Does native bromeliads represent important breeding sites for Aedes aegypti (L.) (Diptera: Culicidae) in urbanized areas?

PUBLIC HEALTH

Does native bromeliads represent important breeding sites for Aedes aegypti (L.) (Diptera: Culicidae) in urbanized areas?

CB Santos; GR Leite; A Falqueto

Unidade de Medicina Tropical, Univ Federal do Espírito Santo, Vitória, ES, Brasil

^{Correspondence}

ABSTRACT

This study evaluates the importance of native bromeliads growing on rocky outcrops interspersed with urbanized areas as breeding sites for the Aedes aegypti (L.) in Vitória, state of Espírito Santo, Brazil. Oviposition traps were installed in backyards of houses in two separate zones. In the first zone houses were up to 50 m away from the rocky outcrops, while in the second zone they were at least at 200 m from the rocky outcrops. Aedes aegypti was significantly more abundant in the latter zone. The finding was that rocky outcrops with native bromeliads, even with the greater availability of potential breeding sites, do not play an important role as breeding sites for A. aegypti. This conclusion supports the hypothesis that the macrobiota of native bromeliads plays an important role in the natural control of A. aegypti. Besides, the interspecific competition between species of mosquitoes and the attractiveness of bromeliads could also be important factors.

Keywords: Dengue, natural control, Brazil

Introduction

The African mosquito Aedes aegypti (L.) became adapted to artificial breeding habitats, accompanying human migrations throughout the tropics and subtropics (Barrett & Higgs 2007). Its preferred breeding sites include artificial containers that allow rainwater to accumulate, particularly in areas of high human population density (Mazine et al 1996). In Brazil, A. aegypti acted as the vector of urban yellow fever in recent decades, and has also been responsible for dengue fever epidemics (Vasconcelos 2002, Braga 2007). Various researchers have reported finding immatures of this species in bromeliads used for urban ornamentation, leading public health authorities to discourage maintenance of these plants in residential areas (e.g. Forattini & Marques 2000, Cunha et al 2002). Aedes aegypti were also reported in native bromeliads growing on rocky outcrops interspersed with urbanized areas in Vitória, state of Espírito Santo, Brazil (Varejão et al 2005). Therefore, the objective of the present study was to evaluate whether native bromeliads in their natural habitat represent important breeding sites for A. aegypti. Bromeliads and the human-produced breeding sites in residences close to rocky outcrops would be readily available and more exposed to infestation by A. aegypti than those situated at greater distances from these rocky outcrops, if bromeliads prove to be playing an important role as breeding sites for this species.

Material and Methods

The study was carried out in the Vitória neighborhoods of Santa Lúcia and Bela Vista (Fig 1), where A. aegypti had already been reported breeding in native bromeliads Billbergia amoena, Billbergia tweedieana, and Vriesea extensa (Varejão et al 2005). The climate of the region is defined by the Köppen-Geiger classification as tropical monsoon (Peel et al 2007), with a mean annual temperature of 25ºC and an annual precipitation of 1100 mm (Hijmans et al 2005). The urbanized part of each neighborhood was situated on a plane area, so the density of the residences and their artificial breeding sites close to the outcrops was similar to those in areas that were more distant. During the study, the house infestation index of Santa Lúcia was 1.1 and that of Bela Vista 2.2 (SESA 2008).

Ten houses situated at distances up to 50 m from rocky outcrops (< 50 m) with native bromeliads and 10 others at distances beyond at least 200 m from the rocks (> 200 m) were randomly selected in each neighborhood. The distance the ovitraps were placed from the rocky outcrops was based on the flight capacity reported for A. aegypti (Liew & Curtis 2004, Russel et al 2005, Maciel-De-Freitas et al 2007). A sample comprising 40 units was included in each survey, and an oviposition trap (ovitrap) was installed in the backyard of each house (Fay & Eliason 1966), as ovitraps are reported to be the most efficient sampling and detection technique for A. aegypti (Braga et al 2000). Five surveys were conducted between 2007 and 2008, when ovitraps were simultaneously installed in the selected houses every three months. These traps remained exposed for five days each time, after which they were retrieved and transported to the laboratory to allow eggs to be counted, and larvae to hatch for species identification (Consoli & Lourenço-de-Oliveira 1994).

Mosquito samples were distributed among groups, according to species and distances between the rocky outcrops and the traps in which they were captured. Paired-samples t-test was applied to the data. This test helps to avoid the influences of the seasons and neighborhood characteristics on the comparisons. The assumption of normality of the data was tested with the Shapiro-Wilk test. If the data contradicted this assumption, a logarithmic transformation was used to correct for normality (Zar 1999).

Results

Of the 200 ovitraps installed during the experiment, 106 were positive, collecting 3,357 eggs. Of these, 979 were collected in ovitraps installed at distances of up to 50 m away from the rocky outcrops and 2,378 in ovitraps at distances of at least 200 m. Of the viable eggs, 723 came from ovitraps at 50 m or closer and 1,739 from ovitraps at 200 m or further away. Aedes aegypti and Aedes albopictus (Skuse) were collected, and their abundance were similar in ovitraps located up to 50 m from the rocky outcrops (< 50 m). Most of the specimens collected at ovitraps located at least at 200 m away (> 200 m) were represented by A. aegypti (Table 1).

Data was log transformed, and the paired-samples t-test showed a significant difference between the A. aegypti groups, indicating their population in areas > 200 m away from the rocky outcrops to be higher than those in areas < 50 m (t = 4.117, P = 0.003; Fig 2). The population of A. aegypti in areas > 200 m away was also higher than that of A. albopictus either at < 50 m (t = 3.485, P = 0.007) or at > 200 m (t = 4.236, P = 0.002) from the rocky outcrops.

Discussion

Peryassú (1908) first reported the presence of A. aegypti in bromeliads used as ornamental plants in urban areas of Rio de Janeiro. Since then, various researchers found the presence of this species in bromeliads cultivated in households, drawing attention to the risk that these plants could pose as additional breeding sites for this and other mosquito species (e.g. Forattini & Marques 2000, Cunha et al 2002). In French Guiana, A. aegypti was found in bromeliads in the rainforests at distances of about 30 km from the nearest human settlement (Fouque et al 2004), and in Brazil it was reported in native bromeliads growing on rocky outcrops in the urbanized areas of Vitória (Varejão et al 2005). However, the importance of native bromeliads in their natural habitat as breeding sites for A. aegypti was unknown.

Our monitoring of ovitraps distributed nearby and far away from rocky outcrops revealed A. aegypti is less abundant in residences situated at distances up to 50 m, as compared with those situated at least at 200 m away from these rocky outcrops. This contradicted the initial expectation that the greater availability of potential breeding sites provided by native bromeliads in the rocky outcrops would facilitate proliferation of this species, raising infestation rates in nearby houses. This finding indicates that rocky outcrops with native bromeliads do not play an important role in providing additional breeding sites for A. aegypti. This was also observed in south Florida, USA, and in southern Brazil (O'meara et al 2003, Varejão et al 2005).

Varejão et al (2005) noted a clear predominance of A. albopictus in native bromeliads in Vitória municipality, as this species is probably better adapted to preserved habitats. Several authors have studied larval competition between A. aegypti and A. albopictus , and A. albopictus is known to have a greater dispersal capability to more undisturbed habitats. Therefore, A. albopictus is able to reach forest margins, while A. aegypti is restricted to urban areas (Ho et al 1989, Rai 1991, Lima-Camara et al 2006).

The high color value (i.e. lightness) of natural bromeliad leaves is likely to deter oviposition by adult A. aegypti in favor of competing oviposition sites of lower color value (Frank 1985). Besides, native bromeliads have a rich macrobiota, including natural predators of mosquitoes (Richardson 1999, Armbruster et al 2002), including the native bromeliads growing on the same rocky outcrops analyzed in this study (Varejão et al 2005), which may probably play an important role in the natural control of A. aegypti.

Despite the abundance of native bromeliads in the rocky outcrops of the study area, it appears that they do not play an important role as breeding sites for A. aegypti. On the contrary, significantly lower infestation rates in houses closest to the rocks suggest that plants might act as traps for these insects. The interspecific competition between species and the attractiveness of bromeliads to this species could also be important factors discouraging their presence.

Acknowledgments

The authors wish to acknowledge the technicians of the Núcleo de Entomologia da Secretaria de Estado da Saúde do Espírito Santo for their help with the fieldwork; the Centro de Controle de Zoonoses da Prefeitura de Vitória for making available the house infestation index data; and Bruce Alexander (London School of Hygiene & Tropical Medicine) for carefully reviewing this manuscript. This work was supported by Fundo de Apoio à Ciência e Tecnologia do Município de Vitória (FACITEC).

Received 06 September 2010 and accepted 13 December 2010

Edited by Neusa Hamada - INPA

• Armbruster P, Hutchinson RA, Gotgreave P (2002) Factor influencing community structure in a South American tank bromeliad fauna. Oikos 96: 225-234.
• Barrett ADT, Higgs S (2007) Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol 52: 209-229.
• Braga IA (2007) Aedes aegypti: histórico do controle no Brasil. Epidemiol Serv Saúde 16: 113-118.
• Braga IA, Gomes AC, Nelson M, Mello RC, Bergamaschi DP, Souza JM de (2000) Comparação entre pesquisa larvária e armadilha de oviposição, para detecção de Aedes aegypti Rev Soc Bras Med Trop 33: 347-353.
• Consoli RAGB, Lourenço-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro, Editora Fundação Oswaldo Cruz, 228p.
• Cunha SP, Alves JR, Lima MM, Duarte JR, Barros LC de, Silva JL da, Gammaro AT, Monteiro Filho OS, Wanzeler AR (2002) Presença de Aedes aegypti em Bromeliaceae e depósitos com plantas no município do Rio de Janeiro, RJ. Rev Saude Publica 36: 244-245.
• Fay RW, Eliason DA (1966) A prefered oviposition site as a surveillance method for Aedes aegypti Mosq News 26: 531-535.
• Forattini OP, Marques GRM (2000) Nota sobre o encontro de Aedes aegypti em bromélias. Rev Saude Publica 34: 543-544.
• Fouque F, Garinci R, Gaborit P (2004) Epidemiological and entomological surveillance of the co-circulation of DEN-1, DEN-2 and DEN-4 viruses in French Guiana. Trop Med Int Health 9: 41-46.
• Frank JH (1985) Use of an artificial bromeliad to show the importance of color value in restricting colonization of bromeliads by Aedes aegypti and Culex quinquefasciatus J Am Mosq Control Assoc 1: 28-32.
• Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 1965-1978.
• Ho BC, Ewert A, Chew L (1989) Interspecific competition among Aedes aegypti, Ae albopictus, and Ae triseriatus (Diptera: Culicidae): larval development in miscid cultures. J Med Entomol 26: 615-623.
• Liew C, Curtis CF (2004) Horizontal and vertical dispersal of dengue vector mosquitoes, Aedes aegypti and Aedes albopictus, in Singapore. Med Vet Entomol 18: 351-360.
• Lima-Camara TN, Honório NA, Loureço-de-Oliveira R (2006) Freqüência e distribuição espacial de Aedes aegypti e Aedes albopictus (Diptera, Culicidae) no Rio de Janeiro, Brasil. Cad Saúde Pública 22: 279-284.
• Maciel-de-Freitas R, Codeço CT, Lourenço-de-Oliveira R (2007) Body size-associated survival and dispersal rates of Aedes aegypti in Rio de Janeiro. Med Vet Entomol 21: 284-292.
• Mazine CAB, Macoris MLG, Andrighetti MTM, Yasumaro S, Silva ME, Nelson MJ, Winch PJ (1996) Disposable containers as larval habitats for Aedes aegypti in a city with regular refuse collection: a study in Marília, São Paulo State, Brazil. Acta Trop 62: 1-13.
• O'meara GF, Cutwa MM, Evans Jr LF (2003) Bromeliad-inhabiting mosquitoes in south Florida: native and exotic plants differ in species compositio. J Vector Ecol 28: 37-46.
• Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Sys Sci 11: 1633-1644.
• Peryassú AG (1908) Os culicídeos do Brasil. Rio de Janeiro, Typographia Leuzinger, 407p.
• Rai KS (1991) Aedes albopictus in the Americas. Annu Rev Entomol 36: 459-484.
• Richardson BA (1999) The Bromeliad microcosm and the assessment of faunal diversity in a Neotropical forest. Biotropica 31: 321-336.
• Russel RC, Webb CE, Williams CR, Ritchie SA (2005) Mark-release-recapture study to measure dispersal of the mosquito Aedes aegypti in Cairns, Queensland, Australia. Med Vet Entomol 19: 451-457.
• SESA - Secretaria de Saúde do Estado do Espírito Santo (2008) Registros de notificação de casos de dengue no estado do Espírito Santo. Vitória, Arquivos da Secretaria de Estado da Saúde, Vitória, ES.
• Varejão JB, Santos CB, Rezende HR, 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: 238-240.
• Vasconcelos PFC (2002) Febre amarela: reflexões sobre a doença, as perspectivas para o século XXI e o risco da reurbanização. Rev Bras Epidemiol 5: 244-258.
• Zar JH (1999) Biostatistical analysis. Upper Saddle River, Prentice Hall, 931p.

Publication Dates

• Publication in this collection
  09 May 2011
• Date of issue
  Apr 2011

History

• Received
  2010
• Accepted
  13 Dec 2010