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First official record of Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the Acre State, Northern Brazil

ABSTRACT

Aedes (Stegomyia) albopictus (Skuse, 1854) was reported in Brazil for the first time in 1986 and has shown marked expansion throughout the Brazilian territory. During a routine activity to control dengue fever conducted by the Division of Entomology of the Municipal Health Department in Rio Branco city, adults and immatures of Culicidae were collected in a peri-urban area. The identified Culicidae forms indicated that they belonged to the species Ae. albopictus. This is the first official record of the presence of Ae. albopictus in the Acre State, confirming its current presence in all Brazilian states.

Mosquitoes; Aedes albopictus; Vectors; Peri-urban; Arboviruses

Aedes (Stegomyia) albopictus (Skuse, 1894) has also been referred to as the Asian tiger mosquito, native to East Asia and the islands of the Western Pacific and Indian oceans11. Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol. 2013;29:460-8.. Currently, the species is found on all continents with the exception of Antarctica11. Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol. 2013;29:460-8.. In Brazil, Ae. albopictus was first detected in 1986, in the Rio de Janeiro State, in a batch of larvae collected from abandoned tires on the Federal Rural University of Rio de Janeiro campus, in Seropedica city22. Carvalho RG, Lourenço-de-Oliveira R, Braga IA. Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas. Mem Inst Oswaldo Cruz. 2014;109:787-96.. In 1986, Ae. albopictus was recorded for the first time in the Minas Gerais and Sao Paulo states. In the following year, this species established itself in all the regions of the Southeastern Brazil states33. La Corte dos Santos R. Updating of the distribution of Aedes albopictus in Brazil (1997-2002). Rev Saude Publica. 2003;37:671-3..

In 2003, Brazil’s national information data on Ae. albopictus distribution was updated, and seven states – namely, Acre, Amapa, Tocantins and Roraima (Northern Brazil) and Ceara, Piaui and Sergipe (Northeastern Brazil) – had not yet officially recorded the existence of this species33. La Corte dos Santos R. Updating of the distribution of Aedes albopictus in Brazil (1997-2002). Rev Saude Publica. 2003;37:671-3.. Nearly twelve years later, some of these Brazilian states recorded the presence of Ae. albopictus, and the absence was noted only in the Acre, Amapa and Sergipe states44. Pancetti FG, Honório NA, Urbinatti PR, Lima-Camara TN. Twenty-eight years of Aedes albopictus in Brazil: a rationale to maintain active entomological and epidemiological surveillance. Rev Soc Bras Med Trop. 2015;48:87-9.. Towards the end of 2014, then again in 2019, the presence of this mosquito vector was reported in the Sergipe and Amapa states, respectively. Acre was the only state that did not have an official record of the existence of this species55. Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386..

In this work, we analyze the first officially reported presence of adults and immature forms (larvae and pupae) of Ae. albopictus in the Acre State.

During routine activities performed to control dengue fever conducted by the Division of Entomology of the Municipal Health Department in Rio Branco city, on March 31, 2022, Ae. albopictus pupae were collected from a peri-urban area of Rio Branco city. This non-residential area is classified as high-risk for the proliferation of vectors (Strategic Point-SP; 10° 00’ 22.8” S; 67° 50’ 57.7” W). After confirming the identification of the Ae. albopictus pupae, the Division of Entomology team conducted new entomological research from April 8 to 13, 2022, covering a radius of approximately 8km from the initial point of the primary collection of the Ae. albopictus pupae (Figure 1). This peri-urban area presented a reduced number of residences and relatively high vegetation cover, which favor the proliferation of this species.

Figure 1
Collection area for immatures and adults of Ae. albopictus: A) Map of Brazil in the lower left corner highlighting the Acre state. In the right corner, Acre state with the Rio Branco city highlighted and the collection area indicated by a circled triangle; B) Peridomiciliary area with high vegetation cover, but with the presence of garbage and discarded tires, demonstrating the presence of artificial breeding sites for the species.

In the second entomological survey, four female adults were collected, using a Pulsar-type net. The larvae were collected with the help of a plastic pipette and stored in plastic tubes. The immature forms were gathered from different artificial breeding sites, such as tires and domestic waste, in addition to their natural breeding sites, such as tree holes.

The collected specimens were sent to the School of Public Health of the University of Sao Paulo, which confirmed that the species was Ae. albopictus, through morphological identification of the larvae, pupae and adult females. Photographs were taken using a Zeiss 2000-C Stereomicroscope and Zeiss AXIO Lab.A1 Microscope (Figures 2 and 3).

Figure 2 represents the four females examined, highlighting the longitudinal band of silvery scales in the mesonotum; on the head, the torus showed a tuft of silvery scales, internally, and the clypeus was without scales; on the anterior leg, the V tarsus has smooth nails.

Figure 2
Female of Ae. albopictus: A) head and mesonotum: 1- longitudinal stripe of silvery scales; 2- silvery scales torus; 3- clypeus without scales; B) V tarsus of the anterior leg: 4- smooth shank nail.

In the larva (Figure 3), short and hyaline lateral spines are prominent on the thorax; on the head, bifurcated bristle 6 and multiple bristles 7 are visible; in the VIII abdominal segment pecten is in a single row, presented as a long spine with a small serrated base or fringes on the lateral bases; in the siphon, the pecten is regularly spaced, and the 1S bristle is composed of two to four branches. In the pupa, the swimming reed possesses long hairs along its edge; in the abdomen, arrow 1 shows dichotomous ramifications; bristle 9 is simple, with tiny side hairs. All these identification features of the morphology of Ae. albopictus adhered to the classification of the Ministry of Health66. Brasil. Ministério da Saúde. Superintendência de Campanhas de Saúde Pública. Resumo dos principais caracteres morfológicos diferenciais do Aedes aegypti e do Aedes albopictus. Brasília: Ministério da Saúde; 1989. and of Consoli and Lourenço-de-Oliveira77. Consoli RA, Lourenço-De-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994..

Figure 3
Larvae and pupae of Ae. albopictus: A) Larvae thorax: 1- short lateral spines; B) Larvae head: 2- forked bristle 6; 3- bristle 7 multiple; C) VIII abdominal segment: 4- pecten in a single row, in the shape of a long spine and serrated base; D) 5- pecten siphon regularly spaced; E) Pupa: 6- swimming reed with long hairs on the edge; F and G) pupal abdomen: 7- bristle 1 with dichotomous bristles; 8- bristle 9 simple with small side hairs.

The specimens of one larva and one pupa per slide, prepared on two separate slides, plus the four adult females were deposited in the Entomological Reference Collection of the Department of Epidemiology, School of Public Health, University of Sao Paulo (Nº E-16223, E-16224, E-16225, E-16226, for females and E-16227 and E-16228 for larva and pupa).

The presence of Ae. albopictus in Acre reinforces the rapid expansion of this species in Brazil. In the Americas, including Brazil, Ae. albopictus is considered a potential vector of the dengue virus (DENV), Zika virus (ZIKV), chikungunya virus (CHIKV) and yellow fever virus (YFV)88. Garcia-Rejon JE, Navarro JC, Cigarroa-Toledo N, Baak-Baak CM. An updated review of the invasive Aedes albopictus in the Americas: geographical distribution, host feeding patterns, arbovirus infection, and the potential for vertical transmission of dengue virus. Insects. 2021;12:967.. Besides, the presence of vertical transmission of these arboviruses among the Ae. albopictus females have already been reported under natural conditions worldwide55. Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386.,88. Garcia-Rejon JE, Navarro JC, Cigarroa-Toledo N, Baak-Baak CM. An updated review of the invasive Aedes albopictus in the Americas: geographical distribution, host feeding patterns, arbovirus infection, and the potential for vertical transmission of dengue virus. Insects. 2021;12:967.

9. Ferreira-de-Lima VH, Lima-Camara TN. Natural vertical transmission of dengue virus in Aedes aegypti and Aedes albopictus: a systematic review. Parasit Vectors. 2018;11:77.
-1010. Ferreira-de-Lima VH, Andrade PD, Thomazelli LM, Marrelli MT, Urbinatti PR, Almeida RM, et al. Silent circulation of dengue virus in Aedes albopictus (Diptera: Culicidae) resulting from natural vertical transmission. Sci Rep. 2020;10:3855.. Vertical transmission appears to be an essential mechanism for maintaining the circulation of the arboviruses during the less favorable periods of transmission. The occurrence of this phenomenon among the Ae. albopictus populations in countries where it is not regarded as a primary vector of arboviruses, such as Brazil, raise concerns regarding the possible role that this species may play in the epidemiological scenario of the transmission of these pathogens55. Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386.,99. Ferreira-de-Lima VH, Lima-Camara TN. Natural vertical transmission of dengue virus in Aedes aegypti and Aedes albopictus: a systematic review. Parasit Vectors. 2018;11:77.,1010. Ferreira-de-Lima VH, Andrade PD, Thomazelli LM, Marrelli MT, Urbinatti PR, Almeida RM, et al. Silent circulation of dengue virus in Aedes albopictus (Diptera: Culicidae) resulting from natural vertical transmission. Sci Rep. 2020;10:3855..

In Brazil, Ae. albopictus is present more abundantly in the sylvatic and rural areas. However, its presence has already been recorded in the peri-urban and urban areas, with immature forms occurring both in the natural and artificial breeding sites55. Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386.,1111. Lima-Camara TN, Honório NA, Lourenço-de-Oliveira R. Freqüência e distribuição espacial de Aedes aegypti e Aedes albopictus (Diptera, Culicidae) no Rio de Janeiro, Brasil. Cad Saude Publica. 2006;22:2079-84.,1212. Ayllón T, Câmara DC, Morone FC, Gonçalves LS, Barros FS, Brasil P, et al. Dispersion and oviposition of Aedes albopictus in a Brazilian slum: initial evidence of Asian tiger mosquito domiciliation in urban environments. PLoS One. 2018;13:e0195014.. In parallel, Ae. albopictus presents eclecticism in relation to the choice of which vertebrate host to blood-feed upon, feeding on both human beings, as well as other vertebrate animals55. Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386.,88. Garcia-Rejon JE, Navarro JC, Cigarroa-Toledo N, Baak-Baak CM. An updated review of the invasive Aedes albopictus in the Americas: geographical distribution, host feeding patterns, arbovirus infection, and the potential for vertical transmission of dengue virus. Insects. 2021;12:967.. Such behavior may favor this species as a bridge vector for the arboviruses that circulate in the sylvatic areas, such as YFV22. Carvalho RG, Lourenço-de-Oliveira R, Braga IA. Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas. Mem Inst Oswaldo Cruz. 2014;109:787-96..

A recent study using secondary data from entomological surveillance in Brazil showed the rapid expansion of Ae. albopictus and indicated the presence of this species in the Acre State in 20201313. Variza PF, Lorenz C, Oliveira JG, Fernandes M, Netto SA, Prophiro JS. Updated spatio-temporal distribution of Aedes (Stegomyia) albopictus in Brazil. Acta Trop. 2022;232:106511.. Nevertheless, it is important to highlight that the first record of Ae. albopictus can only be officially confirmed after collection and identification of the species certified by a reference institution1414. Löwenberg-Neto P, Navarro-Silva MA. Primeiro registro de Aedes albopictus no Estado de Santa Catarina, Brasil. Rev Saude Publica. 2002;36:246-7.

15. Aguiar DB, Fontão A, Rufino P, Macedo VA, Ríos-Velásquez, CM, Castro MG, et al. Primeiro registro de Aedes albopictus (Diptera: Culicidae) em Roraima, Brasil. Acta Amaz. 2008;38:357-60.
-1616. Saraiva JF, Maitra A, Galardo AK, Scarpassa VM. First record of Aedes (Stegomyia) albopictus in the state of Amapá, northern Brazil. Acta Amaz. 2019;49:71-4.. Moreover, the methods used for the surveillance of Aedes with medical importance, especially Aedes aegypti and Ae. albopictus, are highly dependent on human operation and skills to identify the mosquito species, both in the field and laboratory1717. Maciel-de-Freitas R, Lima AW, Araújo SC, Lima JB, Galardo AK, Honório NA, et al. Discrepancies between Aedes aegypti identification in the field and in the laboratory after collection with a sticky trap. Mem Inst Oswaldo Cruz. 2014;109:824-7..

This paper shows for the first time that Ae. albopictus is present in all the Brazilian states, including Acre. With the record of Ae. albopictus in Rio Branco city, it would be interesting to investigate the presence of this species in the other municipalities within Acre. As a result of the presence of this species, new studies on the expansion and bioecology of this vector in the state are encouraged.

In the current context, it is important to include the identification of the species Ae. albopictus in the routine activities performed by the endemic agents. The maintenance of continuous entomological and virological surveillance of the Ae. albopictus, now recorded in all the Brazilian states, is essential to detect any possible change in the role of this species in the dynamics of the transmission of DENV, ZIKV, CHIKV and YFV, in Brazil.

ACKNOWLEDGMENTS

The authors would like to thank the Rio Branco City Hall for the logistical support and Marta Ribeiro Heinisch e Silva for making the map of Figure 1.

REFERENCES

  • 1
    Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol. 2013;29:460-8.
  • 2
    Carvalho RG, Lourenço-de-Oliveira R, Braga IA. Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas. Mem Inst Oswaldo Cruz. 2014;109:787-96.
  • 3
    La Corte dos Santos R. Updating of the distribution of Aedes albopictus in Brazil (1997-2002). Rev Saude Publica. 2003;37:671-3.
  • 4
    Pancetti FG, Honório NA, Urbinatti PR, Lima-Camara TN. Twenty-eight years of Aedes albopictus in Brazil: a rationale to maintain active entomological and epidemiological surveillance. Rev Soc Bras Med Trop. 2015;48:87-9.
  • 5
    Ferreira-de-Lima VH, Câmara DC, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: observations on biology and ecological interactions since its first detection in 1986. Acta Trop. 2020;205:105386.
  • 6
    Brasil. Ministério da Saúde. Superintendência de Campanhas de Saúde Pública. Resumo dos principais caracteres morfológicos diferenciais do Aedes aegypti e do Aedes albopictus. Brasília: Ministério da Saúde; 1989.
  • 7
    Consoli RA, Lourenço-De-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994.
  • 8
    Garcia-Rejon JE, Navarro JC, Cigarroa-Toledo N, Baak-Baak CM. An updated review of the invasive Aedes albopictus in the Americas: geographical distribution, host feeding patterns, arbovirus infection, and the potential for vertical transmission of dengue virus. Insects. 2021;12:967.
  • 9
    Ferreira-de-Lima VH, Lima-Camara TN. Natural vertical transmission of dengue virus in Aedes aegypti and Aedes albopictus: a systematic review. Parasit Vectors. 2018;11:77.
  • 10
    Ferreira-de-Lima VH, Andrade PD, Thomazelli LM, Marrelli MT, Urbinatti PR, Almeida RM, et al. Silent circulation of dengue virus in Aedes albopictus (Diptera: Culicidae) resulting from natural vertical transmission. Sci Rep. 2020;10:3855.
  • 11
    Lima-Camara TN, Honório NA, Lourenço-de-Oliveira R. Freqüência e distribuição espacial de Aedes aegypti e Aedes albopictus (Diptera, Culicidae) no Rio de Janeiro, Brasil. Cad Saude Publica. 2006;22:2079-84.
  • 12
    Ayllón T, Câmara DC, Morone FC, Gonçalves LS, Barros FS, Brasil P, et al. Dispersion and oviposition of Aedes albopictus in a Brazilian slum: initial evidence of Asian tiger mosquito domiciliation in urban environments. PLoS One. 2018;13:e0195014.
  • 13
    Variza PF, Lorenz C, Oliveira JG, Fernandes M, Netto SA, Prophiro JS. Updated spatio-temporal distribution of Aedes (Stegomyia) albopictus in Brazil. Acta Trop. 2022;232:106511.
  • 14
    Löwenberg-Neto P, Navarro-Silva MA. Primeiro registro de Aedes albopictus no Estado de Santa Catarina, Brasil. Rev Saude Publica. 2002;36:246-7.
  • 15
    Aguiar DB, Fontão A, Rufino P, Macedo VA, Ríos-Velásquez, CM, Castro MG, et al. Primeiro registro de Aedes albopictus (Diptera: Culicidae) em Roraima, Brasil. Acta Amaz. 2008;38:357-60.
  • 16
    Saraiva JF, Maitra A, Galardo AK, Scarpassa VM. First record of Aedes (Stegomyia) albopictus in the state of Amapá, northern Brazil. Acta Amaz. 2019;49:71-4.
  • 17
    Maciel-de-Freitas R, Lima AW, Araújo SC, Lima JB, Galardo AK, Honório NA, et al. Discrepancies between Aedes aegypti identification in the field and in the laboratory after collection with a sticky trap. Mem Inst Oswaldo Cruz. 2014;109:824-7.

Publication Dates

  • Publication in this collection
    20 Mar 2023
  • Date of issue
    2023

History

  • Received
    10 Nov 2022
  • Accepted
    6 Feb 2023
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