Neotropical Entomology

, Volume 46, Issue 3, pp 243–255 | Cite as

Why is Aedes aegypti Linnaeus so Successful as a Species?

Forum

Abstract

Diseases transmitted by mosquitoes impose enormous burden towards human morbidity and mortality. Over the last three decades, Brazil has suffered from severe Dengue epidemics. In September 2014, this situation is further complicated by the introduction of two other viruses, Zika and Chikungunya, placing Brazil in a triple epidemic. In this article, we discuss the biology of Aedes aegypti Linnaeus, and the principal initiatives currently used to control mosquito populations and the diseases they transmit. Aedes aegypti has broad global distribution and is involved in the transmission of various arboviral diseases such as Dengue, Zika, and Chikungunya. Several factors contribute to the success of the species, particularly behavioral plasticity, rapid development, desiccation-resistant eggs, resistance to the principle insecticide classes currently available on the market, preference for the urban environment, and proximity to humans. Vector control programs are the best way to reduce the burden of mosquito-borne diseases. Chemical control is most commonly used in recent times, and unfortunately, the results have not been satisfactory but instead, there is increased vector dispersal and, subsequently, the spread of disease epidemics. Investigations of alternative control methods such as release of Wolbachia-infected mosquitoes for blocking vector-borne pathogens, release of transgenic mosquitoes carrying a lethal gene for offspring, and the use of insecticide-dispersing mosquitoes are under way in Brazil, and some have shown promising results. Special emphasis should be placed on integrated management of all available tactics, so as to maximize efforts towards mosquito control. Finally, we emphasize that continuous actions and community participation control initiatives are critically important for success.

Keywords

Mosquitoes, Wolbachia, transgenics, control, arboviruses 

References

  1. Abad-Franch F, Zamora-Perea E, Ferraz G, Padilla-Torres SD, Luz SLB (2015) Mosquito-disseminated pyriproxyfen yields high breeding-site coverage and boosts juvenile mosquito mortality at the neighborhood scale. PLoS Negl Trop Dis 9:1–17CrossRefGoogle Scholar
  2. Abreu FVS, Morais MM, Ribeiro SP, Eiras AE (2015) Influence of breeding site availability on the oviposition behaviour of Aedes aegypti. Mem Inst Oswaldo Cruz 110:669–676CrossRefPubMedPubMedCentralGoogle Scholar
  3. Albeny DS, Martins GF, Andrade MR, Krüger RF, Vilela EF (2011) Aedes aegypti survival in the presence of Toxorhynchites violaceus (Diptera: Culicidae) fourth instar larvae. Zool 28:538–540Google Scholar
  4. Aliota MT, Walker EC, Uribe Yepes A, Dario Velez I, Christensen BM, Osorio JE (2016) The wMel strain of Wolbachia reduces transmission of Chikungunya virus in Aedes aegypti. PLoS Negl Trop Dis 10:1–13Google Scholar
  5. Almerão MP, Fagundes NJR, De Araújo PB, Verne S, Grandjean F, Bouchon D, Araújo AM (2012) First record of Wolbachia in South American terrestrial isopods: prevalence and diversity in two species of Balloniscus (Crustacea, Oniscidea). Genet Mol Biol 35:980–989CrossRefPubMedPubMedCentralGoogle Scholar
  6. Alphey L, Benedict M, Bellini R, Clark GG, Dame D, Service MW, Dobson SL (2010) Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis 10:295–311CrossRefPubMedPubMedCentralGoogle Scholar
  7. Alphey L, McKemey A, Nimmo D, Neira Oviedo M, Lacroix R, Matzen K, Beech C (2013) Genetic control of Aedes mosquitoes. Pathog Glob Health 107:170–179CrossRefPubMedPubMedCentralGoogle Scholar
  8. Andrade CFS, Cabrini I (2007) Controle de pernilongos e borrachudos em áreas urbanas. In: Pinto AS, Rossi MM (eds) Salmeron E Manejo de pragas urbanas. ESALQ, Piracicaba, pp 55–66Google Scholar
  9. Araújo HRC, Carvalho DO, Ioshino RS, Costa-da-Silva AL, Capurro ML (2015) Aedes aegypti Control strategies in Brazil: incorporation of new technologies to overcome the persistence of dengue epidemics. Insects 6:576–594CrossRefPubMedPubMedCentralGoogle Scholar
  10. Azevedo-Santos V, Vitule J, García-Berthou E, Pelicice FM, Simberloff D (2016) Misguided strategy for mosquito control. Science 351:675CrossRefPubMedGoogle Scholar
  11. Baly A, Flessa S, Cote M, Thiramanus T, Vanlerberghe V, Villegas E, Jirarojwatana S, Van Der Stuyft P (2011) The cost of routine Aedes aegypti control and of insecticide-treated curtain implementation. AmJTrop Med Hyg 84:747–752CrossRefGoogle Scholar
  12. Baly A, Toledo ME, Rodriguez K, Benitez JR, Rodriguez M, Boelaert M, Vanlerberghe V, Van der Stuyft P (2012) Costs of dengue prevention and incremental cost of dengue outbreak control in Guantanamo, Cuba. Trop Med Int Heal 17:123–132CrossRefGoogle Scholar
  13. Baly A, Toledo ME, Lambert I, Benítez E, Rodriguez K, Rodriguez E, Vanlerberghe V, Van der Stuyft P (2016) Cost of intensive routine control and incremental cost of insecticide-treated curtain deployment in a setting with low Aedes aegypti infestation. Rev Soc Bras Med Trop 49:418–424CrossRefPubMedGoogle Scholar
  14. Bandi C, Anderson TJ, Genchi C, Blaxter ML (1998) Phylogeny of Wolbachia in filarial nematodes. Proc R Soc London Biol Sci 265:2407–2413CrossRefGoogle Scholar
  15. Bandi C, Trees AJ, Brattig NW (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 98:215–238CrossRefPubMedGoogle Scholar
  16. Boyce R, Lenhart A, Kroeger A, Velayudhan R, Roberts B, Horstick O (2013) Bacillus thuringiensis israelensis (Bti) for the control of dengue vectors: systematic literature review. Trop Med Int Heal 18:564–577CrossRefGoogle Scholar
  17. Braga IA, Valle D (2007) Aedes aegypti: inseticidas, mecanismos de ação e resistência. Epidemiol e Serviços Saúde 16:279–293Google Scholar
  18. Brasil (2009) Diretrizes Nacionais para a prevenção e controle de epidemias de dengue. Ministério da Saúde - Secretaria de Vigilância em Saúde, Séria A. Normas e Manuais Técnicos, Brasília, p 160Google Scholar
  19. Brasil (2015) Governo aciona ações de emergência diante da alta de casos de microcefalia em PE. http://www.brasil.gov.br/saude/2015/11/governo-aciona-acoes-de-emergencia-diante-de-alta-de-casos-de-microcefalia-em-pe. Accessed 10 Nov 2016
  20. Brasil (2016) Alfenas usa peixes no combate ao Aedes aegypti. http://www.blog.saude.gov.br/index.php/combate-ao-aedes/50590-alfenas-usa-peixes-no-combate-ao-aedes-aegypti. Accessed 10 Nov 2016
  21. Buckner EA, Alto BW, Lounibos LP (2013) Vertical transmission of Key West dengue-1 virus by Aedes aegypti and Aedes albopictus (Diptera: Culicidae) mosquitoes from Florida. J Med Entomol 50:1291–1297CrossRefPubMedPubMedCentralGoogle Scholar
  22. Callaway E (2016) Rio fights Zika with biggest release yet of bacteria-infected mosquitoes. Nature 539:17–18CrossRefPubMedGoogle Scholar
  23. Caragata EP, Dutra HLC, Moreira LA (2016) Exploiting intimate relationships: controlling mosquito-transmitted disease with Wolbachia. Trends Parasitol 32:207–218CrossRefPubMedGoogle Scholar
  24. Carvalho DO, McKemey AR, Garziera L, Lacroix R, Donnelly CA, Alphey L, Malavasi A, Capurro ML (2015) Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. PLoS Negl Trop Dis 9:1–15CrossRefGoogle Scholar
  25. Cavalcanti LPG, Soares Pontes RJ, Ferreira Regazzi AC, de Paula FJ, Frutuoso RL, Sousa EP, Dantas Filho FF, de Oliveira Lima JW (2007) Competência de peixes como predadores de larvas de Aedes aegypti, em condições de laboratório. Rev Saude Publica 41:638–644CrossRefPubMedGoogle Scholar
  26. CDC (2016) Mosquito life cycle. http://www.cdc.gov/dengue/resources/factSheets/MosquitoLifecycleFINAL.pdf. Accessed 14 Nov 2016
  27. Chandra G, Bhattacharjee I, Chatterjee SN, Ghosh A (2008) Mosquito control by larvivorous fish. Indian J Med Res 127:13–27PubMedGoogle Scholar
  28. Consoli RAGB, Lourenço de Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Fiocruz, Rio de Janeiro, p 228CrossRefGoogle Scholar
  29. Crow JF (1957) Genetics of insect resistance to chemicals. Annu Rev Entomol 2:227–246CrossRefGoogle Scholar
  30. David MR, Lourenço-de-Oliveira R, De Freitas RM (2009) Container productivity, daily survival rates and dispersal of Aedes aegypti mosquitoes in a high income dengue epidemic neighbourhood of Rio de Janeiro: presumed influence of differential urban structure on mosquito biology. Mem Inst Oswaldo Cruz 104:927–932CrossRefPubMedGoogle Scholar
  31. Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, Morrison AC (2009) Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci 106:11530–11534CrossRefPubMedPubMedCentralGoogle Scholar
  32. Dumler JS, Barbet AF, Bakker CP, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangwira FR (2001) Reorganization of gene in families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasm, Cowdria with Ehriichia with neorickettsia, description of six new species combinations and designatio. Int J Syst Evol Microbiol 51:2145–2165CrossRefPubMedGoogle Scholar
  33. Dutra HLC, dos Santos LMB, Caragata EP, Silva JBL, Villela DAM, Maciel-de-Freitas RM, Moreira LA (2015) From lab to field: the influence of urban landscapes on the invasive potential of Wolbachia in Brazilian Aedes aegypti mosquitoes. PLoS Negl Trop Dis 9:1–22CrossRefGoogle Scholar
  34. Dutra HLC, Rocha MN, Dias FBS, Mansur SB, Caragata EP, Moreira LA (2016) Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe 19:771–774CrossRefPubMedPubMedCentralGoogle Scholar
  35. Eiras AE (2011) Culicidae. In: Neves DP (ed) Parasitologia Humana. Atheneu, São Paulo, pp 387–401Google Scholar
  36. Fares RCG, Souza KPR, Añez G, Rios M (2015) Epidemiological scenario of dengue in Brazil. Biomed Res Int 2015:1–13CrossRefGoogle Scholar
  37. Farnesi LC, Martins AJ, Valle D, Rezende GL (2009) Embryonic development of Aedes aegypti (Diptera: Culicidae): influence of different constant temperatures. Mem Inst Oswaldo Cruz, Rio de Janeiro 104(1): 124–126Google Scholar
  38. Faull KJ, Williams CR (2015) Intraspecific variation in desiccation survival time of Aedes aegypti (L.) mosquito eggs of Australian origin. J Vector Ecol 40:292–230CrossRefPubMedGoogle Scholar
  39. Ferguson NM, Kien DT, Clapham H, Aguas R, Trung VT, Chau TN, Popovici J, Ryan PA, O’Neill SL, McGraw EA, Long VT, Dui le T, Nguyen HL, Chau NV, Wills B, Simmons CP (2015) Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti. Sci Transl Med 7(279):279–237CrossRefGoogle Scholar
  40. Ferreira CP, Yang HM, Esteva L (2008) Assessing the suitability of sterile insect technique applied to Aedes aegypti. J. Biol. Syst. 16:565Google Scholar
  41. Fiocruz (2016a) 10 Minutos contra o Aedes. http://www.ioc.fiocruz.br/dengue/textos/10minutos.html. Accessed 16 Nov 2016
  42. Fiocruz (2016b) Fiocruz apresenta DengueTech em congresso nacional de saúde. http://www.ioc.fiocruz.br/dengue/textos/10minutos.html. Accessed 16 Nov 2016
  43. Forattini OP (2002) Culicidologia Médica. Edusp, São Paulo, p 860Google Scholar
  44. Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, Van den Hurk A, McGraw EA, O'Neill SL (2014) Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis 8:1–10CrossRefGoogle Scholar
  45. Gonçalves KS, Messias MC (2008) Ocorrência de Aedes (Stegomyia) aegypti (Linnaeus, 1762) (Insecta, Diptera, Culicidae) em bromélias, no município do Rio de Janeiro (Rio de Janeiro, Brasil). Biota Neotrop 8:235–237CrossRefGoogle Scholar
  46. Gotoh T, Noda H, Hong XY (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91( 3):208–216Google Scholar
  47. Harris AF, Nimmo D, McKemey AR, Kelly N, Scaife S, Donnelly CA, Beech C, Petrie WD, Alphey L (2011) Field performance of engineered male mosquitoes. Nat Biotechnol 29:1034–1037CrossRefPubMedGoogle Scholar
  48. Harris AF, McKemey AR, Nimmo D, Curtis Z, Black I, Morgan AS, Oviedo MN, Lacroix R, Naish N, Morrison NI, Collado A, Stevenson J, Scaife S, Dafa'alla T, Fu G, Phillips C, Miles A, Raduan N, Kelly N, Beech C, Donnelly CA, Petrie WD, Alphey L (2012) Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nature 30:828–830Google Scholar
  49. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science (80- ) 322:702CrossRefPubMedGoogle Scholar
  50. Hertig M, Wolbach SB (1924) Studies on Rickettsia-Like Micro-Organisms in Insects. J Med Res. 44(3):329–374Google Scholar
  51. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hoffmann AA, Montgomery B, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y, Cook H, Axford J, Callahan AG, Kenny N, Omodei C, McGraw EA, Ryan PA, Ritchie AS, Turelli M, O’Neill SL (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–457CrossRefPubMedGoogle Scholar
  53. Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K, Axford JK, Montgomery B, Turley AP, O'Neill SL (2014) Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8:e3115CrossRefPubMedPubMedCentralGoogle Scholar
  54. Juliano SA, Meara GFO, Cutwa MM (2010) Competing Mosquitoes 130:458–469Google Scholar
  55. Kamtchum-Tatuene J, Makepeace BL, Benjamin L, Baylis M, Solomon T (2016) The potential role of Wolbachia in controlling the transmission of emerging human arboviral infections. Curr Opin Infect Dis 29:1–9CrossRefGoogle Scholar
  56. Kant R, Haq S, Srivastava HC, Sharma VP (2013) Review of the bioenvironmental methods for malaria control with special reference to the use of larvivorous fishes and composite fish culture in central Gujarat, India. J Vector Borne Dis 50:1–12PubMedGoogle Scholar
  57. Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Eco Entomol 48:459–462CrossRefGoogle Scholar
  58. Kraemer MUG, Sinka ME, Duda KA, Mylne A, Shearer FM, Brady OJ, Messina JP, Barker CM, Moore CG, Carvalho RG, Coelho GE, Van Bortel W, Hendrickx G, Schaffner F, Wint GRW, Elyazar IRF, Teng HJ, Hay SI (2015) The global compendium of Aedes aegypti and Aedes albopictus occurrence. Sci Data 2:150035CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lo N, Paraskevopoulos C, Bourtzis K, O'Neill SL, Werren JH, Bordenstein SR, Bandi C (2007) Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol 57:654–657CrossRefPubMedGoogle Scholar
  60. Lourenço de Oliveira R (2015) Biologia e comportamento do vetor. In: Valle D (ed) Dengue: teorias e práticas. Fiocruz, Rio de Janeiro, pp 75–92Google Scholar
  61. Maciel-de-Freitas R, Aguiar R, Bruno RV, Guimarães MC, Lourenço-de-Oliveira R, Sorgin MHF, Struchiner CJ, Valle D, O'Neill SL, Moreira LA (2012) Why do we need alternative tools to control mosquito-borne diseases in Latin America? Mem Inst Oswaldo Cruz 107:828–829CrossRefPubMedGoogle Scholar
  62. McBride CS, Baier F, Omondi AB, Spitzer AS, Lutomiah J, Sang R, Ignell R, Vosshall LB (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515:222–227CrossRefPubMedPubMedCentralGoogle Scholar
  63. McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M, Wang YF, O'Neill SL (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–144CrossRefPubMedGoogle Scholar
  64. Mocellin MG, Simões TC, Nascimento TFS do, Teixeira MLF, Lounibos LP, Oliveira RL (2009) Bromeliad-inhabiting mosquitoes in an urban botanical garden of dengue endemic Rio de Janeiro—are bromeliads productive habitats for the invasive vectors Aedes aegypti and Aedes albopictus? Mem Inst Oswaldo Cruz 104:1171–1176Google Scholar
  65. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O'Neill SL (2009) A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278CrossRefPubMedGoogle Scholar
  66. O’Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A 89:2699–2702CrossRefPubMedPubMedCentralGoogle Scholar
  67. Oliveira SDL, Carvalho DO, Capurro ML (2011) Mosquito transgênico: do paper para a realidade. Rev da Biol 6b:38–43Google Scholar
  68. Oliveira LB, Maria R, Nunes P, Santana M, Rosa A, Mariana N, Nunes F, Bantim I, Calou F, Peron AP, Maria M, Marques M, Michel P, Ferreira P (2015a) Perfil do uso populacional de inseticidas domésticos no combate a mosquitos Profile of the population use of household insecticides against mosquitoes. Semin Ciências Biológicas e da Saúde 36:79–92CrossRefGoogle Scholar
  69. Oliveira CD, Gonçalves DS, Baton L, Shimabukuro PHF, Carvalho FD, Moreira LA (2015b) Broader prevalence of Wolbachia in insects including potential human disease vectors. Bull Entomol Res 105:305–315CrossRefPubMedGoogle Scholar
  70. Oxitec Brasil (2016) Conheça os resultados dos projetos que usaram a tecnologia do Aedes do Bem e reduziram a população selvagem do mosquito transmissor da dengue, Zika e chikungunya. http://br.oxitec.com/. Accessed em 25 Nov 2016
  71. Paploski IAD, Rodrigues MS, Mugabe VA, Kikuti M, Tavares AS, Reis MG, Kitron U, Ribeiro GS (2016) Storm drains as larval development and adult resting sites for Aedes aegypti and Aedes albopictus in Salvador, Brazil. Parasit Vectors 9:1–8CrossRefGoogle Scholar
  72. Parra JRP, Botelho PSM, Correa-Ferreira BS, Bento JMS (2002) Controle biológico no Brasil: parasitoides e predadores. Manole, São Paulo, p 609Google Scholar
  73. Polaszek A (2006) Two words colliding: resistance to changes in the scientific names of animals—Aedes vs Stegomyia. Trends Parasitol 22(1):8–9CrossRefPubMedGoogle Scholar
  74. Popovici J, Moreira LA, Poinsignon A, Iturbe-Ormaetxe I, McNaughton D, O'Neill SL (2010) Assessing key safety concerns of a Wolbachia-based strategy to control dengue transmission by Aedes mosquitoes. Mem Inst Oswaldo Cruz 105:957–964CrossRefPubMedGoogle Scholar
  75. Rapley LP, Russell RC, Montgomery BL, Ritchie SA (2009) The effects of sustained release metofluthrin on the biting, movement, and mortality of Aedes aegypti in a domestic setting. AmJTrop Med Hyg 81:94–99Google Scholar
  76. Reinert JF, Harbach RE, Kitching IJ (2004) Phylogeny and classification of Aedini (Diptera: Culicidae), based on morphological characters of all life stages. Zool J Linnean Soc 142:289–368CrossRefGoogle Scholar
  77. Ritchie SA, Devine GJ (2013) Confusion, knock-down and kill of Aedes aegypti using metofluthrin in domestic settings: a powerful tool to prevent dengue transmission? Parasit Vectors 6:262CrossRefPubMedPubMedCentralGoogle Scholar
  78. Ross PA, Wiwatanaratanabutr I, Axford JK, et al (2017) Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. Plos Pathogens 1–17Google Scholar
  79. Shulse CD, Semlitsch RD, Trauth KM (2013) Mosquitofish dominate amphibian and invertebrate community development in experimental wetlands. J Appl Ecol 50:1244–1256Google Scholar
  80. Silva HH, Da Silva IG (1999) Influência do período de quiescência dos ovos sobre o ciclo de vida de Aedes aegypti (Linnaeus, 1762) (Diptera, Culicidae) em condições de laboratório. Rev Soc Bras Med Trop 32:349–355CrossRefPubMedGoogle Scholar
  81. Silva AS, Lobo KS, Da Silva JS, Vale CFS, Tadei WP, Pineiro VCS (2014) Influência dos fatores abióticos na efetividade de Bacillus thuringiensis var. israelensis (Berliner, 1911) para larvas de Aedes aegypti (Linnaeus, 1762). Rev Cubana Med Trop 66:174–190Google Scholar
  82. SVS (2015) Boletim Epidemiológico Secretaria de Vigilância em Saúde—Ministério da Saúde. http://portalsaude.saude.gov.br/images/pdf/2016/janeiro/07/2015-svs-be-pncd-se48.pdf. Accessed 10 Nov 2016
  83. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:2753–2763CrossRefGoogle Scholar
  84. Thangamani S, Huang J, Hart C, Guzman H, Tesh R (2016) Vertical transmission of Zika virus in Aedes aegypti mosquitoes. Am J Trop Med Hyg 95(5):1169–1173Google Scholar
  85. Tozan Y, Ratanawong P, Louis VR, Kittayapong P, Wilder-Smith A (2014) Use of insecticide-treated school uniforms for prevention of dengue in schoolchildren: a cost-effectiveness analysis. PLoS One 9:1–9. doi:10.1371/journal.pone.0108017 CrossRefGoogle Scholar
  86. Valença MA, Marteis LS, Steffler LM, Silva AM, Santos RLC (2013) Dynamics and characterization of Aedes aegypti (L.) (Diptera: Culicidae) key breeding sites. Neotrop Entomol 42:311–316CrossRefPubMedGoogle Scholar
  87. Valle D, Belinato TA, Martins AJ (2015) Controle químico de Aedes aegypti, resistência a inseticidas e alternativas. In: Valle D (ed) Dengue: teorias e práticas. Fiocruz, Rio de Janeiro, pp 93–126Google Scholar
  88. Van Lenteren JC (2009) Critérios de seleção de inimigos naturais. In: Bueno VHP Controle biológico de pragas: produção massal e controle de qualidade. UFLA, Lavras, p 430Google Scholar
  89. Varejão JBM, Biral Dos Santos C, Ricas Rezende H, Bevilacqua LC, Falqueto A (2005) Criadouros de Aedes (Stegomyia) aegypti (Linnaeus, 1762) em bromélias nativas na Cidade de Vitória, ES. Rev Soc Bras Med Trop 38:238–240CrossRefPubMedGoogle Scholar
  90. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, Leong YS, Dong Y, Axford J, Kriesner P, Lloyd AL, Ritchie AS, O'Neill SL, Hoffmann AA (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450–453CrossRefPubMedGoogle Scholar
  91. Wallace H (2013) Mosquitos geneticamente modificados: preocupações atuais. HEINRICH BOLL, Rio de Janeiro, p 97Google Scholar
  92. Wermelinger ED, Ferreira AP, De Carvalho RW, Da Silva AA, Benigno CV (2015) Aedes aegypti eggs oviposited on water surface collected from field ovitraps in Nova Iguaçu City, Brazil. Rev Soc Bras Med Trop 48:770–772CrossRefPubMedGoogle Scholar
  93. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751CrossRefPubMedGoogle Scholar
  94. WHO (2016) Organização Mundial da Saúde anuncia emergência de saúde pública de importância internacional. http://www.paho.org/bra/index.php?option=com_content&view=article&id=4991:organizacao-mundial-da-saude-declara-emergencia-de-saude-publica-de-importancia-internacional&Itemid=816. Accessed 10 Nov 2016
  95. Wilder-Smith A, Lover A, Kittayapong P, Burnham G (2011) Hypothesis: impregnated school uniforms reduce the incidence of dengue infections in school children. Med Hypotheses 76:861–862CrossRefPubMedGoogle Scholar
  96. Wilder-Smith A, Byass P, Olanratmanee P, Maskhao P, Sringernyuang L, Logan JG, Lindsay SW, Banks S, Gubler D, Louis VR, Tozan Y, Kittayapong P (2012) The impact of insecticide-treated school uniforms on dengue infections in school-aged children: study protocol for a randomised controlled trial in Thailand. Trials 13:1–7CrossRefGoogle Scholar
  97. Wilkerson RC, Linton YM, Fonseca DM, Schultz TR, Price DC, Strickman DA (2015) Making mosquito taxonomy useful: a stable classification of tribe Aedini that balances utility with current knowledge of evolutionary relationships. PLoS One 10:1–26CrossRefGoogle Scholar
  98. Yeap HL, Mee P, Walker T, Weeks AR, O'Neill SL, Johnson P, Ritchie SA, Richardson KM, Doig C, Endersby NM, Hoffmann AA (2011) Dynamics of the “popcorn” Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control. Genetics 187:583–595CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zara ALSA, Maria dos Santos S, Fernandes-Oliveira ES, Carvalho RG, Giovanini EC (2016) Estratégias de controle do Aedes aegypti: uma revisão. Epidemiol e Serviços Saúde 25:391–403Google Scholar
  100. Zeidler JD, Acosta POA, Barrêto PP, Cordeiro JDS (2008) Dengue virus in Aedes aegypti larvae and infestation dynamics in Roraima, Brazil. Rev Saude Pública 42:2–6Google Scholar

Copyright information

© Sociedade Entomológica do Brasil 2017

Authors and Affiliations

  1. 1.Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Centro de Pesquisas René Rachou / Fundação Oswaldo Cruz (CPqRR / Fiocruz)Belo HorizonteBrazil

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