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Published in final edited form as: Zootaxa. 2020 Mar 4;4747(3):zootaxa.4747.3.1. doi: 10.11646/zootaxa.4747.3.1

Updated list of Anopheles species (Diptera: Culicidae) by country in the Afrotropical Region and associated islands

Seth R Irish 1,5, David Kyalo 2, Robert W Snow 2,3, Maureen Coetzee 4
PMCID: PMC7116328  EMSID: EMS102269  PMID: 32230095

Abstract

The distributions of the Afrotropical Anopheles mosquitoes were first summarized in 1938. In 2017, an extensive geocoded inventory was published for 48 sub-Saharan African countries, including information such as sampling methods, collection dates, geographic co-ordinates and the literature consulted to produce the database. Using the information from the 2017 inventory, earlier distribution lists, museum collections and publications since 2016, this paper presents an updated, simplified list of Anopheles species by mainland countries and associated Afrotropical islands, with comments where applicable. It is intended as a supplement to the 2017 geo-coded inventory.

Keywords: Africa, Anopheles, mosquitoes, inventory

Introduction

At the end of the 19th century, the Anopheles mosquitoes of the world became the focus of intense research after they were implicated in the transmission of malaria parasites (Ross 1910). Since then, lists of species recorded for sub-Saharan African countries were published by Evans (1938), Edwards (1941) and de Meillon (1947), with the country lists in Gillies & de Meillon (1968) being the most comprehensive at that time. A supplement to Gillies & de Meillon was subsequently published by Gillies & Coetzee (1987), which provided updated country occurrence records for some species, including newly described species. An interactive list and identification key for Anopheles of the Afrotropical Region was produced in 1998 (Hervy et al. 1998).

Although maps of dominant vector species were produced more recently (Sinka et al. 2010, 2012), these were limited to species involved in malaria transmission. It has taken almost 50 years for complete country lists to be updated. In 2017, Kyalo and co-workers produced a geo-coded inventory of Anopheles species recorded for 48 countries in sub-Saharan Africa, covering almost 120 years of work on this important group of insects (Kyalo et al. 2017). They also produced a freely accessible database of species by country that includes collection information, collection dates, geographic co-ordinates and reference sources that provide historic information on mosquito surveys conducted in Afrotropical countries over the years.

This present paper provides an update of the lists given in Table 3 of Kyalo et al. (2017), with some deletions and some additions of species to countries and notes on the rationale behind the amendments.

Methods

The list of all the species present in each country, from Table 3 in Kyalo et al. (2017), was compared with the Kyalo et al. online database, the VectorMap lists provided by the Walter Reed Biosystematics Unit (WRBU) based in the Smithsonian Institution (http://vectormap.si.edu), records from Gillies & de Meillon (1968) and Gillies & Coetzee (1987) and the database of the Institut de Recherche pour le Développement (IRD) at Montpellier (https://arim.ird.fr/#recherches/index/specimens/routage:home). Species listed in the IRD database but not in the published literature, that are clearly way out of their normal distributions, have not been included in the country lists and require confirmation.

In addition to records from the collections of the National Institute for Communicable Diseases, Johannesburg, South Africa, noted by one of the authors (MC), a visit was made to the Natural History Museum in London, UK by another of the authors (SRI) in January 2019, and records noted during the visit are also included here.

One of the possible uses of these lists is the development of country-specific identification keys. For this reason, both malaria vectors and non-vectors have been included.

Results

Each country list (Appendix) is followed by relevant comments regarding species additions, deletions or points of interest, and references to these are provided.

The Anopheles fauna of mainland Tanzania and Zanzibar are presented separately. In addition to the countries in Kyalo et al. (2017), Anopheles records for Mauritius, La Réunion and Lesotho are presented. No records were found for St. Helena, and despite an early report of Anopheles gambiae s.l. in the Seychelles, it appears that no Anopheles are present there (Robert et al. 2011; Le Goff et al. 2012).

Table 1 provides a list of all the currently recognised species by subgenus, series and authorship. An Excel file providing a single record for each species present in each country can be found at https://doi.org/10.7910/DVN/ PHGADL.

Table 1. Anopheles species of the Afrotropical Region and associated islands.

Subgenus Species and authorship Series
Anopheles caliginosus de Meillon, 1943 Myzorhynchus
Anopheles concolor Edwards, 1938 Anopheles
Anopheles coustani Laveran, 1900 Myzorhynchus
Anopheles crypticus Coetzee, 1995 Myzorhynchus
Anopheles fuscicolor van Someren, 1947 Myzorhynchus
Anopheles namibiensis Coetzee, 1984 Myzorhynchus
Anopheles obscurus (Grünberg, 1905) Myzorhynchus
Anopheles paludis Theobald, 1900 Myzorhynchus
Anopheles symesi Edwards, 1928 Myzorhynchus
Anopheles tenebrosus Dönitz, 1902 Myzorhynchus
Anopheles ziemanni Grünberg, 1902 Myzorhynchus
Cellia amharicus Hunt, Wilkerson & Coetzee, 2013 Pyretophorus
Cellia arabiensis Patton, 1905 Pyretophorus
Cellia ardensis (Theobald, 1905) Neomyzomyia
Cellia argenteolobatus (Gough, 1910) Cellia
Cellia aruni Sobti, 1968 Myzomyia
Cellia austenii (Theobald, 1905) Myzomyia
Cellia azaniae Bailly-Choumara, 1960 Myzomyia
Cellia azevedoi Ribeiro, 1969 Paramyzomyia
Cellia barberellus Evans, 1932 Myzomyia
Cellia berghei Vincke & Leleup, 1949 Myzomyia
Cellia bervoetsi D’Haenens, 1961 Myzomyia
Cellia brohieri Edwards, 1929 Myzomyia
Cellia brucei Service, 1960 Myzomyia
Cellia brumpti Hamon & Rickenbach, 1955 Cellia
Cellia brunnipes (Theobald, 1910) Myzomyia
Cellia buxtoni Service, 1958 Neomyzomyia
Cellia bwambae White, 1985 Pyretophorus
Cellia cameroni de Meillon & Evans, 1935 Neomyzomyia
Cellia carnevalei Brunhes, Le Goff & Geoffroy, 1999 Neomyzomyia
Cellia caroni Adam, 1961 Neomyzomyia
Cellia carteri Evans & de Meillon, 1933 Myzomyia
Cellia christyi (Newstead & Carter, 1911) Pyretophorus
Cellia cinctus (Newstead & Carter, 1910) Neomyzomyia
Cellia cinereus Theobald, 1901 Paramyzomyia
Cellia coluzzii Coetzee & Wilkerson, 2013 Pyretophorus
Cellia comorensis Brunhes, Le Goff & Geoffroy, 1997 Pyretophorus
Cellia confusus Evans & Leeson, 1935 Myzomyia
Cellia cristipalpis Service, 1977 Cellia
Cellia culicifacies Giles, 1901 Myzomyia
Cellia cydippis de Meillon, 1931 Cellia
Cellia dancalicus Corradetti, 1939 Neocellia
Cellia daudi Coluzzi, 1958 Pyretophorus
Cellia deemingi Service, 1970 Neomyzomyia
Cellia demeilloni Evans, 1933 Myzomyia
Cellia distinctus (Newstead & Carter, 1911) Myzomyia
Cellia domicolus Edwards, 1916 Myzomyia
Cellia dthali Patton, 1905 Myzomyia
Cellia dualaensis Brunhes, Le Goff & Geoffroy, 1999 Neomyzomyia
Cellia dureni Edwards, 1938 Neomyzomyia
Cellia eouzani Brunhes, Le Goff & Boussès, 2003 Neomyzomyia
Cellia erepens Gillies, 1958 Myzomyia
Cellia erythraeus Corradetti, 1939 Myzomyia
Cellia ethiopicus Gillies & Coetzee, 1987 Myzomyia
Cellia faini Leleup, 1952 Neomyzomyia
Cellia flavicosta Edwards, 1911 Myzomyia
Cellia fontenillei Barrón, Paupy, Rahola, Akone-Ella, Ngangue, Wilson-Bahun, Pombi, Kengne, Costantini, Simard, González & Ayala, 2019 Pyretophorus
Cellia fontinalis Gillies & de Meillon, 1968 Myzomyia
Cellia freetownensis Evans, 1925 Myzomyia
Cellia funestus Giles, 1900 Myzomyia
Cellia funestus-like species (see Spillings et al., 2009) Myzomyia
Cellia fuscivenosus Leeson, 1930 Myzomyia
Cellia gabonensis Rahola, Makanga & Paupy, 2014 Myzomyia
Cellia gambiae Giles, 1902 Pyretophorus
Cellia garnhami Edwards, 1930 Myzomyia
Cellia gibbinsi Evans, 1935 Myzomyia
Cellia grassei Grjebine, 1953 Neomyzomyia
Cellia grenieri Grjebine, 1964 Neomyzomyia
Cellia griveaudi Grjebine, 1960 Neomyzomyia
Cellia hamoni Adam, 1962 Neomyzomyia
Cellia hancocki Edwards, 1929 Myzomyia
Cellia hargreavesi Evans, 1927 Myzomyia
Cellia harperi Evans, 1936 Myzomyia
Cellia hervyi Brunhes, Le Goff & Geoffroy, 1999 Neocellia
Cellia hughi Lambert & Coetzee, 1982 Myzomyia
Cellia jebudensis Froud, 1944 Neomyzomyia
Cellia keniensis Evans, 1931 Myzomyia
Cellia kingi Christophers, 1923 Neomyzomyia
Cellia kosiensis Coetzee, Segerman & Hunt, 1987 Myzomyia
Cellia lacani Grjebine, 1953 Neomyzomyia
Cellia leesoni Evans, 1931 Myzomyia
Cellia letabensis Lambert & Coetzee, 1982 Myzomyia
Cellia listeri de Meillon, 1931 Paramyzomyia
Cellia lloreti Gil Collado, 1935 Myzomyia
Cellia longipalpis (Theobald, 1903) Myzomyia
Cellia lounibosi Gillies & Coetzee, 1987 Neomyzomyia
Cellia lovettae Evans, 1934 Neomyzomyia
Cellia machardyi Edwards, 1930 Neomyzomyia
Cellia maculipalpis Giles, 1902 Neocellia
Cellia maliensis Bailly-Choumara & Adam, 1959 Neomyzomyia
Cellia marshallii (Theobald, 1903) Myzomyia
Cellia mascarensis de Meillon, 1947 Neomyzomyia
Cellia melas (Theobald, 1903) Pyretophorus
Cellia merus Dönitz, 1902 Pyretophorus
Cellia millecampsi Lips, 1960 Neomyzomyia
Cellia milloti Grjebine & Lacan, 1953 Neomyzomyia
Cellia mortiauxi Edwards, 1938 Myzomyia
Cellia moucheti Evans, 1925 Myzomyia
Cellia mousinhoi de Meillon & de Carvalho Pereira, 1940 Myzomyia
Cellia multicolor Cambouliu, 1902 Paramyzomyia
Cellia multicinctus Edwards, 1930 Neomyzomyia
Cellia murphyi Gillies & de Meillon, 1968 Cellia
Cellia natalensis (Hill & Haydon, 1907) Neomyzomyia
Cellia nili (Theobald, 1904) Neomyzomyia
Cellia njombiensis Peters, 1955 Myzomyia
Cellia notleyi van Someren, 1949 Neomyzomyia
Cellia ovengensis Awono-Ambene, Kengne, Simard, Antonio-Nkondjio & Fontenille, 2004 Neomyzomyia
Cellia parensis Gillies, 1962 Myzomyia
Cellia pauliani Grjebine, 1953 Neomyzomyia
Cellia pharoensis Theobald, 1901 Cellia
Cellia pretoriensis (Theobald, 1903) Neocellia
Cellia quadriannulatus (Theobald, 1911) Pyretophorus
Cellia radama de Meillon, 1943 Neomyzomyia
Cellia rageaui Mattingly & Adam, 1954 Neomyzomyia
Cellia ranci Grjebine, 1953 Neomyzomyia
Cellia rhodesiensis Theobald, 1901 Neomyzomyia
Cellia rivulorum Leeson, 1935 Myzomyia
Cellia rivulorum-like species (see Cohuet et al. 2003) Myzomyia
Cellia rodhaini Leleup & Lips, 1950 Neomyzomyia
Cellia roubaudi Grjebine, 1953 Neomyzomyia
Cellia ruarinus Edwards, 1940 Neomyzomyia
Cellia rufipes (Gough, 1910) Neocellia
Cellia salbaii Maffi & Coluzzi, 1958 Neocellia
Cellia schwetzi Evans, 1934 Myzomyia
Cellia seretsei Abdulla-Khan, Coetzee & Hunt, 1998 Paramyzomyia
Cellia sergentii (Theobald, 1907) Myzomyia
Cellia seydeli Edwards, 1929 Myzomyia
Cellia smithii Theobald, 1905 Neomyzomyia
Cellia somalicus Rivola & Holstein, 1957 Neomyzomyia
Cellia squamosus Theobald, 1901 Cellia
Cellia stephensi Liston, 1901 Neocellia
Cellia swahilicus Gillies, 1964 Cellia
Cellia tchekedii de Meillon & Leeson, 1940 Myzomyia
Cellia theileri Edwards, 1912 Myzomyia
Cellia turkhudi Liston, 1901 Paramyzomyia
Cellia vaneedeni Gillies & Coetzee, 1987 Myzomyia
Cellia vanhoofi Wanson & Lebied, 1945 Neomyzomyia
Cellia vernus Gillies & de Meillon, 1968 Neomyzomyia
Cellia vinckei de Meillon, 1942 Neomyzomyia
Cellia walravensi Edwards, 1930 Myzomyia
Cellia wellcomei Theobald, 1904 Myzomyia
Cellia wilsoni Evans, 1934 Neomyzomyia
Christya* implexus (Theobald, 1903) –
Christya okuensis Brunhes, Le Goff & Geoffroy, 1997 –
Open in a new tab
*

Elevated to subgeneric level by Harbach & Kitching (2016).

Discussion

The species listed per country in Gillies & de Meillon (1968) are not always accompanied by references to published records. This is because M. T. Gillies personally studied the collections in the British, French, Belgian and South African museums to record species deposited in those collections that had never been documented in the published literature. Thus, for example, the inclusion of Anopheles cydippis de Meillon, An. walravensi Edwards and An. ziemanni Grünberg in the Botswana list would all have been based on observations from the collections in the South African Institute for Medical Research in Johannesburg (now the National Institute for Communicable Diseases), and reference to their presence would therefore be Gillies & de Meillon (1968). Further information on the museum specimens examined by Gillies (date of collection, location, collector, etc.) would necessitate a visit to the relevant museums as these details are not provided in Gillies & de Meillon (1968).

Species name changes, border changes and splitting one species into multiple species make maintaining these lists challenging. The use of chromosomal and molecular methods is increasingly being used to understand mosquito taxonomy. The adverb “sensu lato”, or the abbreviation “s.l.”, has been used for Anopheles gambiae Giles and An. funestus Giles where genetic/molecular species identification was not carried out. In particular, the listing of An. gambiae s.l. denotes that no differentiation was made in the past 30 years between An. gambiae sensu stricto (s.s.) and An. coluzzii Coetzee & Wilkerson (previously S and M molecular forms and Savanna and Mopti chromosomal forms, respectively) (Coetzee et al. 2013). Subspecies names are not included in the current list, only the nominal species is given.

Supplementary Material

Appendix

Acknowledgements

SRI is funded by the U.S. President’s Malaria Initiative. MC is funded by a South African National Research Foundation grant #113300. RWS is funded by a Wellcome Trust Principal Fellowship (number 103602) that provides support to DK. RWS is grateful to the UK’s Department for International Development for their support to the project “Strengthening the Use of Data for Malaria Decision Making in Africa” (DFID Programme Code 203155) and acknowledges the support of the Wellcome Trust to the Kenya Major Overseas Programme (number 203077). Erica McAlister is thanked for facilitating the visit to the Natural History Museum in London. Philippe Boussès and an anonymous reviewer are thanked for their constructive review of the manuscript. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Contributor Information

David Kyalo, Email: dkyalo@kemri-wellcome.org.

Robert W. Snow, Email: rsnow@kemri-wellcome.org.

Maureen Coetzee, Email: maureen.coetzee@wits.ac.za.

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