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. Author manuscript; available in PMC: 2022 Sep 7.
Published in final edited form as: J Med Entomol. 2020 Nov 13;57(6):1972–1982. doi: 10.1093/jme/tjaa109

Surveillance of Culicine Mosquitoes in Six Villages of Taita-Taveta County, Kenya, With Host Determinations From Blood-Fed Females

Vanessa Munyao 1,2,✉, Jonathan Karisa 2,3, Carol Munini Munyao 4, Moses Ngari 2, Nelson Menza 1, Norbert Peshu 2, Martin Rono 2,3, Charles Mbogo 2, Joseph Mwangangi 2,3,5
PMCID: PMC7613318  EMSID: EMS152536  PMID: 32533693

Abstract

Culicine mosquitoes are vectors of human disease-causing pathogens like filarial worms and several arthropod-borne viruses (arboviruses). Currently, there has been an increase in emerging and re-emerging vector-borne diseases along coastal Kenya, which has been of major concern in public health. This study aimed at determining culicine mosquito species abundance, diversity and their host feeding preferences in Taita-Taveta County, Coastal Kenya. Entomological sampling was done during the long-wet season (March and May) and long dry season (June to October) 2016−2018. Mosquito sampling was done using CDC light traps and Backpack aspiration for indoor and outdoor environments. All culicine mosquitoes collected were identified morphologically and categorized according to their physiological status. Blood fed culicine mosquitoes were tested for bloodmeal sources using ELISA. In total, 3,278 culicine mosquitoes were collected, of which 738 (22.5 %) were found indoors and 2,540, (77.5 %) outdoors. The mosquitoes consisted of 18 species belonging to four genera: Aedes (7), Culex (8), Mansonia (2), and Coquillettidia (1). Overall, there was high mosquito species diversity (H) in outdoors (H = 2.4339) than in indoors (H =2.2523), whereas even distribution (EH) was higher in indoors (EH = 0.9064) than outdoors (EH = 0.8266). Majorly the bloodmeals identified were from multiple host sources with (51.6%), single hosts (41.3%), and unidentified (7.2%). This study has demonstrated a high diversity of culicine mosquitoes with relaxed feeding tendencies. These mosquitoes are contributing to mosquito biting nuisance and the likelihood of exposure of populations to diseases of public health.

Keywords: abundance, bloodmeal, Culicine, diversity

Graphic abstract.

Graphic abstract

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Over 80% of the population in the world is at the risk of vector-borne diseases including arboviruses, malaria and lymphatic filariasis (WHO 2017). Mosquitoes have played a significant role in the transmission of these pathogens. Notably, the subfamily Culicinae has been incriminated as a major vector of lymphatic filariasis (Derua et al. 2017) and arboviruses such as Rift Valley Fever virus, dengue fever virus, yellow fever virus, and West Nile Virus, (Sang et al. 2010, LaBeaud et al. 2011, Mwaengo et al. 2012, Lutomiah et al. 2016). Culicine mosquitoes of the genus Aedes and Culex encompasses the key species responsible for pathogen transmission. They are responsible in global transmission of diseases of public health interest resulting to lack of health security to both animals and human populations. Bloodmeals are crucial for mosquito oogenesis and reproduction but also an avenue for pathogens uptake from an infected host and eventual transmission to a susceptible one. The preference of the bloodmeal is influenced by several factors including host availability, nutritional requirements, host preferences of the species, and vector density (Zimmerman et al. 2006). For instance, Culex quinquefasciatus (Say) exhibits relaxed feeding tendencies, relying mostly on avian hosts for bloodmeals though in some instances feeding equally on both birds and mammalian hosts hence associated with multiple bloodmeal sources. This feeding tendencies and adaptation greatly increase the chances of lymphatic filariasis and arboviruses transmission (Kilpatrick et al. 2006, Marm Kilpatrick et al.2006, Savage et al. 2007, Garcia-Rejon et al. 2010, Sawabe et al. 2010). Mosquito species abundance and diversity are known to be influenced by factors, such as climate, seasonality, availability of microhabitats for breeding, and physicochemical parameters of breeding sites (Jones et al. 2008, Muturi et al. 2008, Akram et al. 2009, Kim and Tsuda 2010, Midega et al. 2010). Tropical countries have environmental factors that favor an abundance of breeding sites and fast biological development of mosquitoes. Some of these factors contribute to the extensive proliferation of mosquitoes ranging from sporadic floods, irrigation canals, presence of several lakes/rivers, and low altitudes especially around coastal regions (Karungu et al. 2019). Culicine mosquitoes have a wide range of breeding areas; they breed mostly inside or near houses (peri-domestic habitats) in waters with high organic materials, such as canals, ditches, rivers, lakes, swamps, tree holes, and runoff from agricultural plants (Philbert and Ijumba 2013). Culex quinquefasciatus, for instance, prefers to breed in highly organic surface water like domestic collections of water, flooded open drains, flooded latrines, overflow water from houses, kitchens, as well as in-ground − pools, ditches, and shallow wells (Weinstein et al. 1997). Aedes aegypti (Linnaeus) on the other hand breeds in stagnant water in old tires, poorly discarded plastic bottles/cans, storage water tanks, and coconut husks (Philbert and Ijumba 2013).

Recently, coastal region, Kenya, has been a hot spot for emerging and re-emerging arboviral diseases including dengue fever and chikungunya virus. Culicine mosquitoes are believed to be the major drivers of these arboviral disease transmission dynamics (Petersen and Powers 2016; Agha et al. 2017a, b). Emerging and re-emerging of these infectious diseases are often due to arboviruses that are maintained in a zoonotic cycle between mosquito vectors and wildlife species, with spill over to humans in areas where human and wildlife population borders each other (Lindahl et al. 2017). Taita-Taveta County being within the Kenyan coastal region where the emergence and re-emergence of infectious diseases has been reported, it has forest ecology, urban ecology and agro-ecosystem ecology, which contributes to proliferation of mosquitoes. It also borders Tsavo National park, which poses high-risk of spill over because there is human and wildlife population interface. Taita-Taveta County also uses agrochemicals such as herbicides and pesticides that can increase the risk of insecticide resistance to insecticides used in public health for control of mosquitoes such as pyrethroids. Major studies done in Taita-Taveta County since the WHO Global Malaria Eradication Campaign (between 1955 and 1960) (Wilson 1960) were majorly on Anopheles species and no effort has been made to study Culicine mosquitoes which are also important in disease transmission and biting-nuisance. There is no published data on Culicine mosquito species composition, abundance, diversity, and host feeding preferences in Taita-Taveta County. Concerns about the role of local mosquito vectors in the introduction of vector-borne disease to anthropologic environments have created the need for conducting studies on mosquito vector diversity and host preferences for bloodmeal source to improve our understanding of the disease transmission cycles and design effective vector control tools.

Materials and Methods

Study Area

The study was conducted in Taita-Taveta County in the Coastal region of Kenya. The County lies between latitude 3° 24′00″S and longitude 37°41′00″E. Taita-Taveta borders Tsavo national park which is rich in a variety of wild animals and birds. The main economic occupation of the inhabitants in the County are mainly mixed farming, livestock, trade/business, and waged labor. Most households in the study areas prefer keeping goats, chickens, and cattle. The houses are mainly made of concrete or mud walls and iron sheets or palm leaf (Makuti) roofing. The area experiences bimodal rainfall pattern with the mean annual rainfall ranges between 200 and 1,200 mm. Temperature ranges from 21°C to 31°C. Agricultural activities in the county rely on water from four rivers; Tsavo, Lumi, Njoro, Kitobo, and spring water from the foot of Mt. Kilimanjaro.

Six villages were sampled for adult mosquitoes; Chala, Kimundia, King’wareni, Kiwalwa, Mwarusa, and Njoro. Kiwalwa is a highly populated riverine ecosystem. Mwarusa is a flat, swampy area with river Lumi flowing along the edge of the village. Kimundia is swampy, households are sparsely distributed, and some sections of this village are flooded during the rainy seasons. Some parts of Njoro are wet, particularly where river Njoro flows through, while the rest of the village is dry and dusty. Chala is a dry area though, with modern houses, agriculture is done through drip and localized irrigation. The criteria for the selection of these villages were based on riverine, nonriverine ecosystem, and drainage system. The entomological sampling design was based on rainfall pattern, the main wet season (March and May), and dry season (June to October) 2016−2018. During each season, sampling was done once, totaling to six visits per household over the entire period.

Mosquito Collection

Entomological sampling was done using CDC backpack aspirators model 1412 (John W. Hock Company, Gainesville, FL) and Centers for Disease Control (CDC) light traps (John W. Hock Company), which were set indoor and outdoor. CDC light trap, mosquito collection was conducted in 10 randomly selected houses between 1800 and 0600 h. One light trap was hanged at the foot-end of the bed and a second light trap was placed outside the house. Three hundred and twenty light traps were used during the entire sampling frame. Sampling using Backpack aspiration technique was done in the same 10 randomly selected houses in each village. The indoor collection was done in the bedroom and living room. Mosquitoes were aspirated from the walls and all hanging clothing was shaken to expose any uncollected mosquitoes. In each house, mosquito aspiration was done for between 5 and 10 min depending on the size of the house. The collection was done between 0600 and 1000 h. The traps were removed in the morning and all cups containing mosquitoes kept in the cool box for transportation to the KEMRI field laboratory in Taveta.

Mosquito Identification

All mosquitoes collected were morphologically identified in the field as culicine and anopheles and preserved using silica gel and later transported to KEMRI, Center for Geographic Medicine Research Coast for laboratory analysis. Only Culicine mosquitoes were used for this study since the Anopheles mosquitoes were analyzed separately for other study. The collected Culicine were sorted according to sex and species using morphological characteristics as described earlier (Edwards 1941). The females were further grouped into their physiological status (unfed and blood-fed) by examining their abdomen under a stereomicroscope. All blood-fed mosquitoes were kept in labeled vials and preserved awaiting further analysis.

Bloodmeal Analysis

The blood-fed culicine mosquitoes were screened for bloodmeal using direct enzyme-linked immune sorbent assay (ELISA) method as earlier described by (Beier et al. 1988, Mwangangi et al. 2003, Karisa et al. 2019). A panel of antibodies against human, bovine, chicken, and goat were used for bloodmeal source. Positive controls included serum for each host tested, and different combinations of human, bovine, goat, and chicken serum mixtures in PBS. Results were read visually through color change (homogenous greenish-blue color for positive and clear for negative samples).

Data Analysis

Stata statistical package (StataCorp. 2011, Stata Statistical Software: Release 11. College Station, TX: StataCorp LP) (StataCorp 2011) was used to clean, manage, and analyze the data sets. Species composition and spatial heterogeneity were analyzed using χ2. Statistical differences among different species was considered significant when the P-value was below 0.05 (P < 0.05). The Shannon diversity index (H) was used to describe mosquito species diversity in the study sites, Taita-Taveta County, as described earlier (Muturi et al. 2006b). Shannon index accounts for both diversity and evenness of the species present.

The host preference was calculated by expressing the number of mosquitoes positive for each specific host as a proportion of the total mosquitoes tested. This was categorized based on the focal point of collection (indoor and outdoor).

Results

Indoor and Outdoor Culicine Mosquito Species Composition/Abundance

In total, 3,278 adult mosquitoes were collected in both indoor (22.5%, n = 738) and outdoor (77.5%, n = 2,540) environments during the study period. Eighteen species of culicine mosquitoes belonging to genera (Aedes, Culex, Coquillettidia, and Mansonia) were collected in the six sites. The genus Aedes comprised of seven species, whereas Culex comprised of eight species, Coquillettidia comprised of one species, and finally, Mansonia comprised two species. Culex quinquefasciatus was significantly reported in high numbers both indoor (χ2 = 25.1, df = 6, P < 0.001) and outdoor (χ2 = 54.3, df = 6, P < 0.001) across the six sites. From the six sites, Kimundia and King’wareni had the highest number of mosquitoes collected outdoor (43.5%) and indoor (8.1%), respectively (Table 1). Fewer mosquito samples were collected during the dry season compared with wet season, thus we could not report the results per season.

Table 1. Culicine mosquito species composition and abundance in the six villages of Taita-Taveta County, Coastal Kenya.

Mosquito species Chala Kimundia Kiwalwa Mwarusa Njoro King’wareni X2 P-value
Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor
Aedes hirsutus 0 0 293 (21) 40 (25) 12 (6.4) 5 (3.5) 21 (17) 7(11) 37 (9.7) 1 (1.4) 0 0 105.4 - <0.001 <0.001
Aedes aegypti 0 0 3 (0.2) 0 0 0 0 0 0 0 0 0 - - 0.95
Aedes mcintosbi 0 0 139 (9.7) 1 (0.6) 39(21) 7 (4.9) 4 (3.2) 1 (1.6) 32 (8.4) 3(4.1) 0 0 70.3 - <0.001 0.002
Aedes pembaensis 0 0 2 (0.1) 0 0 0 0 0 0 0 0 0 - - 0.98
Aedes simpsoni complex 0 0 1 (0.07) 0 0 2(lo4) 0 0 0 1 (1.4) 0 0 - - 0.96 0.17
Aedes straitipes 0 0 0 0 7(3.7) 1 (0.7) 0 0 0 0 0 0 - - 0.35 0.42
Aedes trickolabis 0 0 8 (0.6) 1 (0.6) 0 0 0 0 0 0 0 0 - - 0.56 0.64
Culex annulioris 0 0 5 (0.4) 0 0 0 0 0 0 1 (1.4) 0 0 - - 0.79 0.23
Culex quinquefasciatus 90 (98) 31 (100) 781 (55) 74 (45) 124 (66) 117 (82) 93 (74) 52 (83) 264(69) 49 (67) 326 (100) 265 (100) 54.3 25.1 <0.001 <0.001
Culex culicioma 0 0 0 0 0 0 1 (0.8) 0 0 0 0 0 - - 0.09
Culex poicilipes 0 0 20 (1.4) 0 0 0 1 (0.8) 0 0 0 0 0 - - 0.02
Culex fuscocephala 0 0 3 (0.2) 0 0 0 0 0 0 0 0 0 - - 0.99
Culex straitipes 0 0 1 (0.07) 0 0 0 0 0 0 0 0 0 - 0.97
Culex νansomereni 0 0 8 (0.6) 0 0 0 0 0 0 1 (1.4) 0 0 - - 0.59 0.23
Culex univittatus 0 0 105 (7.4) 35 (21) 0 9(6.3) 0 1 (1.6) 20 (5.2) 12 (16) 0 0 52.1 - <0.001 <0.001
Coquillettidia aurites 1 (1) 0 8 (0.6) 0 1 (0.5) 0 1 (0.8) 1 (1.6) 18 (4.5) 1 (1.4) 0 0 - - <0.001 0.07
Ma. africana 0 0 0 0 2(1) 0 0 0 1 (0.3) 1 (1.4) 0 0 - - 0.03 0.23
Ma. uniformis 1 (1) 0 49 (3.4) 12 (7.4) 2(1) 2(lo4) 5 (4.0) 1 (1.6) 11 (2.9) 3(4.1) 0 0 - - 0.001 <0.001
Total 92 31 1,426 163 187 143 126 63 383 73 326 265 - - - -
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Culicine Mosquito Species Diversity and Evenness

Overall, there was high mosquito species diversity (H) in outdoors (H = 2.4339) than in indoors (H = 2.2523), whereas evenness (EH) was higher in indoors (EH = 0.9064) than outdoors (EH = 0.8266) (Table 2).

Table 2. Culicine mosquito species diversity and evenness for the six villages in Taita-Taveta County, Kenya.

Distribution Village Indoor Outdoor
Shannon’s diversity index (H) Chala
Kimundia
Kin’gwareni
Kiwalwa
Mwarusa
Njoro
All villages		 0.1312 (1)
0.6913 (7)
0.3675 (1)
0.4589 (7)
0.2630 (6)
0.3402 (10)
2.2523 (12)		 0.1245 (3)
1.1207 (16)
0.2634 (1)
02729 (8)
0.1923 (7)
0.4602 (8)
2.4339 (19)
Shannon’s equitability (EH) Chala
Kimundia
Kin’gwareni
Kiwalwa
Mwarusa
Njoro
All villages		 0.000 (1)
0.3552 (7)
0.000 (1)
0.2358 (7)
0.1468 (6)
0.1477 (10)
0.9064 (12)		 0.1133 (3)
0.4042 (16)
0.000 (1)
0.1312 (8)
0.0988 (7)
0.2213 (8)
0.8266 (19)
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Indoor Species Diversity and Evenness

Kimundia had a higher diversity of mosquito species was observed, with (H = 0.6913) compared with the other sites. Similarly, high species equitability was observed in the same site with EH being (0.3552). Lower species diversity and equitability were reported in Chala (H = 0.1312) and (EH = 0.0000), respectively. King’wareni also had low mosquito’s species equitability with EH of 0.0000 (Table 2).

Outdoor Species Diversity and Evenness

High species diversity and equitability were observed in Kimundia (H = 1.1207) and (EH = 0.4042), respectively, compared with the other sites. Lower species diversity was observed in Chala (H = 0.1245) and evenness was observed in King’wareni (EH = 0.0000) (Table 2).

Bloodmeal Sources of Culicine Mosquitoes

Overall, 1,241 mosquitoes were tested for bloodmeal sources using direct ELISA method. These included; Cx. quinquefasciatus (n = 712), Aedes hirsutus (n = 228), Aedes taylori (n = 222), Aedes mcintoshi (n = 50), Mansonia (n = 12), Culex univittatus (n = 7), Coquillettidia aurites (n = 6), Culex fuscocephala (n= 2), Culex poicilipes (n = 1), and Aedes tricholabis (n = 1). Out of the 1,241 mosquitoes tested for bloodmeal sources, 512 (41.3%) had fed on a single host including human (8.2%, n = 102), goat (5.2%, n = 65), bovine (26.4%, n = 328), and chicken (1.4%, n = 17), whereas (51.6%, n = 640) identified were from mixed/multiple bloodmeal sources. The rest 7.2% were from unknown sources (Table 3). The mosquito species displayed feeding behavior involving bloodmeals from a single host including; Ae. hirsutus, Ae. mcintoshi, Aedes taylori, Ae. tricholabis, Cx. quinquefasciatus, and others (Table 4).

Table 3. Bloodmeal sources for blood fed Culicine mosquitoes collected in six sites of Taita-Taveta County, Coastal Kenya.

Village Mosquito species Number of tested Human(%) Goat (%) Bovine (%) Chicken (%) Mixed (%) Unknown (%)
Chala Kimundia Culex quinque fasciatus     9 0 0 3 (33.3) 0 4 (44.4) 2 (22.2)
Aedes hirsutus 210 3 (1.4) 5 (2.4) 68 (32.4) 1 (0.5) 117 (55.7) 16 (7.6)
Aedes mcintoshi    43 3 (7.0) 5 (11.6) 10 (23.3) 1 (2.3) 23 (53.5) 1 (2.3)
Aedes taylori 222 12 (5.4) 2 (0.9) 44 (19.8) 0 157 (70.7) 7 (3.2)
Aedes tricholabis     1 0 0 1 (100.0) 0 0 0
Coquillettidia aurites     5 1 (20.0) 1 (20.0) 0 0 3 (60.0) 0
Culex fuscocephala     2 0 0 0 0 2 (100.0) 0
Mansonia    10 1 (10.0) 0 2 (20.0) 0 7 (70.0) 0
Culex poicilipes     1 0 0 0 0 1 (100.0) 0
Culex quinque fasciatus 330 15 (4.5) 14 (4.2) 133 (40.3) 5 (1.5) 150 (45.5) 13 (3.9)
Culex univittatus     6 0 1 (16.7) 2 (33.3) 0 2 (33.3) 1 (16.7)
King’wareni Aedes mcintoshi     2 0 0 0 0 2 (100.0) 0
Culex quinque fasciatus    33 4 (12.1) 2 (6.1) 14 (42.4) 2 (6.1) 9 (27.3) 2 (6.1)
Kiwalwa Aedes hirsutus    11 1 (9.1) 1 (9.1) 6 (54.5) 0 2 (18.2) 1 (9.1)
Aedes mcintoshi     3 0 0 0 0 2 (66.7) 1 (33.3)
Mansonia     1 0 1 (100.0) 0 0 0 0
Culex quinque fasciatus 142 43 (30.3) 5 (3.5) 10 (7.0) 7 (4.9) 55 (38.7) 22 (15.5)
Mwarusa Aedes hirsutus     5 0 0 1 (20.0) 0 3 (60.0) 1 (20.0)
Aedes mintoshi     2 0 0 1 (50.0) 0 1 (50.0) 0
Culex quinquefasciatus 136 9 (6.6) 22 (16.2) 23 (16.9) 0 68 (50.0) 14 (10.3)
Njoro Aedes hirsutus     2 0 1 (50.0) 0 0 0 1 (50.0)
Coquillettidia aurites     1 0 1 (100.0) 0 0 0 0
Mansonia     1 0 0 0 0 1 (100.0) 0
Culex quinquefasciatus    62 10 (16.1) 4 (6.5) 10 (16.1) 0 31 (50.0) 7 (11.3)
Culex univittatus      1 0 0 0 1 (100.0) 0 0
Total 1,241 102 (8.2) 65 (5.2) 328 (26.4) 17 (1.4) 640 (51.6) 89 (7.2)
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Table 4. Single host bloodmeal among Culicine mosquitoes in Taita-Taveta County, Coastal Kenya.

Species Location Number of Tested Human (%) Goat (%) Bovine (%) Chicken (%)
Culex quinque fasciatus Indoor 110 62 (56.4) 6 (5.5) 30 (27.3) 12 (10.9)
Outdoor 225 19 (8.4) 41 (18.2) 163 (72.4) 2 (0.9)
Overall 335 81 (24.2) 47 (14.0) 193 (57.6) 14 (4.2)
Aedes hirsutus Indoor 9 0 (0.0) 1 (11.1) 8 (88.9) 0 (0.0)
Outdoor 78 4 (5.1) 6 (7.7) 67 (85.9) 1 (1.3)
Overall 87 4 (4.6) 7 (8.0) 75 (86.2) 1 (1.1)
Aedes mcnitoshi Indoor 1 0 (0.0) 1 (100.0) 0 (0.0) 0 (0.0)
Outdoor 19 3 (15.8) 4 (21.1) 11 (57.9) 1 (5.3)
Overall 20 3 (15.0) 5 (25.0) 11 (55.0) 1 (5.0)
Aedes taylori Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 58 12 (20.6) 2 (3.4) 44 (75.9) 0 (0.0)
Overall 58 12 (20.6) 2 (3.4) 44 (75.9) 0 (0.0)
Aedes tricholabis Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 1 0 (0.0) 0 (0.0) 1 (100) 0 (0.0)
Overall 1 0 (0.0) 0 (0.0) 1 (100.0) 0 (0.0)
Mansonia Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 4 1 (25.0) 1 (25.0) 2 (50.0) 0 (0.0)
Overall 4 1 (25.0) 1 (25.0) 2 (50.0) 0 (0.0)
Culex univittatus Indoor 3 0 (0.0) 1 (33.3) 1 (33.3) 1 (33.3)
Outdoor 1 0 (0.0) 0 (0.0) 1 (100.0) 0 (0.0)
Overall 4 0 (0.0) 1 (25.0) 2 (50.0) 1 (25.0)
All species combined Indoor 123 62 (50.4) 9 (7.3) 39 (31.7) 13 (10.6)
Outdoor 389 40 (10.3) 56 (14.4) 289 (74.3) 4 (1.0)
Overall 512 102 (19.9) 65 (12.7) 328 (64.1) 17 (3.3)
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Most of the multiple feeders preferred bovine-goat combination with a proportion of (45.8%) followed by a combination of bovine-human-goat (24.1%). The least preferred multiple hosts were bovine-chicken-human, chicken-goat and bovine-chicken with 0.6, 1.1, and 1.6%, respectively (Table 5). Culex quinquefasciatus showed different diverse trophic preferences but predominantly fed on bovine-goat and bovine-human-goat combinations (Tables 5 and 6).

Table 5. Multiple host bloodmeal among Culicinemosquitoes inTaita-Taveta County, Coastal Kenya.

Species Location Number of tested BC (%) BCG (%) BCH (%) BCHG (%) BG (%) BH (%) BHG(%) CG (%) CH (%) CHG(%) HG (%)
Culex quinque fasciatus Indoor 72 0 (0.0) 1 (1.4) 0 (0.0) 1 (1.4) 26 (36.1) 3 (4.2) 17 (23.6) 1 (1.4) 8 (11.1) 4 (5.6) 11 (15.3)
Outdoor 245 3(l.2) 6 (2.4) 1 (0.4) 7 (2.9) 124 (50.6) 22 (9.0) 53 (21.6) 3(l.2) 0 (0.0) 4(l.6) 22 (9.0)
Overall 317 3 (0.9) 7 (2.9) 1 (0.3) 8 (2.5) 150 (47.3) 25 (7.9) 70 (22.1) 4(l.3) 8 (2.5) 8 (2.5) 33 (10.4)
Aedes hirsutus Indoor 13 1 (7.7) 0 (0.0) 0 (0.0) 3 (23.1) 7 (53.8) 2 (15.4) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 109 2 (1.8) 1 (0.9) 2 (1.8) 10 (9.2) 48 (44.0) 10 (9.2) 33 (30.3) 1 (0.9) 2 (1.8) 0 (0.0) 0 (0.0)
Overall 122 3 (2.5) 1 (0.8) 2(1.6) 13 (10.7) 55 (45.1) 12 (9.8) 33 (27.0) 1 (0.8) 2(1.6) 0 (0.0) 0 (0.0)
Aedes mcnitoshi Indoor 2 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (50.0) 0 (0.0) 1 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 26 0 (0.0) 0 (0.0) 0 (0.0) 1 (3.8) 13 (50.0) 4 (15.4) 6 (23.1) 0 (0.0) 1 (3.8) 0 (0.0) 1 (3.8)
Overall 28 0 (0.0) 0 (0.0) 0 (0.0) 1 (3.6) 14 (50.0) 4 (14.3) 7 (25.0) 0 (0.0) 1 (3.6) 0 (0.0) 1 (3.6)
Aedes taylori Indoor 2 0 (0.0) 0 (0.0) 0 (0.0) 1 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (50.0) 0 (0.0)
Outdoor 155 4 (2.6) 8 (5.2) 1 (0.6) 2(1.3) 68 (43.9) 22 (14.2) 38 (24.5) 2(1.3) 1 (0.6) 2(1.3) 7 (4.5)
Overall 157 4 (2.5) 8(5.1) 1 (0.6) 3(l.9) 68 (43.3) 22 (14.0) 38 (24.2) 2(1.3) 1 (0.6) 3 (l.9) 7 (4.5)
Culex fusco Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 2 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (100) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Overall 2 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (100) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Mans onia Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 8 0 (0.0) 0 (0.0) 0 (0.0) 1 (12.5) 5 (62.5) 0 (0.0) 1 (12.5) 0 (0.0) 0 (0.0) 0 (0.0) 1 (12.5)
Overall 8 0 (0.0) 0 (0.0) 0 (0.0) 1 (12.5) 5 (62.5) 0 (0.0) 1 (12.5) 0 (0.0) 0 (0.0) 0 (0.0) 1 (12.5)
Culex poicilipes Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 1 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (100) 0 (0.0) 0 (0.0)
Overall 1 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (100) 0 (0.0) 0 (0.0)
Culex univittatus Indoor 0 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Outdoor 2 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (50.0) 0 (0.0) 1 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Overall 2 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (50.0) 0 (0.0) 1 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
All species combined Indoor 89 1 (1.1) 1 (1.1) 0 (0.0) 5 (5.6) 34 (38.2) 5 (5.6) 18 (20.2) 1 (1.1) 8 (9.0) 5 (5.6) 11 (12.4)
Outdoor 551 9(1.6) 15 (2.7) 4 (0.7) 21 (3.8) 259 (47.0) 59 (10.7) 136 (24.7) 6(1.1) 5 (0.9) 6(1.1) 31 (5.6)
Overall 640 10 (1.6) 16 (2.5) 4 (0.6) 26 (4.1) 293 (45.8) 64 (10.0) 154 (24.1) 7(1.1) 13 (2.0) 11 (1.7) 42 (6.6)
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Table 6. Mixed bloodmeal sources of the blood-fed Culicine mosquitoes collected inTaita-Taveta, Coastal Kenya.

Site Species BC (%) BCG(%) BCH(%) BCHG(%) BG(%) BH(%) BHG(%) CG(%) CH(%) CHG(%) HG(%) Total
Chala Kimundia Culexq uinq 0 0 0 1 (25.0) 0 1 (25.0) 1 (25.0) 0 0 0 1 (25.0) 4
Aedes hirsutus 2(1.7) 1 (0.9) 2(1.7) 11 (9.4) 53 (45.2) 12 (10.3) 33 (28.2) 1 (0.9) 2(1.7) 0 0 117
Aedes mcintoshi 0 0 0 1 (4.3) 13 (56.5) 3 (13.0) 6 (26.1) 0 0 0 0 23
Aedes taylori 4 (2.5) 8(5.1) 1 (0.6) 3(lo9) 68 (43.3) 22 (14.0) 38 (24.2) 2(1.3) 1 (0.6) 3(1.9) 7 (4.5) 157
Coq.aurites 0 0 0 0 0 1 (33.3) 2 (66.7) 0 0 0 0 3
Culex fusco 0 0 0 0 0 0 2 (100.0) 0 0 0 0 2
Mansonia 0 0 0 1 (14.3) 5 (71.4) 0 1 (14.3) 0 0 0 0 7
Culex poicilipes 0 0 0 0 0 0 0 0 1 (100.0) 0 0 1
Culex quinq 0 2(1.3) 0 0 85 (56.7) 14 (9.3) 28 (18.7) 2(1.3) 1 (0.7) 3 (2.0) 15 (10.0) 150
Culex univittatus 0 0 0 0 1 (50.0) 0 1 (50.0) 0 0 0 0 2
King’wareni Aedes mcnitoshi 0 0 0 0 0 0 0 0 1 (50.0) 0 1 (50.0) 2
Culex quinq 0 0 0 0 6 (66.7) 0 3 (33.3) 0 0 0 0 9
Kiwalwa Aedes hirsutus 0 0 0 2 (100.0) 0 0 0 0 0 0 0 2
Aedes mcintoshi 0 0 0 0 1 (50.0) 1 (50.0) 0 0 0 0 0 2
Culex quinq 0 0 0 0 26 (47.3) 3 (5.5) 8 (14.5) 1 (1.8) 6 (10.9) 1 (1.8) 7 (12.7) 55
Mwarusa Aedes hirsutus 1 (33.3) 0 0 0 2 (66.7) 0 0 0 0 0 0 3
Aedes mcintoshi 0 0 0 0 0 0 1 (100.0) 0 0 0 0 1
Culex quinq 3 (4.4) 5 (7.4) 0 2 (2.9) 19 (27.9) 4 (5.9) 22 (32.3) 1 (1.5) 1 (1.5) 3 (4.4) 8 (11.8) 68
Njoro Culex quinq 0 0 1 (3.2) 2 (6.5) 14 (45.2) 0 8 (25.8) 0 0 1 (3.2) 2 (6.5) 31
Mansonia 0 0 0 0 0 0 0 0 0 0 1 (100.0) 1
Total 10 (1.6) 16 (2.5) 4 (0.6) 26 (4.1) 293 (45.8) 64 (10.0) 154 (24.1) 7(1.1) 13 (2.0) 11 (1.7) 42 (6.6) 640
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B, bovine; C, chicken; G, goat; H-human.

Discussion

In this study, we sought out to understand culicine mosquito species composition, abundance, diversity, and distribution within Taita- Taveta County. Our data present the first comprehensive analysis of culicine mosquito vector species density and composition in the region. The six villages involved in the study had significant spatial heterogeneity in terms of mosquito densities and species. The highest abundance was reported in areas where agricultural activities were carried out and in swampy areas, such as Kimundia, Kingw’areni, and Kiwalwa. Kimundia recorded the highest mosquito density, which could be attributed to ideal breeding habitats of culicine mosquito species. The mosquito larval ecology including nature of breeding habitats and the human-related activities such as irrigated agriculture with poor water channels and nonengineered irrigation canals contributed significantly to mosquito abundance and diversity. Previous studies done in Kenya have reported a positive relationship between habitat type, diversity, and mosquito species richness (Muturi et al. 2007). Similar results have been reported in Mwea irrigation scheme, Kenya, where there was high mosquito density which was due to agriculture activities (Mutero et al. 2004). This present study also supports an observation by (Afrane et al. 2012) that larval abundance, survival, and production of adult mosquitoes in irrigated vegetable farms are quite high and, therefore, contributing to high adult mosquito density. This demonstrates that mosquito productivity is a function of the availability of mosquitoes breeding habitats with more mosquitoes being found in areas with available stagnant water (Muturi et al. 2006a, Mwangangi et al. 2010)

Culicine mosquitoes are the most common with diverse flexible breeding habitats. Culex quinquefasciatus, Ae. hirsutus, Cx. univittatus, and Ae. mcintoshi were highly sampled mosquito species from all the six sites of Taita-Taveta County. Cx. quinquefasciatus mosquitoes for instance are known to breed in habitats with high organic content mostly in irrigation farms, swamps, rivers, latrines, uncovered septic tanks, drainage, rain pools, ditches, tree holes, and banana axles (Subra 1981, Irving-Bell et al. 1987, Aigbodion et al. 2011), which were present in the study area. The presence of these mosquito species in the study area poses a potential risk of mosquito-borne diseases such as lymphatic filariasis and RVFV to the human population (Mwandawiro et al. 1997, Woods et al. 2002, LaBeaud et al. 2011, Sang et al. 2017). Besides the potential for pathogen transmission, culicine mosquitoes are mostly involved in biting nuisance especially outdoors where most adult vector control tools are not in place. With the presence of vectors for bancroftian filariasis and arboviruses, outdoor mosquito control initiatives should be put in place to target mosquitoes of diverse feeding and resting behaviors. This could be done by exploring larval source management strategies integrated with scale-up of long-lasting insecticide-impregnated nets (LLINs) at the universal level through integrated vector management (IVM) package (WHO 2012).

Mosquito feeding preferences is a key determinant of disease transmission (Garcia-Rejon et al. 2010, Sawabe et al. 2010, Janssen et al. 2015). Host preference for culicine mosquitoes in Taita-Taveta County showed that these mosquitoes were relaxed feeders taking bloodmeals from several and available vertebrate hosts. When the human host was not readily available, culicine mosquitoes sought for alternative hosts available which are often in close proximity to human dwellings (Ijumba and Lindsay 2001). Culicine mosquitoes in Taita-Taveta County showed a high host preference on bovine (single host) and bovine/goat (multiple hosts) (zoophilic nature) over human hosts (anthropophilic nature). These results were in agreement with the previous study that reported high zoophilic nature of culicine mosquito in Mwea irrigation scheme, Kenya (Muturi et al. 2008). The low anthropophilic and high zoophilic nature of culicine mosquitoes observed in our study could be both advantageous and disadvantageous to bancroftian filariasis and RVF transmission, respectively. Low anthropophilic nature of Cx. quinquefasciatus may disfavor transmission of Bancroftian filariasis. This could be possible due to the loss of a significant number of worms to the wrong host, or by failing to pick up enough microfilaria that can sustain transmission. Bancroftian filariasis transmission is very inefficient because there is no parasite multiplication in the mosquito and continuous exposure to many infective bites is necessary for transmission to occur (Hairston and de Meillon 1968, Bockarie et al. 2002). On the negative, high zoophilic nature of Aedes and Culex mosquito species poses a high risk of Rift Valley Fever (RVF) virus transmission to domestic animals including cattle, goats, and sheep (Tchouassi et al. 2016). The feeding pattern for these culicine mosquito species in Taita-Taveta County, therefore, present an ideal condition for RVF, and efforts should be made to establish the risk factors of the disease in similar areas and to develop sustainable mosquito surveillance and control systems.

Our results demonstrated that nearly all the species examined fed on multiple hosts within a single gonotrophic cycle. High mosquito density in these areas where agricultural activities are highly practised enforces the use of bed nets and other protective measures against mosquito bite consequently reverting mosquitoes to feeding on domestic animals because humans are not easily accessible (Muriu et al. 2008). Interestingly, 7.2% of the bloodmeal samples were not from any of the four hosts tested an indication that culicine mosquitoes in this area have a wide host range. Other livestock and animals present in the study area were dogs, cats, wild birds, house rats, and rodents, but due to logistical limitations and unavailability of anti-seras against these mentioned animals, we were restricted to conducting ELISA tests against them. These findings highlight the need to include a variety of possible hosts when conducting mosquito host choice studies.

This study demonstrated a marked difference in species composition, abundance, and distribution of culicine mosquitoes in the six villages of Taita-Taveta County, Kenya. The study demonstrated that culicine mosquitoes in Taita-Taveta County were highly zoophilic and that multiple feeding within the same gonotrophic cycle was common among these species. The results of this study show that there is a need to scale up vector control interventions to target outdoor mosquitoes which will ensure a significant reduction in mosquito populations.

Acknowledgements

We acknowledge the support of the entomological field assistant mainly Gabriel Nzai, Shida David, and Festus Yaah and KEMRI team in Taveta Saidi Matano, Samuel Mukunde, and Muckoi Fundi. We acknowledge the support from the Department of Health County Government of Taita Taveta and the Taveta Sub-County Public Health Department. We appreciate the support from the local administration team (Chiefs, Balozi wa Nyumba Kumi ‘ambassadors’) and the communities in the six villages. We would also like to acknowledge Christopher Nyundo of the KEMRI-Wellcome Trust Research Programme for helping in developing the study site map. Funding was provided by the Government of Kenya through Kenya Medical Research Institute Internal Research Grants (KEMRI-IRG) Grant Number INNOV/IRG/020/2.

Footnotes

Ethical Considerations

The study was approved by the KEMRI Scientific and Ethics Review Unit (SERU) Protocol (KEMRI/SERU/CGMRC/035/3219). Oral consent was also obtained from the household members before mosquito collection commenced.

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