ABSTRACT.
This study examined whether Aedes aegypti extends its human blood seeking activity into night hours. Human landing catches (HLC) were conducted hourly from early morning (04:30) to late evening (21:30) in urban and rural sites in Kisumu County in western Kenya, and in Kwale County at the coast. Out of 842 female Ae. aegypti mosquitoes, 71 (8.5%) were collected at night (nocturnal), 151 (17.9%) at twilight (crepuscular), and 620 (73.6%) during the day (diurnal). Three-fold and significantly more Ae. aegypti female mosquitoes were collected during the twilight (crepuscular) hours than night (nocturnal) hours. Significantly more Ae. aegypti female mosquitoes were collected during daytime (diurnal) than night time (nocturnal). In general, the number of mosquitoes collected reduced as darkness increased. Extended time into the night to seek for blood meals enhances chances for Ae. aegypti to contact humans and transmit arboviruses diseases.
Aedes aegypti is the principal vector of human arboviral diseases including Yellow fever, chikungunya, dengue, and Zika viruses.1 The ancestry of Ae. aegypti is traced back to Sub-Saharan Africa, where one form, Ae. aegypti aegypti, was domesticated (breeding in human surroundings and adapting to human blood meals) and then transported on trading ships to America, then to Asia and Australia, whereas the other form, Ae. aegypti formosus, still exists in forests in Sub-Saharan Africa.2,3 The adaptation of Ae. aegypti aegypti to human blood meals has resulted in the synchronization of its blood-seeking activities to mainly daytime (diurnal) and twilight (crepuscular) times, when chances of finding humans are high.4–7 A small fraction of its blood-seeking activities extend into the night (nocturnal) within urban areas.8 This study examined whether Ae. aegypti human blood seeking activity extends into pre-sunrise and post-sunset hours in rural and urban sites in western and coastal Kenya.
Human landing catches were conducted from early morning (04:30) to late evening (21:30) in June, September, and December in 2017 and in March and June in 2018 in two sites in western and coastal Kenya. These sites were: urban site in Kisumu (0°5′15.22478″S, 34°46'22.3284″E, altitude 1,186 meters above sea level [m.a.s.l.]) and rural site in Chulaimbo (0°2′17.2500″S, 34°38′18.1998″E, 1372 m.a.s.l.) in Kisumu County, and urban site in Ukunda (4°16′38.8992″S, 39°34′9.0012″E, 23 m.a.s.l.) and rural site in Msambweni (4°27′58.4382″S, 39°28′17.8716″E, 20 m.a.s.l.) in Kwale County. Human landing catches were conducted as described by Ndenga and others.7 In summary, two homesteads were selected in each of the four sites for sampling of Ae. aegypti mosquitoes. Adults (≥18 years old), who resided within the sampling area (assumed to be exposed to similar possible mosquito bites) and who provided written informed consent volunteered to catch mosquitoes by HLC. They were all trained before they started the catching of mosquitoes. Two teams of two people each sampled indoors and outdoors (∼3–5 m from the house). Both collectors sat on chairs, with one exposing both legs, and the other collecting mosquitoes landing on the partner’s legs using a mouth aspirator. The team members changed roles hourly. Two sets of collectors were used: the first set worked from 04:30 to 12:30 and the second from 12:30 to 21:30. Mosquitoes collected each hour were put in a pre-labeled plastic cup and provided with 10% sugar solution on cotton wool. All labeled plastic cups were put in cooler boxes with ice packs, and then transported to the insectaries at Kenya Medical Research Institute (KEMRI), Center for Global Health Research (CGHR) station at Kisian in Kisumu for the western sites and at the Vector Borne Disease Control Unit in Msambweni County Referral Hospital, Kwale County for the coastal sites. All mosquitoes were killed by placing them at −20°C for 15 minutes and identified by genus (Aedes, Anopheles, or Culex) and sex.9,10 However, we could not further identify Ae. aegypti mosquitoes either as Ae. aegypti aegypti or Ae. aegypti formosus.
This study obtained ethical approval from both Stanford University Institutional Review Board (Protocol ID 31488 and IRB Number 6208) and Kenya Medical Research Institute Ethical Review Committee (SSC No. 2611). Data were recorded daily, entered into a Microsoft Excel database, summarized by descriptive analysis and analyzed using generalized estimating equations (GEE) on count data that were fitted with a negative binomial distribution with a log link function. Univariate analysis was done for each of the parameters separately. Parameters with P ≤ 0.05 in the univariate analysis were included in multivariate analysis.
A total of 842 female Ae. aegypti mosquitoes were collected: 496 (58.9%) and 346 (41.1%) in the western and coastal sites, respectively. Mosquitoes collected per site were: 101 (12.0%) in Chulaimbo; 395 (46.9%) in Kisumu; 85 (10.1%) in Msambweni, and 261 (31.0%) in Ukunda. A total of 186 (22.1%) and 656 (77.9%) mosquitoes were collected in the rural (Chulaimbo and Msambweni) and urban sites (Kisumu and Ukunda), respectively. Mosquitoes collected indoor were 204 (24.2%) and outdoor were 638 (75.8%).
Out of the 842 female Ae. aegypti mosquitoes, 71 (8.5%) were collected at night (nocturnal), 151 (17.9%) at twilight (crepuscular), and 620 (73.6%) during the day (diurnal). A total of 89 Ae. aegypti mosquitoes were collected from 04:30 to 06:30 and 133 from 18:30 to 21:30 both indoors and outdoors, and in the rural and urban sites in Kisumu and Kwale counties. The average numbers of Ae. aegypti mosquitoes that were collected during daytime (diurnal), at night (nocturnal), and at twilight (crepuscular) varied among the four sites (Msambweni, Ukunda, Chulaimbo, and Kisumu) with the highest number in Ukunda at twilight (Figure 1). In general, the number of mosquitoes collected reduced as darkness increased.
Figure 1.
Average numbers of Aedes aegypti female mosquitoes collected by human landing catches.
The total numbers of Ae. aegypti female mosquitoes collected in urban sites (Kisumu and Ukunda) (N 2,040; OR 2.9 (2.0–4.1); P < 0.001) and outdoors (N 2,040; OR 3.0 (2.4–3.9); P < 0.001) were 3-fold and significantly more than those collected in the rural sites (Chulaimbo and Msambweni) and indoors, respectively. Similarly, 3-fold and significantly more Ae. aegypti female mosquitoes were collected during the twilight (crepuscular) hours (N 480; OR 3.1 (2.0–4.7); P < 0.001) than night (nocturnal) hours. Significantly more Ae. aegypti female mosquitoes were collected during daytime (diurnal) hours (N 2,880; OR 2.2 (1.2–4.0); P = 0.010) than night time (nocturnal) hours.
The collection of Ae. aegypti female mosquitoes at night (nocturnal) confirms that this species extends its blood-seeking activities in the pre-sunrise and post-sunset hours. This extension was conspicuous outdoors, in both the urban and rural sites, and indoors, only in the urban site. A similar host-seeking behavior was observed in Trinidad8 where 90% of Ae. aegypti were caught during daylight (diurnal) and twilight (crepuscular) and 10% in the night (nocturnal). This highlights the need to modify the general description of Ae. aegypti as only a daytime feeder, that takes blood meals early in the morning and in the evening before dusk.9,11 The feeding activity period needs to include pre-sunrise and post-sunset blood-seeking behavior. Ongoing urbanization, specifically more artificial light at night (ALAN) increases nocturnal human activities, and is resulting in extended Ae. aegypti blood-feeding behavior.12,13 This may lead to increased transmission of arboviruses such as dengue, chikungunya, Yellow Fever, and Zika in urban areas, and increased rates of diseases.
In conclusion, Ae. aegypti extends its blood seeking activities into the pre-sunrise and post-sunset hours. This behavior, coupled with human nocturnal outdoor activities, might enhance chances of human-vector contact hence increase the transmission of arboviruses.
ACKNOWLEDGMENTS
We thank the local residents and their leaders who volunteered and offered their assistance during data collection activities. We appreciate Kenya Medical Research Institute staff, all project staff in Kisumu, Kwale, and at Stanford University in California, for all their assistance. This paper is published with the permission from the Director Kenya Medical Research Institute.
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