Dispersion of Aedes aegypti (Linnaeus, 1762) and Aedes albopictus (Skuse, 1894) in the rural zone of north Paraná State

HUMAN AND ANIMAL HEALTH

Dispersion of Aedes aegypti (Linnaeus, 1762) and Aedes albopictus (Skuse, 1894) in the rural zone of north Paraná State

José Lopes^I,*; Emerson Augusto Castilho Martins^I; Osmar de Oliveira^II; Valdecir de Oliveira^II; Bertolino Pedro de Oliveira Neto^II; José Eduardo de Oliveira^II

^IDepartamento de Biologia Animal e Vegetal; Universidade Estadual de Londrina; C. P. 6001; 86051-970; Londrina - PR - Brazil

^IIInstituto de Saúde do Paraná; 17º Regional de Saúde; Trav. Goiânia, 152; 86020-170; Londrina - PR - Brazil

ABSTRACT

Seventy-two tyres were placed in four transects (Northern, Southern, Eastern and Western), every 5 km, from the Londrina city limits to the rural areas, to verify the dispersion of Aedes aegypti and Ae. albopictus vectors. Mosquito larvae were collected fortnightly from August 1998 to August 1999. Data were organized according to the average number of larvae collected for each species in each collection site. A total of 62,517 mosquito larvae were collected and distributed into the following species: Aedes albopictus (21.71%); Ae. aegypti (5.54%); Ae. terrens (0.53%); Ae. fluviatilis (0.36%); Anopheles argyritarsi (0.01%); Culex quinquefasciatus (48.37%); Cx. mollis (8.88%); Cx. eduardoi (8.65%); Cx. corniger (0.61%); Cx. bigoti (0.24%); Cx. grupo coronator (0.12%); Limatus durhanii (4.61%) e Toxorhynchites sp. (0.32%). There was a drastic decrease in the Ae. aegypti population from the city limits to the rural area (x₁= 21.72 ± 4.71; x₂=0.00) and an increase in the population of Ae. albopictus (x₁ = 15.64 ± 2.73; x₂ = 38.37 ± 8.87). Aedes aegypti was not present in the collection sites located 30 km away from the urban area; however, Ae. albopictus was found in all the sites. Although the frequency rate for the Aedes aegypti was low, both species were dispersed in the rural area studied. The redimensioning of these vectors’ control areas is recommended since rural areas can function as reservoirs for these species.

Key words:Aedes, population dispersion; dengue, prevention and control; breeding sites

RESUMO

Com o objetivo de avaliar a dispersão de Aedes aegypti e Ae. albopictus para a área rural, foram instalados pneus em quatro transectos (Norte, Sul, Leste e Oeste), a cada 5 Km, do limite da zona urbana de Londrina em direção a zona rural. Larvas de Culicidae foram coletadas quinzenalmente de agosto de 1998 a agosto de 1999. Um total de 62.517 larvas de Culicidae foram coletadas, distribuídas entre as seguintes espécies: Aedes albopictus (21.71%); Ae. aegypti (5.54%); Ae. terrens (0.53%); Ae. fluviatilis (0.36%); Anopheles argyritarsi (0.01%); Culex quinquefasciatus (48.37%); Cx. mollis (8.88%); Cx. eduardoi (8.65%); Cx. corniger (0.61%); Cx. bigoti (0.24%); Cx. grupo coronator (0.12%); Limatus durhanii (4.61%) e Toxorhynchites sp. (0.32%). Houve uma drástica diminuição na população de Ae. aegypti dos limites da cidade para a zona rural (x₁= 21.72 ± 4.71; x₂=0.00) e um aumento da população de Ae. albopictus (x₁ = 15.64 ± 2.73; x₂ = 38.37 ± 8.87). Aedes aegypti não foi encontrado somente nos pontos situados a 30 Km da cidade; no entanto, Ae. albopictus foi encontrado em todos os pontos. Conclui-se que ambas espécies encontram-se dispersas para a zona rural da área estudada e que é necessário um redimensionamento da área de controle destes vetores, já que a zona rural pode servir como um refúgio destas espécies.

INTRODUCTION

Aedes (Stegomyia) aegypti (L., 1762) is the main dengue vector species found in urban areas. In some Brazilian regions, this virulent disease has reached epidemic levels, with the detection of the D1, D2, D3 and D4 sorotypes. Aedes (Stegomyia) albopictus (Skuse, 1894) is the main dengue and yellow fever vector found in the Asian continent, whereas in Brazil its vectorial activity has not been proved yet. However, Mitchell and Miller (1990) reported a dengue virus vertical transmission by one Brazilian population of Ae. albopictus. Serufo et al. (1993) detected in Campos Altos, Minas Gerais, Brazil, Ae. albopictus larva infected by the D1 virus.

Aedes aegypti is a highly domesticated mosquito, which prefers to lay eggs in artificial breeding places widely found in tropical urban areas. The dumping of used tyres and plastic containers has increased in the last few years, contributing to the increase of Ae. aegypti populations in tropical urban areas. Since these items retain water, they turn into breeding places, potentially increase the incidence of diseases caused by the etiological agents transmitted by these mosquitoes (Gubler, 1998).

The presence of Ae. albopictus in South America was firstly reported by Forattini (1986), who confirmed the homology and sympatricity in Ae. aegypti and Ae. albopictus, and the greater degree of exofilia and wild habits in Ae. albopictus. In the urban area of Londrina, Paraná, Brazil, Ae. aegypti was first detected in 1985, by Lopes et al (1993) and the Ae. albopictus was first detected by FUNASA (Fundação Nacional da Saúde) in 1993.

Recent research on the presence of Ae. aegypti and Ae. albopictus in urban areas has investigated the dispersion capacity of these species either by mark-release-recapture techniques (Edman et al., 1998; Muir and Kay, 1998) or by feeding females with blood containing rubidium, a substance that can be detected in eggs through atomic spectroscopy (Reiter, 1996). These studies showed that contrary to the current concepts of dispersion, Ae. aegypti females dispersed up to 800 m to lay their eggs. This dispersion pattern is related to weather conditions and to the availability of larval habitats (Edman et al., 1998). Thus, the elimination of breeding places can stimulate dispersion and/or increase the egg- laying period. Campaigns against dengue in Brazil are carried out by eradicating egg-laying sites and by forcing the vector species to disperse to the most remote areas away from the city or to the city’s surrounding areas in search of breeding sites. The government had recently concluded the first phase of a national Ae. aegypti eradication campaign (PEAa); however, results were unsatisfactory. More scientific information on the biological and ecological characteristics of this vector species is necessary for the development of further control actions.

The objective of this study was to evaluate the possible dispersion pattern of Ae. aegypti and Ae. albopictus in the periurban and rural areas of Metropolitan region of Londrina, Paraná, Brazil.

MATERIAL AND METHODS

Four transects oriented to the cardinal points were drawn from the city limits of Londrina, Paraná (23º08’47"S; 50º52’23"W), to the rural areas, as far as the neighboring counties of Cambé, Ibiporã, Sertanópolis and Rolândia (Fig. 1). The experiment was divided into 2 phases:

Phase 1: From 08.01.98 to 02.01.99

Five collection sites, set 5 km apart from each other, were established for each transect, starting at the city limit. Three tyres filled with two liters of water were placed vertically at three locations: one near the house, another at 10m from the house and other 20m from the house.

Phase 2: From 03.01.99 to 08.01.99

With the detection of Ae. albopictus and Ae. aegypti dispersion during the first phase of this study, especially in the tyres placed at collection sites closer to the city limit, a re-organization of the sites was made. All sites set along the Northern and Western transects were eliminated, and two new sites were added: one 25 km from the city limit and the other 30 km. As for the Southern transects, collection sites set at 5 and 15 km away from the city limit were eliminated and a new one was added at 25 km. A new site was added at 25 km from the city limit along the eastern transect, and the collection site at the city limit was eliminated. During this phase, all tyres placed 20 km away from the houses were eliminated.

Collection sites were checked fortnightly and the material was collected by taking all the water out of the tyres through a 100 mm meshed sieve, into a silver tray and then into a plastic receptacle. Next, the water was poured back into the tyres and filled with more water to reach the level whenever needed. First, second and third instar larva were kept alive to mature to the fourth instar. Pupae were bred into adults. Fourth instar larva and exuvia were mounted on microscope slides containing Hoyer’s medium for specific identification. One sample of collected larva was reared to compare the larva exuvia to their respective adults. Data on temperature and precipitation were provided by IAPAR (Instituto Agronômico do Panará). Experimental data were organized in a graph according to distances, larval means and standard errors, to detect differences which could represent the dispersion of these species.

RESULTS

This study was carried out from August 1998 to August 1999, with pause in collects during the month of January, 1999. From the 24 collections, 62,517 samples of 13 species of Culicidae were identified (Table 1). Aedes albopictus was the most commonly found species (21.7%), outnumbered only by the Culex quinquefasciatus (48.4%), a native species (Table 2). Culex quinquefasciatus was the most abundant species in the periurban area, and was outnumbered by Ae. albopictus in the more distant collection sites (Fig. 2). Aedes aegypti population density decreased significantly as the transect moved farther from urban areas whereas the opposite happened with Ae. albopictus (Fig 2).

In this study, farm houses were always surrounded by orchards and brushwood. This could influence the activity of these hematophagus insects. Figure 2 shows the data collected from tyres placed at 0, 10 and 20 m from houses. No significant differences were found among the Ae. aegypti collected from tyres placed at these distances. Data showed that in the distances in which Ae. albopictus was more abundant, Ae. aegypti density was smaller (Fig. 3). Aedes aegypti was most frequently found in the Northern transect, followed by the Western, Southern and Eastern transects, respectively. Aedes albopictus also showed preference for the Northern transect, however, the transect with the lowest frequency was the Southern and there were no significant differences between the Eastern and the Western transects (Fig. 4).

Both species were abundant during the first semester: Ae. albopictus in March and April and Ae. aegypti in June (Fig. 5). During the Ae. albopictus high frequency months, the precipitation was less than 130 mm per month.

DISCUSSION

A large number of Ae. aegypti and Ae. albopictus were collected from the tyres placed in the periurban and rural areas of Londrina, Paraná. At the most distant sites, Ae. albopictus was more than Cx. quinquefasciatus. Data suggested some type of competition, once Cx. quinquefasciatus showed low density where the Ae. albopictus was highly dense. Aedes albopictus was an introduced species that showed more competitive advantages over the native species Cx. quinquefasciatus. Moreover, Cx. quinquefasciatus tolerated more polluted water, condition find frequently in urban areas. Service (1966) reported on a similar situation in Africa, right after WWII, when Culex fatigans Wieldmann, 1828, an introduced species, displaced Cx. nebulosus Theobald, 1901. Rios et al. (1978) reported on the adaptative advantages of Ae. aegypti over the Cx. fatigans since the metabolics produced by the first species made it difficult for the latter to procreate.

Aedes aegypti was significantly abundant in the collections carried out in the periurban area, confirming its well-known urban habits; Aedes albopictus, on the other hand, was abundant at the collection sites located 30 km from the city limits. There was a tendency for the Ae. albopictus population to increase as collection site distances increased. According to O’Meara et al.(1995) Ae. albopictus prevailed under an apparent lack of human resources for blood meals in Southern Florida. This could explain the high density of Ae. albopictus observed in this study at collection sites away from the city where blood repast resources were limited. The decrease in Ae. aegypti numbers as distances from the city limit increased, could not be ignored because the mosquito was present in all the collection sites located up to 25 km away from the urban area. In Brazil, control campaigns for this vector has been carried out by eliminating breeding sites which, according to Edman et al. (1998), could induce dispersion. This effect can happen by the many control campaigns being conducted in Londrina.

The presence of Ae. aegypti in rural areas produces an increase in the incidence of public health problems/diseases since these campaigns seldom reach these areas, which could become reservoirs for the mosquito.

There was no significant preference by the Ae. aegypti for the tyres placed at different distances from houses; however, Ae. albopictus was frequently found 10 m from the house, which could indicate endophilia.

The highest dispersion of Ae. aegypti and Ae. albopictus was found along the Northern transect, located next to the PR-445 state highway, an area with several gas stations and restaurants, and close to Warta Village and to the Ibiporã and Sertanópolis counties. Results from the Western transect, which showed the second highest larval mean for Ae. aegypti, could have been influenced by the proximity of the urban areas of the Cambé and Rolândia counties. The Western transect ran through the least urbanized areas which could explain the greatest mean difference between Ae. albopictus and Ae. aegypti as well as the smallest density for the latter.

Rain indexes influence the availability of breeding sites for the Culicidae as higher indexes tend to produce an increase in the population density of some species after a certain period, as the number of breeding places increases during the rainy months (Marquetti et al., 1986). The temperature, however, influences insect metabolism directly, since they are ectotherms and their vital activities are regulated by external temperature. Aedes aegypti density increased when the temperature was at its lowest mean and the rain index for the previous month was relatively low. However, Ae. albopictus population density increased after rain index was associated with high temperatures, going down as the index decreased. This is an expected behavior for the Culicidae. It could be inferred that the high Ae. albopictus population density observed in the breeding places could have had a negative influence on the settling of Ae aegypti under good temperature and humidity conditions. Data from Juliano (1998) corroborated with this finding by showing that the presence of Ae. aegypti persisted only in places where its interspecific competition with Ae. albopictus was less intense. Some other non-evaluated factors could have influenced the low means obtained for the species during the first part of the experiment. One of the probable factors could be the presence of substances produced by larva in the water inside the tyres, which could be attracting pregnant females to lay eggs, since the water was poured back into the tyre after the larva were collected.

Results from this study showed that Ae. aegypti and Ae. albopictus were found in the rural areas of Londrina, the first species being less abundant and the latter well-adapted to the area’s conditions. We recommend the inclusion of the rural areas in future methods for controlling these mosquitoes in Londrina, Paraná, Brazil.

AKNOWLEDGEMENTS

We would like to thank Maria Carolina Gomiero Oricolli, a graduate student, for her technical assistance, MSc. João A. C. Zequi and MSc. Paulo A. C. Pereira for their scientific consultancy, and IAPAR for providing temperature and rain index information

Received: November 05, 2002;

Revised: June 12, 2003;

Accepted: May 11, 2004.

• Edman, J. D.; Scott, T. W.; Costero, A.; Morrison, A. C.; Harrington, L. C. and Clark, G. G. (1998), Aedes aegypti (Diptera: Culicidae) movement influenced by availability of oviposition sites. J. Med. Entomol., 35 : (4), 578-583.
• Forattini, O. P. (1986), Identificação de Aedes (Stegomyia) albopictus (SKUSE) no Brasil. Rev. Saúde Pública, 20, 244-245.
• Gubler, D. J. (1998), Dengue and dengue hemorragic fever. Clin. Microbiol. Rev., 11, 480-496.
• Juliano, S. A. (1998), Species introduction and replacement among mosquitoes: interespecific resource competition or apparent competition? Ecology, 1, 255-268.
• Lopes, J.; Silva, M. A. N.; Borsato, A. M.; Oliveira, V. D. R. B. and Oliveira, F. J. A. O. (1993), Aedes (Stegomyia) aegypti L. e a culicideofauna associada em área urbana da região Sul, Brasil. Rev. Saúde Pública, 27 : (5), 326-333.
• Marquetti, M. C. F.; Lazano, J. A. and Ortega, A. N. (1986), Influencia de algunos facores abióticos sobre lãs fluctuaciones de la poblacion larval de Culex quinquefasciatus Say, 1823 (Diptera: Culicidae). Rev. Cubana Med. Trop., 38 : (3), 281-288.
• Mitchell, C. J. and Miller, B. R. (1990), Vertical transmission of Dengue Viruses vy strains of Aedes albopictus recently introduced into Brazil. J. Am. Mosq. Control Assoc., 6 : (2), 251-253.
• Muir, L. E. and Kay, B. H. (1998), Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am. J. Trop. Med. Hyg., 58 : (3), 277-282.
• OMeara, G. F.; Evans Jr., L. F.; Gettman, A. D. and Cuda, J. P. (1995), Spread of Aedes albopictus and decline of Ae. aegypti (Diptera: Culicidae) in Florida. J. Med. Entomol., 32 : (4), 554-562.
• Reiter, P. (1996), Oviposition et dispersión dAedes aegypti dans lenvironnement urbain. Bull. Soc. Pathol. Exot., 89 : (2), 120-122.
• Rios, A. A.; Machado-Allison, C. E.; Rabinovich, J. E. and Rodriguez, D. J. (1978) Competencia intra e iterespecifica en Aedes aegypti (L.) y Culex fatigans Wied. (Diptera: Culicidae) en condiciones de laboratorio. Acta Cient. Venez., 29 : (6), 467-472.
• Serufo, J. C.; Deoca, H. M.; Tavares, V. A.; Souza, A. M.; Rosa, R. V. and Jamal, M. C. et al. (1993) Isolation of Dengue Virus type-1 from larvae of Aedes albopictus in Campos Altos City, State of Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz, 88 : (3), 503-504.
• Service, N. M. (1966), The replacement of Culex nebulosus Theo. by Culex pipens fatigans Wied. (Diptera: Culicidae) in Towns in Nigeria. Bull. Entomol. Res., 56, 407-415.

*

Author for correspondence

Publication Dates

• Publication in this collection
  23 Nov 2004
• Date of issue
  Sept 2004

History

• Received
  05 Nov 2002
• Reviewed
  12 June 2003
• Accepted
  11 May 2004