosquiTRAPs, respectively.

Received: 1/21/2008

Revised: 4/25/2008

Approved: 6/16/2008

Research supported by Programa de Desenvolvimento Tecnológico em Saúde Pública - Rede de Dengue/Fiocruz (PDTSP/Fiocruz, RV 08); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Proc. 306111/2003-9), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; Proc. E-26/100.609/2007).

• 1. Braks MAH, Honório NA, Lourenço-de-Oliveira R, Juliano SA, Lounibos LP. Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida. J Med Entomol. 2003;40(6):785-94.
• 2. Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária do Brasil. Rio de Janeiro: Fiocruz; 1994.
• 3. Costa-Ribeiro MC, Lourenço-de-Oliveira R, Failloux AB. Higher genetic variation estimated by microsatellites compared to isoenzyme markers in Aedes aegypti from Rio de Janeiro. Mem Inst Oswaldo Cruz. 2006;101(8):917-21. DOI: 10.1590/S0074-02762006000800015
• 4. Costa-Ribeiro MC, Lourenço-de-Oliveira R, Failloux AB. Geographic and temporal genetic patterns of Aedes aegypti populations in Rio de Janeiro, Brazil. Trop Med Int Health. 2006;11(8):1276-85. DOI: 10.1111/j.1365-3156.2006.01667.x
• 5. Edman JD, Scott TW, Costero A, Morrison AC, Harrington LC, Clark GG. Aedes aegypti (Diptera: Culicidae) movement influenced by availability of oviposition sites. J Med Entomol 1998;35(4):578-83.
• 6. Favaro EA, Dibo MR, Mondini A, Ferreira AC, Barbosa AA, Eiras AE, Barata EA, Chiaravalloto Neto F. Physiological state of Aedes (Stegomyia) aegypti mosquitoes captured with MosquiTRAPs in Mirassol, São Paulo, Brazil. J Vector Ecol 2006;31(2):285-291.
• 7. Forattini OP. Entomologia Médica. São Paulo: EDUSP; 1962.
• 8. Gomes AC, Silva NN, Bernal RT, Leandro AS, Camargo NJ, Silva AM, et al. Especificidade da armadilha Adultrap para capturar fêmeas de Aedes aegypti (Diptera: Culicidae). Rev Soc Bras Med Trop. 2007;40(2):216-9. DOI: 10.1590/S0037-86822007000200014
• 9. Harrington LC, Buonaccorsi JP, Edman JD, Costero A, Kittayapong P, Clark GG, et al. Analysis of survival of young and old Aedes aegypti (Diptera: Culicidae) from Puerto Rico and Thailand. J Med Entomol. 2001;38(4):537-47.
• 10. Honório NA, Silva WC, Leite PJ, Gonçalves JM, Lounibos LP, Lourenço-de-Oliveira R. Dispersal of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in an urban endemic dengue area in the State of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2003;98(2):191-8.
• 11. Lillie TH, Marquardt WC, Jones RH. The flight range of Culicoides mississippiensis (Diptera: Ceratopogonidae). Can Entomol. 1981;113(5):419-26.
• 12. Lourenço-de-Oliveira R, Vazeille M, Filippis AMB, Failloux AB. 2004. Aedes aegypti in Brazil: genetically differentiated populations with high susceptibility to dengue and yellow fever viruses. Trans R Soc Trop Med Hyg. 2004;98(1):43-54. DOI: 10.1016/S0035-9203(03)00006-3
• 13. 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):659-665.
• 14. Maciel-de-Freitas R, Brocki-Neto RW, Gonçalves JM, Codeço CT, Lourenço-de-Oliveira R. Movement of dengue vectors between human modified environment and an urban Forest in Rio de Janeiro. J Med Entomol. 2006;43(6):1112-20. DOI: 10.1603/0022-2585(2006)43[1112:MODVBT]2.0.CO;2
• 15. Maciel-de-Freitas R, Marques WA, Peres RC, Cunha SP, Lourenço-de-Oliveira R. Variation in Aedes aegypti (Diptera: Culicidae) container productivity in a slum and a suburban district of Rio de Janeiro during dry and wet seasons. Mem Inst Oswaldo Cruz. 2007;102(4):489-96. DOI: 10.1590/S0074-02762007005000056
• 16. Morris CD, Larson VL, Lounibos LP. Measuring mosquito dispersal for control programs. J Am Mosq Control Assoc. 1991;7(4):608-15.
• 17. Muir LE, Kay BH. Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am J Trop Med Hyg. 1998;58(3):277-82.
• 18. Reiter P, Amador MA, Anderson RA, Clark GG. 1995. Short report: Dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium-marked eggs. Am J Trop Med Hyg. 1995;52(2):177-9.
• 19. Rutledge LC, Ward RA, Gould DJ. Studies on the feeding response of mosquitoes to nutritive solutions in a new membrane feeder. Mosq News. 1964;24(4):407-9.
• 20. Service MW. Mosquito (Diptera: Culicidae) dispersal: The long and short of it. J Med Entomol. 1997;34(6):579-88.
• 21. Trpis M, Hausermann W, Craig Jr GB. Estimates of population size, dispersal, and longevity of domestic Aedes aegypti (Diptera: Culicidae) by mark-release-recapture in the village of Shauri Moyo in eastern Kenya. J Med Entomol. 1995;32(1):27-33.
• 22. Tsuda Y, Takagi M, Wang S, Wang Z, Tang L. Movement of Aedes aegypti (Diptera: Culicidae) released in a small isolated village on Hainan Island, China. J Med Entomol. 2001;38(1):93-8.
• 23. Zar JH. Biostatistical analysis. London: Prentice Hall; 1999.

a

Isle of Anglesey: Kovach Computing Services 2007 [cited 2007 May 9]. Available from:

http://www.kovcomp.com/Oriana

Publication Dates

• Publication in this collection
  06 Aug 2010
• Date of issue
  Feb 2009

History

• Accepted
  16 June 2008
• Reviewed
  25 Apr 2008
• Received
  21 Jan 2008