Abstract
Prediction of arboviral disease outbreaks and planning for appropriate control interventions require knowledge of the mosquito vectors involved. Although mosquito surveys have been conducted in different regions of Uganda since the mid 30’s such studies have not been carried out in Mpigi District. In October 2011, we conducted mosquito collections in Mpigi district to determine species composition and relative abundance of the different species. The survey was conducted in four villages, Njeru, Ddela, Kiwumu and Nsumbain Kammengo sub-county, Mpigi district, Uganda. CDC light traps baited with dry ice (carbon dioxide) were used to capture adult mosquitoes. A total of 54,878 mosquitoes comprising 46 species from eight genera were collected. The dominant species at all sites was Coquilletidia (Coquilletidia) fuscopennata Theobald (n=38,059, 69%), followed by Coquillettidia (Coquillettidia) metallica Theobald (n=4,265, 7.8%). The number of species collected varied from 17 in the genus Culex to 1 in the genus Lutzia. Of the 46 species identified, arboviruses had previously been isolated from 28 (60.9%) suggesting a high potential for arboviral transmission and/or maintenance in Mpigi District.
Keywords: mosquito, Mpigi, species composition, Uganda
Introduction
Mosquitoes of Uganda were extensively investigated between the mid-1930s and the early 1970s [1]. During that period more than 220 mosquito species were recorded and approximately 20% were implicated in arbovirus transmission [2]. Because of these investigations, Uganda is currently a known hotspot for emergence of arboviruses of public health and veterinary importance [3, 4]. Although earlier studies have described species composition, distribution, behavior and preferred habitat of mosquitoes in Uganda, most of these studies were conducted >40 years ago and only in limited areas of the country [1, 5–17]. Such information has been more recently updated by Mutebi et al [1] for western Uganda and Kaddumukasa et al. [18] for Zika Forest. In the intervening years arthropod surveillance activities in Uganda have mainly been limited to collections related to specific taxonomic questions or to monitoring vectors during outbreaks, such as the O’nyong-nyong virus(ONNV) outbreak in 1996 [19, 20]. Therefore, more generalized mosquito surveys are needed to develop distribution maps of medically significant vector species to facilitate prediction and planning for appropriate control strategies for arboviral outbreaks.
We report here a description of mosquitoes of Mpigi district in central Uganda, an area for which mosquito species composition and abundance data is not available. This study was part of the arbovirus surveillance program recently established at the Uganda Virus Research Institute (UVRI) in Entebbe, Uganda, in collaboration with the US Centers for Disease Control and Prevention. This study is a first step toward surveillance for arboviruses of public health and veterinary importance in Mpigi District.
Materials and Methods
Collection sites
Mosquito collections were conducted in Kammengo Sub County, Mpigi District in central Uganda (Fig. 1). This district is approximately 37 km west of Kampala and borders Wakiso District to the North and East, Kalungu District to the South, Butambala District to the West and Mityana District to the North-West. Mosquitoes were collected from four villages: Njeru (Lat 0.113533, Lon 32.22035), Ddela (Lat 0.106433, Lon 32.2248), Kiwumu (Lat 0.086867, Lon 32.234183) and Nsumba (Lat 0.083467, Lon 32.206917) (Fig. 1). The distance between the collection sites ranged from 0.9 km (Njeru to Ddela) to 3.6 km (Njeru to Nsumba) with a median distance of 3.1 km. The altitude at the study site was between 1166m and 1194m above sea level. The collection sites were in plantations and small gardens close to residential areas and near wetlands that stretch to the shores of Lake Victoria. The primary occupation of the local population in the area is subsistence farming; mostly small scale banana and coffee plantations, vegetable fields and/or gardens and limited rearing of cattle, goats, ducks, chickens and other farm animals.
Fig. 1.
Location of collection sites in Mpigi District, Uganda.
Mosquito collection
Mosquito collections were made from October 15 through 24, 2011. CDC light traps baited with dry ice (carbon dioxide) were suspended on tree branches in coffee plantations, banana plantations and bushes near homes. Twenty five CDC light traps were hung at each site at approximately 5:00pm, left overnight for about 14 hours and collected each morning at approximately 8:00am. Collections were made at each site for 2 nights. The contents of the traps were sorted into cryovials and transported frozen in liquid nitrogen dry shippers to the UVRI laboratory in Entebbe where they were stored at −80°C until identification.
Mosquitoes were identified to species using the morphological keys of Edwards [21], Huang [22], Jupp [23], Gilles and De Mellion [24], and Gilles and Coetzee[25]. Specimens were pooled by species, sex, feeding status and parity and stored at −80°C for virus isolation studies. Voucher specimens were retained for each species for future reference and identification consultation.
Diversity Indices
Species richness and diversity were calculated for each collection location. While species richness is the number of mosquito species at each location, species diversity takes into account both species richness and the relative abundance of each species. Species diversity was estimated by using the Simpson Index[26]. The Simpson Index was calculated as D=Σn(n−1)/N(N−1) where n= the total number of mosquitoes of a particular species and N=the total number of mosquitoes of all species in each collection. We also report the Simpson’s Index of Diversity (1-D), which is interpreted as the greater the index value, the greater the sample diversity.
Results and Discussion
A total of 54,878 mosquitoes belonging to 9 genera and 45 species were identified. The number of mosquitoes collected from the individual sites was: Njeru (n=16,403), Ddela (n=16,818), from Kiwumu (n=12,099) and Nsumba (n=9,555). Table 1 lists the species captured by collection site. Twenty (44.4%) of the 45 species were captured at all four collection sites which suggests differences in species composition between the sites despite their close proximity (Table 1). Recently Mutebi et al. [1] reported differences in species composition between the adjacent sites of Mweya and Maramagambo in western Uganda which suggested that the geographic distance between sites may not be a major determining factor. However, it is important to note that Maramagambo is a forest ecosystem whereas Mweya is an open grassland and therefore the differences in species composition between these two sites may be attributed to differences between the ecosystems. In the present study, 98.5% of the collection belonged to species found at all four sites; the majority of the species that were not captured at all four sites were captured in low numbers. This was most likely due to low abundance or because the species were not strongly attracted to CO2-baited light traps. Species diversity for the four collection sites, estimated by using the Simpson Index/Index of Diversity which takes into consideration the relative abundance of mosquitoes in each species, ranged from 0.42 – 0.53 (Table 1)[26]. These values suggest that overall the four collection sites supported similar species diversity.
Table 1.
Mosquito species collected in Mpigi District, central Uganda, in October 2011.
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| Genus | Subgenus | Species | Number collected (%)
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| Njeru | Ddela | Kiwumu | Nsumba | All sites | ||||||||
| Aedes | Aedimorphus | argenteopunctatus (Theobald) | 3 | (0.02) | 3 | (0.01) | ||||||
| cumminsii (Theobald) | 26 | (0.16) | 26 | (0.05) | ||||||||
| phyllolabis Edwards | 25 | (0.16) | 10 | (0.06) | 10 | (0.08) | 10 | (0.10) | 55 | (0.10) | ||
| tarsalis (Newstead) | 3 | (0.02) | 3 | (0.01) | ||||||||
| Finlaya | ingrami Edwards | 1 | (0.01) | 1 | (0.01) | 2 | (0.00) | |||||
| Neomelaniconion | circumluteolus (Theobald) | 136 | (0.85) | 112 | (0.67) | 113 | (0.93) | 40 | (0.42) | 401 | (0.73) | |
| mcintoshi Huang | 19 | (0.12) | 25 | (0.15) | 25 | (0.21) | 22 | (0.23) | 91 | (0.17) | ||
| Stegomyia | aegypti (L.) | 1 | (0.01) | 6 | (0.04) | 8 | (0.07) | 15 | (0.03) | |||
| simpsoni groupa | 1 | (0.01) | 2 | (0.02) | 3 | (0.01) | ||||||
| species | 4 | (0.02) | 8 | (0.07) | 12 | (0.02) | ||||||
| Anopheles | Anopheles | coustani Laveran | 5 | (0.03) | 7 | (0.04) | 1 | (0.01) | 13 | (0.02) | ||
| implexus (Theobald) | 10 | (0.06) | 10 | (0.02) | ||||||||
| Cellia | gambiae groupb | 26 | (0.15) | 26 | (0.05) | |||||||
| Coquillettidia | Coquillettidia | aurites (Theobald) | 186 | (1.16) | 187 | (1.11) | 155 | (1.28) | 75 | (0.78) | 603 | (1.10) |
| fraseri (Theobald) | 774 | (4.82) | 1292 | (7.68) | 476 | (3.93) | 587 | (6.14) | 3129 | (5.70) | ||
| fuscopennata (Theobald) | 11508 | (71.73) | 11412 | (67.86) | 9175 | (75.83) | 6444 | (67.44) | 38539 | (70.23) | ||
| maculipennis (Theobald) | 238 | (1.48) | 135 | (0.80) | 148 | (1.22) | 90 | (0.94) | 611 | (1.11) | ||
| metallica (Theobald) | 1142 | (7.12) | 1754 | (10.43) | 689 | (5.69) | 674 | (7.05) | 4259 | (7.76) | ||
| pseudoconopas (Theobald) | 52 | (0.32) | 134 | (0.80) | 57 | (0.47) | 53 | (0.55) | 296 | (0.54) | ||
| versicolor (Barraud) | 49 | (0.31) | 124 | (0.74) | 56 | (0.46) | 229 | (0.42) | ||||
| species | 15 | (0.09) | 16 | (0.13) | 31 | (0.06) | ||||||
| Culex | Culex | antennatus (Becker) | 52 | (0.32) | 29 | (0.17) | 19 | (0.16) | 41 | (0.43) | 141 | (0.26) |
| decens groupc | 176 | (1.10) | 373 | (2.22) | 261 | (2.16) | 377 | (3.95) | 1187 | (2.16) | ||
| neavei Edwards | 9 | (0.05) | 7 | (0.06) | 80 | (0.84) | 96 | (0.17) | ||||
| ornatothoracis Theobald | 56 | (0.35) | 44 | (0.26) | 42 | (0.35) | 45 | (0.47) | 187 | (0.34) | ||
| perfuscus Edwards | 11 | (0.12) | 11 | (0.02) | ||||||||
| pipiens (L.) | 2 | (0.01) | 2 | (0.00) | ||||||||
| quinquefasciatus Say | 2 | (0.02) | 2 | (0.00) | ||||||||
| trifilatus Edwards | 1 | (0.01) | 19 | (0.20) | 20 | (0.04) | ||||||
| Culiciomyia | cinerellus Edwards | 1 | (0.01) | 1 | (0.00) | |||||||
| Culiciomyia | cinereus Theobald | 257 | (1.60) | 117 | (0.70) | 21 | (0.17) | 67 | (0.70) | 462 | (0.84) | |
| nebulosus Theobald | 23 | (0.14) | 13 | (0.08) | 116 | (1.21) | 152 | (0.28) | ||||
| Eumelanomyia | insignis (Carter) | 22 | (0.14) | 37 | (0.22) | 24 | (0.20) | 30 | (0.31) | 113 | (0.21) | |
| rubinotus Theobald | 50 | (0.31) | 29 | (0.17) | 103 | (0.85) | 66 | (0.69) | 248 | (0.45) | ||
| Kitzmelleria | moucheti Evans | 5 | (0.03) | 1 | (0.01) | 4 | (0.04) | 10 | (0.02) | |||
| Oculeomyia | annulioris Theobald | 1212 | (7.55) | 746 | (4.44) | 439 | (3.63) | 486 | (5.09) | 2883 | (5.25) | |
| annulioris consimilis Newstead | 13 | (0.08) | 20 | (0.17) | 33 | (0.06) | ||||||
| poicilipes Theobald | 3 | (0.02) | 3 | (0.01) | ||||||||
| species | 14 | (0.15) | 14 | (0.03) | ||||||||
| Hodgesia | Hodgesia | sanguinae Theobald | 17 | (0.11) | 17 | (0.03) | ||||||
| species | 32 | (0.20) | 32 | (0.06) | ||||||||
| Lutzia | Metalutzia | tigripes de Grandpre & de Charmoy | 26 | (0.16) | 36 | (0.21) | 18 | (0.15) | 28 | (0.29) | 108 | (0.20) |
| Mansonia | Mansonioides | africana (Theobald) | 4 | (0.02) | 10 | (0.08) | 2 | (0.02) | 16 | (0.03) | ||
| africana nigerrima Theobald | 178 | (1.11) | 90 | (0.54) | 68 | (0.56) | 63 | (0.66) | 399 | (0.73) | ||
| uniformis (Theobald) | 65 | (0.41) | 32 | (0.19) | 32 | (0.26) | 36 | (0.38) | 165 | (0.30) | ||
| Mimomyia | Mimomyia | hispida (Theobald) | 2 | (0.02) | 2 | (0.00) | ||||||
| Uranotaenia | Pseudoficalbia | mashonaensis Theobald | 2 | (0.01) | 2 | (0.02) | 4 | (0.01) | ||||
| Uranotaenia | alboabdominalis Theobald | 3 | (0.02) | 3 | (0.01) | |||||||
| palidocephala Theobald | 21 | (0.13) | 25 | (0.15) | 63 | (0.52) | 47 | (0.49) | 156 | (0.28) | ||
| species | 26 | (0.21) | 25 | (0.26) | 51 | (0.09) | ||||||
| Total | 16403 | 16818 | 12099 | 9555 | 54875 | |||||||
| Grand total | 54,875 | |||||||||||
| D | 0.51 | 0.48 | 0.58 | 0.47 | 0.51 | |||||||
| 1-D | 0.49 | 0.52 | 0.42 | 0.53 | 0.49 | |||||||
The Ae. simpsoni group includes Ae. simpsoni s.s. (Theobald), Ae. bromeliae (Theobald), Ae. gandaensis Huang, Ae. josiahae Huang, Ae. kivuensis Edwards, Ae. lilii (Theobald), Ae. strelitziae Muspratt, Ae. subargenteus Edwards, and Ae. woodi Edwards[22].
The An. gambiae group consist of at least six species An. gambiae s.s. Giles, An. arabiensis Patton, An. quadriannulatus Theobald, An. melas Theobald, An. merus Dönitz, and An. bwambae White (Gilles and Coetzee 1987).
The Culex decens group includes Cx. decens Theobald and Cx. invidiosus Theobald (Edwards 1941).
Figure 2 summarizes the species richness or number of species in each genus collected at the four sites. The highest number of species was in the genus Culex at all four sites (Figure 2). At three sites, Ddela, Kiwumu and Nsumba, the second highest number of species was in the genus Coquillettidia and the third in the genus Aedes (Figure 2). At Njeru, the second highest number of species was in the genus Aedes, and the third in genus Coquillettidia (Table 2). Overall species richness by genus ranged from 37.0% in the genus Culex (37% of all species collected were in the genus Culex) to 2.2% in Hodgesia and Mimomyia (Fig. 2). The genus Culex was highest in species richness comprising 17 species (n=5,548, 10.1% of the total collection), followed by the genus Aedes (n=611, 1.1%) with 9 species (19.6%) (Table 1, Fig 2). Although the genus Coquillettidia had the highest number of mosquitoes captured (n=47,697, 86.9%), it ranked third in terms of species richness with 8 species (17.4%) (Table 1, Fig 2). The Uranotaenia and Mansonia genera had identical species richness with 6.5% each of the total species identified (Fig 2). The rest of the species were in the genera Anopheles, Hodgesia and Mimomyia and had minimal contribution to the total species richness in the area (Fig 2).
Figure 2.
Number of mosquito species collected in each genus by study site.
The most abundant mosquitoes were in the genus Coquillettidia followed by the genus Culex (Table 1). The predominant species collected was Coquillettidia (Coquillettidia) fuscopennata (Theobald) (n=38,059, 69.4%), followed by Coquillettidia (Coquillettidia) metallica (Theobald) (n=4,265, 7.8%) and Coquillettidia (Coquillettidia) fraseri (Theobald) (n=3,129, 5.7%) (Table 1). Coquillettidia species are often the principal species collected near water/wetlands which are their preferred larval habitats. The ecology of the study area in Mpigi District included freshwater swampland in addition to small scale agricultural landscapes adjacent to human habitation, therefore, the large numbers of Coquillettidia mosquitoes collected was not unexpected. The next most abundant species collected were Culex (Oculeomyia) annulioris Theobald (n=2,883, 5.3%) and Culex (Culex) decens group Theobald and Culex (Culex) invidiosus Theobald)(n=1,187, 2.2%) (Table 1)[21]. Additional species contributing >0.5% to the collection included Coquillettidia (Coquillettidia) maculipennis (Theobald) (n=611, 1.1%), Coquillettidia (Coquillettidia) aurites (Theobald)(n=603, 1.1%), Coquillettidia (Coquillettidia) cristata (Theobald) (n=480, 0.9%), Culex (Culiciomyia) cinereus (Theobald)(n=462, 0.8%), Aedes (Neomelaniconion) circumluteolus (Theobald) (n=401, 0.7%), Mansonia (Mansonioides) africana nigerrima Theobald (n=399, 0.7%) and Coquillettidia (Coquillettidia) pseudoconopas (Theobald) (n=296, 0.5%) (Table 1).
Of the 46 mosquito species collected in this study arboviruses of medical and veterinary importance had previously been isolated from 28 (60.9%) suggesting roles in the transmission or the maintenance of these arboviruses. This shows a high potential for maintenance and transmission of arboviruses of medical and veterinary importance in Mpigi District. A comprehensive list of arboviruses that have been isolated from mosquito species collected in Uganda has been published by Mutebi et al. [1]. For many of these species it is unknown whether they play a significant role in epidemic or enzootic virus transmission. However, certain species in the collection are known to be epidemic/enzootic vector species including Aedes (Stegomyia) aegypti (L.), a principal vector of Yellow fever virus (YFV) [27, 28], Chikungunya virus [29], Dengue viruses[30] and Zika virus [31]. Similarly, members of the Aedes (Stegomyia) simpsoni group have been shown to be epidemic vectors of YFV [32, 33] and members of the Anopheles (Cellia) gambiae group are vectors of ONNV[20, 34]. Additionally epidemic and epizootic transmission of Rift Valley fever virus has been implicated for several species collected in Mpigi district including Aedes (Neomelaniconion) mcintoshi/circumluteolus, Mansonia (Mansonioides) africana (Theobald), Mansonia (Mansonioides) uniformis (Theobald), Culex (Culex) pipiens (L.), Culex (Culex) quinquefasciatus Say, Culex (Oculeomyia) annulioris Theobald and Culex (Oculeomyia) poicilipes Theobald[35–40]. Some known disease vectors identified in this collection were not captured at all four sites suggesting non-uniform distribution of these vectors in the study sites and an uneven risk of disease transmission across the region. For example members of the Anopheles (Cellia) gambiae group were only detected at Ddela and not at any other study site (Table 1). Similarly, Culex (Culex) pipiens (L) was only detected at Ddela (Table 1). Interestingly Culex (Culex) quinquefasciatus Say, which is closely related to Cx. pipiens, was only detected at Nsumba and not at any other study site (Table 1). Both Cx. pipiens and Cx. quinquefasciatus which are commonly captured in C02-baited light traps were found in low numbers suggesting that the densities of these two species were low at the study sites. Cx. pipiens and Cx. quinquefasciatus are commonly associated with human residences (domestic species). Since collections in this study were conducted in domestic and peridomestic areas, our observations suggest that the risk of Cx. pipiens and Cx. quinquefasciatus-transmitted pathogens is low in this area.
To our knowledge this is the first documented account of the mosquito fauna of Mpigi District in central Uganda. All of the 45 species identified had previously been identified elsewhere in Uganda and do not represent new introductions to the country. Species richness in this area was high and >60% of the mosquito species collected have been previously documented as potential arbovirus vectors. Increased human activity and encroachment in to undeveloped areas in this region presents a potential risk for exposing humans to arboviral diseases. Historical records show that Uganda has experienced numerous outbreaks of arboviral disease including YFV and ONNV[20, 41] and many known arboviruses were first isolated from Uganda[3, 4]. Further study is necessary to determine the seasonal variation in mosquito species composition and abundance in this region. Additionally, virus isolation from collected mosquitoes will be conducted to identify arboviruses that are currently circulating in the area. Such information will be invaluable in predicting and controlling potential outbreaks of arboviral disease in this region.
Acknowledgments
We would like to thank the Chairman and the local health officials of Kammengo Sub County for granting us permission to conduct these studies. We especially thank the residents of Njeru, Ddela, Kiwumu and Nsumba villages for giving us free access to their properties. We also thank John-Bosco Lwanga, Julius Mugga and Godfrey Kyazze for their assistance during the mosquito collection in the field. This study was supported with funds from the US Centers for Disease Control and Prevention (CDC) and USAID Emerging Pandemic Threat Program.
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