Update of the Culicoides (Diptera: Ceratopogonidae)
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Belkharchouche et al. Parasites Vectors (2020) 13:463 https://doi.org/10.1186/s13071-020-04335-4 Parasites & Vectors RESEARCH Open Access Update of the Culicoides (Diptera: Ceratopogonidae) species checklist from Algeria with 10 new records Mounira Belkharchouche1,2,3,4*, Selima Berchi3, Bruno Mathieu5, Ignace Rakotoarivony4,6, Maxime Duhayon4,6, Thierry Baldet6,7 and Thomas Balenghien6,8,9* Abstract Background: The Culicoides fauna of Algeria has been historically investigated, leading to the description of many new species by Kiefer in the 1920s, Clastrier in the 1950s or Callot in the 1960s and to a comprehensive inventory by Szadziewski in the 1980s. The emergence of bluetongue in the late 1990s enhanced Culicoides collections made in the country over the last two decades, but information remained mostly unpublished. The aim of this study is therefore to provide a comprehensive and updated checklist of Culicoides biting midge species in Algeria. Methods: The literature (published and grey, in French and in English) from 1920 to date on Culicoides collections in Algeria was collected and analyzed in the light of the current taxonomic and systematic knowledge and methods. Fresh Culicoides material was also analyzed using light/suction trap collections carried out from November 2015 to September 2018 in nine localities of the ‘wilayah’ of Tiaret (northwestern Algeria). Slide mounted specimens were identifed morphologically using the interactive identifcation key IIKC and original descriptions. Specimens were then compared with non-type material originating from diferent countries and partly with type material. Results: A total of 13,709 Culicoides, belonging to at least 36 species within 10 subgenera, were examined leading to 10 new records in Algeria, including C. chiopterus, C. dewulf, C. navaiae, C. grisescens, C. paradoxalis, C. shaklawensis, C. simulator, C. univittatus, C. achrayi and C. picturatus. These new records and all previous records provided by the literature review were discussed. Conclusions: We propose a Culicoides checklist for the Algerian fauna of 59 valid species, including species mainly with a large Palaearctic distribution and a specifc Mediterranean distribution, and only a few species from the Afro- tropical region. Among them, several species, mainly of the subgenera Avaritia and Culicoides, are confrmed or prob- able vectors of arboviruses important in animal health. Keywords: Ceratopogonidae, Culicoides, New records, Bluetongue, Algeria Background involved in the transmission of many arboviruses that Biting midges of the genus Culicoides Latreille (Diptera: afect humans, such as Oropouche virus, ruminants, Ceratopogonidae) are small hematophagous dipterans, such as bluetongue virus (BTV) and Schmallenberg virus from 1 to 4 mm long [1]. Culicoides are biological vectors (SBV), and equids, such as African horse sickness virus (AHSV) [2], but also several parasites, mainly nematodes *Correspondence: [email protected]; [email protected] that can infect humans or animals [3]. Currently, the 2 Faculté des Sciences de la Nature et de la Vie, Université Ibn Khaldoun, B.P.75 Zaaroura, Tiaret 1400, Algérie 8 CIRAD, UMR ASTRE, 10101 Rabat, Morocco Full list of author information is available at the end of the article © 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. Belkharchouche et al. Parasites Vectors (2020) 13:463 Page 2 of 15 1368 valid species described worldwide are placed in 32 years after these diferent episodes of BTV transmission, subgenera and 38 species groups (not placed to a subge- limited-scale surveys for Culicoides were carried out in nus), whereas 13% of the world fauna are not placed in northern and southern Algeria [36–38], before nation- any subgenus or group [4]. wide entomological surveillance was implemented in Te worldwide Culicoides fauna has been diversely 2007 by the National Institute of Veterinary Medicine investigated by a number of authors. In the western Pal- [39, 40]. Moreover, extensive collections have been car- aearctic region, several monographs and catalogues are ried out in the eastern part of Algeria [41, 42]. Altogether, still considered as a reference for the Culicoides fauna these recent studies increased the total number of species [5–7], whereas an interactive identifcation key has been recorded in Algeria to 52 by identifying 12 new species developed for Culicoides females [8]. Te Afrotropical for the Algerian fauna. fauna has benefted from various contributions, includ- In this paper, we aimed to produce a comprehensive ing those of Khamala & Kettle [9] for eastern Africa and checklist of Culicoides species in Algeria, including a Glick [10] for Kenya in particular. Northern Africa is list of confrmed or probable BTV and AHSV vectors. located in the southwestern part of the Palaearctic region For this purpose, we compiled and discussed the exist- and separated from the Afrotropical region by the Sahara ing known information from published and from grey Desert. Te fauna of this region is composed mainly by literature and examined new material collected using UV species belonging to the Palaearctic fauna, along with light/suction traps carried out from November 2015 to some of the Afrotropical fauna. September 2018 in the ‘wilayah’ of Tiaret (northwestern In the Maghreb, Culicoides inventories have been car- Algeria). ried out since the beginning of the 20th century, frstly with taxonomic interest enhanced in the 1960s after the Methods emergence of AHSV in Morocco in 1965 [11–14]. In this Published papers (in French and English) related to country, additional ecological studies were carried out Culicoides collections in Algeria were collated following ® after the 1989–1991 AHSV outbreaks [15, 16]. Invento- searches of classical bibliographic databases (PubMed ries of Culicoides were then re-launched in the Maghreb and Google Scholar) and on institutional open access after the BTV emergence in the Mediterranean basin repositories (Agritrop from Cirad and Horizon from in the 2000s and the implementation of national-scale IRD). Te unpublished ‘grey’ literature (feld reports and entomological surveys [17, 18]. Currently, 54 species of theses) was collated from the two latter databases and Culicoides have been recorded in Morocco [19] and 35 in from personal databases of authors, but also by contact- Tunisia [20]. In Algeria, studies on Culicoides have been ing authors of the publications and the teams working on particularly intense in the frst half of the 20th century, Culicoides in Algeria. Te literature from 1920 to date with investigations carried out during the 1920s [21–23], was analyzed in light of the current taxonomic and sys- the 1930s [24], and the 1950s [25, 26], but also after the tematic knowledge and methods. 1965 ASHV outbreaks [27]. Altogether, these authors We examined Culicoides individuals collected using reported the presence of 21 species, including the fol- UV light/suction traps, from November 2015 to Septem- lowing 11 still valid species described from Algeria: C. ber 2018, from nine localities in the ‘wilayah’ of Tiaret. sergenti Kiefer; C. foleyi Kiefer; C. nudipennis Kiefer; C. Te collected Culicoides were transferred to 70% ethanol parroti Kiefer; C. saevus Kiefer; C. sahariensis Kiefer; C. for preservation. Te study area is located in the western algeriensis Clastrier; C. begueti Clastrier; C. cataneii Clas- part of the ‘Hauts Plateaux’ (Highlands or High plateaus), trier; C. semimaculatus Clastrier; and C. marcleti Callot, a steppe-like region between the Tell and Saharan Atlas Kremer & Basset. After collections in diferent regions of ranges in northwestern Algeria. It is dominated by a con- Algeria carried out in the early 1980s, Szadziewski [28] tinental and semi-arid climate, characterized by very dry reported 30 species, including 19 new records for the summers (300–500 mm per year, with a drought of 6 to Algerian fauna, increasing the number of known species 8 months) and cold winters (average annual temperature in Algeria to 40. Tis inventory encompassed several spe- ranging from 13 to 17 °C) [43]. Mainly dedicated to pas- cies known as confrmed or probable BTV vectors, such toral activities, the Tiaret region encompasses forested as C. imicola Kiefer, C. obsoletus Meigen, C. scoticus areas composed by cork and holm oaks, Aleppo pine and Downes & Kettle within the subgenus Avaritia and C. cypresses. newsteadi Austen, C. pulicaris (Linnaeus) and C. puncta- From the material available, we selected a series of tus (Meigen) within the subgenus Culicoides [29–33]. specimens that exhibited a variety of wing patterns, and From 2000 to 2011, three BTV serotypes were reported also those with plain wings. Before identifcation, the in Algeria, leading to 297 outbreaks in 2000 (BTV-2), 263 specimens were dissected and slide mounted follow- in 2006 (BTV-1) and six in 2011 (BTV-4) [34, 35]. A few ing the Wirth & Martson [44] procedure. Slide mounted Belkharchouche et al. Parasites Vectors (2020) 13:463 Page 3 of 15 specimens were therefore identifed morphologically to North Africa. We produced a cox1 barcode sequence of the species level using the interactive identifcation key the C.