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(Diptera: Culicidae). II. Fourth-Instar Larvae Sallum et al. Parasites Vectors (2020) 13:582 https://doi.org/10.1186/s13071-020-04299-5 Parasites & Vectors RESEARCH Open Access Identifcation keys to the Anopheles mosquitoes of South America (Diptera: Culicidae). II. Fourth-instar larvae Maria Anice Mureb Sallum1*, Ranulfo González Obando2, Nancy Carrejo2 and Richard C. Wilkerson3,4,5 Abstract Background: Accurate species identifcation of South American anophelines using morphological characters of the fourth-instar larva is problematic, because of the lack of up-to-date identifcation keys. In addition, taxonomic studies, employing scanning electron microscopy of the eggs and DNA sequence data, have uncovered multiple complexes of morphologically similar species, and resulted in the resurrection of other species from synonymy, mainly in the subgenus Nyssorhynchus. Consequently, the identifcation keys urgently need to be updated to provide accurate morphological tools to identify fourth-instar larvae of all valid species and species complexes. Methods: Morphological characters of the fourth-instar larvae of South American species of the genus Anopheles were examined and employed to elaborate a fully illustrated identifcation key. For species for which no specimens were available, illustrations were based on published literature records. Results: A fully illustrated key to the fourth-instar larvae of South American species of the genus Anopheles (Diptera: Culicidae) is presented. Defnitions of the morphological terms used in the key are provided and illustrated. Conclusions: Morphological identifcation of South American Anopheles species based on the fourth-instar larvae has been updated. Characters of the spiracular apparatus were determined useful for the identifcation of morpholog- ically similar species, in the Strodei Group and some taxa in the Myzorhynchella Section. The single versus branched abdominal seta 6-IV used to diferentiate Myzorhynchella species from other Nyssorhynchus species was shown to be variable in Myzorhynchella species. Also, the abdominal setae 1-IV,V of Anopheles atacamensis and Anopheles picti- pennis were shown to be slightly serrate at the edges. Recognition of this character is important to avoid inaccurate identifcation of these species as members of the subgenus Anopheles. Keywords: Anopheles, Morphology, Illustrations, Identifcation key, Fourth-instar larvae Background remains an important cause of morbidity and mortality General introductory comments, distributions and spe- in endemic tropical and subtropical countries throughout cies authors and publication dates are given in Part I [1] the world. Malaria occurrence is afected by several factors of this series of four articles. Despite the continuous inter- including those of the parasites, human host, anopheline ventions to control and eliminate malaria, this disease mosquitoes and environment [2]. Because of its intrinsic complexity, in order to reach an efective and sustainable control of malaria it is necessary to adopt an integrated *Correspondence: [email protected] approach delineated on the evidence of local characteris- 1 Departamento de Epidemiologia, Faculdade de Saúde Pública, tics of the disease and transmission dynamics [3]. Tus, Universidade de São Paulo, Avenida Doutor Arnaldo 715, São Paulo, São Paulo CEP01246-904, Brazil the public health policy for malaria control demands inter- Full list of author information is available at the end of the article ventions focused on the local anopheline vector species © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Sallum et al. Parasites Vectors (2020) 13:582 Page 2 of 25 and empirical feld-knowledge on the characteristics of identifcation was based on the morphology of the male the local populations behavior and ecology [4]. Diferent genitalia and females. Photomicrographs were taken with mosquito species exhibit distinct preferences for blood- a digital Canon Eos T3i (Canon, USA) camera, attached feeding on animals or humans, place where females take to a Leitz Diaplan microscope, using the Helicon Focus their blood-feeding, peak biting time, resting places and software (https ://www.helic onsof t.com/helic onsof t-produ habitats. Tese biological characteristics of vector species cts/helic on-focus /) that was used to build single in-focus need to be considered for the choice of an efective vec- images by stacking multiple images of the same structure. tor control intervention. It is important to note that vec- Tese in-focus images were, then, employed to draw the tor control interventions need to be delineated for the line illustrations of the characters in CorelDRAW soft- local vector species, thus an accurate species identifcation ware (https ://www.corel draw.com/en/produ ct/corel draw/ is of vital importance for control, surveillance, and feld essen tials /?topNa v=en). Except for one fgure, illustra- malariology studies. Misidentifcation will cause error for a tions are not to scale, but the proportions of the charac- decision-making control programme that is based on met- ters in the drawings are maintained. Te morphological rics of transmission and local vector species [3]. Actions terminology employed in the key are defned and illus- for vector control encompasses activities focused on the trated in accordance with Harbach & Knight [5, 6]. Te larval habitat to prevent the production of adult mos- key is modifed after Faran & Linthicum [7] and Forattini quitoes. Tis requires specifc measures that are defned [8], with additional characters proposed herein. Te spe- taken into consideration feld-collected data of the vector cies included in this Part II are listed in Table 1 of Sallum population, and accurate identifcation of species and their et al. [1] except for An. acanthotorynus Komp, 1937, An. habitats. Te fastest, easiest, and cheapest way to identify albertoi Unti, 1941, An. arthuri Unti, 1941, An. bustaman- feld-collected mosquitoes for surveillance and control tei Galvão, 1955, An. canorii Flock & Abonnenc, 1945, An. programmes is based on morphological characteristics. evandroi da Costa Lima, 1937, An. nigritarsis (Chagas, Tis activity is usually conducted by feld-entomologists 1907), An. pseudomaculipes (Chagas in Peryassú, 1908), conducting mosquito collections, dissections of females An. pseudopunctipennis levicastilloi Leví Castillo, 1944, in malaria endemic areas. A dichotomous morphologi- An. pseudopunctipennis neghmei Mann, 1950, An. pseu- cal key is proposed with the purpose of providing a tool dopunctipennis noei Mann, 1950, An. pseudopunctipennis for identifcation of Anopheles species in South America patersoni Alvarado & Heredia, 1947, An. pseudopuncti- based on the morphology of the fourth-instar larvae. Te pennis rivadeneirai Leví Castillo, 1945, An. rachoui Gal- key includes major vectors, local vectors and species that vão, 1952, An. sanctielii Senevet & Abonnenc, 1938 and have not been involved in the malaria transmission but An. striatus SantʼAna & Sallum, 2016. can emerge and become dominant in human-dominated environments. Results and discussion Glossary of morphological terms Methods All mosquitoes pass through four larval instars (stadia, Morphological characters of the fourth-instar larvae of stages). As in all insects, mosquitoes have three body South American species of the genus Anopheles Meigen regions. Tese are well diferentiated in mosquito larvae: were examined and employed to construct a fully illus- the head (C), thorax (T) and abdomen (A) (Fig. 1). Mos- trated identifcation key. Te primary types (holotypes quito larvae are metapneustic, meaning there is a single and paratypes) and other feld-collected specimens depos- pair of respiratory openings caudally. Species of the sub- ited in the Coleção Entomológica de Referência, Facul- family Anophelinae Grassi, 1900, which includes the genus dade de Saúde Pública, Universidade de São Paulo, São Anopheles Meigen, 1818, difer from the other culicid sub- Paulo, Brazil (FSP-USP), Museo de Entomología, Univer- family, Culicinae Meigen, 1818, in that the larval stages do sidad del Valle, Santiago de Cali, Colombia (MUSENUV) not possess a respiratory siphon, but instead have paired and the US National Mosquito Collection, Smithsonian spiracular openings on a clearly diferentiated plate. Institution, Washington, DC, USA (USNMC) were exam- Te larval cuticle (exoskeleton) bears a number of ined to discover characters to be used in the key based on features of taxonomic utility. Te most distinctive of larval morphology. For species
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