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

The distributions of the Afrotropical Anopheles mosquitoes were first summarized in 1938. In 2017, an extensive geo-coded 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.

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 ).

Although maps of dominant vector species were produced more recently (Sinka , 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 ). 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 , 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 , 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 , 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 ; Le Goff ).

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	–

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 ). Subspecies names are not included in the current list, only the nominal species is given.