A review of the mosquito species (Diptera: Culicidae) of Bangladesh

Background Diseases caused by mosquito-borne pathogens remain an important source of morbidity and mortality in Bangladesh. To better control the vectors that transmit the agents of disease, and hence the diseases they cause, and to appreciate the diversity of the family Culicidae, it is important to have an up-to-date list of the species present in the country. Original records were collected from a literature review to compile a list of the species recorded in Bangladesh. Results Records for 123 species were collected, although some species had only a single record. This is an increase of ten species over the most recent complete list, compiled nearly 30 years ago. Collection records of three additional species are included here: Anopheles pseudowillmori, Armigeres malayi and Mimomyia luzonensis. Conclusions While this work constitutes the most complete list of mosquito species collected in Bangladesh, further work is needed to refine this list and understand the distributions of those species within the country. Improved morphological and molecular methods of identification will allow the refinement of this list in years to come.


Background
Several diseases in Bangladesh are caused by mosquitoborne pathogens. Malaria remains an important cause of morbidity and mortality, particularly in the Chittagong Hill tracts and in the border belt areas [1]. Lymphatic filariasis continues to be a problem, despite multiple rounds of mass drug administration [2]. Dengue, Japanese encephalitis, and chikungunya viruses are also transmitted by mosquitoes in Bangladesh [3]. As knowledge of faunal diversity and vector control is often an important component of disease control, it is important to correctly identify and understand the bionomics of the species involved in transmission.
To this end, previous authors have worked to compile lists of the mosquito species present in Bangladesh, by compiling species records from the country. The mosquitoes of Bangladesh have been recorded in several such lists over the past century. James [4], Covell [5,6], Christophers [7], Barraud [8] and Puri [9,10] described the mosquito fauna of British India, from which some records for locations in present-day Bangladesh can be extracted. After the separation of Pakistan and India in 1947, Aslamkhan [11] published checklists for mosquito species, indicating which were found in East Pakistan (Bangladesh). After the independence of Bangladesh in 1971, Ahmed [12] published an updated checklist in 1987, including many new records. More recently, Bashar et al. [13] published a checklist for the Anopheles mosquitoes of Bangladesh, but no comprehensive list of all species of mosquitoes present in the country has been published for nearly 30 years. Over the decades, deforestation and increased agricultural practices may have altered the diversity and abundance of mosquitoes throughout the country [14][15][16]. Therefore, the aim of this work was to produce an updated list of all mosquito species reportedly present in Bangladesh, with information on their collection.

Methods
PubMed and the US Armed Forces Pest Management Board Literature Retrieval Service (before it was terminated), were searched using the terms "mosquito" and "Bangladesh." Articles found were searched for the descriptions of the original collections of mosquitoes identified to species. Articles only citing another article's collections (second-hand accounts) were not included. The reference list of collected articles was searched for additional articles.
National libraries of Bangladesh were also searched for articles. All articles were entered onto a spreadsheet to facilitate calculation of the number of species and the number of records for each species.
Additionally, one of us (HMA) provided records from studies that included the use of light traps (CDC miniature light trap, model 512, John W. Hock Co., Gainesville, Florida, USA), resting collections and BG-Sentinel traps (Biogents AG, Regensberg, Germany) (publications in preparation). The descriptions of the collection sites are provided in the discussion below.

Results
Records were found for 123 species of Culicidae reported from Bangladesh. The records ranged in date from 1908 to 2016. These species are listed below, alphabetically by genus, subgenus, and species. Aedes species follow the classification provided by Wilkerson et al. [17], whereas all other genera follow the classification provided by the Mosquito Taxonomic Inventory [18]. In accordance with Article 51.3 of the International Code of Zoological Nomenclature, the authorship and date of species names enclosed in parentheses indicate that the species was originally described as a member of a genus other than the one in which it is currently placed, e.g. Aedes aegypti (Linnaeus, 1762) was originally described as Culex aegypti Linnaeus, 1762. The numbers following species names refer to articles where the records were published.  (Theobald, 1908) [11, 12, 21, 24, 27-29, 38, 39] 19. Ae. (Phg.) khazani Edwards, 1922 [8,12,24,26,28,29] 20. Ae. (Phg.) lophoventralis (Theobald, 1910) [11,12,28,29,36,37] A, B, C, and D), which are distinguishable based on morphological, chromosomal, and molecular differences [129,130]. As of yet, no determination has been made of which species of the Subpictus Complex are present in Bangladesh. Anopheles culicifacies is an important malaria vector in the Indian Sub-continent, but its importance in Bangladesh appears to be limited. The Culicifacies Complex is comprised of species A, B, C, D, and E [131]. Little is known of the species present in Bangladesh, particularly as very few specimens have been found in the past 20 years [22,63], but recently species B, C, and E were found in Kuhalong, near Bandarban town [14]. The Sundaicus Complex comprises four coastal species: An. sundaicus, An. epiroticus, An. sundaicus D, and An. sundaicus E [132]. While it would appear that An. epiroticus is most likely the species present in coastal areas of Bangladesh, due to the limited geographic provenance of the other species, this awaits confirmation using molecular methods [132]. Anopheles annularis is a complex of two species, A and B [133], which can be distinguished using chromosomal or molecular methods [134]. The Fluviatilis Complex is composed of four sibling species, S, T, U, and V [135], but it is not known which species are present in Bangladesh. The Maculatus Complex (a.k.a. Maculatus Group) consists of nine species, but Anopheles maculatus is comprised of chromosomal forms B and E [136,137]. Rongnoparut et al. [138] stated that chromosomal form B is found north of 13°N, but further work on the group is necessary to know which members are present in Bangladesh. The Barbirostris Complex is composed of seven formally named species, but it seems more species will be added [139,140]. Only An. barbirostris (s.l.) has been reported from Bangladesh, but it is clear that more work is needed to know which species of the complex are present in the country. The Minimus Complex includes three species: An. harrisoni, An. minimus and An. yaeyamaensis (known only from Japan). Anopheles minimus (s.l.) has been found in Bangladesh [14], but further work is needed to know if An. harrisoni (previously known as species C) is present in the country [141]. Finally, the Dirus Complex comprises seven species, of which it appears An. baimaii is the species present in Bangladesh [14,92,142].
There are a number of species that have only been reported in Bangladesh since the list of Ahmed [12]. Larvae of Ae. gardnerii imitator were collected from a tree hole in a botanical garden in Dhaka during 2004 [60]. Adults of Ar. kesseli were taken in resting collections and light traps in Rajshahi Division [19], and adults of Ar. theobaldi were collected in a forested area in Habiganj district (Sylhet Division) [103]. Culex annulus has been collected in Habiganj and Moulavibazar districts in Sylhet Division, as well as on St. Martin's Island, and in the Sundarbans [35,47,48]. Two adults of Ma. annulata and three of Ur. rampae were collected in light traps in Rajshahi Division [19]. Culex fragilis was collected in resting catches in Patrokhola tea garden, Moulavibazar (Sylhet Division) [35]. Additionally, one of us (HMA) recently identified three species new to Bangladesh, which will be reported in publications currently in preparation. Anopheles pseudowillmori were collected in light traps placed in a room with sleeping people (18:00 to 06:00). Nine specimens were collected in Kuhalong and Rajbila unions of Bandarban district between 2009 and 2012. Three Ar. malayi females were collected in BG-Sentinel traps that were placed indoors in Rajshahi and Chapai Nawabganj districts between November 2014 and September 2015. Mimomyia luzonensis was collected using the same method in Dhaka and Chapai Nawabganj districts, and four specimens were collected between September 2014 and September 2015.
Two species listed in Ahmed [12] are excluded from the list. Ahmed [12] listed Ae. pipersalatus with reference to Barraud [30]. In the older reference, a record is provided for Madhupur in Bengal, attributed to Charles Paiva, an entomologist educated in Calcutta, who then took up a position at the Indian Museum in Calcutta where he worked until his death in 1919 [148]. There is a sub-district called Madhupur near Dhaka in Bangladesh, however, there is also a Madhupur in West Bengal in India. As we could not find any further evidence to which Madhupur was intended, and as no further records of Ae. pipersalatus in Bangladesh were found, we have removed this species from the list of species known to occur in the country. We have also removed the separate listing of An. gigas subspecies simlensis [149], which has been reported only once, from Rangpur [6], as it is represented by An. gigas in the species list.
Armigeres obturbans has been listed in several records, but it appears that this species was regularly confused with the common Ar. subalbatus. Furthermore, Thurman [150] noted that the distribution of Ar. obturbans is limited to Sulawesi, so it seems likely that the records for Ar. obturbans in Bangladesh refer to Ar. subalbatus. We have therefore removed Ar. obturbans from the species list for Bangladesh.

Conclusions
The list provided here is the most complete list compiled since the work of Ahmed [12], nearly 30 years ago. The up-dated list will serve as a basis for the development of identification keys and will hopefully spur on research on the bionomics of these species. These tools will be important for the reduction of diseases in Bangladesh caused by mosquito-borne pathogens.