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Immature Aedes mosquitoes colonize Culex quinquefasciatus breeding sites in neighborhoods in the municipality of Olinda, State of Pernambuco

Abstract

Introduction

The present study shows the colonization of Aedes mosquitoes in breeding sites specific for Culex quinquefasciatus in neighborhoods in the municipality of Olinda.

Methods

Samples were collected between May 2011 and June 2012 from breeding sites positive for Cx. quinquefasciatus by using a ladle and manual suction pump.

Results

Aedes aegypti (0.12%), Aedes albopictus (0.03%), and Cx. quinquefasciatus (99.8%) were found across the breeding sites.

Conclusions

The presence of Aedes ssp. in several Cx. quinquefasciatus breeding sites with a heavy load of organic material demonstrates the need to review the concepts and methods used for treatment, as the use of specific larvicide for breeding sites of Culex.

Aedes aegypti ; Colonization; Breeding


The control of urban mosquito populations, especially those of Aedes aegypti Linnaeus (1762), Aedes albopictus Skuse (1894), and Culex quinquefasciatus Say (1823) (Diptera: Culicidae), is necessary because of the involvement of these species in the transmission of human pathogens such as dengue, yellow fever, chikungunya, the Zika virus, filariasis, West Nile virus, and encephalitis, which cause discomfort to human beings and impact quality of life1. Powell JR, Tabachnick WJ. History of domestication and spread of Aedes aegypti - A Review. Mem Inst Oswaldo Cruz 2013; 108:11-17.,2. Zinser M, Ramberg F, Willott E. Culex quinquefasciatus (Diptera: Culicidae) as a potential West Nile virus vector in Tucson, Arizona: blood meal analysis indicates feeding on both humans and birds. J Insect Sci 2004; 4:3..

The selection of breeding sites for egg-laying may be associated with factors present in the water, such as organic material, chemical compounds, and the presence of immature, among others3. Barbosa RMR, Regis L, Vasconcelos RL, Leal WS. Culex mosquitoes (Diptera: Culicidae) egg laying in traps loaded with Bacillus thuringiensis variety israelensis and baited with skatole. J Med Entomol 2010; 47:345-348.. Under present conditions, the abundance of egg-laying sites for mosquitoes in cities complicates the monitoring of these insects and makes proper inspection impossible, frustrating efforts to reduce population densities, especially in the case of Aedes ssp.

Given the importance of developing new strategies for combating mosquito vectors, the present study aimed to identify the colonization of Ae. aegypti in breeding sites positive for Cx. quinquefasciatus in neighborhoods with high and low infestation in the municipality of Olinda, which forms part of the Metropolitan Region of Recife, in the Brazilian State of Pernambuco.

Samples were collected between May 2011 and June 2012. The Municipality of Olinda is located at latitude 8°0′48″S and longitude 34°50′42″W, 6km Northeast of Recife, the capital of Pernambuco. The municipality has an area of 41,681km2 and an estimated population of 377,779 inhabitants4. Instituto Brasileiro de Geografia e Estatística (IBGE). População e domicílios. Censo 2010. [Cited July 10 2010] Available at: www.ibge.gov.br/.
www.ibge.gov.br/...
. This region is divided into 33 neighborhoods, grouped into two Sanitary Districts (I and II). The study investigated Cx. quinquefasciatus breeding sites located in the neighborhoods of Sanitary District I (Caixa d'Água, Passarinho, Águas Compridas, Aguazinha, Peixinhos, Alto da Conquista, Alto do Sol Nascente, Alto da Bondade, Sapucaia, São Benedito, Vila Popular, Jardim Brasil, Salgadinho, and Sítio Novo), and strata with high and low infestation with Ae. aegypti were selected using the Rapid Aedes aegypti Survey Index [LIRAa/2011- Olinda Environmental Surveillance Center - Centro de Vigilância Ambiental de Olinda (CEVAO)].

All Culex quinquefasciatus breeding sites identified during the study possessed water with organic matter (decomposing plant and animal debris) content and little to no movement. These environmental conditions are conducive to the development of the immature stages of the species5. Ministério da Saúde. Secretaria de Vigilância em Saúde, Departamento de Vigilância Epidemiológica. Guia de vigilância do Culex quinquefasciatus, Coordenação: Francisco Anilton Alves Araújo, Marcelo Santalucia, 3a ed. Brasília: MS; 2011.. The breeding sites were identified and registered according to location and structural conditions. The density of larvae and pupae (DLP) was estimated using five samples from each site, four in the corners and one in the center, for restricted environments such as tanks. In larger environments, such as ditches and canals, samples were collected only from the edges, with a sample taken every 3m on alternate sides when the site length was between 20 and 50m and every 5m when the site length was over 50m6. Fundação Nacional de Saúde (FUNASA). Controle de Vetores. Procedimentos de Segurança. Brasília: FUNASA; 2001.. Samples were initially collected using a ladle, but this apparatus was replaced in the course of the study by a manual suction pump, which could more easily obtain the immature specimens at the bottoms of the breeding sites.

All collected samples were placed in plastic containers (250ml) and taken to the Entomology Laboratory of the Olinda Center for Environmental Surveillance for counting and species identification. In the laboratory, the collected larvae and pupae were placed in test tubes in 70°GL ethanol for identification. The culicids were identified according to external morphological characteristics on a slide under a stereoscopic microscope, using dichotomous keys described in the literature7. Forattini OP. Culicidologia Médica: Identificação, Biologia, Epidemiologia. Vol. II, São Paulo: Editora da Universidade de São Paulo; 2002.. The numbers of immature individuals at each breeding site were compared using simple analysis of variance (ANOVA). The analyses were made in Statistica 7.0 (StatSoft) at a significance level of 5%.

A total of 11,006 immature culicid specimens were collected, of which 9,129 (82.9%) larvae and 1,861 (16.9%) pupae were of Cx. quinquefasciatus, 12 (0.11%) larvae and 1 (0.01%) pupa were of Ae. aegypti, and 3 (0.03%) larvae were of Ae. albopictus (Table 1).

TABLE 1
Total number of larvae and pupae collected from different breeding sites in the 14 neighborhoods of Sanitary District I, Olinda, State of Pernambuco, 2012.

All breeding sites were positive for Cx. quinquefasciatus, including waterholes, canals, channels, drains, junction boxes, inspection tanks, water tanks, and ditches. The numbers of immature Cx. quinquefasciatus found in these different types of breeding site did not differ (p > 0.05). Four sites tested positive for Aedes ssp.: a waterhole, junction box, inspection tank, and ditch (Table 1). The numbers of immature Ae. aegypti [F (7,93) = 3.1570] and Ae. albopictus [F(7,93) = 3.1570] were both significantly different (p < 0.05) in the different breeding sites. Table 2 shows that of the 14 neighborhoods inspected, only 4 contained breeding sites that tested positive for Aedes ssp. (Caixa d'Água, Passarinho, Peixinhos, and Vila Popular).

TABLE 2
Total number of Aedes ssp. larvae and pupae collected at different breeding sites located in the neighborhoods of Peixinhos, Passarinho, Caixa d'Água, and Vila Popular, Olinda, State of Pernambuco, 2012.

Culex quinquefasciatus, the predominant species found among the breeding sites, prefers to lay its eggs in sites with heavy loads of organic matter, and its genetic and ecological adaptations ensure its greater survival in anthropogenic environments8. Lopes J. Mosquito (Diptera: Culicidae) ecology of natural and artificial rural breeding places in northern Parana, Brazil. V. Larvae captured in artificial reservoirs installed in ciliary forest. Rev Saude Publica 1997; 31:370-377..

Aedes aegypti, described as a wild species that originated in Africa, has undergone changes and adaptations in egg-laying behavior over time, as it has accompanied the constant global evolution of human habitation1. Powell JR, Tabachnick WJ. History of domestication and spread of Aedes aegypti - A Review. Mem Inst Oswaldo Cruz 2013; 108:11-17.. Aedes albopictus is a wild species that originated in Asia, has adapted to the urban environment, and is currently found in many different artificial and natural receptacles9. Forattini OP, Marques GRAM, Kakitani I, Brito M, Sallum MAM. Significado epidemiológico dos criadouros de Aedes albopictus em bromélias. Rev Saude Publica 1998; 32:186-188.. Inadequate disposal of receptacles capable of retaining water has facilitated the development of mosquito groups with the genetic flexibility to develop in these artificial habitats8. Lopes J. Mosquito (Diptera: Culicidae) ecology of natural and artificial rural breeding places in northern Parana, Brazil. V. Larvae captured in artificial reservoirs installed in ciliary forest. Rev Saude Publica 1997; 31:370-377..

Aedes aegypti is capable of laying groups of eggs in any receptacle in which water can accumulate1010 . Regis L, Silva SB, Melo-Santos MAV. Developing new approaches for detecting and preventing Aedes aegypti population outbreaks: basis for surveillance, alert and control system. Mem Inst Oswaldo Cruz 2008; 103:50-59.. Other biological features of this species, such as its high fertility and fecundity rate, short life cycle, capacity to adapt to environmental changes, and the resistance of its eggs to water, have also contributed to its rapid population growth1111 . Schofield C. Vector population responses to control intervention. Ann Soc Belg Med Trop 1991; 71: 201-217..

The artificial breeding sites for Ae. aegypti and Ae. albopictus previously described in the literature have included discarded containers, such as cans, bottles, and plastic packaging, and water reservoirs. Natural breeding sites include tree trunks1212 . Natal D. Bioecologia do Aedes aegypti. São Paulo. Biológico 2002; 64:205-207. and bodies of water rich in organic material, mainly vegetation1313 . Forattini OP, Brito M. Reservatórios domiciliares de água e controle do Aedes aegypti. Rev Saude Publica 2003; 37:676-677..

Although junction boxes, inspection tanks, and ditches are not common egg-laying or breeding sites for Ae. aegypti, all these habitats tested positive for the species in the present study, as did waterholes for Ae. albopictus. These breeding sites are typically dark locations, with little ventilation and a high concentration of volatile organic matter, making them appropriate spots for this opportunistic species to produce offspring. As further proof of the flexibility of the species, Barrera and colleagues1414 . Barrera R, Amador M, Diaz A, Smith J, Munoz-Jordan JL, Rosario Y. Unusual productivity septic tanks and its implications for dengue control. Med Vet Entomol 2008; 22:62-69. found Ae. aegypti larvae in septic tanks in Puerto Rico.

During sample collection in the neighborhoods, it was observed that most areas lacked basic sanitation, contributing to the large number of breeding sites testing positive for Cx. quinquefasciatus, and that socioeconomic conditions were poor, providing potential breeding grounds for Ae. aegypti and leading to a high risk of dengue fever. Ferreira and Neto1515 . Ferreira AC, Neto FC. Infestação de área urbana por Aedes aegypti e relação com níveis socioeconômicos. Rev Saude Publica 2007; 41:6. corroborated the findings of the present study, arguing that factors such as basic sanitation and the cultural and socioeconomic features of communities influence mosquito density and that knowledge of such factors is indispensable for better controlling vectors and reducing the number of dengue fever outbreaks.

Thus, the presence of immature Ae. aegypti and Ae. albopictus in Cx. quinquefasciatus breeding sites demonstrates the need to review the concepts and methods used for treatment of specific larvicide for breeding sites of Culex, which may have been rendered obsolete by changes in the behavior of these vectors. The introduction of new measures for monitoring and controlling vectors is thus necessary to ensure the efficiency of the entomological surveillance system.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

ACKNOWLEDGMENTS

The authors wish to thank the Olinda Environmental Surveillance Center (CEVAO) for laboratory infrastructure; the vector control manager, and Dra. Eloína Santos for the statistical analysis.

REFERENCES

  • 1
    Powell JR, Tabachnick WJ. History of domestication and spread of Aedes aegypti - A Review. Mem Inst Oswaldo Cruz 2013; 108:11-17.
  • 2
    Zinser M, Ramberg F, Willott E. Culex quinquefasciatus (Diptera: Culicidae) as a potential West Nile virus vector in Tucson, Arizona: blood meal analysis indicates feeding on both humans and birds. J Insect Sci 2004; 4:3.
  • 3
    Barbosa RMR, Regis L, Vasconcelos RL, Leal WS. Culex mosquitoes (Diptera: Culicidae) egg laying in traps loaded with Bacillus thuringiensis variety israelensis and baited with skatole. J Med Entomol 2010; 47:345-348.
  • 4
    Instituto Brasileiro de Geografia e Estatística (IBGE). População e domicílios. Censo 2010. [Cited July 10 2010] Available at: www.ibge.gov.br/.
    » www.ibge.gov.br/
  • 5
    Ministério da Saúde. Secretaria de Vigilância em Saúde, Departamento de Vigilância Epidemiológica. Guia de vigilância do Culex quinquefasciatus, Coordenação: Francisco Anilton Alves Araújo, Marcelo Santalucia, 3a ed. Brasília: MS; 2011.
  • 6
    Fundação Nacional de Saúde (FUNASA). Controle de Vetores. Procedimentos de Segurança. Brasília: FUNASA; 2001.
  • 7
    Forattini OP. Culicidologia Médica: Identificação, Biologia, Epidemiologia. Vol. II, São Paulo: Editora da Universidade de São Paulo; 2002.
  • 8
    Lopes J. Mosquito (Diptera: Culicidae) ecology of natural and artificial rural breeding places in northern Parana, Brazil. V. Larvae captured in artificial reservoirs installed in ciliary forest. Rev Saude Publica 1997; 31:370-377.
  • 9
    Forattini OP, Marques GRAM, Kakitani I, Brito M, Sallum MAM. Significado epidemiológico dos criadouros de Aedes albopictus em bromélias. Rev Saude Publica 1998; 32:186-188.
  • 10
    Regis L, Silva SB, Melo-Santos MAV. Developing new approaches for detecting and preventing Aedes aegypti population outbreaks: basis for surveillance, alert and control system. Mem Inst Oswaldo Cruz 2008; 103:50-59.
  • 11
    Schofield C. Vector population responses to control intervention. Ann Soc Belg Med Trop 1991; 71: 201-217.
  • 12
    Natal D. Bioecologia do Aedes aegypti. São Paulo. Biológico 2002; 64:205-207.
  • 13
    Forattini OP, Brito M. Reservatórios domiciliares de água e controle do Aedes aegypti. Rev Saude Publica 2003; 37:676-677.
  • 14
    Barrera R, Amador M, Diaz A, Smith J, Munoz-Jordan JL, Rosario Y. Unusual productivity septic tanks and its implications for dengue control. Med Vet Entomol 2008; 22:62-69.
  • 15
    Ferreira AC, Neto FC. Infestação de área urbana por Aedes aegypti e relação com níveis socioeconômicos. Rev Saude Publica 2007; 41:6.

Publication Dates

  • Publication in this collection
    Nov-Dec 2014

History

  • Received
    16 May 2014
  • Accepted
    1 Oct 2014
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