Mosquitoes of Western Uganda

Abstract

The mosquito fauna in many areas of western Uganda has never been studied and is currently unknown. One area, Bwamba County, has been previously studied and documented but the species lists have not been updated for more than 40 years. This paucity of data makes it difficult to determine which arthropod-borne viruses pose a risk to human or animal populations. Using CO₂ baited-light traps, from 2008 through 2010, 67,731 mosquitoes were captured at five locations in western Uganda including Mweya, Sempaya, Maramagambo, Bwindi (BINP), and Kibale (KNP). Overall, 88 mosquito species, 7 subspecies and 7 species groups in 10 genera were collected. The largest number of species was collected at Sempaya (65 species), followed by Maramagambo (45), Mweya (34), BINP (33), and KNP (22). However, species diversity was highest in BINP (Simpson’s Diversity Index 1-D = 0.85), followed by KNP (0.80), Maramagambo (0.79), Sempaya (0.67), and Mweya (0.56). Only six species (Aedes (Aedimorphus) cumminsii (Theobald), Aedes (Neomelaniconion) circumluteolus (Theobald), Culex (Culex) antennatus (Becker), Culex (Culex) decens group, Culex (Lutzia) tigripes De Grandpre and De Charmoy, and Culex (Oculeomyia) annulioris Theobald), were collected from all 5 sites suggesting large differences in species composition among sites. Four species (Aedes (Stegomyia) metallicus (Edwards), Anopheles (Cellia) rivulorum Leeson, Uranotaenia (Uranotaenia) chorleyi Edwards, and Uranotaenia (Uranotaenia) pallidocephala Theobald) and one subspecies (Aedes (Stegomyia) aegypti formosus (Walker)) were collected in Bwamba County for the first time. This study represents the first description of the mosquito species composition of Mweya, Maramagambo, BINP and KNP. At least 50 species collected in this study have previously been implicated in the transmission of arboviruses of public health importance suggesting a high potential for maintenance and transmission of a wide variety of arboviruses in western Uganda.

Introduction

A considerable amount of information on species composition and ecology of the mosquitoes of Uganda was compiled between the mid-1930s and the early 1970s. The bulk of this information was from the entomological investigations component of the arbovirus surveillance program conducted at the Uganda Virus Research Institute (UVRI) in Entebbe. The UVRI, then known as the Yellow Fever Research Institute, was established in 1936 by the International Division of the US Rockefeller Foundation. Its primary mission was to study yellow fever epidemiology in eastern Africa and, specifically, to investigate the extent of the spread of yellow fever virus (YFV) eastward from West Africa. In the course of these investigations mosquito species composition for some locations in Uganda were described (Smithburn et al. 1941, Smithburn and Haddow 1944, Smithburn and Haddow 1946, Smithburn et al. 1946, Haddow 1946, Haddow et al. 1948, Haddow and Mahaffy 1949, Haddow and van Someren 1950, Haddow et al. 1951, Smithburn and Haddow 1951, Dick and Haddow 1952). However, arbovirus surveillance was undertaken in only a few areas and therefore mosquito species compositions for much of Uganda are unknown. Further, mosquito species composition descriptions were not compiled in concise regional mosquito species lists but rather were scattered in numerous publications many of which are older archives or obscure regional journals that are not easily accessible. The only exception is the monograph by Haddow et al. (1951) which described in detail the more than 160 mosquito species records from Bwamba County in western Uganda for the ten year period from 1936 to 1946. Unfortunately, the efforts initiated by the Rockefeller Institute were interrupted by the civil instabilities in Uganda during the 1970s and 1980s. Recently, arbovirus research and surveillance activities have resumed at UVRI, but have mainly been limited to monitoring outbreaks, such as the O’nyong-nyong virus (ONNV) outbreak in 1996 (Lutwama et al. 1999). Currently, most species composition descriptions date between the mid-1930s and the early 1970s, and no records have been updated for over 40 years.

In 2008, the US Centers for Disease Control and Prevention (CDC) and UVRI re-established the arbovirus surveillance program with the primary aim of screening for and describing arboviruses of public health and veterinary importance currently circulating within Uganda. In this manuscript, we describe and discuss mosquito species composition at five locations in western Uganda including: Sempaya, in Semliki National Park (SNP), Mweya, in Queen Elizabeth National Park (QENP), Maramagambo Forest, in QENP, Bwindi Impenetrable National Park (BINP) and Kibale National Park (KNP) and discuss their possible role as arbovirus vectors.

Materials and Methods

Study sites

A map showing the location of the five study sites is provided in Figure 1 and Figure 2 includes photographs depicting the typical vegetation/landscape at each site.

Fig. 1.

A map of Uganda showing the locations of Sempaya, in Semliki National Park, Mweya and Maramagambo Forest, in Queen Elizabeth National Park, Bwindi Impenetrable National Park and Kibale National Park in western Uganda.

Fig. 2.

Photographs illustrating the general vegetation and topology of each of the study sites A) Sempaya, B) Mweya, C) Maramagambo, D) Kibale and E) Bwindi.

Sempaya village (0^O 49’ N: 30^O 10’E) is located in SNP, which is in extreme western Uganda in Bwamba County (Bundibugyo District), west of the Ruwenzori mountain range (Fig. 1). It is located between the Buranga hot springs and the foothills of the Ruwenzori mountain range approximately 15 km northwest of Fort Portal. The ecosystem of SNP is primarily that of dense, moist, semi-deciduous, tropical lowland forest (Fig. 2A) and is part of the great Ituri Forest that stretches into the Democratic Republic of Congo. Rainfall occurs year round with peaks from March to May, and September to December; average rainfall at the study site is 2,558 mm per annum (Monaghan et al. 2012, Haddow 1945). The mean annual temperature is 24.7^OC with a range of 19.6–29.4^OC (Monaghan et al. 2012). The altitude at the trap site was between 678 m and 753 m above sea level.

Mweya, located roughly in the middle of QENP (0^O 11’ S: 29^O 54’ E) is at the junction between Lake Edward and the Kazinga Channel (Fig. 1). The trap locations were close to Mweya Safari Lodge at an altitude of 917–956 m above sea level. The ecosystem of Mweya is mostly open savannah and grassland vegetation (Fig. 2B). Mweya is characterized by two wet seasons, March to May and October to December, and the average annual precipitation at the study site is 809 mm (Monaghan et al. 2012). The average daily temperature is 24.7°C (range 20.2–30.3°C) (Monaghan et al. 2012).

Maramagambo (0° 16’ S: 30° 03’ E), is a large, moist, semi-deciduous forest (Fig. 2C) in the southeastern extremity of QENP, west of the Kyambura escarpment (Fig. 1). It is located approximately 20 km east of Mweya at an altitude of approximately 969 m above sea level (Monaghan et al. 2012). Similar to Mweya, there are two wet seasons, March to May and October to December. The average annual precipitation and average daily temperature are the same as Mweya.

Kibale National Park (0° 34’ N: 30° 22’ E) is located in Kabarole District, approximately 35 km east of Fort Portal (Fig. 1). The park encompasses approximately 766 km² and the predominant ecosystem is moist, medium altitude, evergreen and semi-deciduous forest (Fig. 2D). Mosquito trapping sites were on the perimeter of the Makerere University Biological Field Station. The altitude range at the study site is 1,390–1,625 m above sea level. The average annual temperature is 19.3°C (range 16.2–23.6°C), and the average annual rainfall is 1,671 mm (mailto:http://weber.ucsd.edu/~jmoore/apesites/Kibale/Kibale.html).

Bwindi Impenetrable National Park (01°03′S 29°43′E) is located in southwestern Uganda on the eastern edge of the Albertine Rift Valley (Fig. 1). It encompasses 331 km² consisting of both medium altitude, moist, evergreen forest and high altitude, submontane forest (Langdale-Brown et al. 1964) (Fig. 2E). Bwindi is one of the most diverse forest ecosystems in East Africa, with at least 223 known trees species which is approximately 53% of Uganda’s tree flora (Kakuru 1993). Mosquito collections for this study were conducted close to the park headquarters near the Buhoma gate. At this location, the annual mean temperature range was 16.9–20.7°C (Monaghan et al. 2012). Annual rainfall at the study site ranges from 1,590 mm to 1,807 mm (Monaghan et al. 2012) occurring year round with two peaks, from March to April and from September to November (Eilu and Obua 2005). The elevation at the study site is 1,470–2,165 m above sea level (Monaghan et al. 2012).

Mosquito Collections

Mosquitoes were captured by using CDC miniature light traps (Clarke Mosquito Control, Roselle, IL) with dry ice, a source of carbon dioxide, as an attractant. At Sempaya, 3 collection trips were conducted from November 8–12, 2008, June 7–12, 2009, and January 15–18, 2010. Twelve to 24 traps were used and approximately half of them were placed in the forest, ≥50 m apart to minimize interference. The remaining traps were placed along forest edges, approximately 100 m apart in locations sheltered from direct sunlight and wind.

Three collection trips were conducted at Mweya, November 14–17, 2008, June 14–20 2009, and January 19–21, 2010. Traps were placed in two general areas: 1) adjacent to the student hostels on the eastern side of Mweya Safari Lodge and 2) adjacent to the jetty and along the Kazinga Channel north of the lodge. Twelve to 24 traps were split equally between the jetty and hostel areas. The collection site near the hostel was mostly flat savannah grassland with scattered shrubs; traps were placed within the shrubs to protect them from direct sunlight and wind. The collection area adjacent to the jetty was in a lightly-wooded, small valley sheltered from the wind where the nearby banks of the Kazinga Channel were covered with papyrus and other fresh water hydrophytes. Traps here were hung in the trees.

Two collection trips were conducted in Maramagambo Forest June 16–18, 2009 and January 19–22, 2010. We used 6–24 traps, all of which were placed along the trail to the python cave within the forest. Maramagambo is not a typically dense tropical forest exhibiting little undergrowth due to clearing of fire materials by local inhabitants; therefore, the traps were placed approximately 100 m apart to minimize interference.

Two collection trips were conducted in BINP: January 23–26, 2010 and June 14–17, 2010. On each trip, 24 traps were used. On the first trip 20 traps were placed along trails and paths in the forest and four traps were placed near the Buhoma Gate administration buildings and in the Buhoma Lodge yard, in a clearing at the northern edge of the park. On the second trip half of the traps were placed outside the forest in the Bwindi Community Hospital yard, the Buhoma Primary School yard, in several banana and tea plantations, and in communal grazing fields adjacent to BINP. The rest of the traps were placed along trails in the forest.

A single collection trip was made to KNP from June 19–22, 2010. Twenty four traps were used at this location, all of which were placed on the boundaries of a clearing around the Makerere University Biological Field Station (MUBFS) on the western edge of the park. The traps were hung approximately 50 m apart on tree branches.

Mosquito processing

Mosquitoes were collected from traps each morning, chilled on dry ice, separated from other arthropods and counted into cryotubes. The tubed mosquito samples were kept frozen either on dry ice or in liquid nitrogen dry shippers until shipped to the CDC laboratory in Fort Collins, CO, for identification and processing. At the CDC, the mosquitoes were identified to species on the basis of morphological characters by using the keys of Edwards (1941), Jupp (1985), Gilles and De Mellion (1968), Gilles and Coetzee (1987) and Huang (2004), supplemented with notes by Haddow et al. (1951), Gillett (1946), Corbet (1958) and Gillett (1972). Voucher specimens for each species were kept for future reference and for identification consultations.

Diversity Indices

Species richness and species diversity were calculated for each location and collection period. Species richness is reported as the number of mosquito species at each location. Species diversity was estimated by calculating the Simpson Index (Simpson 1949). The Simpson Index (D), which accounts for both species richness and the relative abundance of each species, was calculated as D = Σ n(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. For simplicity, we also report the Simpson’s Index of Diversity (1-D), which is interpreted as the greater the index, the greater the sample diversity. An index of 0 would indicate perfect homogeneity whereas an index of 1 would indicate perfect heterogeneity.

Results and Discussion

A total of 67,731 adult mosquitoes were collected from all 5 locations (Table 1), with 39,037 collected at Mweya, 22,498 at Sempaya, 1,567 at Maramagambo, 1,705 at BINP, and 2,924 at KNP. Ten mosquito genera, (Aedes, Anopheles, Coquillettidia, Culex, Culiseta, Eretmapodites, Mansonia, Mimomyia, Orthopodomyia, and Uranotaenia) were represented in the collections, but not all 10 genera were collected from any single location (Fig. 3). The greatest generic richness was found at Sempaya (9 genera), followed by BINP (8), Maramagambo (7), Mweya (6) and lastly KNP (5) (Fig. 3). The absence of certain genera at some sites is intriguing and suggests discontinuity in mosquito generic distribution in western Uganda. For example, the genus Uranotaenia was not collected from KNP or Mweya, however, collections were conducted during only one season at KNP therefore limited sampling may have precluded capture of specimens in this genus. In contrast, collections at Mweya comprised multiple seasons in different years suggesting that the genus Uranotaenia is either extremely rare or completely absent at this location. An additional example, the genus Mimomyia was not collected in KNP or Maramagambo (Fig. 3) and the genera Eretmapodites and Mansonia were not collected in KNP. The genera Orthopodomyia and Culiseta were only collected in KNP and Sempaya, respectively, (Table 1) and only in small numbers suggesting either the abundance of these genera is low or that they were not attracted to the CO₂-baited light traps.

Table 1.

Number of mosquito species and subspecies collected at five locations in western Uganda from 2008 to 2010.

			Collection Site
Genus	Subgenus	Species	Bwindi	Kibale	Maramagambo	Mweya	Sempaya
Aedes	Aedimorphus	abnormalis kabwachensis Edwards				4
		albocephalus (Theobald)			117	28	1007
		argenteopunctatus (Theobald)				1
		cumminsii (Theobald)	6	1	115	2	585
		domesticus (Theobald)					17
		hirsutus (Theobald)				2	1
		leptolabis Edwards					1
		mutilus Edwards			2		1
		natronius Edwards				19	7
		quasiunivittatus (Theobald)		2
		stenoscutus Edwards					29
		stokesi Evans					8
		tarsalis (Newstead)	15	117	5		405
		tricholabis Edwards			1
	Diceromyia	taylori Edwards			1
	Finlaya	ingrami Edwards	1	4			5
	Mucidus	grahamii (Theobald)					3
	Neomelaniconion	albothorax (Theobald)			3	19	1601
		circumluteolus (Theobald)	11	18	334	20	281
		mcintoshi Huang				1
		palpale Newstead	1
		taeniarostris (Theobald)			1		6
		taeniarostris/carteri			1
	Stegomyia	aegypti Linnaeus		1		6	6
		aegypti formosus (Walker)		1		39	24
		apicoargenteus group1		2			3
		dendrophilus group2			1		15
		fraseri (Edwards)			7
		luteocephalus (Newstead)			1		1
		metallicus (Edwards)				68	16
		simpsoni group3				6	17
Aedes		species				32	14
	Zavortinkius	longipalpis (Gruenberg)			1		1
Aedes		species				2	13
Anopheles	Anopheles	coustani Laveran			1
		implexus (Theobald)	3	60	11
		obscurus (Gruenberg)			1		1
		paludis Theobald					8
		symesi Edwards				166
		ziemanni Greunberg			1	74
	Cellia	demeilloni Evans					2
		domicola Edwards			5
		funestus group4			1		1
		gambiae group5			1	11	413
		longipalpis/funestus					2
		pharoensis Theobald				3
		rivulorum Leeson					5
Anopheles		species			4	7
Coquillettidia	Coquillettidia	aureus (Edwards)					1
		aurites (Theobald)	60		20		22
		fraseri (Theobald)	483	123		7	29
		aurites/fraseri					5
		fuscopennata (Theobald)		564	371		370
		maculipennis (Theobald)	96	1119	29		227
		metallica (Theobald)	2		72	164	94
		microannulata (Theobald)			2		1
		pseudoconopas (Theobald)	47	85		2	1516
		versicolor (Edwards)	3	96
		species	2		2		7
Culex	Culex	antennatus (Becker)	2	3	5	307	34
		decens group6	240	285	51	1	190
		duttoni Theobald			1	63	1
		ingrami Edwards		3	1
		neavei Theobald	13		165	14751	139
		ornatothoracis Theobald					1
		perfuscus Edwards			2		11407
		pipiens complex7	5				7
		pipiens Linnaeus	1
		pruina Theobald	1		60
		quasiguiarti Theobald	1				7
		quinquefasciatus Say	4			5	33
		terzii Edwards				2
		toroensis macrophyllus Edwards & Gibbins	1
		trifilatus Edwards	74	15
		trifilatus aenescens Edwards	84	107
		watti Edwards	1	25		1	2
		zombaensis Theobald			10	5
	Culiciomyia	cinerellus Edwards			1
		cinereus Theobald	14			143	13
		macfiei Edwards		2
		mongiro Van Someren			4		87
		nebulosus Theobald	81	45	8		193
	Eumelanomyia	horridus Edwards					15
		insignis (Carter)	1		7	8	11
		rubinotus Theobald		3		20	37
		simpliciforceps Edwards		31
	Kitzmilleria	moucheti Evans	28		13		65
	Lutzia	tigripes De Grandpre & De Charmoy	4	4	2	2	11
	Oculeomyia	annulioris Theobald	39	10	4	4	51
		annulioris consimilis Newstead	257	140
		aurantapex jinjaensis Edwards		9
		poicilipes (Theobald)			2	19710	337
Culex		species	100	47	68	9	1590
Culiseta	Theomyia	fraseri Edwards					2
Eretmapodites		chrysogaster Graham	1		2		329
Mansonia	Mansonioides	africana (Theobald)			35	801	56
		africana nigerrima Theobald	4		1
		uniformis (Theobald)			1	2162	7
Mimomyia	Etorleptiomyia	mediolineata (Theobald)				1	23
	Mimomyia	hispida (Theobald)	1
		mimomyiaformis (Newstead)				359	1
		plumosa (Theobald)	1				20
Orthopodomyia		species		2
Uranotaenia	Pseudoficalbia	mashonaensis Theobald	2		5		925
		musarum Edwards			3		16
		nivipous Theobald					10
	Uranotaenia	alboabdominalis Theobald			1		8
		balfouri Theobald	1				1
		chorleyi Edwards	3				11
		connali Edwards	1		3		84
		pallidocephala Theobald	10		1		3
Totals			1705	2924	1567	39037	22498

¹The Ae. apicoargenteus group includes Ae. apicoargenteus s.s. (Theobald), Ae. blacklocki (Evans), Ae. denderensis Wolfs, Ae. ealaensis Huang, Ae. fraseri (Edwards), Ae. schwetzi Edwards & Ae. soleatus Edwards (Huang 2004).

²The Ae. dendrophilus group includes Ae. amaltheus De Meillon & Lavoipierre, Ae. bambusae Edward, Ae. deboeri Edwards, Ae. demeilloni Edwards, Ae. dendrophilus s.s. Edwards, Ae. hansfordi Huang, Ae. heischi Van Someren, Ae. keniensis Van Someren, Ae. kenyae Van Someren & Ae. masseyi Edwards (Huang 2004).

³The 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 & Ae. woodi Edwards (Huang 2004).

⁴The Anopheles funestus group includes An. funestus s.s., An. rivulorum Leeson, An. leesoni Evans, An. vaneedeni Gillies & Coetzee, An. parensis Gillies, An. confusus Evans & Leeson, An. aruni Sobti, An. fuscivenosus Leeson, and An. brucei Service (Gilles & Coetzee 1987).

⁵The Anopheles gambiae group consist of at least 6 species An. gambiae s.s. Giles, An. arabiensis Patton, An. quadriannulatus Theobald, An. melas Theobald, An. merus Dönitz & An. bwambae White (Gilles & Coetzee 1987).

⁶The Culex decens group includes Cx. decens Theobald & Cx. invidiosus Theobald (Edwards 1941).

⁷In sub-Saharan Africa the Culex pipiens complex consists of Cx. pipiens Linneaus & Cx. quinquefasciatus Say (Edwards 1941).

Fig. 3.

Number of mosquito species collected in each genus by study site.

In Sempaya, Mweya and BINP, Culex species made up the largest proportion of the collections, whereas Aedes and Coquillettidia species made up the largest proportion of the collections at Maramagambo and KNP, respectively. Overall, the most diverse genera in the collections were Culex (27 species) and Aedes (26 species) (Fig. 3), and Culex species made up by far the largest proportion of the total collection (51,346 mosquitoes) (Table 1). The second and third most frequently collected species were in the genus Coquillettidia (5,621 mosquitoes) and Aedes (5,086 mosquitoes), respectively (Table 1). It is interesting to note that mosquitoes in the genus Coquillettidia were very common in the forest ecosystems of Sempaya, Maramagambo, KNP and BINP but relatively rare in Mweya which is mostly open grassland (Figs. 2 and 3). Coquillettidia mosquitoes were sixth in abundance in Mweya with only 173 (0.43%) specimens collected. In contrast Coquillettidia mosquitoes were the most abundant in Kibale (67.96%), second most abundant in BINP (40.7%) and Maramagambo (31.66%), and third most abundant in Sempaya (10.1%).

Overall a total of 88 mosquito species, 7 subspecies and 7 species groups were identified in western Uganda (Table 1). The greatest species richness was collected at Sempaya (65 species), followed by Maramagambo (45), Mweya (34), BINP (33), and KNP (22) (Table 1). Of the 100 species, subspecies and species groups collected, only 6 were collected from all 5 sites: Aedes (Aedimorphus) cumminsii (Theobald), Aedes (Neomelaniconion) circumluteolus (Theobald), Culex (Culex) antennatus (Becker), Culex (Culex) decens group, Culex (Lutzia) tigripes De Grandpre and De Charmoy and Culex (Oculeomyia) annulioris Theobald (Table 1). The wide range of variation in species composition among the sites is of interest considering that four of the five sites (Sempaya, KNP, Maramagambo and BINP) are similar tropical forest ecosystems and that all of the study sites were within a relatively short distance (< 240 km) of each other (Fig. 1). This suggests that microecosystems play a significant role in determining species composition.

Diversity indices for each collection are reported in Tables 2 – 6. On average, species diversity was highest in BINP (Simpson’s Diversity Index 1-D = 0.85), followed by KNP (0.80), Maramagambo (0.79), Sempaya (0.67), and Mweya (0.56). While Sempaya had the highest species richness, it was not consistently the most biologically diverse. This finding is likely due to Culex (Culex) perfuscus Edwards comprising a large proportion of the collections from this site in November 2008 and June 2009 (Table 2). Species diversity fluctuated widely at Sempaya among the three sampling periods, ranging from 0.37 – 0.91. While the overall numbers of mosquitoes collected at Maramagambo and BINP (Tables 4 and 5) was relatively low, these two locations had the highest species richness and their biological diversity index was consistently high during both seasons sampled at each of these locations.

Table 2.

Mosquito species collected at Sempaya, Semliki National Park, Uganda, in November 2008, June 2009 and January 2010. Simpson’s Index (D) and Simpson’s Index of Diversity (1-D) for each collection trip are presented at the bottom of the table.

			Number collected (%)
Genus	Subgenus	Species	November 2008		June 2009		January 2010
Aedes	Aedimorphus	albocephalus	6	(0.14)	901	(5.43)	100	(6.54)
		cumminsii	5	(0.11)	576	(3.47)	4	(0.26)
		domesticus			13	(0.08)	4	(0.26)
		hirsutus			1	(0.01)
		leptolabis			1	(0.01)
		mutilus			1	(0.01)
		natronius			6	(0.04)	1	(0.07)
		stenoscutus			29	(0.17)
		stokesi			7	(0.04)	1	(0.07)
		tarsalis	17	(0.39)	344	(2.07)	44	(2.88)
	Finlaya	ingrami			5	(0.03)
	Mucidus	grahamii			3	(0.02)
	Neomelaniconion	albothorax	94	(2.15)	1309	(7.88)	198	(12.96)
		circumluteolus	77	(1.76)	154	(0.93)	50	(3.27)
		taeniarostris			6	(0.04)
	Stegomyia	aegypti			6	(0.04)
		aegypti formosus			21	(0.13)	3	(0.20)
		apicoargenteus group1			1	(0.01)	2	(0.13)
		dendrophilus group2			15	(0.09)
		luteocephalus			1	(0.01)
		metallicus			16	(0.10)
		simpsoni group3			17	(0.10)
		species			13	(0.08)	1	(0.07)
	Zavortinkus	longipalpis			1	(0.01)
Aedes		species	6	(0.14)			7	(0.46)
Anopheles	Anopheles	obscurus			1	(0.01)
		paludis			8	(0.05)
	Cellia	demeilloni			2	(0.01)
		gambiae group5	79	(1.81)	206	(1.24)	128	(8.38)
		funestus group4					1	(0.07)
		longipalpis/funestus			2	(0.01)
		rivulorum			5	(0.03)
Coquillettidia	Coquillettidia	aureus			1	(0.01)
		aurites			14	(0.08)	8	(0.52)
		fraseri			27	(0.16)	2	(0.13)
		aurites/fraseri	5	(0.11)		(0.00)
		fuscopennata	50	(1.15)	189	(1.14)	131	(8.57)
		maculipennis	8	(0.18)	208	(1.25)	11	(0.72)
		metallica	3	(0.07)	58	(0.35)	33	(2.16)
		microannulatus			1	(0.01)
		pseudoconopas	56	(1.28)	1401	(8.44)	59	(3.86)
Coquillettidia		species	7	(0.16)
Culex	Culex	antennatus			34	(0.20)
		decens group6	9	(0.21)	163	(0.98)	18	(1.18)
		duttoni					1	(0.07)
		neavei	3	(0.07)	97	(0.58)	39	(2.55)
		ornatothoracis			1	(0.01)
		perfuscus	3429	(78.59)	7839	(47.20)	139	(9.10)
		pipiens			7	(0.04)
		quasiguiarti				(0.00)	7	(0.46)
		quinquefasciatus			33	(0.20)
		watti	1	(0.02)			1	(0.07)
	Culiciomyia	cinereus			12	(0.07)	1	(0.07)
		mongiro	61	(1.40)	24	(0.14)	2	(0.13)
		nebulosus	8	(0.18)	131	(0.79)	54	(3.53)
	Eumelanomyia	horridus	2	(0.05)	13	(0.08)
		insignis	2	(0.05)	5	(0.03)	4	(0.26)
		rubinotus	36	(0.83)			1	(0.07)
	Kitzmilleria	moucheti	1	(0.02)	37	(0.22)	27	(1.77)
	Lutzia	tigripes	2	(0.05)	8	(0.05)	1	(0.07)
	Oculeomyia	annulioris			50	(0.30)	1	(0.07)
		poicilipes	335	(7.68)	2	(0.01)
Culex		species	5	(0.11)	1545	(9.30)	40	(2.62)
Culiseta	Theomyia	fraseri					2	(0.13)
Eretmapodites		chrysogaster	13	(0.30)	16	(0.10)	300	(19.63)
Mansonia	Mansonioides	africana	1	(0.02)	42	(0.25)	13	(0.85)
		uniformis	6	(0.14)	1	(0.01)
Mimomyia	Etorleptiomyia	mediolineata			18	(0.11)	5	(0.33)
	Mimomyia	mimomyiaformis					1	(0.07)
		plumosa	18	(0.41)	2	(0.01)
Uranotaenia	Pseudoficalbia	mashonaensis			870	(5.24)	55	(3.60)
		musarum	7	(0.16)	7	(0.04)	2	(0.13)
		nivipous			7	(0.04)	3	(0.20)
	Uranotaenia	alboabdominalis	1	(0.02)	4	(0.02)	3	(0.20)
		balfouri			1	(0.01)
		chorleyi	10	(0.23)	1	(0.01)
		connali			65	(0.39)	19	(1.24)
		pallidocephala			2	(0.01)	1	(0.07)
Totals			4363		16607		1528
Grand Total:		22,498
D			0.63		0.25		0.09
1-D			0.37		0.75		0.91

^1–6 refer to footnotes of table 1.

Table 6.

Mosquito species collected at Kibale National Park, Uganda, in June 2010. Simpson’s Index (D) and Simpson’s Index of Diversity (1-D) are presented at the bottom of the table.

			Number collected (%)
			June 2010
Genus	Subgenus	Species
Aedes	Aedimorphus	cumminsii	1	(0.03)
		quasiunivittatus	2	(0.07)
		tarsalis	117	(4.00)
	Finlaya	ingrami	4	(0.10)
	Neomelaniconion	circumluteolus	18	(0.62)
	Stegomyia	aegypti	1	(0.03)
		aegypti formosus	1	(0.03)
		apicoargenteus group1	2	(0.07)
Anopheles	Anopheles	implexus	60	(2.05)
Coquillettidia	Coquillettidia	fraseri	123	(4.21)
		fuscopennata	564	(19.29)
		maculipennis	1119	(38.27)
		pseudoconopas	85	(2.91)
		versicolor	96	(3.28)
Culex	Culex	antennatus	3	(0.10)
		decens group6	285	(9.75)
		neavei	3	(0.10)
		trifilatus	15	(0.51)
		trifilatus aenescens	107	(3.66)
		watti	25	(0.85)
	Culiciomyia	macfiei	2	(0.07)
		nebulosus	45	(1.54)
	Eumelanomyia	rubinotus	3	(0.10)
		simpliciforceps	31	(1.06)
	Lutzia	tigripes	4	(0.10)
	Oculeomyia	annulioris	10	(0.34)
		annulioris consimilis	140	(4.79)
		aurantapex jinjaensis	9	(0.31)
Culex		species	47	(1.61)
Orthopodomyia		species	2	(0.07)
Grand Total			2,924
D			0.20
1-D			0.80

^{1 & 6}refer to footnotes on table 1.

Table 4.

Mosquito species collected at Maramagambo, Queen Elizabeth National Park, Uganda, in June 2009 and January 2010. Simpson’s Index (D) and Simpson’s Index of Diversity (1-D) for each collection trip are presented at the bottom of the table.

			Number collected (%)
			June 2009		January 2010
Genus	Subgenus	Species
Aedes	Aedimorphus	albocephalus	11	(1.94)	106	(10.60)
		cumminsii	17	(3.00)	98	(9.80)
		mutilus			2	(0.20)
		tarsalis	1	(0.18)	4	(0.40)
		tricholabis	1	(0.18)
	Diceromyia	taylori	1	(0.18)
	Neomelaniconion	albothorax	1	(0.18)	2	(0.20)
		circumluteolus	277	(48.85)	57	(5.70)
		taeniarostris			1	(0.10)
		taeniarostris/carteri			1	(0.10)
	Stegomyia	dendrophilus group2			1	(0.10)
		fraseri	5	(0.88)	2	(0.20)
		luteocephalus	1	(0.18)
	Zavortinkus	longipalpis			1	(0.10)
Anopheles	Anopheles	coustani	1	(0.18)
		implexus			11	(1.10)
		obscurus			1	(0.10)
		ziemanni			1	(0.10)
	Cellia	domicola			5	(0.50)
		funestus group4	1	(0.18)
		gambiae group5	1	(0.18)
Anopheles		species			4	(0.40)
Coquillettidia	Coquillettidia	aurites	9	(1.59)	11	(1.10)
		fuscopennata	141	(24.87)	230	(23.00)
		maculipennis	1	(0.18)	28	(2.80)
		metallica	11	(1.94)	61	(6.10)
		microannulata	2	(0.35)
Coquillettidia		species			2	(0.20)
Culex	Culex	antennatus	4	(0.71)	1	(0.10)
		decens group6	7	(1.23)	44	(4.40)
		duttoni	1	(0.18)
		ingrami			1	(0.10)
		neavei	7	(1.23)	158	(15.80)
		perfuscus	2	(0.35)
		pruina			60	(6.00)
		zombaensis	10	(1.76)
	Culiciomyia	cinerellus	1	(0.18)
		mongiro	2	(0.35)	2	(0.20)
		nebulosus	8	(1.41)
	Eumelanomyia	insignis	3	(0.53)	4	(0.40)
	Kitzmilleria	moucheti	7	(1.23)	6	(0.60)
	Lutzia	tigripes	2	(0.35)
	Oculeomyia	annulioris	1	(0.18)	3	(0.30)
		poicilipes	2	(0.35)
Culex		species	15	(2.65)	53	(5.30)
Eretmapodites		chrysogaster	2	(0.35)
Mansonia	Mansonioides	africana	4	(0.71)	31	(3.10)
		africana nigerrima	1	(0.18)
		uniformis	1	(0.18)
Uranotaenia	Pseudoficalbia	mashonaensis			5	(0.50)
		musarum	2	(0.35)	1	(0.10)
	Uranotaenia	alboabdominalis	1	(0.18)
		connali	2	(0.35)	1	(0.10)
		pallidocephala			1	(0.10)
			567		1000
Grand Total:	1,567
D			0.30		0.12
1-D			0.70		0.88

^{2, 4, 5 & 6}refer to the footnotes of table 1.

Table 5.

Mosquito species collected at Bwindi Impenetrable Forest, Uganda, in January and June 2010. Simpson’s Index (D) and Simpson’s Index of Diversity (1-D) for each collection trip are presented at the bottom of the table.

			Number collected (%)
Genus	Subgenus	Species	January 2010		June 2010
Aedes	Aedimorphus	cumminsii			6	(0.6)
		tarsalis	10	(1.5)	5	(0.5)
	Finlaya	ingrami			1	(0.1)
	Neomelaniconion	circumluteolus			11	(1.1)
		palpale			1	(0.1)
Anopheles	Anopheles	implexus	3	(0.4)
Coquillettidia	Coquillettidia	aurites	23	(3.4)	37	(3.6)
		fraseri	214	(31.2)	269	(26.4)
		maculipennis	53	(7.7)	43	(4.2)
		metallica	1	(0.1)	1	(0.1)
		pseudoconopas	7	(1.0)	40	(3.9)
		versicolor			3	(0.3)
Aedes		species	2	(0.3)
Culex	Culex	antennatus			2	(0.2)
		decens group6	115	(16.8)	125	(12.3)
		neavei			13	(1.3)
		pipiens			1	(0.1)
		pipiens/quinquefasciatus	5	(0.7)
		quasiguiarti			1	(0.1)
		quinquefasciatus			4	(0.4)
		pruina	1	(0.1)
		toroensis macrophyllus	1	(0.1)
		trifilatus	1	(0.1)	73	(7.2)
		trifilatus aenescens	2	(0.3)	82	(8.1)
		watti	1	(0.1)
	Culiciomyia	cinereus	9	(1.3)	3	(0.3)
		nebulosus	45	(6.6)	38	(3.7)
	Eumelanomyia	insignis			1	(0.1)
	Kitzmilleria	moucheti	10	(1.5)	18	(1.8)
	Lutzia	tigripes	3	(0.4)	1	(0.1)
	Oculeomyia	annulioris	29	(4.2)	10	(1.0)
		annulioris consimilis	81	(11.8)	176	(17.3)
Culex		species	58	(8.5)	42	(4.1)
Eretmapodites		chrysogaster			1	(0.1)
Mansonia	Mansonioides	africana nigerrima			4	(0.4)
Mimomyia	Mimomyia	hispida			1	(0.1)
		plumosa			1	(0.1)
Uranotaenia	Pseudoficalbia	mashonaensis			2	(0.2)
	Uranotaenia	balfouri			1	(0.1)
		chorleyi	3	(0.4)
		connali			1	(0.1)
		pallidocephala	10	(1.5)
Totals			687		1,018
Grand Total:	1,705
D			0.16		0.13
1-D			0.84		0.87

⁶refer to footnotes on table 1.

Mosquito collections at Sempaya

At Sempaya, 22,498 mosquitoes were collected: 4,343 in November 2008, 16,607 in June 2009 and 1,528 in January 2010 (Table 2). A total of 65 mosquito species in 9 genera (Aedes, Anopheles, Coquillettidia, Culex, Culiseta, Eretmapodites, Mansonia, Mimomyia and Uranotaenia) were collected at this site (Table 2). The largest number of species were in the genera Aedes and Culex (19 species each), followed by Coquillettidia (8), Uranotaenia (8), Anopheles (4), Mimomyia (3), Mansonia (2) and 1 each in the genera Culiseta and Eretmapodites (Fig. 3). The number of species collected was 27 in November 2008, 59 in June 2009 and 38 in January 2010 (Table 2) suggesting seasonal variation in species abundance and composition. The species captured most frequently at Sempaya was Cx. perfuscus, which made up 50.7% of the mosquitoes collected (Table 2). This differs from previously published collection records for this area which reported that the most frequently captured species were Aedes (Stegomyia) africanus (Theobald), Mansonia (Mansonioides) africana (Theobald) and Anopheles (Celia) gambiae (Giles) (Haddow 1945, Haddow et al. 1947, Haddow et al. 1951, Haddow and Mahaffy 1949). However, these previous studies used human-baited collection methods which would not have attracted the non-anthropophilic Cx. perfuscus (Haddow et al. 1951). The proportion of Cx. perfuscus varied dramatically between the three Sempaya collection trips. In November 2008, this species made up 78.6% of the Sempaya collection, while in June 2009 and January 2010 47.2% and 9.1% were Cx. perfuscus, respectively. These differences may be attributed to availability of suitable Cx. perfuscus breeding sites which are primarily ground pools that are reduced during dry seasons, especially the extended dry season in January. In support of this hypothesis, the lowest numbers of Cx. perfuscus were collected in January 2010 (Table 2). In addition to Cx. perfuscus, the other common species at Sempaya, were Aedes (Neomelaniconion) albothorax (Theobald) (7.1%), Coquillettidia (Coquillettidia) pseudoconopas (Theobald) (6.7%), Aedes (Aedimorphus) albocephalus (Theobald) (4.5%) and Ae. cumminsii. (2.6%) (Table 2).

Four species, Aedes (Stegomyia) metallicus (Edwards), Anopheles (Cellia) rivulorum Leeson, Uranotaenia (Uranotaenia) chorleyi Edwards, and Uranotaenia (Uranotaenia) pallidocephala Theobald and one subspecies, Aedes (Stegomyia) aegypti formosus (Walker), were collected in Bundibugyo District (Sempaya site) for the first time. Although Ae. aegypti formosus was first described by Walker in 1848, it was not until 1957 that a formal description for this subspecies was published by Mattingly (1957) and a more detailed description has subsequently been published by Huang (2004). Therefore, it is possible that the Aedes (Stegomyia) aegypti Linnaeus listed in Bundibugyo District (Bwamba County) (Haddow 1945, Haddow et al. 1947, Haddow et al. 1951, Haddow and Mahaffy 1949) included Ae. aegypti formosus since these subspecies are morphologically very similar and no formal description was available at the time of the collections.

Nearly all of the mosquito species collected in Sempaya had previously been listed in Bundibugyo District by Haddow et al. (1951), suggesting little change in the mosquito fauna of the area in the past 60 years. As mentioned above, the method widely used to collect mosquitoes in Uganda from the mid-1930’s to the early 1970’s was human-baited catches and therefore, in contrast to our collections, the most abundant mosquito species reported in Bundibugyo District at that time were the highly anthropophilic Ae. africanus, An. gambiae and Mn. africana (Haddow 1945, Haddow et al. 1947, Haddow et al. 1951, Haddow and Mahaffy 1949). Aedes africanus is very reluctant to enter enclosed spaces such as mosquito traps and none were captured in our study. Similarly, our CO₂-baited light traps captured only modest numbers of An. gambiae and Ms. africana compared to the previous studies in this region.

Mosquito collections at Mweya

To our knowledge, the mosquitoes of Mweya, or QENP in general, have not been previously described. A total of 39,037 mosquitoes were collected at Mweya (8,678 in November 2008, 20,888 in June 2009 and 9,471 in January 2010) belonging to 34 species, 2 subspecies and 3 species groups in six genera (Aedes (10 species), Anopheles (3), Coquillettidia (3) Culex (14), Mansonia (2) and Mimomyia (2)) (Table 1 and Fig. 3). The most abundant species collected was Culex (Oculeomyia) poicilipes Theobald accounting for 50.5% of the Mweya collection, followed by Culex (Culex) neavei Theobald (37.8%), Mansonia (Mansonioides) uniformis (Theobald) (5.5%) and M. africana (2.1%) (Table 3). Each of the remaining 30 species made up less than 1% of the total collection (Table 3). Culex poicilipes and Cx. neavei, were the predominant species captured at Mweya; they were 88.3% of the total collections at this location (Tables 1 and 3). The relative abundance of Cx. neavei varied from 19.1% in November 2008, to 48.1% in June 2009 to 32.2% in January 2010 (Table 3). June and January are dry seasons; therefore, Cx. neavei was more abundant in the dry seasons compared to the wet season. On the other hand, the proportion of Cx. poicilipes was highest during the wet season in November 2008 (72.8%) and lower in the dry seasons in June 2009 (44.5%) and January 2010 (43.4%) (Table 3).

Table 3.

Mosquito species collected at Mweya, Queen Elizabeth National Park, Uganda, in November 2008, June 2009 and January 2010. Simpson’s Diversity Index (D) and Simpson’s Index of Diversity (1-D) for each collection trip are presented at the bottom of the table.

			Number collected (%)
Genus	Subgenus	Species	November 2008		June 2009		January 2010
Aedes	Aedimorphus	abnormalis kabwachensis	1	(0.01)	2	(0.01)	1	(0.01)
		albocephalus	1	(0.01)	22	(0.11)	5	(0.05)
		argenteopunctatus	1	(0.01)
		cumminsii					2	(0.02)
		hirsutus			2	(0.01)
		natronius					19	(0.20)
	Neomelaniconion	albothorax			9	(0.04)	10	(0.11)
		circumluteolus			16	(0.08)	4	(0.04)
		mcintoshi	1	(0.01)
	Stegomyia	aegypti			6	(0.03)
		aegypti formosus	18	(0.21)	17	(0.08)	4	(0.04)
		metallicus	44	(0.51)	17	(0.08)	7	(0.07)
		simpsoni group3			6	(0.03)
		(Stegomyia) species	9	(0.10)	14	(0.07)	9	(0.10)
Aedes		species					2	(0.02)
Anopheles	Anopheles	symesi	2	(0.02)	9	(0.04)	155	(1.64)
		ziemanni	1	(0.01)	13	(0.06)	60	(0.63)
	Cellia	gambiae group5	3	(0.03)	6	(0.03)	2	(0.02)
		pharoensis			2	(0.01)	1	(0.01)
Anopheles		species			1	(0.00)	6	(0.06)
Coquillettidia	Coquillettidia	fraseri			4	(0.02)	3	(0.03)
		metallica	1	(0.01)	123	(0.59)	40	(0.42)
		pseudoconopas			2	(0.01)
Culex	Culex	antennatus			230	(1.10)	77	(0.81)
		decens group6					1	(0.01)
		duttoni			54	(0.26)	9	(0.10)
		neavei	1661	(19.14)	10038	(48.06)	3052	(32.22)
		quinquefasciatus	1	(0.01)	2	(0.01)	2	(0.02)
		terzii			2	(0.01)
		watti					1	(0.01)
		zombaensis			4	(0.02)	1	(0.01)
	Culiciomyia	cinereus	5	(0.06)	117	(0.56)	21	(0.22)
	Eumelanomyia	insignis			5	(0.02)	3	(0.03)
		rubinotus	1	(0.01)	1	(0.00)	18	(0.19)
	Lutzia	tigripes			2	(0.01)
	Oculeomyia	annulioris			4	(0.02)
		poicilipes	6316	(72.78)	9287	(44.46)	4107	(43.36)
Culex		species					9	(0.10)
Mansonia	Mansonioides	africana	76	(0.88)	196	(0.94)	529	(5.59)
		uniformis	499	(5.75)	476	(2.28)	1187	(12.53)
Mimomyia	Etorleptiomyia	mediolineata			1	(0.00)
	Mimomyia	mimomyiaformis	37	(0.43)	198	(0.95)	124	(1.31)
			8,678		20,888		9,471
Grand Total:	39,037
D			0.57		0.43		0.31
1-D			0.43		0.57		0.69

^{3, 5 & 6}refer to the footnotes of table 1.

Mosquito Collections in Maramagambo Forest

Like Mweya, the mosquito fauna of Maramagambo Forest, also located in QENP, have never been described. A total of 1,567 mosquitoes belonging to seven genera and 45 species were collected in Maramagambo Forest, 567 in June 2009 and 1000 in January 2010 (Tables 1 and 4). The most commonly captured species at this site were Coquillettidia (Coquillettidia) fuscopennata (Theobald) (23.7%), Ae. circumluteolus (21.3%), Cx. neavei (10.5%), Ae. albocephalus (7.5%), Ae. cumminsii (7.3%) Coquillettidia (Coquillettidia) metallica (Theobald) (4.6%), Culex (Culex) pruina Theobald (3.8%) and Cx. decens group (3.3%) (Tables 1 and 4). Some variation in species composition was observed between collections from June 2009, when 35 species were collected, and January 2010, when 30 species were collected. Coquillettidia fuscopennata was the most frequently collected species on both trips to Maramagambo Forest (Table 4) indicating a dominant presence of this species across seasons. The Kazinga Channel, located adjacent to Maramagambo Forest is edged with papyrus swamps, the preferred breeding habitat for Cq. fuscopennata, which may explain the dominance of this species here. In contrast, the relative abundance of the other frequently captured species Ae. albocephalus, Ae. cumminsii, Ae. circumluteolus, Cq. metallica, Cx. neavei and the Cx. decens group varied dramatically between the two collection trips (Table 4). Aedes circumluteolus was much more abundant in June 2009 (48.85%) compared with January 2010 (5.7%), whereas Ae. albocephalus, Ae. cumminsii, Cq. metallica, Cx. neavei and the Cx. decens group were more abundant in January 2010 (10.6%, 9.8%, 6.1%, 15.8%, and 4.4%, respectively) compared with June 2009 (1.94%, 3%, 1.94%, 1.23%, and 1.23%, respectively) (Table 4). Although both Mweya and Maramagambo Forest are in QENP (Figs. 1 and 3) the most frequently captured mosquito species at these two sites differed. The number of Cx. poicilipes collected in Mweya was 19,710, whereas only 2 were collected in Maramagambo (Table 1). On the other hand, 371 Cq. fuscopennata were collected in Maramagambo Forest and none were collected in Mweya (Table 1). Taken together these observations suggest strong habitat segregation by Cq. fuscopennata and Cx. poicilipes for forest and open grassland ecosystems respectively. Further, of the 63 species collected at Mweya and Maramagambo Forest combined, only 16 (25.4%) (Table 1) were collected at both sites showing substantial species composition differences between these two sites despite the close proximity of these two locations. The fact that Mweya is an open grassland and Maramagambo is a tropical forest may explain the species composition differences observed between these two locations.

Mosquito Collections in Bwindi Impenetrable National Park

To our knowledge, this is the first description of the mosquito fauna of BINP. Collections at this site yielded 1,705 mosquitoes; 685 in January 2010 and 1,018 in June 2010 (Tables 1 and 5). A total of 33 species, 4 subspecies and 1 species group belonging to eight genera (Tables 1 and 5) were identified. The species most frequently captured were Coquillettidia (Coquillettidia) fraseri (Theobald), (28.4%), Culex (Oculeomyia) annulioris consimilis Newstead (15.1%), Cx. decens group (14.1%), Coquillettidia (Coquillettidia) maculipennis (Theobald) (5.6%), Culex(Culex) trifilatus aenescens Edwards (4.8%), Culex (Culiciomyia) nebulosus Theobald (4.8%), Culex(Culex) trifilatus Edwards (4.4%) and Coquillettidia (Coquillettidia) aurites (Theobald) (3.4%) (Table 5). There was little variation in relative abundance of most species between seasons. However, seasonal variations were observed between January and June collections for Cx. trifilatus aenescens (0% and 8.1%, respectively) and for Cx. trifilatus (1% and 7.2%, respectively). Despite these few exceptions, the general lack of variation in the seasonal abundance of species suggests little variation in weather and habitat conditions between seasons in BINP.

Mosquito Collections in Kibale Forest

Two thousand nine hundred and twenty-four mosquitoes were collected during the single collection trip at KNP in January 2010 (Tables 1 and 6). A total of 22 species, 4 subspecies and species groups belonging to 5 genera were identified from this location. The most frequently captured species was Cq. maculipennis which was 38.3% of the KNP collection followed by Cq. fuscopennata (19.3%), Cx. decens group (9.8%), Cx. annulioris consimilis (4.8%), Cq. fraseri (4.2%) and Ae. tarsalis (4%) (Table 6). To our knowledge this is the first documented account of the mosquito fauna of KNP. Most striking was that only a single species in the genus Anopheles, (Anopheles (Anopheles) implexus (Theobald)), was detected at this location and was only 2.1% of the total collection (Table 6). However, collecting An. implexus in KNP was not surprising because it is predominantly a forest species (McCrae et al. 1976) and KNP is a forest ecosystem. Further, unlike most mosquito species, the population size of An. implexus is not affected by rainfall patterns (McCrae et al. 1976); therefore, populations are usually detectable throughout the year.

Culex neavei morphological variations

Numerous morphological variations were noted for Cx. (Culex) neavei, specifically regarding the post-spiracular scales, hind tibia, and sternites. Identification of this species was challenging due the inconsistency of morphological characters observed among individuals within and between collection sites, and was confounded by the conflicting species descriptions of Edwards (1941) and Jupp (1971, 1972). These morphological variations are summarized in Table 7 and pictured in Fig 4. Of the specimens analyzed in Table 7, there was no consistent combination of characters noted among specimens from different locations. All character traits reported previously for this species were noted in our collections, and were consistent with the variations reported by Haddow et al. (1951).

Table 7.

Morphological variations in Culex (Culex) neavei from Uganda. Each row of checkmarks for Bwindi, Kibale, Maramagambo, Mweya, and Semliki (Sempaya) represents the characters present on a single specimen from this study. References 1 – 4 list the character combinations noted in previous studies.

	Morphological character
Location	Post-spiracular scales		White spot at apex of hind tibia		Sternites
	Present	Absent	Distinct	Indistinct
throughout Africa1		√		√	pale
Bwamba County, Uganda2	√	√	√	√	sometimes with dark scales (several variations listed)
South Africa3	√		√		dark apical lateral triangles; sometimes has dark scales medially
throughout Africa4	√		√		dark apical lateral triangles sometimes absent
Bwindi	√			√	pale
	√		√		pale with dark medial apical triangles
	√		√		pale with dark scales medially
Kibale	√		√		mostly dark; white scales only on basal margins
Maramagambo	√			√	pale with dark medial apical triangles
	√			√	pale
	√		√		pale with dark medial apical triangles
	√		√		pale with dark scales medially
Mweya	√			√	pale
	√			√	pale with dark medial apical triangles
	√		√		pale with dark scales medially
		√		√	pale with dark scales medially
		√	√		pale with dark scales medially
Semliki		√	√		pale with dark medial apical triangles
	√			√	pale
	√		√		pale with dark scales along apical margin
	√			√	pale with dark scales along apical margin
	√		√		pale with dark scales medially
	√		√		pale

¹Edwards (1941)

²Haddow et al. (1951)

³Jupp (1971)

⁴Jupp (1972)

Fig. 4.

Morphological variations observed in the hind tibia (A-B), post-spiracular area (C-D) and sternum (E-J) of Culex (Culex) neavei Theobald from Uganda. A) Distinct white spot at the apex of the hind tibia. B) Indistinct white spot at the apex of the hind tibia. C) Post-spiracular scales present (solid arrow); pre-alar scales (dashed arrow). D) Post-spiracular scales absent (solid arrow); pre-alar scales (dashed arrow). E) Sternites pale. F) Sternites pale with a few black scales medially. G) Sternites pale with narrow black apical bands. H) Sternites pale with wide black apical bands. I) Sternites with median apical black triangles. J) Sternites mostly black with pale scales along basal and lateral margins.

Potential medical importance

A list of mosquito species collected in western Uganda and the arboviruses of medical importance that have previously been isolated from these species are presented in Table 8. Of the 102 mosquito species, subspecies and species groups collected in this study, at least 50 have been implicated in the transmission of arboviruses of public health importance (Table 8). The major epidemic vector species include Ae. aegypti, the principal vector of YFV (Monath 1988, Germain et al. 1980), Chikungunya virus (CHIKV) (Jupp and McIntosh, 1988), Dengue viruses (DENV) (Gubler 1986) and Zika virus (ZIKAV) (Marchette et al. 1969). Members of the Ae. simpsoni complex, and specifically Aedes (Stegomyia) bromeliae Huang, are epidemic vectors of YFV (Mahaffy et al. 1942, Huang 1986). Aedes (Stegomyia) luteocephalus (Newstead) is a vector of YFV (Germain et al. 1980), CHIKV (Jupp and McIntosh, 1988), DENV (Diallo et al. 2003) and ZIKAV (Marchette et al. 1969). Anopheles (Cellia) funestus Giles and An. gambiae s.l. are vectors of O’nyong nyong virus (ONNV) (Williams et al. 1965, Lutwama et al. 1999) and Aedes (Diceromyia) taylori Edwards is a vector of YFV (Monath 1988).

Table 8.

Mosquito species collected in western Uganda from which arboviruses of medical importance have previously been isolated. The list shows some of the medically important arboviruses previously isolated from each species.

Genus	Subgenus	Species	Arbovirus(es)
Aedes	Aedimorphus	abnormalis	MIDV1, PGAV1, SFV1, 4, SPOV1, 5, WSLV1, 5, CHIKV5
		albocephalus	MIDV1, WNV1, 19
		argenteopunctatus	BUNV1, 5, MIDV1, 5, PGAV1, 5, SFV1, 4, 18, SHOV1, 5, WSLV1, 5, CHIKV5, NRIV5
		cumminsii	DENV-21, 5, MIDV1, 3, 5, PGAV1, 5, RVFV1, 2, 5, 20, SHOV1, 3, SPOV1, 4, 5, WSLV1, 5, SINV3 CHIKV5
		domesticus	WSLV1, 5, BUNV5
		mutilus	CHIKV5
		tarsalis	MIDV1, 5, PGAV1, SHOV1, 5, WSLV1, 5, ZIKAV1, 5, RVFV2, 17
	Diceromyia	taylori	DENV-21, 5, 22, YFV1, 5, 6, CHIKV5, ZIKAV 5, ORUV5
	Finlaya	ingrami	CHIKV5
	Mucidus	grahami	CHIKV5, ZIKAV5
	Neomelaniconion	albothorax	WNV1, 5
		circumluteolus	BUNV1, GERV1, LEBV1, MIDV1, 4, PGAV1, 5, RVFV1, SHOV1, SPOV1, WSLV1, 4, 5, WNV1, 5, 19
		mcintoshi	RVFV8, WSLV5, NRIV5
		taeniarostris	CHIKV5, ZIKAV5, WSLV5
	Stegomyia	aegypti	CHIKV1, 5, DENV-11, DENV-21, 22, DENV-31, DENV-41, DUGV1, ORUV1, 5, USUV1, VEEV1, WNV1, 5, 19, YFV1, 5, 8, 21, ZIKAV1, 5, 23,, SFV5, WSLV5, BBKV5
		apicoargenteus	ZIKAV7
		dendrophilus	RVFV2, 10
		luteocephalus	CHIKV1, 5, DENV-21, 5, 22, PGAV1, 5, YFV5, 6, ZIKAV1, 5, 24, WSLV5
		metallicus	YFV5, 6, WSLV5, ZIKAV5
		simpsoni group	YFV6, 13, 14, BBKV5, NRIV5
Anopheles	Anopheles	coustani	CHIKV1, 5, PGAV1, 5, WNV1, 19, NRIV5
	Cellia	demicola	WSLV5
		funestus complex	BWAV1, 5, 24, CHIKV1, 5, ONNV1, 5, 9, 15, 16, ORUV1, 5, PGAV1, 5, SFV1, 4, WSLV1, 5, TATV5, NDOV5, TATV4, 5
		gambiae s.l.	BWAV1, 5, CHIKV1, ILEV1, 5, MIDV 1, 5, ONNV1, 5, 15, 16, ORUV1, 5, ZIKAV1, 5, TATV5, NRIV5, NDOV5, BGIV5, TATV4, 5
		pharoensis	SINV1, WSLV5, NRIV5, BGIV5
Coquillettidia	Coquillettidia	aurites	USUV1, TATV4, 5
		fuscopennata	SINV1, 10, CHIKV10, YFV1, 6
		maculipennis	CHIKV5
		metallica	MIDV1, 5, WNV1, 19, BBKV5
Culex	Culex	antennatus	PGAV1, WNV1, 5, 19, RVFV2, 20, SINV1, WSLV5, BBKV5, NRIV5
		decens group	WNV5, 19, CHIKV5, BBKV5
		neavei	SPOV1, 4, WNV5, 8, 12, 19, SINV8, BBKV5 KOUV5
		perfuscus	ORUV1, 5, USUV1, 5, WNV1, 5, 19, WSLV1, 5, SINV5, BBKV5
		pipiens	JBEV1, LACV1, SFV1, SLEV1, TAHV1, WEEV1, WNV19, BANV 5, BUNV5
		pruina	SINV1, 5, WNV1, 5, 19
		quinquefasciatus	CHIKV1, 5, EEEV1, KUNV1, MTBV1, MURV1, OROV1, RRV1, SLEV1, SINV1, VEEV1, WANV1, WEEV1, WNV1, 5, 19, BBKV5
		univittatus	SINV1, 25, SPOV1, USUV1, 5, WSLV1, WNV1, 5, 19
		zombaensis	BUNV1, 5, PGAV1, RVFV2
	Culiciomyia	cinereus	CHIKV5, MIDV5, BBKV5
		nebulosus	MIDV5, BBKV5, BGIV5
	Eumelanomyia	rubinotus	BANV1, GERV1, 5, RVFV2
	Lutzia	tigripes	SINV1, 5, BBKV5
	Oculeomyia	annulioris	MIDV5, WSLV5
	Oculeomyia	poicilipes	RVFV5, 11, WNV5, 12, 19, MIDV5, PGAV5, BBKV5, NRIV5
Eretmapodites		chrysogaster	MIDV1, 5, RVFV1, 2,, SFV5
Mansonia	Mansonioides	africana	BANV1, BUNV1, 5, 12, CHIKV1, 5, LEBV1, MIDV1, 5, PGAV1, 5, SHOV1, SPOV1, 4, USUV1, 5, WSLV1, 5, RVFV5, 20, WNV5, BBKV5
		uniformis	BUNV1, 5, 12, MIDV1, 5, RRV1, SPOV1, 4, WSLV1, 5, ZIKAV1, 5, WNV5, 11, CHIKV5, BANV5, RVFV5
Mimomyia	Mimomyia	hispida	WNV5, 12, 19, BBKV5
		plumosa	PGAV5
Uranotaenia	Pseudoficalbia	mashonaensis	WSLV5

¹The International Catalogue of Arboviruses.

²Meegan & Bailey 1988.

³McIntosh et al. 1972.

⁴ARBOCAT (http://wwwn.cdc.gov/arbocat/index.asp).

⁵Institut Pastuer de Dakar. Rapport Annuel, 2000.

⁶Monath 1988.

⁷McCrae & Kirya 1982.

⁸McIntosh 1986.

⁹Lutwama et al. 1999.

¹⁰Woodhall 1964.

¹¹Diallo et al. 2005.

¹²Traore-Lamizana 2001.

¹³Mahaffy et al. 1942.

¹⁴Smithburn & Haddow 1946.

¹⁵Williams et al. 1965.

¹⁶Corbet et al. 1961.

¹⁷Smithburn et al. 1948

¹⁸MacIntosh et al. 1961.

¹⁹Hubálek & Halouzka 1999.

²⁰Fontenille et al. 1998.

²¹Germain et al. 1980.

²²Diallo et al. 2003.

²³Marchette et al. 1969.

²⁴Lee & Moore 1972.

²⁵Jupp et al. 1986.

BANV = Banzi virus. BBKV = Babanki virus. BGIV = Bangui virus. BUNV = Bunyamwera virus. BWAV = Bwamba virus. CHIKV = Chikungunya virus. DENV-1 = Dengue type 1 virus. DENV-2 = Dengue type 2 virus. DEN-3 = Dengue type 3 virus. DEN4 = Dengue type 4 virus. DUGV = Dugbe virus. EEEV = Eastern Equine Encephalitis virus. GERV = Germiston virus. ILEV = Ilesha virus. JBEV = Japaneese Encephalitis virus. KOUV = Koutango virus. KUNV = Kunjin virus. LACV = LaCrosse Encephalitis virus. LEBV = Lebombo virus. MIDV = Middelburg virus. MTBV = Marituba virus. MURV = Murray Valley virus. NDOV = Nyando virus. NRIV = Ngari virus. ONNV = Onyong-Nyong virus. OROV = Oropouche virus. ORUV = Orungo virus. PGAV = Pongola virus. RRV = Ross River virus. RVFV = Rift Valley Fever virus. SFV = Semliki Forest virus. SHOV = Shokwe virus. SINV = Sindbis virus. SLEV = St. Louis Encephalitis virus. SPOV = Spondweni virus. TAHV = Tahyna virus. TATV = Tataguine virus. USUV = Usutu virus. VEEV = Venezuelan Equine Encephalitis virus. WANV = Wanowrie virus. WEEV = Western Equine Encephalitis virus. WSLV = Wesselsbron virus. WNV = West Nile virus. YFV = Yellow Fever virus. ZIKAV = Zika virus.

All species listed in Table 8 have previously been documented with naturally acquired infections of arboviruses of public health importance. These species may be involved in natural arbovirus cycles as principal or secondary epidemic vectors, primary or secondary enzootic vectors or as incidental vectors with unknown epidemiological importance. The presence of 50 mosquito species in western Uganda linked to a wide range of arboviruses suggests that there is the potential for maintenance and transmission of numerous arboviruses there, as well as the potential for outbreaks of arboviral diseases in this region. Field mosquito studies in Uganda are ongoing and are an important component of the arbovirus surveillance program. Eventually, the studies will include large areas in all provinces of the country. Our studies will update species lists for areas where the mosquito fauna has previously been described and will describe mosquito species compositions for areas where the diversity of the mosquito fauna is currently unknown. This mosquito species composition data will be invaluable in the future as a tool to predict the potential for emerging arboviral disease in Uganda.