Mansonia spp. (Diptera: Culicidae) associated with two species of macrophytes in a Varzea lake, Amazonas, Brazil

Ruth Leila Menezes Ferreira¹, Eleny da Silva Pereira^{1, 2}, Nélia Teresinha Ferreira Har¹, Neusa Hamada¹

Recibido: 24-iv-2002
Aceptado: 14-x-2002
Correcciones devueltas por el autor: 09-x-2002

Ferreira RLM, Pereira ES, Har NTF, Hamada N. 2003. Mansonia spp. (Diptera: Culicidae) associated with two species of macrophytes in a Varzea lake, Amazonas, Brazil. Entomotropica 18(1):21-25.

Mansonia spp. larvae, in association with two species of macrophytes (Eichhornia crassipes and Ceratopteris sp.), were studied. Also, Mansonia spp. larval infection by Trichomycetes fungi was verified. The samples were collected in Camaleão Lake, Amazonas, Brazil, during four different periods of the year: high water, falling water, low water and rising water. A total of 705 Mansonia larvae were collected; 26% were in the 1^st to 3^rd instars and 74% were in the 4^th instar. E. crassipes had higher numbers of Mansonia spp. larvae (n = 623) than Ceratopteris sp. (n = 82). Four Mansonia species were collected (M. humeralis, M. indubitans, M. amazonensis and M. titillans); the first of these was the most abundant species in the four sampling periods and in both plant species studied. Trichomycetes fungi were not observed infecting the digestive tracts of the dissected Mansonia spp. larvae (n = 190).

Additional key words: Aquatic insects, aquatic plants, mosquitoes, Trichomycetes.

Resumo

Ferreira RLM, Pereira ES, Har NTF, Hamada N. 2003. Mansonia spp. (Diptera: Culicidae) associadas a duas especies macrofitasem um lago de Varzea, Amazonas, Brasil. Entomotropica 18(1):21-25.

Larvas de Mansonia spp. em associação com duas espécies de macrófitas (Eichhornia crassipes e Ceratopteris sp.) foram estudadas. A infecção larval de Mansonia spp. por fungos Trichomycetes também foi verificada. As amostras foram coletadas no Lago Camaleão, Amazonas, Brasil, em quatro períodos do ano: cheia, vazante, seca e enchente. Um total de 705 larvas de Mansonia foram coletadas; sendo 26% do 1⁰ ao 3⁰ estádio e 74% do 4⁰ estádio. E. crassipes apresentou um maior número de larvas de Mansonia spp. (n = 623) do que Ceratopteris sp. (n = 82). Quatro espécies de Mansonia foram coletadas (M. humeralis, M. indubitans, M. amazonensis e M. titillans); M. humeralis foi a espécie mais abundante nos quatro períodos amostrados e nas duas espécies de plantas. Fungos Trichomycetes não foram observados infectando o trato digestivo das larvas de Mansonia spp. dissecadas (n = 190).

Palavras chaves adicionais: Insetos aquáticos, mosquitos, plantas aquáticas, Trichomycetes.

Introduction

Female Mansonia are known for their hematophagic behavior, and, when in high density, they can cause serious medical and social problems, as has occurred in some hydroelectric dams in the Amazon region (Tadei et al. 1991). Females have both diurnal and nocturnal activity, making life difficult for humans and other animals in places where Mansonia females are found in high density. As in all hematophagous insects, some species in this genus have potential as vectors of etiologic agents that cause diseases such as arboviruses to humans and other animals (Karabatsos 1985).

The immature live associated with aquatic plants, obtaining O₂ from the plant tissues and ingesting suspended organic matter by filter feeding. In the Amazon region aquatic plants grow in abundance in inundated areas and maintain large populations of invertebrates and vertebrates (Junk 1973); they are a fundamental part of this ecosystem. When the ecosystem is disturbed and loses its equilibrium, the aquatic plants quickly increase their populations, causing serious problems (Tadei et al. 1991). Culicidae species other than those in the genus Mansonia that are closely associated with aquatic plants include Aedeomyia squamipennis (Lynch Arribálzaga), Coquillettidia sp., Culex sp., Uranotaenia sp. and Anopheles sp. (Lounibos and Escher 1985; Tadei 1990).

Trichomycetes (Zygomycota) fungi are obligate symbionts associated with the digestive tracts of various insects and other arthropods. The relationship of Trichomycetes to their hosts is generally commensalistic, but it can be pathogenic or mutualistic (Lichtwardt 1986; López Lastra 1990). Smittium morbosum Sweeney can be pathogenic to species of Anopheles, Aedes and Culex (Sweeney 1981); other species may have this same relationship and with adequate studies could be used to control populations of species that are noxious to humans.

Knowledge of the distribution of mosquito species, their habitats and control agents is essential to developing integrated control methods for these insects, which can be very annoying at high density. In Central Amazonia, biological studies of Mansonia are limited to the reports by Ferreira (1999), Ferreira & Nunes de Mello (1999) about Mansonia eggs, larvae and pupae on Eichhornia crassipes (Mart.) Solms. (Pontederiaceae) and Pistia stratiotes Linnaeus; (Araceae). The objectives of the present study are to survey the Mansonia spp. associated with E. crassipes and Ceratopteris sp. at different water levels of the Negro River and to verify the larval infection of Mansonia spp. by Trichomycetes fungi.

Materials and Methods

The present study was done in Camaleão Lake, Marchantaria Island, Iranduba County (AM), Brazil (60º00'N; 3º15'S) (Figure 1). This island is located 15 km from the city of Manaus and it is surrounded by white water of the Solimões (Upper Amazon) River, near the meeting of the black and white waters of the Negro and Solimões Rivers. Lake Camaleão is part of the floodplain or várzea where the water is rich in sediments and nutrients, with distinct inundation and non-inundation periods (Junk 1973).

Information on the water level of the Negro River was used to determine the inundation period in the study area. These data were obtained at the Capitania dos Portos (port authority) in Manaus, AM, and were composed of daily measurements made at Manaus. The present study was done in four distinct periods: high water (June), falling water (August), low water (October) and rising water (March), 1998/99 in Ceratopteris sp. and E. crassipes meadows, both species of plant are known to hold Mansonia spp. (Ferreira 1999a, b).

Sampling was done in four E. crassipes meadows and four Ceratopteris sp. meadows chosen randomly at points between the Solimões River and the center of the lake. In each meadow the plants were collected from the water and immediately placed in a net (40 x 30 x 10 cm) and transferred to a plastic container (55 x 30 x 7 cm). The plant roots were cut with scissors and knife. Eleven liters (0.011m³) of roots were collected in each meadow. Before cutting the roots, the plants used to fill the 11-liter container were counted. Each plastic container of roots was closed with a lid and transported to the laboratory. The larvae that came out of the roots were collected using plastic pipettes and taken to the laboratory in a plastic container containing a small aquatic plant and water from the habitat. Identification to species was based on Ronderos & Bachman (1963), and only last-instar larvae were identified at the specific level.

A total of 190 last-instar larvae were dissected to observe the presence of Trichomycetes fungi associated with their digestive tracts, following the technique of Lichtwardt (1986). The technique consists of pulling out the median and posterior intestines through a ventral-median incision in the larva, placing these structures in distilled water under a cover slip and examining them under a compound microscope to verify the presence of Trichomycetes fungal structures.

Results and Discussion

A total of 705 Mansonia larvae were collected; 26% (n = 82) were in the first to third instars and 74% (n = 623) were in the fourth instar. Both sampled plant species showed differences in larval mean density (larvae/m³ and larvae/plant), in the four periods evaluated (Tables I and II). Four Mansonia species were collected in the study area: M. humeralis (Dyar & Knab), M. indubitans Dyar & Shannon, M. titillans (Walker) and M. amazonensis (Theobald). Mansonia indubitans is reported for the first time in Camaleão Lake, the other three species were already reported, based on egg masses, by Ferreira & Nunes de Mello (1999). Ferreira (1999) studied Mansonia spp. in E. crassipes and P. stratiotes, reporting higher densities of larvae and pupae in E. crassipes than in P. stratiotes in the falling-water period (August-October). Mansonia (Mansonia) is neotropical, and some species such as M. indubitans and M. titillans reach the extreme southern portion of the nearctic region. According to Guimarães (1997), this subgenus has 13 species, 10 of which occur in Brazil and six in Amazonia (Cerqueira 1961).

Mansonia humeralis was the most abundant species in the four periods evaluated and in both species of aquatic plant studied. These results agree with the observations of egg masses by Ferreira (1999), who reported that 74% of egg masses collected in Camaleão Lake belonged to M. humeralis.

Last-instar larvae of three Mansonia species were collected in the high-water period in Ceratopteris sp., four species in falling water, two in low water and none in rising water. In E. crassipes, four Mansonia species were collected in the first three periods evaluated, and in the fourth period three species were collected, M. amazonensis being the species that was not collected in this period.

The data indicate that Ceratopteris sp. not only shelters a lower number of Mansonia spp., but also has a lower Mansonia species richness in some periods of the year.

We suggest the following hypotheses to explain this fact: a) the size of the aerenquima in E. crassipes is larger than in Ceratopteris sp.; Eichhornia can therefore hold more oxygen and could maintain a greater number of larvae; b) the fact that the root tissues of Ceratopteris sp. are more rigid would impede perforation by the larval siphon; or c) based on the fact that many species in the Pteridophyta division have toxic secondary substances (Tokarnia et al. 1979), Ceratopteris sp. may have secondary substances that would be noxious or repellent to Mansonia larvae.

In the studied period mean density of Mansonia spp. larvae was 708 specimens/m³ and 0.37 specimens/plant in E. crassipes and 93 specimens/m³ and 0.03 specimens/plant in Ceratopteris sp. The highest numbers of larvae on the two plants occurred mainly in the low- and falling-water periods (Tables I, II; Figs 2a, b). It is possible that this happens because the larger amount of nutrients present in the rising period allow the growth rate to increase; aquatic plants proliferate and provide more shelter and food to associated fauna (Junk 1970).

None of the dissected last-instar larvae (n = 190) was infected with Trichomycetes species. In Argentina, García et al. (1995) observed that only 1.8% of dissected M. titillans and M. indubitans were infected with Smittium sp. (Trichomycetes: Harpellales). Experiments in the laboratory indicated that spore production decreases as a function of increasing temperature in three species of Smittium (Lichtwardt 1986). Since the water temperature of Mansonia spp. habitat in the study area was high (29ºC to 32ºC), it is possible that temperature is related to the absence of Trichomycetes in the dissected Mansonia spp. larvae.

Table I. Mean density (larvae/m³ and larvae/plant) and relative percentage (%) of Mansonia spp. (Diptera:Culicidae) on 
Eichhornia crassipes (Pontederiaceae), in Camaleão Lake, Iranduba County, Amazonas, Brazil, in the June 1998 - March 1999 period.

Table II. Mean density (larvae/m³ and larvae/plant) and relative percentage (%) of Mansonia spp. (Diptera:Culicidae) on Ceratopteris sp. (Parkeriaceae), in Camaleão Lake, Iranduba County, Amazonas, Brazil, in the June 1998 - March 1999 period.

Acknowledgments

Fernando P. Gouveia, Luís Aquino and Aldenira F. Oliveira collaborated in the fieldwork. P.M. Fearnside made helpful suggestions on the manuscript. The second and third authors received fellowships from Pibic/Inpa/CNPq.

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