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Revision of the Leucosphyrus Group of Anopheles (Cellia) (Diptera, Culicidae)

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Revision of the Leucosphyrus Group of Anopheles (Cellia) (Diptera, Culicidae) Revision of the RevisionLeucosphyrus Groupof the of AnophelesLeucosphyrus (Cellia) group of Anopheles (Cellia) 1 (Diptera, Culicidae)1 Maria Anice Mureb Sallum2,3, E L Peyton2, Bruce Arthur Harrison4 & Richard Charles Wilkerson2 1This research was performed under a Memorandum of Understanding between the Walter Reed Army Institute of Research and the Smithsonian Institution, with institutional support provided by both organizations. The material to be published reflects the views of the authors and should be not construed to represent those of the Department of the Army or the Department of Defense. This publication is partially supported by FAPESP (05/00372-9), São Paulo, Brazil. / and U. S. NRC DAM D 17-00-2-0002 to MAMS. 2Department of Entomology, Walter Reed Biosystematics Unit, Museum Support Center, Smithsonian Institution, 4210 Silver Hill Road, Suitland, MD, 20746, U.S.A. 3Núcleo de Pesquisa Taxonômica e Sistemática em Entomologia Médica, Faculdade de Saúde Pública, Universidade de São Paulo, Brazil. Avenida Dr. Arnaldo 715, São Paulo, São Paulo, Brazil, 01246-904. 4NC DENR Public Health Pest Managment 585 Waughtown Street Winston-Salem, NC 27107, U.S.A. ABSTRACT. Revision of the Leucosphyrus Group of Anopheles (Cellia) (Diptera, Culicidae). This is a comprehensive revision of 20 species of the Leucosphyrus Group of the Neomyzomyia Series of Anopheles (Cellia). Morphological description of the adults, male and female, male genitalia, pupa and fourth-instar larva are provided for each taxon in addition to bionomics, distribution data and systematic discussion for each species, including diagnostic characters. Identification keys for females and fourth-instar larvae are provided. When possible medical importance of each species is included. Illustrations of of the adults, fourth-instar larvae and pupae are provided. Distribution maps for each species are mainly based on the material examined; however, when possible published data were also used. Tables on adult character variations, fourth-instar larval and pupal setal branching are included as appendices. A neotype for An. takasagoensis Morishita and An. sulawesi Koesoemawinangoen, and a lectotype for An. balabacensis Baisas, are designated. The authorship of An. sulawesi previously cited as Waktoedi is corrected to Koesoemawinangoen. KEYWORDS. Anophelinae; Cellia; Distribution; Morphology; Revision; Taxonomy. RESUMO. Revisão do Grupo Leucosphyrus de Anopheles (Cellia) (Diptera, Culicidae). Apresenta-se a revisão taxonômica de 20 espécies do Grupo Leucosphyrus da Série Neomyzomyia de Anopheles (Cellia). Apresentam-se as descrições morfológicas dos adultos, machos e fêmeas, genitália masculina, pupa e larva de quarto estádio, bem como dados de bionomia, distribuição e discussão sistemática para cada espécie, incluindo caracteres diagnósticos. Foram acrescentadas chaves dicotômicas de identificação para as espécies, utilizando caracteres dos adultos fêmeas e larvas de quarto estádio. Quando possível, foram incluídos dados sobre a importância médica de cada espécie. Foram também apresentadas ilustrações dos adultos, das larvas de quarto estádio e das pupas. Os mapas de distribuição das espécies foram elaborados com base no material examinado, no entanto, quando possível utilizou-se dados adicionais publicados na literatura. Fornecem-se tabelas com as variações dos caracteres dos adultos, das cerdas das larvas de quarto estádio das pupas. São designados os neótipos de An. takasagoensis Morishita e An. sulawesi Koesoemawinangoen, e o lectótipo de An. balabacensis Baisas. O nome do autor de An. sulawesi previamente citado como sendo Waktoedi foi corrigido para Koesoemawinangoen. PALAVRAS CHAVE. Anophelinae; Cellia; Distribuição; Morfologia; Revisão; Taxonomia. Species belonging to the genus Anopheles Meigen are The internal classification within the subgenus Cellia was vectors of parasites of the genus Plasmodium that cause first proposed by Edwards (1932) and later modified by several human malaria, a primarily tropical disease that threatens 42 authors as seen in Harbach (2004). The subgenus Cellia was percent of the world population in 100 countries and territories. demonstrated to be monophyletic based on cladistic analyses The World Health Organization estimates the annual global of both morphological characters (Sallum et al. 2000) and DNA incidence of acute malaria cases at 300-500 million, resulting in sequence data of several mitochondrial and nuclear genes an estimated 1.5 to 2.7 million deaths per year, of which (Krzywinski et al. 2001a,b; Sallum et al. 2002). approximately one million occur among children less than five The Leucosphyrus Group belongs in the Neomyzomyia years of age. In addition to their role as primary vectors of Series of the subgenus Cellia (King & Baisas 1936; Colless malaria, mosquitoes of the genus Anopheles additionally 1956b; Reid & Knight 1961; Reid 1968) and currently includes impact human health by transmitting lymphatic filariasis 14 named species, two geographical forms (Peyton 1989), and (Service 1993) and various mosquito-borne viruses (Gillies & six recently described species (Sallum et al. 2005). The Coetzee 1987). geographical distribution of the Leucosphyrus Group ranges The subgenus Cellia includes 224 of the 465 Anopheles from southwestern India eastwards to southern China, Taiwan, species and is divided into 6 informal series: Cellia, Myzomyia, mainland Southeast Asia, Indonesia and the Philippines (Fig. Neocellia, Neomyzomyia, Paramyzomyia and Pyretophorus. 1) (Reid 1968; Reid 1970). The internal classification of the Revista Brasileira de Entomologia 49(Supl. 1): 1-152, dezembro 2005 2 Sallum et al. Leucosphyrus Group, its species, and geographical instigated a number of additional multidisciplinary studies distribution are listed in Table 1. (Baimai et al. 1984a,b; Baimai & Green 1985; Baimai et al. 1987). This study of the Leucosphyrus Group is a product of The studies of Baimai and collaborators, as well as other over 25 years of planned collaborative efforts by many independent workers, continued and eventually helped to individuals. It started in 1977 when EL Peyton (deceased) of distinguish additional members of the group. the U. S. Army’s Medical Entomology Project at the Peyton (1989) corroborated the classification of Colless Smithsonian Institution, initiated a morphological study of (1956b) and Reid (1968) for the Leucosphyrus Group and the species in the Leucosphyrus Group. At that time the group confirmed the Hackeri (as Elegans), Leucosphyrus, and Riparis was defined by the works of Colless (1956b, 1957) and Reid Subgroups (Table 1). These three subgroups are distinguished (1968), who recognized six species, two subspecies, and five based on the ratio of the length of the proboscis to the length geographical forms that contained several important malaria of the forefemur (Fig. 2). The Leucosphyrus Group was vectors in Southeast Asia. After six months of examining demonstrated to be monophyletic and the earliest-diverged specimens available for study in the Smithsonian Institution, lineage within the subgenus Cellia (Sallum et al. 2000). it became apparent that more species were probably involved, However, phylogenetic relationships within the Leucosphyrus but additional specimens were needed to continue the study. Group, such as the monophyly of the Hackeri, Leucosphyrus, In early 1978, Peyton and Harrison started a cooperative study and the Riparis Subgroups, and relationships among species with Harrison conducting field studies that targeted have not been tested using phylogenetic methods. populations of the group, making larval and adult collections Furthermore, the systematics of the Leucosphyrus Group is for rearing adults with associated larval and pupal exuviae, problematic because it is a morphologically homogeneous establishing colonies, conducting crossing studies, and group and identification of its species from a single life stage shipping study specimens back to the Smithsonian Institution. using morphological features is difficult and sometimes The initial product of this joint arrangement was the discovery impossible. Consequently, in order to distinguish the species and description (Peyton & Harrison 1979) of a new species, correctly it is necessary to use all life stages (adult, pupa, and An. dirus Peyton and Harrison, masquerading as An. fourth-instar larva), ultrastructure of eggs (Damrongphol & balabacensis Baisas, which until that time had been recognized Baimai 1989), and also alternative methods for identification as a primary vector of human malaria in an area stretching from such as those developed by Baimai et al. (1987), Baimai et al. east India to the Philippines. Shortly thereafter eggs were (1988c,d), Sawadipanich et al. (1990), Walton et al. (1999), obtained and specimens reared of an uncommon species from Huong et al. (2001), and Manguin et al. (2002). Taiwan previously considered a synonym of An. balabacensis. The Leucosphyrus Subgroup includes the Dirus Complex, Those specimens plus the few available pinned feral specimens the Leucosphyrus Complex, An. baisasi Colless, and the revealed the Taiwan specimens to be a valid species, An. geographical form named Con Son. The Dirus Complex takasagoensis Morishita, which was distinct from An. comprises seven species (Table 1). Whereas Peyton & balabacensis. These discoveries meant that An. balabacensis, Harrison (1979) relied heavily on morphological characters of considered at that time as a primary vector of malaria the adult,
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