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Ecological aspects of mosquitoes (Diptera: Culicidae) in the gallery forest of Brasília National Park, Brazil, with an emphasis on potential vectors of yellow fever

Abstract

Introduction

We analyzed the vertical and monthly distributions of culicid species in the gallery forest of Brasília National Park, with an emphasis on the potential vectors of yellow fever (YF).

Methods

Between September 2010 and August 2011, mosquitoes were captured on the ground and in the canopy of the forest for five consecutive days per month, from nine to 15 hours. The mosquitoes were examined to verify natural infection with flaviviruses by isolation in Aedes albopictus Skuse, 1864 cells followed by indirect immunofluorescence.

Results

We identified 2,677 culicids distributed in 29 species. Most of the mosquitoes were captured at ground level (69%) during the rainy season (86%). The most abundant species were Sabethes (Sabethes) albiprivus Theobald, 1903; Limatus durhamii Theobald, 1901; Haemagogus (Conopostegus) leucocelaenus Dyar & Shannon, 1924; Haemagogus (Haemagogus) janthinomys Dyar, 1921; Aedes (Ochlerotatus) scapularis Rondani, 1848; Psorophora (Janthinosoma) ferox Von Humboldt, 1819; and Aedes (Ochlerotatus) serratus Theobald, 1901. Limatus durhamii, Limatus durhamii, Psorophora ferox, Aedes scapularis and Aedes serratus showed significant differences (p<0.05) in their habitat use. Limatus durhamii was found more often in the canopy, unlike the other species. During the rainy season, the most abundant species were Sa. albiprivus, Haemagogus leucocelaenus and Limatus durhamii. During the dry season, the potential YF vectors exhibited a very low frequency and abundance, except Aedes scapularis and Aedes serratus. No flavivirus was detected in the 2,677 examined mosquitoes.

Conclusions

We recommend continued and systematic entomological monitoring in areas vulnerable to the transmission of YF in the Federal District of Brazil.

Flavivirus; Haemagogus ; Mosquitoes; Vector ecology


INTRODUCTION

Mosquitoes have been widely studied because of their role in the transmission of tropical diseases, such as malaria, dengue and yellow fever101 Marcondes CB. Entomologia Médica e Veterinária. São Paulo: Atheneu; 2011.. According to Mathers et al.202 Mathers CD, Lopez AD, Murray CJL. The burden of disease and mortality by condition: data, methods and results for 2001. In: Lopez AD, Mathers CD, Ezzati M, Jamison DR, Murray CJL, editors. Global burden of disease and risk factors. New York: Oxford University Press/The World Bank. 2006. p. 45-240., infectious diseases transmitted by mosquitoes have a high impact on public health and are responsible for approximately 15% of all disability adjusted life years (DALYs) attributed to infectious and parasitic diseases throughout the world.

Yellow fever (YF) is an acute febrile illness that results from infection by an arbovirus of the genus Flavivirus 303 Vasconcelos PFC. Febre amarela: reflexões sobre a doença, as perspectivas para o século XXI e o risco de reurbanização. Rev Bras Epidemiol 2002; 5:244-258. that remains endemic or enzootic in Africa and South and Central America101 Marcondes CB. Entomologia Médica e Veterinária. São Paulo: Atheneu; 2011.,404 Organização Mundial de Saúde (OMS). Yellow fever: Geographical distribution. [Internet]; [updated 2011 December 1, cited 2011 December 12]. Available at: http://www.who.int/csr/disease/yellowfev/ impact1/en/.
http://www.who.int/csr/disease/yellowfev...
,505 Barrett ADT, Higgs S. Yellow fever: a disease that has yet to be conquered. Ann Rev Entomol 2007; 52:209-229.. In the urban cycle of YF, humans are the only known vertebrate host of the virus, and it is transmitted by the vector Aedes (Stegomyia) aegypti Linnaeus, 1762606 Tauil PL. Aspectos críticos do controle da febre amarela no Brasil. Rev Saude Publica 2010; 44:555-558.. In contrast, sylvatic YF is primarily associated with nonhuman primates (NHP), and its vectors are female mosquitoes of the genus Haemagogus Williston, 1876, Sabethes Robineau-Desvoidy 1827 and Aedes Meigen 1818 in South and Central America707 Dégallier N, Travassos-da-Rosa APA, Hervé JP, Travassos-da-Rosa JFS, Vasconcelos PFC, Mangabeira-da-Silva CJ, et al. A comparative study of yellow fever in Africa and South America. Braz J Assoc Advanc Science 1992; 44:143-161.,808 Forattini OP. Culicidologia Médica: identificação, biologia e epide-miologia. Vol. 2. São Paulo: EDUSP; 2002..

According to Tauil909 Tauil PL, Santos JB, Moraes MAP. Febre Amarela. In: Coura JR, editor. Dinâmica das doenças infecciosas e parasitárias. Rio de Janeiro: Ed. Guanabara; 2005. p. 1755-1765, Brazil is the country with the largest endemic area of sylvatic YF in the world, at approximately 5 million km202 Mathers CD, Lopez AD, Murray CJL. The burden of disease and mortality by condition: data, methods and results for 2001. In: Lopez AD, Mathers CD, Ezzati M, Jamison DR, Murray CJL, editors. Global burden of disease and risk factors. New York: Oxford University Press/The World Bank. 2006. p. 45-240.. Between the years 2000 and 2009, a total of 320 human cases of YF, including 152 deaths, were recorded in 15 states. Between 2007 and 2009, outbreaks of sylvatic YF and epidemics in the NHP population occurred in several Brazilian states, primarily in the extra-Amazonian region1010 Gomes AC, Torres MAN, Paula MB, Fernandes A, Marassá AM, Consales CA, et al. Ecologia de Haemagogus e Sabethes (Diptera: Culicidae) em áreas epizoóticas do vírus da febre amarela, Rio Grande do Sul, Brasil. Epidemiol Serv Saude 2010; 19:101-113.,1111 Araújo FAA, Ramos DG, Santos AL, Passos PHO, Elkhoury ANSM, Costa ZGA, et al. Epizootias em primatas não humanos durante reemergência do vírus da febre amarela no Brasil, 2007 a 2009. Epidemiol Serv Saude 2011; 20:527-536..

During the last outbreak (2007-2008) in the Federal District (FD), 90 human cases of YF were suspected, 15 of which were confirmed to be sylvatic YF: two were in 2007 (one was autochthonous) (SINAN-net), and 13 were in 2008 (six were autochthonous)1212 Secretaria de Estado de Saúde do Distrito Federal. Diretoria de Vigilância Epidemiológica. Informativo Epidemiológico (malária, febre amarela, esquistossomose, febre maculosa, DCA e DCJ) Ano 2, nº 2 - Julho de 2012.. [Internet]; [updated 2013 July 1, cited 2013 July 10]. Available at: http://www.saude.df.gov.br/outros-links/437-informes-epidemiologicos-malaria-febre-amarela-esquistossomose-febre-maculosa-dca-e-dcj.html/.
http://www.saude.df.gov.br/outros-links/...
. During the same period, the deaths of several NHP cases were reported, three of which were attributed to YF1111 Araújo FAA, Ramos DG, Santos AL, Passos PHO, Elkhoury ANSM, Costa ZGA, et al. Epizootias em primatas não humanos durante reemergência do vírus da febre amarela no Brasil, 2007 a 2009. Epidemiol Serv Saude 2011; 20:527-536.. Entomological investigations discovered mosquitoes related to the transmission of this arbovirus, and the YF virus was isolated from Haemagogus (Haemagogus) janthinomys Dyar, 1921 and Haemagogus (Conopostegus) leucocelaenus Dyar & Shannon, 19241313 Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463..

The Brasilia National Park (BNP) is a tourist destination that receives approximately 260,000 visitors a year. This preservation area contains populations of NHPs1414 Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) [Internet]; [updated 2012 January 2, cited 2012 January 10]. Available at: http://www.icmbio.gov.br/portal/o-que-fazemos/visitacao/ucs-abertas-a-visitacao/213-parque-nacional-de-brasilia.
http://www.icmbio.gov.br/portal/o-que-fa...
and mosquitoes of the genus Sabethes and Haemagogus1313 Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463.,1515 Santos JP, Obara MT, Cavalcante KLRJ, Steinke E. Culicídeos encontrados em áreas próximas à piscina velha do Parque Nacional de Brasília, DF. Rev Bras Geogr Med Saude 2008; 3:157-162.. It is noteworthy that during the outbreak of sylvatic YF that occurred between 2007 and 2008 in the FD, multiple NHPs died in the BNP1313 Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463.,1515 Santos JP, Obara MT, Cavalcante KLRJ, Steinke E. Culicídeos encontrados em áreas próximas à piscina velha do Parque Nacional de Brasília, DF. Rev Bras Geogr Med Saude 2008; 3:157-162.. Therefore, it is important to understand the ecological aspects of the mosquito species in the BNP, with an emphasis on the YF potential vectors. Moreover, the detection of flaviviruses in mosquitoes captured in this conservation unit is important information for the surveillance of this arbovirus in the FD.

In this context, the objectives of the present study were the following: I) to analyze the richness and abundance of the mosquitoes captured during different seasons in different strata of the gallery forest of the BNP, with an emphasis on potential YF vectors; and II) to determine the percentage of the captured mosquitoes that are infected with a flavivirus.

METHODS

Study area

The FD is located in the Central-West region of Brazil between the parallels 15º 30' and 16º 03' south latitude and the meridians 47º 25' and 48º 12' west longitude, within the Cerrado biome. The average annual temperature ranges from 18ºC to 22ºC. The average annual rainfall varies between 1,200mm and 1,700mm1616 Silva JMC, Felfili JM, Nogueira PE, Rezende AV. Análise florística das Matas de Galeria no Distrito Federal. In: Ribeiro JF, editor. Cerrado: Matas de Galeria. Brasília: Embrapa; 1998. p. 53-84., but it is unevenly distributed over the year, with a well-defined dry season. The monthly distribution of rainfall accumulated in the FD can be grouped into four quarterly periods. The months between June and August register an average rainfall of zero (the dry period). In April, May and September, there is an average rainfall of 70mm (the intermediate period). Between October and December, an average rainfall of 216mm is observed (the first quarter of rainfall), and between January and March, an average rainfall of 220mm is observed (the second quarter of rainfall)1717 Instituto Nacional de Meteorologia (INMET) [Internet]; [updated 2012 Marh 1, cited 2011 March 26]. Available at: http://www.inmet.gov.br/html/clima/graficos/plotGraf.php?chklist=2%2C&capita=brasilia%2C&peri=99%2C&per6190=99&precipitacao=2&brasilia=16&Enviar=Visualizar/.
http://www.inmet.gov.br/html/clima/grafi...
.

The BNP, which is administered by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), is an approximately 42,389-hectare environmental conservation area that contains a great diversity of flora and fauna. This park is also a leisure option for residents of the City of Brasilia, and its pools serve as the main attractions. The BNP is situated in the northwestern portion of the FD, approximately 10 km from the city center1414 Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) [Internet]; [updated 2012 January 2, cited 2012 January 10]. Available at: http://www.icmbio.gov.br/portal/o-que-fazemos/visitacao/ucs-abertas-a-visitacao/213-parque-nacional-de-brasilia.
http://www.icmbio.gov.br/portal/o-que-fa...
and just 2km from the Setor Habitacional Noroeste (SHN), whose construction began at the end of 20091818 Companhia Imobiliária de Brasília (TERRACAP). [Internet]; [updated 2012 Marh 1, cited 2012 March 10]. Available at: http://www.terracap.df.gov.br/internet/index.php?sccid=35&ctuid=479.
http://www.terracap.df.gov.br/internet/i...
.

Two capture areas in the gallery forest near the old pool of the BNP were chosen, with a distance of 200m from one another (Area 1 coordinates: latitude 15° 44'13.5"S and longitude 47° 55' 37.6"W; Area 2 coordinates: latitude 15° 44'18.6"S and longitude 47° 55'41.6"W). The choice of these areas was based on the presence of suitable trees for the construction of platforms. In each area, a platform was built 6m above the ground.

Mosquito capture

Mosquitoes were captured using entomological netting and manual aspirators1919 Ministério da Saúde. Secretaria de Vigilância em Saúde. Nota técnica Nº 59/2011. Recomendações de priorização das atividades de investigação entomológica e padronização dos métodos de coleta de amostras para diagnóstico laboratorial de Febre Amarela. [Internet]; [updated 2012 May 1, cited 2012 May 28]. Available at: http://portal.saude.gov.br/ portal/arquivos/pdf/nt_59_2011_in_entm_fbr_amarl_corr_02_01_2012.pdf.
http://portal.saude.gov.br/ porta...
. From September 2010 to August 2011, adult mosquitoes were captured each month for five consecutive days from 9a.m. to 3p.m. with a one hour interval between noon and 1p.m., for a total capture effort of 60 days. Entomological capture is a routine activity of the Diretoria de Vigilância Ambiental em Saúde do Distrito Federal (DIVAL) and was performed by health agents who were properly immunized and trained for this purpose. Using proper safety procedures and personal protective equipment, two individuals worked simultaneously in each sampling area; one on the ground and another on the platform 6m above the ground.

Mosquito identification

At the end of the daily activities, the captured specimens were taken to the DIVAL's entomology laboratory and anesthetized by cooling to -6°C. The specimens were transferred to labeled tubes and kept in liquid nitrogen.

The captured mosquitoes were identified with the aid of the dichotomous keys available from Consoli and Lourenço-de-Oliveira2020 Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p. and Forattini808 Forattini OP. Culicidologia Médica: identificação, biologia e epide-miologia. Vol. 2. São Paulo: EDUSP; 2002.. The identification occurred on a cold table at -26°C with the aid of a stereoscopic microscope (Olympus Optical CO., Tokyo, Japan). After identification, the mosquitoes were divided into 302 batches according to species and capture area and stored in liquid nitrogen. Subsequently, the mosquitoes were sent to the Laboratório Central de Saúde Pública (LACEN) of the FD for flavivirus isolation.

Virus isolation

The technique used to isolate the flaviviruses from the mosquitoes in LACEN/DF is based on the sensitivity of Aedes albopictus Skuse, 1864 cells (clone C6/36) to several flaviviruses21. To cultivate these cells, cell culture bottles containing Leibovitz L-15 (r) medium were used.

Each batch contained between 1 and 20 specimens of a single mosquito species. Each batch was homogenized in Eppendorf tubes with an antibiotic solution containing penicillin, streptomycin and amphotericin B and then individually inoculated into culture tubes containing C6/36 cells, which were maintained in an incubator at 24°C to 25°C for approximately eight days. Once grown, the inoculated cells were observed daily using an inverted optical microscope to visualize any possible cytopathic effects. Confirmation of viral infection was obtained by indirect immunofluorescence with polyclonal flavivirus antibodies2222 Gubler DJ, Kuno G, Sather E, Valez M, Olivre A. Mosquito cell cultures and specific monoclonal antibodies in surveillance for dengue viruses. Am J Trop Med Hyg 1984; 33:158-165..

Data analysis

To verify sampling sufficiency, the species accumulation curve was analysed2323 Gotelli N, Colwell R. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 2001; 4:379-391.,2424 Cardoso JC, Paula MB, Fernandes A, Santos E, Almeida MAB, Fonseca DF, et al. Ecological aspects of mosquitoes (Diptera: Culicidae) in an Atlantic Forest area on the North coast of Rio Grande do Sul State, Brazil. J Vector Ecol 2011; 36:175-186.. The species constancy during the sampling was assessed by the formula C%=(p/N).100, where p=the number of sampling occasions in which a species was captured and N=the total number of captures. The species were then grouped into constancy categories, such as constant (C>50%), accessory (C>25-50%) and accidental (C<25%)2525 Silveira Neto S, Nakano O, Barbin D, Nova NAV. Manual de ecologia dos insetos. São Paulo: CERES; 1976.. To determine the categories of dominance, the classification established by Friebe26 was determined using the formula D%=(i/t).100, where i=the total number of individuals in the species and t=the total number of individuals captured. Thus, the established categories were eudominant (D>10%), dominant (D>5-10%), subdominant (D 2-5%), eventual (D 1-2%) and rare (D<1%).

To measure the mosquito diversity patterns, the indices of Shannon-Wiener diversity, Shannon-Wiener evenness and Berger Parker dominance were used. Data analysis was performed using the program Diversidade de Espécies (DivEs), version 2.02727 Rodrigues WC. DivES - Diversidade de espécies. Versão 2.0. Software e Guia do Usuário - 2005. [Internet]; [updated 2012 March 1, cited 2011 March 25]. Available at: http://www.ebras.vbweb.com.br.
http://www.ebras.vbweb.com.br...
.

The variation in the number of mosquitoes caught between rainfall periods (dry, intermediate, first rainfall quarter and second rainfall quarter) was analyzed using the Kruskal-Wallis test. In this analysis, we considered the daily abundance of seven species captured in the study to be the dependent variable. The daily occurrence of these species on the ground and in the canopy over the 60-day period was compared using chi-squared tests. The tests were performed in the Statistica(r) program, with significance set at 5%.

RESULTS

Between September 2010 and August 2011, 2,677 female mosquitoes belonging to the Culicinae (n=2,607, 97.4%) and Anophelinae (n=70, 2.6%) subfamilies were captured in the BNP. The Culicinae fauna included specimens of 10 genera and 25 species (Table 1). In total, 1,848 (69%) mosquitoes were captured at ground level.

According to the species accumulation curve (Figure 1), the overall sampling effort (60 days) was satisfactory to represent the species richness, indicating a trend towards stabilization of the number of accumulated species from the 54th day.

FIGURE 1
- Species richness curve of mosquitoes captured between September 2010 and August 2011 at Brasilia National Park, Federal District, Brazil.
TABLE 1
- Number of mosquitoes captured in the different strata (ground and canopy) and the classifications of dominance and the constancy of species at Brasilia National Park, Federal District, Brazil, from September 2010 to August 2011.

The most abundant species were Sabethes (Sabethes) albiprivus Theobald, 1903; Limatus durhamii Theobald, 1901; Haemagogus (Conopostegus) leucocelaenus Dyar & Shannon, 1924; Haemagogus (Haemagogus) janthinomys Dyar, 1921; Aedes (Ochlerotatus) scapularis Rondani, 1848; Psorophora (Janthinosoma) ferox Von Humboldt, 1819; and Aedes (Ochlerotatus) serratus Theobald, 1901. Together, these seven species accounted for 86.4% of the total number of mosquitoes captured. The other species were represented by few individuals, and six species were represented by a single specimen (Figure 2).

FIGURE 2
- Abundance distribution curve of mosquitoes captured between September 2010 and August 2011 at Brasilia National Park, Federal District, Brazil.

The seven most abundant species were also classified as constant. Five species were classified as accessories, and 17 others were classified as accidental. It was also observed that, in terms of dominance, only three species were eudominant (Sa. albiprivus, Li. durhamii and Hg. leucocelaenus). Another three were dominant (Hg. janthinomys, Ae. scapularis and Ps. ferox), four were subdominant (Ae. serratus, Cq. arribalzagae, Anopheles kompi and Sa. belisarioi), two were classified as eventual and all of the others were considered rare (Table 1).

*Dom: dominance; **Const: constancy; Rr: rare (D<1%); Ac: accidental (C<25%); D: dominant (D>5-10%); C: constant (C>50%); Sd: subdominant (D>2-5%); A: accessory (C>25-50%); Ev: eventual (D>1-2%); E: eudominant (D>10%).

With respect to the monthly distribution, the mosquito abundance was higher during the first and second quarter of rainfall. The largest number of mosquitoes at both the canopy and ground levels was captured during the first quarter of rainfall (Table 2).

TABLE 2
Rainfall classes and number of mosquitoes captured at both the canopy and ground levels in the gallery forest of Brasilia National Park, Federal District, Brazil, from September 2010 to August 2011.

The highest diversity (H'=0.961), evenness (J=0.671) and richness (N=27) of mosquito species were detected at ground level. The Berger-Parker dominance index was similar for the ground (Dbp=0.034) and the canopy (Dbp=0.035). For the different rainfall classes, we observed a greater richness during the second quarter of rainfall (N=21). The greatest evenness was observed during the intermediate period (J=0.820), and the highest level of dominance was observed during the dry season (Dbp=0.147).

The number of captured specimens differed statistically according to rainfall period for Li. durhamii (Kruskal-Wallis H 3,60=35.2, p<0.01), Hg. leucocelaenus (Kruskal-Wallis H3.60=41.1, p<0.01), Hg. janthinomys (Kruskal-Wallis H3.60=37.6, p<0.01), Sabethis albiprivus (Kruskal-Wallis H3.60=37.4, p<0.01), Ps. ferox (Kruskal-Wallis H3.60=18.6, p < 0.01) and Ae. serratus (Kruskal-Wallis H3.60=17.5, p<0.01). These species were more abundant during the rainy quarters. During the dry season, the potential YF vectors exhibited very low frequency and abundance, with the exception of Ae. scapularis and Ae. serratus.

Significant differences were detected between the occurrence of mosquitoes on the ground and in the canopy for the species Hg. janthinomys2=4.9, p=0.02), Li. durhamii2=4.0, p=0.04), Ps. ferox (χ2=3.9, p=0.04), Ae. scapularis2=12.1, p<0.01) and Ae. serratus2=24.4, p<0.01). Except for Hg. janthinomys, these species were more frequent on the ground. With respect to the monthly abundance of these mosquitoes, it was observed that Hg. janthinomys was more abundant in the canopy, in contrast to the other species (Figure 3).

FIGURE 3
Number of mosquitoes of species that are potential vectors of YF in Brasilia National Park, Federal District, Brazil, on the ground and in the canopy between September 2010 and August 2011. Only the most abundant species (>100 individuals captured) are listed. Hg.: Haemagogus; Ae.: Aedes ; Sa.: Sabethes; Ps.: Psorophora; YF: yellow fever.

None of the 302 batches of mosquitoes (N=2,677) sent to the Virology Laboratory-LACEN/DF for arbovirus isolation tested positive for flaviviruses.

DISCUSSION

The present study shows that the abundance and species richness of mosquitoes in the gallery forest of the BNP are higher on the ground and during the rainy season. Even species with recognized acrodendrophilic habits, such as Hg. janthinomys, were captured on the ground; these results are similar to those of Alencar et al.2828 Alencar J, Lorosa ES, Dégallier N, Serra-Freire NM, Pacheco JB, Guimarães AE. Feeding patterns of Limatus durhamii (Diptera: Culicidae) in different regions of Brazil. J Med Entomol 2005; 42: 981-985. and Ramirez et al.2929 Ramírez P, John E, Yanoviak SP, Lounibos LP. Distribución vertical de Limatus durhamii (Dyar) (Diptera: Culicidae) en bosques de la amazonía peruana. Rev Peru Med Exp Salud Publica 2007; 24: 40-45.. These results indicate that precipitation is a crucial factor explaining the richness and abundance of Culicidae fauna in the gallery forests of the Cerrado, as has already been observed in other Brazilian biomes808 Forattini OP. Culicidologia Médica: identificação, biologia e epide-miologia. Vol. 2. São Paulo: EDUSP; 2002.,3030 Julião GR, Abad-Franch R, Lourenço-de-Oliveira R, Luz SLB. Measuring mosquito diversity patterns in an Amazonian terra firme rain forest. J Med Entomol 2010; 47:121-128.,3131 Ribeiro ALM, Miyazaki MS, Zeilhofer P. Spatial and temporal abundance of three sylvatic yellow fever vectors in the influence area of the Manso hydroelectric power plant, Mato Grosso, Brazil. J Med Entomol 2012; 49:223-226..

Among the species identified in the BNP, 11 have been previously found to be naturally infected with the YF virus: Ae. aegypti, Ae. scapularis, Ae. serratus, Ps. albipes, Ps. ferox, Hg. leucocelaenus, Hg. janthinomys, Hg. tropicalis, Sa. chloropterus, Sa. soperi and Sa. albiprivus 1313 Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463.,2020 Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p.,3232 Ministerio de Salud y Ambiente Argentina. Instituto Nacional de Enfermedades Virales Humanas. Informe Anual 2009 - 2010. Pergamino: Ministerio de Salud y Ambiente; 2011.

33 Ministério da Saúde. Secretaria de Vigilância em Saúde Guia de vigilância epidemiológica. Ministério da Saúde. 7th ed. Brasília: Ministério da Saúde; 2009.

34 Cardoso JC, Almeida MAB, Santos E, Fonseca DF, Sallum MAM, ?Noll CA, et al. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis 2010; 16:1918-1924.

35 Mondet B, Vasconcelos PFC, Travassos-da-Rosa APA, Rodrigues SG, Travassos-da-Rosa JFS, Bicout DJ. Isolation of yellow fever virus from nulliparous Haemagogus (Haemagogus) janthinomys in western Amazonian. Vector Borne Zoonotic Dis 2002; 2:47-50.
-3636 Vasconcelos PFC, Sperb AF, Monteiro HAO, Torres MAN, Souza MRS, Vasconcelos HB, et al. Isolations of yellow fever from Haemagogus leucocelaenus in Rio Grande do Sul, Brazil in the Southern Cone. Trans R Soc Trop Med Hyg 2003; 97:60-62.
. Moreover, the natural infection of Hg. janthinomys and Hg. leucocelaenus by the YF virus has been previously reported in the administrative region of São Sebastião, FD1313 Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463.. However, none of the 302 batches of 2,677 mosquitoes examined were infected with flaviviruses. This may be because of a low rate of infection among primates in the BNP, as this work was conducted during the interepidemic period. Furthermore, the infection of mosquitoes by the YF virus tends to be low, even in areas of YF outbreaks. The results of Cardoso et al.3434 Cardoso JC, Almeida MAB, Santos E, Fonseca DF, Sallum MAM, ?Noll CA, et al. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis 2010; 16:1918-1924. reinforce this hypothesis, showing that Hg. leucocelaenus and Ae. serratus in YF outbreak areas have minimum infection rates of 3.70 and 1.88, respectively.

Three specimens of Ae. aegypti were detected in the gallery forest of the BNP. The occurrence of this species in urban environments has been widely reported3737 Braga IA, Valle D. Aedes aegypti: histórico do controle no Brasil. Epidemiol Serv Saude 2007; 16:113-118.; however, the occurrence of Ae. aegypti in sylvatic environments is rare. Barbosa et al.3838 Barbosa MGV, Fé NF, Marcião AHR, Silva APT, Monteiro WM, Guerra MVF, et al. Registro de Culicidae de importância epidemiológica na área rural de Manaus, Amazonas. Rev Soc Bras Med Trop 2008; 41:658-663. and Soares et al.3939 Soares VARC, Rodrigues WC, Cabral MMO. Estudo de áreas e depósitos preferenciais de Aedes albopictus (Skuse, 1894) e Aedes aegypti (Linnaeus, 1762) no Município de Paracambi - Rio de Janeiro, Brasil. Entomobrasilis 2008; 1:63-68. reported the presence of this species in a rural area in the states of Amazonas and Rio de Janeiro. Tauil606 Tauil PL. Aspectos críticos do controle da febre amarela no Brasil. Rev Saude Publica 2010; 44:555-558. highlights the difficulty of identifying whether some cases of YF are transmitted by sylvatic or urban vectors. Considering that the sampling areas were located near recreational areas in the BNP, it is possible that the specimens of Ae. aegypti captured in the gallery forest were from artificial breeding sites. Future monitoring studies of mosquitoes in gallery forests may better clarify the occurrence of Ae. aegypti in sylvatic environments.

Environments that are still considered sylvatic are strongly influenced by the rapid urbanization process, in which population and housing growth generate anthropogenic changes that contribute to the establishment of mosquito species that are better adapted to the human environment4040 Forattini OP, Kakitani L, Marques GRAA, Brito M. Formas imaturas de anofelineos em recipientes artificiais. Rev Saude Publica 1998; 32:189-191.. The FD has undergone considerable environmental changes caused by the expansion of its urban area, which can change the behavior of the mosquito species present in the BNP. The occurrence of species that are adapted to urban anthropogenic environments, such as Ae. aegypti and Culex (Culex) quinquefasciatus Say, 1823, could be attributed to ecological changes that occurred with the construction of the Setor Habitacional Noroeste.

Aedes albopictus was also found during the survey. The ability of this species to transmit arboviruses has already been demonstrated4141 Gomes AC, Torres MAN, Gutierrez MFC, Lemos FL, Lima MLN, Martins JF, et al. Registro de Aedes albopictus em áreas epizoóticas de febre amarela nas Regiões Sudeste e Sul do Brasil (Diptera: Culicidae). Epidemiol Serv Saude 2008; 17:71-76.

42 Johson BW, Chambers TV, Crabtree MB, Filippis AMB, Vilarinhos PTR, Resende MC, et al. Vectors competence of Brazilian Aedes aegypti and Aedes albopictus for Brazilian yellow fever virus isolate. Trans R Soc Trop Med Hyg 2003; 96:611-613.
-4343 Lourenço-de-Oliveira R, Vazeille M, Filippis AMB, Failloux AB. Large genetic differentiation and low variation in vector competence for dengue and yellow fever viruses of Aedes albopictus from Brazil, the United States and Cayman Islands. Am J Trop Med Hyg 2003; 69:105-114.. It is noteworthy that Ae. albopictus has been documented as naturally infected with the virus that causes eastern equine encephalitis4444 Gerhardt RR, Gottfried KL, Apperson CL. First isolation of La Crosse virus from naturally infected Aedes albopictus. Emerg Infect Dis 2001; 7:807-811.,4545 Mitchell CJ. Vector competence of North and South American strains of Aedes albopictus for certain arboviruses: a review. J Am Mosq Control Assoc 1991; 7:446-451. and with dengue virus during an outbreak that occurred in Mexico4646 Ibañez-Bernal S, Briseño B, Mutebi JP, Argot E, Rodríguez G, Martínez-Campos C, et al. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 1997; 11:305-309.. Some authors admit the possibility that Ae. albopictus may become a vector that connects sylvatic and urban cycles of YF in Brazil2020 Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p.,3939 Soares VARC, Rodrigues WC, Cabral MMO. Estudo de áreas e depósitos preferenciais de Aedes albopictus (Skuse, 1894) e Aedes aegypti (Linnaeus, 1762) no Município de Paracambi - Rio de Janeiro, Brasil. Entomobrasilis 2008; 1:63-68.,4747 Miller BR, Ballinger ME. Aedes albopictus mosquitoes introduced into Brazil: vector competence for yellow fever and dengue viruses. Trans R Soc Trop Med Hyg 1988; 82:476-477.. Gomes et al.4141 Gomes AC, Torres MAN, Gutierrez MFC, Lemos FL, Lima MLN, Martins JF, et al. Registro de Aedes albopictus em áreas epizoóticas de febre amarela nas Regiões Sudeste e Sul do Brasil (Diptera: Culicidae). Epidemiol Serv Saude 2008; 17:71-76. and Albuquerque et al.4848 Albuquerque CMR, Melo-Santos MAV, Bezerra MAS, Barbosa RMR, Silva DF, Silva E. Primeiro registro de Aedes albopictus em área da Mata Atlântica, Recife, PE, Brasil. Rev Saúde Pública 2000; 34:314-315. point to the need to monitor this species in Brazil.

There are few studies related to the vertical distribution of mosquitoes in the Central-West Region of Brazil4949 Pinheiro FP, Travassos da Rosa APA, Moraes MAP. An epidemic of yellow fever in Central Brazil, 1972-1973. II. Ecological studies. Am J Trop Med Hyg 1981; 30:204-211.. In the present study, we detected a higher occurrence of Hg. janthinomys in the canopy, reinforcing the known acrodendrophilic behavior of this species2929 Ramírez P, John E, Yanoviak SP, Lounibos LP. Distribución vertical de Limatus durhamii (Dyar) (Diptera: Culicidae) en bosques de la amazonía peruana. Rev Peru Med Exp Salud Publica 2007; 24: 40-45.,5050 Pinto CS, Confalonieri UEC, Mascarenhas BM. Ecology of Haemagogus sp. and Sabethes sp. (Diptera: Culicidae) in relation to the microclimates of the Caxiuanã National Forest, Pará, Brazil. Mem Inst Oswaldo Cruz 2009; 104:592-598.. Specimens of Hg. leucocelaenus were very common on the ground. Forattini et al.5151 Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173. in São Paulo and Pinto et al.5050 Pinto CS, Confalonieri UEC, Mascarenhas BM. Ecology of Haemagogus sp. and Sabethes sp. (Diptera: Culicidae) in relation to the microclimates of the Caxiuanã National Forest, Pará, Brazil. Mem Inst Oswaldo Cruz 2009; 104:592-598. in Pará also reported the predominance of Hg. leucocelaenus on the ground. However, Guimarães et al.5252 Guimarães AE, Arle M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro, Brasil: II. Distribuição vertical. Mem Inst Oswaldo Cruz 1985; 80:171-185. showed that 74% of Hg. leucocelaenus specimens were captured in the canopy at the National Park of the Serra dos Orgãos, Rio de Janeiro. Ae. scapularis and Ae. serratus showed significant differences in habitat use and were more abundant on the ground. The same preference for these species to occur at ground level has also been observed by Fe et al.5353 Fé NF, Barbosa MGV, Fé FAA, Guerra MVF, Alecrim WD. Fauna de Culicidae em municípios da zona rural do Estado do Amazonas, com incidência de febre amarela. Rev Soc Bras Med Trop 2003; 36:343-348., Forattini et al.5151 Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173., Guimaraes et al.5252 Guimarães AE, Arle M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro, Brasil: II. Distribuição vertical. Mem Inst Oswaldo Cruz 1985; 80:171-185. and Julião et al.3030 Julião GR, Abad-Franch R, Lourenço-de-Oliveira R, Luz SLB. Measuring mosquito diversity patterns in an Amazonian terra firme rain forest. J Med Entomol 2010; 47:121-128.. Moreover, the highest occurrence of Ps. ferox at ground level was also observed by Forattini et al.5151 Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173..

There is evidence that vertical distribution differences between and within species depends upon the type of vegetation cover. Forattini et al.5151 Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173. suggested that a vertical distribution difference is most evident in tropical rain forests, where the trees are tall and dense. In less dense forests and in places with long dry seasons, these differences tend to decrease, as observed in the present study.

Other important factors influencing the vertical distribution of mosquitoes are vertical mobility and daily activity. According to Service5454 Service MW. Mosquitoes (Culicidae). In: Lane RP, Crosskey RW, editors. Medical insects and arachnids. London, United Kingdom: Chapman & Hall 1993. p. 120-240, mosquitoes can be attracted to a feeding source at a distance of seven to 30 meters. Forattini et al.5151 Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173. and Vasconcelos et al.5555 Vasconcelos PFC, Travassos-da-Rosa APA, Rodrigues SG, Travasso-da-Rosa ES, Monteiro HAO, Cruz ACR, et al. Yellow fever in Pará State, Amazon Region of Brazil, 1998-1999: entomologic and epidemiologic findings. Emerg Infect Dis 2001; 7:565-569. showed that even species that were predominantly active in the higher levels of the canopy, such as Hg. janthinomys, often move to ground level when they detect the presence of a feeding source. Moreover, Guimarães et al.5252 Guimarães AE, Arle M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro, Brasil: II. Distribuição vertical. Mem Inst Oswaldo Cruz 1985; 80:171-185. showed differences in the vertical distribution of An. cruzii captured at different periods of the day, with the highest number of specimens found in the canopy at night. Therefore, the vertical movement of mosquitoes can weaken the evidence of vertical stratification of species, and it obviously influences the dynamics of pathogen transmission3030 Julião GR, Abad-Franch R, Lourenço-de-Oliveira R, Luz SLB. Measuring mosquito diversity patterns in an Amazonian terra firme rain forest. J Med Entomol 2010; 47:121-128..

The effects of rainfall on the total abundance of mosquitoes captured were evident. There was a strong influence of rainfall on the annual cycle of the species of Sabethes and Haemagogus, which have eggs that are very resistant to desiccation and sometimes require repeated contact with water to hatch2020 Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p.. Similar situations related to these genera have been described in Mato Grosso3131 Ribeiro ALM, Miyazaki MS, Zeilhofer P. Spatial and temporal abundance of three sylvatic yellow fever vectors in the influence area of the Manso hydroelectric power plant, Mato Grosso, Brazil. J Med Entomol 2012; 49:223-226. and Tocantins5656 Silva JS, Pacheco JB, Alencar J, Guimarães AE. Biodiversity and influence of climatic factors on mosquitoes (Diptera: Culicidae) around the Peixe Angical hydroelectric scheme in the state of Tocantins, Brazil. Mem Inst Oswaldo Cruz 2010; 105:155-162.. Studies in southern Brazil10 and in Trinidad5757 Tikasingh ES, Hull B, Laurent E, Chadee DD. Entomological activities during the yellow fever epidemic in Trinidad, 1978-1980. Bull Soc Vect Ecol 1990; 15:41-47. also indicated a higher occurrence of Hg. leucocelaenus during the rainy months. The highest occurrence of A. scapularis, A. serratus and Ps. ferox in the rainy season is also in agreement with the literature2020 Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p..

The present study increases the information available regarding the ecology of important YF virus vectors in Central Brazil. Although seroepidemiological surveys indicate that YF control efforts have achieved good results5858 Machado VW, Vasconcelos PFC, Silva EVP, Santos JB. Serologic assessment of yellow fever immunity in the rural population of a yellow fever-endemic area in Central Brazil. Rev Soc Bras Med Trop 2013; 46:166-171., entomological monitoring is recommended in the BNP and in other areas that are susceptible to the transmission of the YF virus. We emphasize that the BNP is located 10km from the center of Brasília and 2km from the Setor Habitacional Noroeste, where many apartments are being constructed. Furthermore, there are houses located at the edge of a roadway that is very close to the park. Because the flying range of YF vectors can reach 500m5959 Reiter P, Amador MA, Anderson RA, Clark GG. Short report: dispersal of Aedes aegypti in an urban area after blood feeding as marked by rubidium marked eggs. Am J Trop Med Hyg 1995; 52:177-179., there is the possibility of sylvatic YF transmission to people who reside close to the BNP and to park visitors. This transmission would be more likely during periods of NHP epidemics, when the natural infection rate of mosquitoes tends to be higher3434 Cardoso JC, Almeida MAB, Santos E, Fonseca DF, Sallum MAM, ?Noll CA, et al. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis 2010; 16:1918-1924.. Although no viral isolates were obtained from the specimens captured in this study, studies related to the ongoing natural infection of mosquitoes is of paramount importance as a means of predicting events related to YF and other arboviruses. Such information will contribute to a better understanding of the true role of the vector species that occur within Central Brazil. It is also recommended that the relevant agencies give special attention to the deaths of NHPs and to the vaccination programs against YF for visitors to the BNP.

We would like to acknowledge the technicians at DIVAL for their dedication and commitment to implementing the captures and especially to Crispim Carvalho da Silva for the accuracy in the construction of the platforms and to Deusédimo Coelho Mesquita for performing the georeferencing of the capture areas. We would also like to acknowledge ICMBio and the entire team of environmental agents at the BNP for their support and for allowing this research to take place and Dr. Pedro Tauil and Dr. Marcos Takashi Obara for reviewing the manuscript.

REFERENCES

  • 01
    Marcondes CB. Entomologia Médica e Veterinária. São Paulo: Atheneu; 2011.
  • 02
    Mathers CD, Lopez AD, Murray CJL. The burden of disease and mortality by condition: data, methods and results for 2001. In: Lopez AD, Mathers CD, Ezzati M, Jamison DR, Murray CJL, editors. Global burden of disease and risk factors. New York: Oxford University Press/The World Bank. 2006. p. 45-240.
  • 03
    Vasconcelos PFC. Febre amarela: reflexões sobre a doença, as perspectivas para o século XXI e o risco de reurbanização. Rev Bras Epidemiol 2002; 5:244-258.
  • 04
    Organização Mundial de Saúde (OMS). Yellow fever: Geographical distribution. [Internet]; [updated 2011 December 1, cited 2011 December 12]. Available at: http://www.who.int/csr/disease/yellowfev/ impact1/en/.
    » http://www.who.int/csr/disease/yellowfev/ impact1/en/.
  • 05
    Barrett ADT, Higgs S. Yellow fever: a disease that has yet to be conquered. Ann Rev Entomol 2007; 52:209-229.
  • 06
    Tauil PL. Aspectos críticos do controle da febre amarela no Brasil. Rev Saude Publica 2010; 44:555-558.
  • 07
    Dégallier N, Travassos-da-Rosa APA, Hervé JP, Travassos-da-Rosa JFS, Vasconcelos PFC, Mangabeira-da-Silva CJ, et al. A comparative study of yellow fever in Africa and South America. Braz J Assoc Advanc Science 1992; 44:143-161.
  • 08
    Forattini OP. Culicidologia Médica: identificação, biologia e epide-miologia. Vol. 2. São Paulo: EDUSP; 2002.
  • 09
    Tauil PL, Santos JB, Moraes MAP. Febre Amarela. In: Coura JR, editor. Dinâmica das doenças infecciosas e parasitárias. Rio de Janeiro: Ed. Guanabara; 2005. p. 1755-1765
  • 10
    Gomes AC, Torres MAN, Paula MB, Fernandes A, Marassá AM, Consales CA, et al. Ecologia de Haemagogus e Sabethes (Diptera: Culicidae) em áreas epizoóticas do vírus da febre amarela, Rio Grande do Sul, Brasil. Epidemiol Serv Saude 2010; 19:101-113.
  • 11
    Araújo FAA, Ramos DG, Santos AL, Passos PHO, Elkhoury ANSM, Costa ZGA, et al. Epizootias em primatas não humanos durante reemergência do vírus da febre amarela no Brasil, 2007 a 2009. Epidemiol Serv Saude 2011; 20:527-536.
  • 12
    Secretaria de Estado de Saúde do Distrito Federal. Diretoria de Vigilância Epidemiológica. Informativo Epidemiológico (malária, febre amarela, esquistossomose, febre maculosa, DCA e DCJ) Ano 2, nº 2 - Julho de 2012.. [Internet]; [updated 2013 July 1, cited 2013 July 10]. Available at: http://www.saude.df.gov.br/outros-links/437-informes-epidemiologicos-malaria-febre-amarela-esquistossomose-febre-maculosa-dca-e-dcj.html/.
    » http://www.saude.df.gov.br/outros-links/437-informes-epidemiologicos-malaria-febre-amarela-esquistossomose-febre-maculosa-dca-e-dcj.html/
  • 13
    Obara MT, Monteiro H, Paula MB, Gomes AC, Yoshizawa MAC, Lira-Vieira AR, et al. Infecção natural de Limatus durhamii e Haemagogus leucocelaenus pelo vírus da Febre Amarela no Distrito Federal, Brasil. Epidemiol Serv Saude 2012; 21:457-463.
  • 14
    Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) [Internet]; [updated 2012 January 2, cited 2012 January 10]. Available at: http://www.icmbio.gov.br/portal/o-que-fazemos/visitacao/ucs-abertas-a-visitacao/213-parque-nacional-de-brasilia.
    » http://www.icmbio.gov.br/portal/o-que-fazemos/visitacao/ucs-abertas-a-visitacao/213-parque-nacional-de-brasilia
  • 15
    Santos JP, Obara MT, Cavalcante KLRJ, Steinke E. Culicídeos encontrados em áreas próximas à piscina velha do Parque Nacional de Brasília, DF. Rev Bras Geogr Med Saude 2008; 3:157-162.
  • 16
    Silva JMC, Felfili JM, Nogueira PE, Rezende AV. Análise florística das Matas de Galeria no Distrito Federal. In: Ribeiro JF, editor. Cerrado: Matas de Galeria. Brasília: Embrapa; 1998. p. 53-84.
  • 17
    Instituto Nacional de Meteorologia (INMET) [Internet]; [updated 2012 Marh 1, cited 2011 March 26]. Available at: http://www.inmet.gov.br/html/clima/graficos/plotGraf.php?chklist=2%2C&capita=brasilia%2C&peri=99%2C&per6190=99&precipitacao=2&brasilia=16&Enviar=Visualizar/.
    » http://www.inmet.gov.br/html/clima/graficos/plotGraf.php?chklist=2%2C&capita=brasilia%2C&peri=99%2C&per6190=99&precipitacao=2&brasilia=16&Enviar=Visualizar/
  • 18
    Companhia Imobiliária de Brasília (TERRACAP). [Internet]; [updated 2012 Marh 1, cited 2012 March 10]. Available at: http://www.terracap.df.gov.br/internet/index.php?sccid=35&ctuid=479.
    » http://www.terracap.df.gov.br/internet/index.php?sccid=35&ctuid=479
  • 19
    Ministério da Saúde. Secretaria de Vigilância em Saúde. Nota técnica Nº 59/2011. Recomendações de priorização das atividades de investigação entomológica e padronização dos métodos de coleta de amostras para diagnóstico laboratorial de Febre Amarela. [Internet]; [updated 2012 May 1, cited 2012 May 28]. Available at: http://portal.saude.gov.br/ portal/arquivos/pdf/nt_59_2011_in_entm_fbr_amarl_corr_02_01_2012.pdf.
    » http://portal.saude.gov.br/ portal/arquivos/pdf/nt_59_2011_in_entm_fbr_amarl_corr_02_01_2012.pdf
  • 20
    Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Fiocruz; 1994. 228p.
  • 21
    Igarashi A. Isolation of a Singh's Aedes albopictus cell clone sensitive to dengue and chikungunya viruses. J Gen Virol 1978; 40:531-544.
  • 22
    Gubler DJ, Kuno G, Sather E, Valez M, Olivre A. Mosquito cell cultures and specific monoclonal antibodies in surveillance for dengue viruses. Am J Trop Med Hyg 1984; 33:158-165.
  • 23
    Gotelli N, Colwell R. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 2001; 4:379-391.
  • 24
    Cardoso JC, Paula MB, Fernandes A, Santos E, Almeida MAB, Fonseca DF, et al. Ecological aspects of mosquitoes (Diptera: Culicidae) in an Atlantic Forest area on the North coast of Rio Grande do Sul State, Brazil. J Vector Ecol 2011; 36:175-186.
  • 25
    Silveira Neto S, Nakano O, Barbin D, Nova NAV. Manual de ecologia dos insetos. São Paulo: CERES; 1976.
  • 26
    Friebe B. Zur Biologie eines Buchenwaldbodens. Die Käferfauna. Carolinea 1983; 41:45-80.
  • 27
    Rodrigues WC. DivES - Diversidade de espécies. Versão 2.0. Software e Guia do Usuário - 2005. [Internet]; [updated 2012 March 1, cited 2011 March 25]. Available at: http://www.ebras.vbweb.com.br.
    » http://www.ebras.vbweb.com.br
  • 28
    Alencar J, Lorosa ES, Dégallier N, Serra-Freire NM, Pacheco JB, Guimarães AE. Feeding patterns of Limatus durhamii (Diptera: Culicidae) in different regions of Brazil. J Med Entomol 2005; 42: 981-985.
  • 29
    Ramírez P, John E, Yanoviak SP, Lounibos LP. Distribución vertical de Limatus durhamii (Dyar) (Diptera: Culicidae) en bosques de la amazonía peruana. Rev Peru Med Exp Salud Publica 2007; 24: 40-45.
  • 30
    Julião GR, Abad-Franch R, Lourenço-de-Oliveira R, Luz SLB. Measuring mosquito diversity patterns in an Amazonian terra firme rain forest. J Med Entomol 2010; 47:121-128.
  • 31
    Ribeiro ALM, Miyazaki MS, Zeilhofer P. Spatial and temporal abundance of three sylvatic yellow fever vectors in the influence area of the Manso hydroelectric power plant, Mato Grosso, Brazil. J Med Entomol 2012; 49:223-226.
  • 32
    Ministerio de Salud y Ambiente Argentina. Instituto Nacional de Enfermedades Virales Humanas. Informe Anual 2009 - 2010. Pergamino: Ministerio de Salud y Ambiente; 2011.
  • 33
    Ministério da Saúde. Secretaria de Vigilância em Saúde Guia de vigilância epidemiológica. Ministério da Saúde. 7th ed. Brasília: Ministério da Saúde; 2009.
  • 34
    Cardoso JC, Almeida MAB, Santos E, Fonseca DF, Sallum MAM, ?Noll CA, et al. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis 2010; 16:1918-1924.
  • 35
    Mondet B, Vasconcelos PFC, Travassos-da-Rosa APA, Rodrigues SG, Travassos-da-Rosa JFS, Bicout DJ. Isolation of yellow fever virus from nulliparous Haemagogus (Haemagogus) janthinomys in western Amazonian. Vector Borne Zoonotic Dis 2002; 2:47-50.
  • 36
    Vasconcelos PFC, Sperb AF, Monteiro HAO, Torres MAN, Souza MRS, Vasconcelos HB, et al. Isolations of yellow fever from Haemagogus leucocelaenus in Rio Grande do Sul, Brazil in the Southern Cone. Trans R Soc Trop Med Hyg 2003; 97:60-62.
  • 37
    Braga IA, Valle D. Aedes aegypti: histórico do controle no Brasil. Epidemiol Serv Saude 2007; 16:113-118.
  • 38
    Barbosa MGV, Fé NF, Marcião AHR, Silva APT, Monteiro WM, Guerra MVF, et al. Registro de Culicidae de importância epidemiológica na área rural de Manaus, Amazonas. Rev Soc Bras Med Trop 2008; 41:658-663.
  • 39
    Soares VARC, Rodrigues WC, Cabral MMO. Estudo de áreas e depósitos preferenciais de Aedes albopictus (Skuse, 1894) e Aedes aegypti (Linnaeus, 1762) no Município de Paracambi - Rio de Janeiro, Brasil. Entomobrasilis 2008; 1:63-68.
  • 40
    Forattini OP, Kakitani L, Marques GRAA, Brito M. Formas imaturas de anofelineos em recipientes artificiais. Rev Saude Publica 1998; 32:189-191.
  • 41
    Gomes AC, Torres MAN, Gutierrez MFC, Lemos FL, Lima MLN, Martins JF, et al. Registro de Aedes albopictus em áreas epizoóticas de febre amarela nas Regiões Sudeste e Sul do Brasil (Diptera: Culicidae). Epidemiol Serv Saude 2008; 17:71-76.
  • 42
    Johson BW, Chambers TV, Crabtree MB, Filippis AMB, Vilarinhos PTR, Resende MC, et al. Vectors competence of Brazilian Aedes aegypti and Aedes albopictus for Brazilian yellow fever virus isolate. Trans R Soc Trop Med Hyg 2003; 96:611-613.
  • 43
    Lourenço-de-Oliveira R, Vazeille M, Filippis AMB, Failloux AB. Large genetic differentiation and low variation in vector competence for dengue and yellow fever viruses of Aedes albopictus from Brazil, the United States and Cayman Islands. Am J Trop Med Hyg 2003; 69:105-114.
  • 44
    Gerhardt RR, Gottfried KL, Apperson CL. First isolation of La Crosse virus from naturally infected Aedes albopictus. Emerg Infect Dis 2001; 7:807-811.
  • 45
    Mitchell CJ. Vector competence of North and South American strains of Aedes albopictus for certain arboviruses: a review. J Am Mosq Control Assoc 1991; 7:446-451.
  • 46
    Ibañez-Bernal S, Briseño B, Mutebi JP, Argot E, Rodríguez G, Martínez-Campos C, et al. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 1997; 11:305-309.
  • 47
    Miller BR, Ballinger ME. Aedes albopictus mosquitoes introduced into Brazil: vector competence for yellow fever and dengue viruses. Trans R Soc Trop Med Hyg 1988; 82:476-477.
  • 48
    Albuquerque CMR, Melo-Santos MAV, Bezerra MAS, Barbosa RMR, Silva DF, Silva E. Primeiro registro de Aedes albopictus em área da Mata Atlântica, Recife, PE, Brasil. Rev Saúde Pública 2000; 34:314-315.
  • 49
    Pinheiro FP, Travassos da Rosa APA, Moraes MAP. An epidemic of yellow fever in Central Brazil, 1972-1973. II. Ecological studies. Am J Trop Med Hyg 1981; 30:204-211.
  • 50
    Pinto CS, Confalonieri UEC, Mascarenhas BM. Ecology of Haemagogus sp. and Sabethes sp. (Diptera: Culicidae) in relation to the microclimates of the Caxiuanã National Forest, Pará, Brazil. Mem Inst Oswaldo Cruz 2009; 104:592-598.
  • 51
    Forattini OP, Lopes OS, Rabello EX. Investigações sobre o comportamento de formas adultas de mosquitos silvestres no Estado de São Paulo, Brasil. Rev Saude Publica 1968; 2:111-173.
  • 52
    Guimarães AE, Arle M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro, Brasil: II. Distribuição vertical. Mem Inst Oswaldo Cruz 1985; 80:171-185.
  • 53
    Fé NF, Barbosa MGV, Fé FAA, Guerra MVF, Alecrim WD. Fauna de Culicidae em municípios da zona rural do Estado do Amazonas, com incidência de febre amarela. Rev Soc Bras Med Trop 2003; 36:343-348.
  • 54
    Service MW. Mosquitoes (Culicidae). In: Lane RP, Crosskey RW, editors. Medical insects and arachnids. London, United Kingdom: Chapman & Hall 1993. p. 120-240
  • 55
    Vasconcelos PFC, Travassos-da-Rosa APA, Rodrigues SG, Travasso-da-Rosa ES, Monteiro HAO, Cruz ACR, et al. Yellow fever in Pará State, Amazon Region of Brazil, 1998-1999: entomologic and epidemiologic findings. Emerg Infect Dis 2001; 7:565-569.
  • 56
    Silva JS, Pacheco JB, Alencar J, Guimarães AE. Biodiversity and influence of climatic factors on mosquitoes (Diptera: Culicidae) around the Peixe Angical hydroelectric scheme in the state of Tocantins, Brazil. Mem Inst Oswaldo Cruz 2010; 105:155-162.
  • 57
    Tikasingh ES, Hull B, Laurent E, Chadee DD. Entomological activities during the yellow fever epidemic in Trinidad, 1978-1980. Bull Soc Vect Ecol 1990; 15:41-47.
  • 58
    Machado VW, Vasconcelos PFC, Silva EVP, Santos JB. Serologic assessment of yellow fever immunity in the rural population of a yellow fever-endemic area in Central Brazil. Rev Soc Bras Med Trop 2013; 46:166-171.
  • 59
    Reiter P, Amador MA, Anderson RA, Clark GG. Short report: dispersal of Aedes aegypti in an urban area after blood feeding as marked by rubidium marked eggs. Am J Trop Med Hyg 1995; 52:177-179.

Publication Dates

  • Publication in this collection
    15 Oct 2013

History

  • Received
    05 July 2012
  • Accepted
    01 Oct 2013
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