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Anopheline Species Complexes in Brazil. Current Knowledge of Those Related to Malaria Transmission

Maria Goreti Rosa-Freitas Ricardo Lourenço-de-Oliveira Carlos José de Carvalho-Pinto Carmen Flores-Mendoza Teresa Fernandes Silva-do-Nascimento About the authors


A summary of the problems related to the systematics of primary and secondary Brazilian anophelines vectors of malaria is presented.

Anopheles systematics; species complexes; malaria vectors; Nyssorhynchus; Kerteszia

Anopheline Species Complexes in Brazil. Current Knowledge of Those Related to Malaria Transmission

Vol. 93(5): 651-655

Maria Goreti Rosa-Freitas/+, Ricardo Lourenço-de-Oliveira*, Carlos José de Carvalho-Pinto*/**, Carmen Flores-Mendoza*, Teresa Fernandes Silva-do-Nascimento*

Laboratório de Sistemática Bioquímica, Departamento de Bioquímica e Biologia Molecular *Laboratório de Transmissão de Hematozoários, Departamento de Entomologia, Instituto Oswaldo Cruz, Av. Brasil 4365,

21045-900 Rio de Janeiro, RJ, Brasil **Departamento de Microbiologia e Parasitologia,

Universidade Federal de Santa Catarina, Florianópolis, SC, Brasil

A summary of the problems related to the systematics of primary and secondary Brazilian anophelines vectors of malaria is presented.

Key words: Anopheles systematics - species complexes - malaria vectors - Nyssorhynchus - Kerteszia



Many neotropical anopheline species are either candidates or formed by complex of cryptic species. The taxonomic elucidation of these complexes reflects on the epidemiology of malaria transmission and ultimately to the control.

In Brazil, there are 54 species belonging to five subgenera of Anopheles Meigen (Nyssorhynchus, Kerteszia, Stethomyia, Lophopodomyia, Anopheles). Anopheline species reported as human malaria vectors in the country belong to the subgenera Nyssorhynchus and Kerteszia (Deane 1986, Consoli & Lourenço-de-Oliveira 1994).

In the subgenus Nyssorhynchus, the species found harboring human plasmodia include Anopheles darlingi Root 1926, An. aquasalis Curry 1932, An. albitarsis sensu lato Lynch-Arribálzaga 1878 (including An. deaneorum Rosa-Freitas 1989), An. oswaldoi Peryassú 1922, An. nuneztovari Gabaldon 1940 and An. triannulatus (Neiva & Pinto 1922). In the subgenus Kerteszia natural infections were reported for An. cruzii Dyar & Knab 1908, An. bellator Dyar & Knab 1906 and An. homunculus Komp 1937. It is our opinion that other species reported naturally infected do not play a role in malaria maintenance as they are exophilic, zoophilic, of low density and their distribution and frequency do not coincide with that of malaria. Except for An. darlingi, the natural history of the species listed above points out for zoophilic and/or exophilic behavior in some areas, in such a fashion that their role in malaria transmission is doubted (Deane 1986). Are these characteristics an indication that these species are indeed complexes?

To decide whether a given species is high polymorphic or a complex of closely related species, integrated approach studies on distinct populations, including on that of the type-localities and where morphological/behavioral/molecular differences have been reported, are mandatory. Most of the Brazilian anopheline species has been taxonomically investigated by morphology, behavior and molecular tools such as isoenzymes and DNA analyses (mitochondrial and ribosomal DNA restriction analysis, random amplification and sequencing of specific regions) as summarized on Table.

More than 99% of the malaria cases reported in Brazil occur in the Amazon in which transmission is due to Nyssorhynchus species only.

An. darlingi is the most important Brazilian malaria vector (Shannon 1933, Rachou 1958). The species is the most anthropophilic and endophilic among the Amazonian anophelines. It is frequently found infected and its distribution and density are clearly related to malaria transmission. Even though many populations of the species have been lately reported as biting outdoors, An. darlingi continues successfully transmitting malaria both indoors and at the close vicinity of the houses (Lourenço-de-Oliveira 1995). Isoenzymatic, behavioral and mitochondrial DNA studies on either Brazilian (Rosa-Freitas et al. 1992, Freitas-Sibajev et al. 1995) or other Latin-American (Manguin et al. 1998) populations, showed that An. darlingi is a monotypic species.

An. aquasalis is the lowland coastal vector in Brazil. Chromosomal banding pattern and mtDNA restriction profiles of specimens from Venezuela and Brazil were identical (Moncada-Pérez & Conn 1991, Conn et al. 1993a). Isoenzymes from three populations of Venezuela and Surinam (Steiner et al. 1981) and two from Brazil (Flores-Mendoza 1994) with behavioral differences also revealed only intraspecific variation. Egg morphology of An. aquasalis varies intraspecifically (Maldonado et al. 1997). In fact, variation was seen in a single female oviposition (Flores-Mendoza 1994). Results of mitochondrial DNA and egg morphology analyses however, suggest that there might be an interspecific division in An. aquasalis populations north and south of the Amazon River delta (Conn et al. 1993a, Linley et al. 1993).

An. albitarsis is a complex formed by, at least, four sibling species: An. marajoara Galvão & Damasceno 1942, An.albitarsis sensu stricto Lynch-Arribálzaga 1878, An. deaneorum and a fourth form to be formally described (Rosa-Freitas et al. 1990, Wilkerson et al. 1995). Since An. deaneorum is the only morphologically distinguishable member of the albitarsis complex, the role of each member in malaria transmission has not been determined yet. The incrimination of other members of the complex, except An. deaneorum (Klein et al. 1991a, b), were based solely on their presumed geographical distribution.

An. oswaldoi has been regarded as a potential malaria vector in some localities of the Amazon (Arruda et al. 1986, Oliveira-Ferreira et al. 1990, Branquinho et al. 1996) although some authors believe that most populations of this species are much more related to the natural environment and prefer to feed on animals than on man indoors (Deane et al. 1948, Consoli & Lourenço-de-Oliveira 1994, Lourenço-de-Oliveira & Luz 1996). The taxonomic status of the species is under investigation (PhD work of CFM). Preliminary results from morphological analyses demonstrate that at least two forms are present under An. oswaldoi: An. oswaldoi sensu stricto and An. konderi Galvão & Damasceno 1942, distinguished pratically only by the shape of the apex of aedeagus (Causey et al. 1946, Lounibos et al. 1997).

Morphology, behavior, cytogenetics, isoenzymes and mtDNA studies favor the existence of at least two cryptic species in An. nuneztovari: one in Venezuela and Colombia northwest of Orinoco and another in the Amazon (Conn et al. 1993b, Fritz et al. 1994, Linley et al. 1996). The species is considered a primary malaria vector in Venezuela and Colombia (Gabaldon 1969, Gabaldon et al. 1975). In Brazil however, the species is not related to malaria transmission, although natural infection by Plasmodium vivax has been detected in areas where darlingi was the primary vector (Arruda et al. 1986).

An. triannulatus is constituted by at least three sibling forms. These forms can be differentiate morphologically (egg, larva and male genitalia) and isoenzymatically (Silva-do-Nascimento 1995). The typical triannulatus is the most known and largely distributed form. The other two forms seem to be restricted mostly to central Brazil and are not related to malaria transmission.

The mosquitoes of the subgenus Kerteszia share the common characteristic of using bromeliads as breeding places. An exception is An. (Ker.) bambusicolus Komp 1937 that also breeds in bamboo.

An. (Kersteszia) cruzii and An. bellator were primary vectors of the malaria once endemic in southeastern/southern Brazil (Rachou 1958). An. cruzii is currently involved in the maintenance of the oligosymptomatic malaria occurring in the valleys of the Atlantic Coastal Rain Forest in both Rio de Janeiro and São Paulo states (Carvalho et al. 1988, Azevedo 1997, Branquinho et al. 1997). Larval differences were observed in An. cruzii populations from Rio de Janeiro and Santa Catarina (Zavortink 1973). Besides, chromosomal banding pattern differences were also found among several An. cruzii populations (Ramirez 1989, Dessen pers. comm.). An. homunculus is a morphologically close related species and there is the possibility of being a sibling species in the cruzii complex (PhD work of CJCP). The remaining Kerteszia species do not seem to be important in malaria transmission in Brazil.

In summary, An. darlingi is a monotypic species. An. aquasalis and An. nuneztovari are possibly complexes. An. albitarsis, An. triannulatus and An. oswaldoi are complexes of species. Anopheline species of the subgenus Kersteszia are still under investigation (Table).

The refinement of the taxonomic tools and the addition of other populations are likely to lead to new insights into the knowledge and understanding of the neotropical species complexes.


+Corresponding author.


Received 15 June 1998

Accepted 30 July 1998

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Publication Dates

  • Publication in this collection
    14 Oct 1998
  • Date of issue
    Sept 1998


  • Accepted
    30 July 1998
  • Received
    15 June 1998
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