Analysis of the 24-Hour Biting Patterns and Human Exposures to Malaria Vectors in South-Eastern Tanzania

doi:10.21203/rs.3.rs-4844193/v1

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Analysis of the 24-Hour Biting Patterns and Human Exposures to Malaria Vectors in South-Eastern Tanzania

https://doi.org/10.21203/rs.3.rs-4844193/v1

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Background

Afrotropical malaria vectors are generally believed to bite nocturnally, leading to the predominant use of Insecticide-Treated Nets (ITNs), which target indoor, nighttime-biting mosquitoes. This focus is reinforced by biases in entomological surveys, which largely overlook daytime mosquito activity. However, recent evidence challenges this paradigm, showing that Anopheles biting can extend way into the daytime, coinciding with human activities at dawn, daytime, and evenings, suggesting a broader risk spectrum and potential protection gaps. This study therefore investigated the diurnal and nocturnal biting patterns of the malaria vectors, Anopheles arabiensis and Anopheles funestus in south-eastern Tanzania, to better understand the scope of residual transmission and inform strategies for improved control.

Methods

Host-seeking mosquitoes were collected hourly using miniaturized double net traps, indoors and outdoors over 24-hour periods between June 2023 and February 2024. Concurrently, human activities indoors and outdoors were monitored half-hourly to correlate with mosquito collections. A structured questionnaire was used to assess household members’ knowledge, perceptions, and experiences regarding exposure to mosquito bites during both nighttime and daytime.

Results

Nocturnal biting by An. arabiensis peaked between 7pm and 11pm, while An. funestus peaked later, between 1am and 3am. Daytime biting accounted for 15.03% of An. gambiae catches, with peaks around 7-11am and after 4pm; and 14.15% of An. funestus catches, peaking around mid-mornings, from 10am-12pm. Night-time exposure to An. arabiensis was greater outdoors (54.5%), while daytime exposure was greater indoors (80.4%). For An. funestus, higher exposure was observed indoors both at nighttime (57.1%) and daytime (69%). Plasmodium falciparum sporozoites were detected in both day-biting and night-biting An. arabiensis. Common daytime activities potentially exposing residents during peak biting hours included household chores, eating, sleeping (including due to sickness), resting under shades or verandas, and kids playing. From evenings onwards, exposures coincided with resting, socializing before bedtime, and kids playing. Nearly all survey respondents (95.6%) reported experiencing daytime mosquito bites, but only 28% believed malaria was transmissible diurnally.

Conclusion

This study updates our understanding of malaria vector biting patterns in south-eastern Tanzania, revealing considerable additional risk in the mornings, daytime, and evenings. Consequently, ITNs, which primarily target nocturnal mosquitoes, may have larger protection gaps than previously thought. Complementary strategies are needed to holistically suppress vectors regardless of biting patterns (e.g. using larval source management) and to extend personal protection limits (e.g. using repellents). Additionally, community engagement and education on mosquito activity and protective measures could significantly reduce malaria transmission risk.

Persistent malaria transmission

human behavior

day-biting Anopheles mosquitoes

ITNs

Ifakara

Despite significant advances, malaria is still a substantial public health threat globally, with approximately 249 million cases and over 608,000 deaths in 2022 [1]. The main prevention strategies, Insecticide-Treated Nets (ITNs) and Indoor Residual Spraying (IRS) have significantly reduced malaria incidence, together contributing to nearly 80% of the progress made in Africa against the disease, according to a 2015 publication [2]. Similarly in Tanzania, the adoption of ITNs and IRS, augmented with effective case management, has achieved notable reductions in malaria prevalence over recent years, cutting prevalence from 14% in 2016 to 8% in 2022 [3, 4]. These developments have inspired the prospects for potential elimination across many endemic regions, including those where transmission has been historically intense.

ITNs and IRS primarily target the nocturnal and indoor-biting behaviors of the major Afro-tropical malaria vectors, Anopheles gambiae sensu lato and Anopheles funestus, effectively transforming human dwellings into lethal traps that reduce malaria transmission [5]. While these interventions primarily address indoor behaviors, their mosquitocidal attributes can accrue significant community-level benefits even for non-users [6–8], underscoring their critical role in tailored vector control strategies for public health management. Moreover, in certain circumstances, these tools can, to a certain degree also impact vector populations that bite outdoors [9–11].

Despite significant advances in vector control, the path to malaria elimination faces numerous biological and behavioral challenges. The main threats include insecticide resistance, which diminishes the effectiveness of ITNs and IRS [12, 13], and drug resistance, particularly concerning artemisinin-based therapies crucial for treating malaria [14–16]. Additionally, mutations like the HRP2 gene deletion complicate malaria diagnosis by making parasites undetectable by standard rapid tests [17, 18]. The invasion and spread of the Asian malaria vector, Anopheles stephensi, particularly in urban eastern African settings, introduces a new dynamic, as this vector is less affected by traditional control measures [19–22]. In many settings, these challenges are further complicated by behavioral adaptations among vectors, such as increased outdoor feeding and biting during the day time, in early evenings and mornings when people are not under ITNs, allowing malaria transmission to persist despite high intervention coverage [23–27]. In one study in Bangui, Central African Republic, approximately 20–30% of daily exposure to indoor Anopheles biting happened during the day, suggesting a significant protection gap in such settings [23]. These changes underscore the need for dynamic vector management strategies that adapt to evolving vector behaviors to maintain the effectiveness of malaria interventions.

Unlike ITNs, which are mostly targeted at nocturnal biting behaviors of the main vectors like An. gambiae s.l. and An. funestus, IRS targets resting mosquitoes and Larval Source Management targets mosquitoes at source [28–30]. These two strategies can therefore, to a large degree be agnostic of the peak mosquito biting activity times [31], and LSM in particular can remain effective despite biological threats like insecticide resistance and outdoor biting [31, 32]. Unfortunately, for most people in sub-Saharan Africa, their defense against malaria is derived primarily from the protection offered by ITNs during nighttime when these vectors are most active. Moreover, the evidence is increasing of daytime biting by Africa’s main malaria vector species, coinciding with periods when people are engaged in activities such as farming and fetching water, and thus are not protected by ITNs [33–38]. This behavior, whether innate or emergent in response to current interventions, significantly broadens the risk spectrum, further expanding the already substantial gaps in protection by strategies designed primarily for nocturnal intervention.

This evidence underscores a critical oversight in current vector control strategies, necessitating a re-evaluation and possible expansion of intervention focus to encompass vector activities during the daytime. Such adjustments are essential not only for safeguarding at-risk populations throughout their active hours but also for reducing the residual transmission of malaria. The profound implication of these studies is that ongoing malaria control efforts might be compromised by previously underappreciated vector behaviors, highlighting the need for a nuanced and flexible approach to both the surveillance and control strategies, to accommodate the full behavioral spectrum of malaria vectors. In places where the main malaria vectors include An. funestus, especially in east and southern Africa [39], the increasing evidence of daytime and early morning biting behaviors can be particularly concerning. While the IRS, which has historically been common in this region, may continue to be effective against these behaviors [31], its deployment is increasingly declining, in part because of logistical challenges, housing modifications, and diminishing community acceptance – and this can lead to upsurges in malaria cases [40–42].

The majority of field studies on malaria vectors have concentrated on the nighttime activities of the vectors, in line with the operational hours of ITNs. This predominant focus has led to a significant gap in understanding vector behaviors during the daytime, including early mornings and early evenings, times when human activity and human-mosquito interactions can be high but protection is low. This methodological bias has not only skewed the understanding of vector behavior and limited the effectiveness of interventions designed with a nocturnal bias. For these reasons, there is a pressing need for comprehensive studies that include 24-hour behavioral assessments of vectors, which will inform the development of responsive and effective malaria control measures across the vector’s entire activity spectrum. Additionally, residents in malaria-endemic areas generally have diverse behaviors and housing structures that influence exposure to mosquito bites [25, 43–45], potentially compromising the effectiveness of ITNs and the IRS. Despite the high coverage of these interventions, persistent malaria transmission in places such as rural southeastern Tanzania [46], underscores the necessity for detailed studies on vector behaviors beyond traditional monitoring hours. Understanding these local dynamics is essential for designing interventions that effectively curb malaria transmission, aligning with the elimination goals of many endemic countries.

This study therefore aimed to investigate the diurnal and nocturnal biting patterns of two major vectors, An. arabiensis and An. funestus in rural southeastern Tanzania – in an area characterized by high ITN usage but persistent moderate to high malaria prevalence [47]. The study also examined human activities and behaviors that could influence malaria vector biting risk both inside and outside homes. By analyzing these 24-hour patterns of exposure, we aimed to better elucidate the gaps in control of the persistent malaria transmission in the area and to inform improved strategies for control and elimination.

Study area

The study was conducted in two rural villages, Tulizamoyo and Minepa, in Ulanga District within the Kilombero Valley in southeastern Tanzania, from June 2023 to February 2024 (Fig. 1). This valley experiences moderate to high malaria transmission, with prevalence rates varying from less than 1% in semi-urban areas to over 50% in rural [47]. Malaria prevention in the area predominantly involves the use of ITNs, distributed primarily through the National Malaria Control Program via mass distribution campaigns and supplementary channels such as antenatal visits and school net distribution programs. Currently, more than 77% of households have at least one ITN [4]. Houses in these villages are typically constructed of mud or brick walls, occasionally plastered with concrete, and are roofed with either grass thatch or metal. The main economic activity is small-scale rice farming, sometimes supported by irrigation. The climatic conditions, with annual rainfall ranging from 1200 mm to 2100 mm and temperatures fluctuating between 23°C and 27°C [48], can support moderate to high mosquito densities year-round, and also continuous malaria transmission. An. funestus and An. arabiensis are the main vectors, the former being responsible for more than 80% of malaria transmission, even where the latter is the more abundant [46, 49–51]

Study design

This study involved concurrent entomological data collection and human behavior observations (HBOs) both indoors and outdoors over 24-hour periods in the study area. Additionally, community perceptions and knowledge about day-biting mosquitoes and the associated risk of diseases were assessed through a structured questionnaire in a community survey. In each village, 12 sentinel houses reflecting local architectural styles were randomly chosen for weekly routine entomological surveillance and human behavior surveys. Then, 16 adult males were recruited upon written informed consent from each village; and were trained in mosquito collection methods, including the use of the miniaturized double net (DN-Mini) technique [10] to participate in the study. The houses were sampled in rounds of four every two days with breaks to allow rest periods for volunteers, and time for the scientists and technicians to process the samples.

Sampling and processing of adult mosquitoes

Host-seeking mosquitoes were collected both indoors and outdoors using a miniaturized double net trap (DN-Mini) across 32 nights in each village (Fig. 2). The DN-Mini is an exposure-free sampling method that allows for direct estimation of the mosquito biting risk and can be used indoors or outdoors [10, 52]. The indoor DN-Mini trap was placed in the living room while the outdoor trap was placed under tree shades with a radius of 5–10 meters away from the sentinel house. Mosquito collections were done hourly for 24 hours, starting from 7 am to 7 am the following morning, by teams of four trained volunteers working in 6-hour shifts to minimize fatigue and reduce collection bias. Each volunteer, stationed either inside or outside the target house, used a mouth aspirator to collect mosquitoes from the outer chambers of the DN-Mini every hour starting the 50th minute.

The collected mosquitoes were separated by hours of collection. Each morning, the mosquitoes were identified based on their morphological characteristics using taxonomic keys [53]. They were sorted by species, location, and physiological status (unfed, fed, semi-gravid, and gravid). Non-gravid females of An. gambiae s.l. and An funestus s.l. were dissected to assess physiological age by assessing parity, following the Detinova method [54]. Samples were then stored in labeled micro-centrifuge tubes for further analysis. Polymerase Chain Reaction (PCR) and Enzyme-Linked Immunosorbent Assay (ELISA) were used to analyze pooled hourly samples for sibling species identification [55, 56] and detection of Plasmodium Circumsporozoite proteins [57, 58], providing insights into malaria transmission dynamics.

Observations of the behaviors and activities of household members in the peri-domestic area

In addition to the entomological surveys, direct observations of human activities and movements were done to enable the quantification of exposures to mosquito bites in relation to human activities within the household vicinity. Data on human behaviors and activities in the peri-domestic area was collected half-hourly alongside mosquito sampling at the same houses to assess human exposure to mosquito bites over 24-hour periods, both indoors and outdoors. Behavioral data were collected in a subset of the selected sentinel houses for entomological surveys in each village using a standardized observation form, pre-outlined with common activities as previously described [25]. The houses were selected based on the presence of a willing qualified observer who was able to read and write. The observers, who were either consenting household members or trained relatives, tallied all the observed activities hourly, noting the age and sex of individuals involved. Each observer continuously tracked different activities conducted by household members from 7 am in the morning, throughout the day and until all members had retired to bed at night. At that point, the observations stopped and were only resumed the following morning as soon as the first household member rose to begin daily activities.

Assessment of knowledge, perceptions and experiences of community members regarding the risk of mosquito bites outside periods when ITNs are used

To understand community awareness regarding mosquito bites and associated disease risks outside of ITN protection hours, including mornings, daytime, and evenings, a structured questionnaire survey was done targeting household representatives in the same study villages. The survey, conducted in Swahili language, examined the awareness and knowledge of community members as well as their daily activities that could expose them to mosquito bites. This information was used to construct a typical day for household members, correlating their activities with the observed 24-hour mosquito biting patterns to enhance understanding of malaria transmission risk. A systematic random sampling approach was used to select households for participation. Kobo Toolbox software [59] was used to administer the survey via electronic tables, facilitated by trained interviewers. The survey was done between December 2023 and February 2024. A list of all households was obtained from the village leaders, and 91 households were randomly selected per village.

A total of 182 households participated in the survey. This sample size was estimated using a formula for determining a single population proportion [60], i.e. \(\:n=\:\frac{{Z}^{2}*p\:(1-p)}{{d}^{2}}\), where \(\:n\) was the sample size, \(\:z\) was the statistic value at a 95% confidence level (1.96), \(\:d\) was the level of precision (0.05), and p, the proportion of malaria prevalence in children in the Morogoro region (0.06) [4]. This calculation gave an initial sample size of approximately 87 households. Since the survey was conducted in two villages, this number was doubled to 174 households. Additionally, to account for a potential 5% non-response rate, 9 more households were added, bringing the total to 182 households. In each village, sampling began by randomly selecting the first household and then continued systematically using a predetermined sampling interval.

Data analysis

Data were initially entered into Microsoft Excel and then imported into R statistical software version 4.3.1 for further processing and analysis [61]. A generalized linear mixed model (GLMM) fitted with a Bayesian approach was used [62], to model the hourly abundance of mosquitoes per person. The model incorporated time of collection and location as predictor variables, and mosquito counts as the response variable. Household ID and day of collection were included as random effects to account for variability between days and households. Mosquito counts were modeled using Poisson distributions with a log-link function. Each mosquito species was modeled separately. To attain convergence, each model species was run for 10⁴ iterations with 1,000 burn-in periods. Model diagnostics included visual inspection of trace plots and evaluation using Gelman-Rubin statistics to assess convergence. Graphical representations were produced using the ggplot2 package [63]. Correlation between human behavior and mosquito biting was done using descriptive statistics and visualization was done using figures [25, 64]. The results were expressed as relative risks with 95% credible intervals

Additionally, descriptive analyses were used to assess household members’ understanding and perceptions of the risk of mosquito bites and malaria transmission throughout the day, particularly during the daytime. Continuous variables were expressed as means and categorical variables were expressed as percentages.

Mosquito catches indoors and outdoors during nighttime and daytime collections

A total of 10,987 female Anopheles mosquitoes and 23,367 female Culicine mosquitoes (Culex pipiens and Ma. uniformis) were collected (Table 1). Of all female Anopheles mosquitoes collected during the study, the majorities were caught at night, from 7 pm to 6 am, (85.2%), and only 14.8% were caught during the day (6 am to 7 pm). The Cumulative percentages of the catches are shown in Fig. 3. During the nighttime collections, 45.6% of all Anopheles mosquitoes were caught indoors while outdoor collections comprised 54.4% (Table 1). However, during the day, indoor collections of Anopheles accounted for 79.3%, and outdoor collections for 20.7%. Culicine mosquitoes were also mainly caught at night (77.8%), with 48.5% of these nighttime collections being indoors and 51.5% outdoors. Daytime Culicine collections were 75.1% indoors and 24.9% outdoors. Most of the Anopheles mosquitoes were An. arabiensis (10,283; 93.6%) and An. funestus (410; 3.7%). The other Anopheles species included Anopheles coustani (232; 2.1%), Anopheles squamosus (52; 0.5%), and Anopheles pharoensis. On the other hand, the non-Anopheles mosquitoes comprised 19,785 (85%) Culex quinquefasciatus and 3,582 (15%) Mansonia uniformis. In line with the objectives of the study, further statistical analysis focused on the two predominant malaria vectors, An. arabiensis and An. funestus.

Table 2 shows the results of a generalized linear model fitted using the Bayesian approach to examine the hourly abundance of mosquitoes caught per person between indoor and outdoor locations. The average biting rate was 0.75 for An. arabiensis and 0.02 for An. funestus indoors, compared to 0.72 and 0.01 outdoors, respectively. The model revealed no significant differences in the indoor versus outdoor biting rates for either species (An. arabiensis RR = 0.97, 95%CI: 0.93–1.01; An. funestus RR = 0.70, 95%CI: 0.57–0.85).

Table 1

Diversity and densities of mosquitoes collected during the survey, using human-baited double net traps placed indoors or outdoors during daytime and nighttime.
	Nighttime Mosquito Collections			Daytime Mosquito collections			Total
	Indoors	Outdoors	Totals (indoor & outdoor catches)	Indoors	Outdoors	Totals (indoor & outdoor catches)	Totals (Night & day catches
Anopheles species
An. arabiensis	3976 (45.5%)	4761 (54.5%)	8737	1243 (80.4%)	303 (19.6%)	1546	10283
An. funestus	201 (57.1%)	151 (42.9%)	352	40 (69.0%)	18 (31.0%)	58	410
An. coustani	67 (31.6%)	145 (68.4%)	212	7 (35.0%)	13 (65.0%)	20	232
An. pharoensis	16 (32.0%)	34 (68.0%)	50	1 (50.0%)	1 (50%)	2	52
An. squamous	6 (66.7%)	3 (33.3%)	9	0 (0.0%)	1 (100%)	1	10
Total	4266 (45.6%)	5094 (54.4%)	9360	1291 (79.3%)	336 (20.7%)	1627 (100%)	10987
Percentage Nighttime vs. Daytime catches	85.2%			14.8%			100%
Other species (Culicines)
Cx. quinquefasciatus	8001 (53.5%)	6960 (46.5%)	14961	3685 (76.4%)	1139 (23.6%)	4824	19,785
Ma. uniformis	910 (26.6%)	2513 (73.4%)	3423	59 (37.1%)	100 (62.9%)	159	3582
Total	8911 (48.5%)	9473 (51.5%)	17484 (100%)	3744 (75.1%)	1239 (24.9%)	4983 (100%)	23367
Percentage Nighttime vs. Daytime catches	77.8%			22.2%			100%

Table 2

Mean number of mosquitoes per person per hour
Species	Location	Total catch	Mean [95% CI] *	RR [95% CI]
An. arabiensis	Indoors	5,219	0.75 [0.54, 1.03]	1
An. arabiensis	Outdoors	5,064	0.72 [0.52, 1.00]	0.97 [0.93, 1.01]
An. funestus	Indoors	241	0.02 [0.01, 0.04]	1
An. funestus	Outdoors	169	0.01 [0.006, 0.03]	0.70 [0.57, 0.85]

24-Hr biting patterns of the main malaria vectors

Host-seeking activity of the two primary species, An. arabiensis and An. funestus was markedly higher at night compared to daytime. During the nighttime, the numbers of An. arabiensis and An. funestus caught were 8737 and 352 respectively, while during daytime the numbers caught were 1546 and 58 respectively (Table. 3). Overall, daytime biting accounted for 15.03% of An. gambiae catches, and 14.15% of An. funestus catches. Also, night-time exposure to An. arabiensis was greater outdoors (54.5%), while daytime exposure was greater indoors (80.4%). For An. funestus, higher exposure was observed indoors both at nighttime (57.1%) and daytime (69%).

During the night, An. arabiensis exhibited peak biting activity in the first half of the night between 7 pm and 11 pm, starting while significant fractions of people were indoors or outdoors, and continuing as people were getting indoors and going to bed, then decreased towards morning. Conversely, An. funestus displayed peak indoor biting activity later at night between 1 am and 3 am, when most people were asleep and likely under their bed nets. Additional peak activity for both An. arabiensis and An. funestus was observed during the morning hours both indoors and outdoors, coinciding with the time people were awake, had exited their bed nets, and were already outside engaging in routine morning activities. During the day, An. arabiensis had higher indoor biting rates with peaks between 7 am and 11 am, and again from 4 pm onwards. The other species, An. funestus had a small peak between 10am and 12 pm, with less obvious preference for indoors over outdoor locations (Fig. 4).

The mean number of bites per person per hour during daytime and nighttime shows that An. gambiae had a higher biting rate at night compared to daytime for both indoor and outdoor locations. Indoor nighttime biting for An. gambiae was 1.15 bites per person per hour, while outdoor nighttime biting was slightly higher at 1.38 bites per person per hour. Daytime biting rates for An. gambiae were lower, with indoor biting at 0.25 and outdoor biting at 0.06 bites per person per hour. An. funestus had significantly lower biting rates overall, with indoor nighttime biting at 0.04 and outdoor at 0.03 bites per person per hour. Daytime biting for An. funestus was minimal, with indoor rates at 0.004 and outdoor rates at 0.002 bites per person per hour (Table. 3).

Table 3

Mean number of bites per person per hour during daytime and nighttime
Species	Location	Total	Daytime catches			Nighttime catches
Species	Location	Total	Mean [95% CI]*	RR [95% CI]	Total	Mean [95% CI]*	RR [95% CI]
An. gambiae	Indoor	1,243	0.25 [0.15, 0.43]	1	3,976	1.15 [0.84, 1.58]	1
An. gambiae	Outdoor	303	0.06 [0.04, 0.11]	0.24 [0.21, 0.28]	4,761	1.38 [1.01, 11.89]	1.20 [1.15, 1.25]
An. funestus	Indoor	40	0.004 [0.001, 0.012]	1	201	0.04 [0.02, 0.07]	1
An. funestus	Outdoor	18	0.002 [0.000, 0.01]	0.44 [0.25, 0.78]	151	0.03 [0.01, 0.05]	0.75 [0.61, 0.93]

Physiological states, parity, and Plasmodium infection rates of the malaria vectors collected

Of the 10,693 female An. arabiensis and An. funestus mosquitoes collected, 70.0% were unfed, 21.4% were gravid, 7.0% fed, and 1.6% were semi-gravid. Slightly more than half of the host-seeking female An. arabiensis (58.4%) and 52.5% of An. funestus caught during the daytime were unfed. The parity rate for An. arabiensis caught during the daytime was 82.57% indoors and 79.47% outdoors, while for An. funestus it was 84.44% indoors and 66.67% outdoors. Similarly, during nighttime, the parity rate for An. arabiensis was 78.99% indoors and 78.2% outdoors, and for An. funestus it was 84.67% indoors and 66.86% outdoors. No significant difference was detected in the proportion of parous An. arabiensis and An. funestus mosquitoes collected indoors and outdoors (An. arabiensis RR = 0.82, 95%CI: 0.55,1.22; An. funestus RR = 0.37, 95%CI: 0.07, 1.83), and (An. arabiensis RR = 0.95, 95%CI: 0.85, 1.07; An. funestus RR = 0.37, 95%CI: 0.07, 1.83), respectively. However, An. funestus and An. arabiensis caught indoors during daytime and nighttime had higher parity rates compared to respective outdoor catches between day and night (Table. 4). Despite the lower numbers collected during the daytime, the indoor and outdoor hourly parity rates were higher during the daytime than at night (Fig. 5).

Regarding Plasmodium sporozoite infections, a total of 3,095 female Anopheles arabiensis mosquitoes (1,832 collected indoors and 1,263 outdoors) were tested, with only one sporozoite-positive mosquito found in each subset. The positive indoor mosquito was captured between 7:00 am and 7:50 am, while the positive outdoor mosquito was caught between 11:00 pm and 11:50 pm. Additionally, 178 female Anopheles funestus mosquitoes (97 indoors and 81 outdoors) were tested out of 410 collected during the entire study period, but no infections were detected.

Table 4

Parity rate indoors vs outdoors during daytime and nighttime
	Location	No. Parous	Daytime catches		No. Parous	Nighttime catches
	Location	No. Parous	Proportion parous [95% CI]*	OR [95% CI]	No. Parous	Proportion parous [95% CI]*	OR [95% CI]
An. gambiae	Indoors	635/769	82.57 [79.73, 85.10]	1	2272/2876	78.99 [77.48,80.43]	1
An. gambiae	Outdoors	151/190	79.47 [73.14, 84.63]	0.82 [0.55, 1.22]	3026/3871	78.2 [76.84, 79.43]	0.95 [0.85, 1.07]
An. funestus	Indoors	38/45	84.44 [70.80, 92.40]	1	127/150	84.67 [70.79,92.40]	1
An. funestus	Outdoors	6/9	66.67 [33.34, 88.89]	0.37 [0.07, 1.83]	113/169	66.86 [33.34,88.89]	0.37 [0.07, 1.83]

Human exposure to mosquito bites indoors and outdoors

Analysis of the human behaviour data alongside the entomological data showed that overall, the majority of exposure to An. arabiensis occurred outdoors during the first part of the night between 7 pm and 11 pm, before most people went to bed, with additional exposure in the morning hours between 4 am and 6 am when most people were awake. Outdoor exposure continued throughout daytime hours when most people were active outdoors, with a small peak between 8 am and 10 am (Fig. 6). In contrast, the bulk of exposure to An. funestus occurred indoors during late-night hours between 1 am and 2 am when most people were indoors and under bed nets. Outdoor exposure to An. funestus was slightly higher during the first half of the night between 8 pm and 10 pm when people were still outdoors, and during early morning hours between 4 am and 6 am. During the daytime, exposure to An. funestus occurred mostly indoors across most of the hours except during midday when outdoor exposure increased coincidentally with the biting pattern, peaking from 10 am to 12 pm (Fig. 7).

When accounting for location, the proportion of exposure to An. arabiensis and An. funestus bites occurring indoors (πi) for unprotected individuals was 0.652 for and 0.754 respectively, while for protected individuals or LLIN users (πi, p), the proportion of exposure occurring indoors for LLIN users (πi, p) was 0.229 and 0.271 respectively. When accounting for time, the proportion of exposure to An. arabiensis and An. funestus bites occurring in daylight for unprotected individuals was (πd) was 0.100 and 0.080 while for LLIN users, the proportion of exposure occurring during daylight (πd, p) was 0.154 and 0.207 respectively. For children under five years, the proportion of exposure occurring indoors (πi) was 0.689 for An. arabiensis and 0.815 for An. funestus while, the proportion of exposure occurring indoors for those protected by LLINs (πi, p) was 0.239 and 0.337 respectively. In terms of time, the proportion of exposure occurring during daylight (πd) was 0.097 for An. arabiensis and 0.082 for An. funestus while the proportion of exposure occurring during daylight for those protected by LLINs (πd, p) was 0.164 and 0.249 respectively (Table: 5)

Routine household activities within the peri-domestic area

During early night hours (18:00–10:00), most family members were indoors but outside their bed nets mainly resting, chatting outside bed nets, playing, and walking around and others were still outdoors engaged in almost the same activities as above. From 10:00 to 04:00, most people (adults and children) were indoors and under the protection of bed nets after which the proportion of people outdoors started to increase between 04:00 and 07:00. During broad daylight between 07:00 to 17:00, people were significantly present outdoors walking around, eating, resting under tree shades or verandas, and playing. Popular activities that kept people indoors during the daytime included chatting outside bed nets, resting after work playing, walking around, and eating (Figure: 7).

Table 5

Mosquito-Human Behavior Interactions
Variable	Exposure	An arabiensis	An. funestus
Exposure of all family members	Indoor exposure risk for individuals not using ITNs (πi)	0.65	0.75
	Indoor exposure risk for individuals using ITNs (πi,p)	0.23	0.27
	Daytime exposure risk for individuals not using ITNs (πd)	0.10	0.08
	Daytime exposure risk for individuals using ITNs (πd,p)	0.15	0.21
Exposure of children below school age	Indoor exposure risk for individuals not using ITN (πi)	0.69	0.82
	Indoor exposure risk for individuals using ITN (πi,p)	0.24	0.34
	Daytime exposure risk for individuals not using ITNs (πd)	0.10	0.08
	Daytime exposure risk for individuals using ITNs (πd,p)	0.16	0.24
Exposure of females Exposure of males	Indoor exposure risk for individuals not using ITN (πi)	0.51	0.41
	Indoor exposure risk for individuals using ITN (πi,p)	0.23	0.13
	Daytime exposure risk for individuals not using ITNs (πd)	0.17	0.10
	Daytime exposure risk for individuals using ITNs (πd,p)	0.16	0.12
	Indoor exposure risk for individuals not using ITN (πi)	0.52	0.41
	Indoor exposure risk for individuals using ITN (πi,p)	0.23	0.13
	Daytime exposure risk for individuals not using ITNs (πd)	0.16	0.10
	Daytime exposure risk for individuals using ITNs (πd,p)	0.16	0.12

Results of the community survey: sociodemographic of study participants

Of the 182 household representatives interviewed, 72.0% (n = 131) were females and 28.0% (n = 51) were males (Table 6). The largest age group was 25–34 years old, comprising (48.9% (n = 89) of the participants. Approximately 67.0% (n = 122) had completed primary education. The primary economic activity was crop production, involving 78.6% (n = 143) of the participants, with 48.9% (n = 89) having a minimum monthly income of at least 200,000 shillings. More than half of households had 4–6 occupants 58.2% (n = 106), and over 42.9% (n = 78) had at least two children, while 10.4% (n = 19) had pregnant women. Regarding malaria prevention, 57.1% (n = 104) of households had at least 1–2 bed nets, and 39.0% (n = 71) had 3–4 occupants sleeping under bed nets. Most houses were typically constructed with mud and grass thatched roofs 33.5% (n = 61), open eaves 77.5% (n = 141), and unscreened windows 73.6% (n = 134), while 46.2% (n = 84) of the walls had holes (Table 7).

Knowledge and perceptions about day-biting mosquitoes

Regarding awareness of day-biting mosquitoes, 135 (74.2%) of the representatives said they were aware and 94.8% (n = 128) of them admitted experiencing mosquito bites during daytime. Interestingly, only 28.9% (n = 39) of them knew that malaria could be transmitted by day-biting mosquitoes, while the majority 57.8% (n = 78) believed that day-biting mosquitoes were just common nuisance biters. Only 26.7% (n = 36) of the participants reported making any deliberate efforts to guard against day-biting mosquitoes. The bulk of biting was reported to occur during early morning hours between 07:00 and 09:00hrs 33.3% (n = 45), and late morning hours between 09:00 and 11:00hrs 23.7% (n = 32). Children under five years 28.9% (n = 39), mothers 25.9% (n = 35), and school children 20.7% (n = 28) were identified as the most at-risk groups. The main reason was that most of these people spent much of their daytime at home. Activities that kept most of them indoors during the daytime were sleeping 28.1% (n = 38), house chores 15.6% (n = 21), and resting after work 26.7% (n = 36), while activities like resting under tree shades 25.9% (n = 35), cooking 19.3% (n = 26), eating 25.2% (n = 34) and sharing stories kept them outdoors (Table 7).

A day in the respondent's life during wet and dry seasons

During the wet season, nearly half (49.6%, n = 67) of the respondents reported waking up between 05:00–06:00 am, and 41.5% (n = 56) reported waking up between 06:00–07:00 am. Major reasons for waking up early were mainly house chores (60.7%, n = 82), and eating breakfast (42%, n = xx) indoors, while outdoor activities included cooking breakfast (28.2%, n = 38) and cleaning the compound (31.1%, n = 42). Farming activities dominated the morning activities away from the peri-domestic spaces (81.5%, n = 110). Similarly, during the dry season, most of the respondents (46.7%, n = 63) reported waking up between 06:00–07:00 am. Reasons for waking up early included cooking breakfast (60.7%, n = 82), and cleaning the compound (37.0%, n = 50) indoors, while outdoor activities included cooking breakfast (24.0%, n = 32) and cleaning the compound (31.1%, n = 42).

Table 6

Sociodemographic characteristics of study participants
Variables	Overall (N = 182)
Sex of respondent
Female	131 (72.0%)
Male	51 (28.0%)
Age of household members
18–24	10 (5.5%)
25–34	89 (48.9%)
35–44	34 (18.7%)
45–54	24 (12.6%)
55–64	18 (9.9%)
65+	8 (4.4%)
Educational status of household members
Primary/lower	122 (67.0%)
Secondary	44 (24.2%)
University/college	16 (8.8%)
Occupation of the respondent
Retail business	9 (4.9%)
Crop production and livestock-keeping	16 (8.8%)
Crop production	143 (78.6%)
Livestock keeping	11 (6.0%)
Others	3 (1.6%)
Monthly income (Tanzania Shillings)
100,000	26 (14.3%)
200,000	89 (48.9%)
300000+	67 (36.8%)
Family size
1–3	46 (25.3%)
4–6	106 (58.2%)
6+	30 (16.5%)
Number of children under five years in the household
0	19 (10.4%)
1–2	78 (42.9%)
3–4	555(30.2%)
5+	30 (16.5%)
Pregnant women present
Yes	19 (10.4%)
No	163 (89.6%)

Table 7

House characteristics and interventions used
Variables	Overall (N = 182)
Number of bed nets present
1–2	104 (57.1%)
3–4	54 (29.7%)
5+	24 (13.2%)
Number of people sleep under a bed net
0	27 (14.8%)
1–2	51 (28.0%)
3–4	71 (39.0%)
5+	33 (18.1%)
Window status
Screened	48 (26.4%)
Unscreened	134 (73.6%)
House type
Plastered brick walls + metal sheet roof	2 (13.2%)
Unplastered brick walls + metal sheet roof	21 (11.5%)
Mud wall + metal sheet roof	33 (18.1%)
Plastered brick walls + grass thatched roof	8 (4.4%)
Unplastered brick walls + grass thatched roof	35 (19.2%)
Mud wall + grass thatched roof	61 (33.5%)
Door status
Closed	121 (65.4%)
Open	64 (34.8%)
Eave status
Closed	41 (22.5%)
Open	141 (77.5%)
Wall status
Holes absent	98 (54.8%)
Holes present	84 (46.2%)

Table 8

Knowledge and perceptions about day-biting mosquitoes
Variables	Percentages
Aware of day-biting mosquitoes (N = 182)
Yes	135 (74.2%)
No	35 (19.2%)
I don't know	12 (6.6%)
Experienced mosquito bites during daytime (N = 135)
Yes	128 (94.8%)
No	6 (4.4%)
I don't know	1 (0.4%)
Aware if malaria can be transmitted by day-biting mosquitoes (N = 135)
Yes	39 (28.9%)
No	78 (57.8%)
I don't know	18(13.3%)
Time of day mosquitoes bite (N = 135)
Early morning between 07:00–09:00 am	45 (33.3%)
Late mornings between 09:00–11:00 am	32(23.7%)
Midday between 11:00–02:00 pm	17 (12.6%)
Early evening between 02:00–04:00 pm	13 (9.6%)
Late evening between 04:00–07:00 pm	20 (14.8%)
I don’t know	8 (5.9%)
Make efforts to guard against day biting mosquitoes (N = 135)
Yes	36 (26.7%)
No	90 (66.7%)
I don’t know	9 (6.7%)
Family members always present at home during the daytime (N = 135)
Children 5 years and below	39 (28.9%)
School-aged children	28 (20.7%)
Elderly (65+) and disabled	7(5.2%)
Fathers	14 (10.4%)
Mothers	35 (25.9%)
Reasons for staying indoors (N = 135)
Sickness	11 (8.1%)
House chores	21 (15.6%)
Sleeping	38 (28.1)
Reading	7 (5.2%)
Resting after work	36 (26.7%)
Eating	9 (6.7%)
Other	3 (2.2%)
Reasons for staying outdoors (N = 135)
Extreme heat inside	11 (8.1%)
Cooking	26 (19.3%)
Sleeping	15 (11.1%)
Eating	34 (25.2%)
Resting under tree shade	35 (25.9%)
Sharing stories	9 (6.7%)
Other	5 (3.7%)

Current malaria prevention tools, notably ITNs and IRS, have yielded significant gains but remain challenged by numerous biological threats such as insecticide resistance and variations in vector behaviors [34, 65–69]. These interventions primarily target the nocturnal and indoor-biting behaviors of the major Afro-tropical malaria vectors, including An. gambiae sensu lato and An. funestus, which are the main vectors in Tanzania. These vectors are most active during the night when people are typically protected by ITNs. However, there is mounting evidence showing significant extended biting activity among these vectors, coinciding with periods when people are engaged in activities such as farming, fetching water, and other livelihood tasks, leaving them unprotected by ITNs [25, 43, 70–72]. One reason for the historical neglect of these biting patterns is the biases in traditional entomological survey methods, which typically overlook daytime mosquito activity [73, 74]. Since such atypical behaviors might reflect a broader risk spectrum and multiple potential protection gaps beyond the reach of ITNs, there is a need to investigate these patterns in different contexts. This study therefore investigated the 24-hour patterns of mosquito bites and human exposures, focusing on both the diurnal and nocturnal biting patterns of the malaria vectors in rural southeastern Tanzania.

Overall, the findings of this study suggest that while most of the biting activity of the two dominant malaria vectors, An. funestus and An. arabiensis remains at night, the risk of day-biting malaria vectors is not insignificant. This new paradigm challenges the current near-universal focus on nighttime interventions and underscores the need to address residual malaria transmission through enhanced vector control strategies that consider both diurnal and nocturnal biting patterns.

It was observed that nocturnal biting by An. arabiensis peaked between 7 pm and 11 pm, while An. funestus exhibited a delayed peak, being most active from 1 am to 3 am. These patterns have been observed in multiple studies before [25, 75–78], and An. arabiensis are in particular known to be very active in early evenings and early sessions of the night, often readily biting outdoors or indoors. This species is therefore less readily impacted by ITNs than the more endophilic, endophagic, and late-biting An. funestus [46, 79] The daytime host-seeking collections, from 6 am to 7 pm, accounted for 14–15% of the total host-seeking mosquitoes for both species. It was shown, however, that the daytime hourly pattern of the host-seeking females was only marginally different between these species, the observed differences being mostly due to the higher densities of An. funestus caught in this study. Notably, An. arabiensis displayed increased activity from 7 am to 11 am and a sharp rise in the early evening from 6 pm to 7 pm, whereas An. funestus showed smaller daytime peaks from 10 am to 12 pm. This daytime activity of major malaria vectors, though modest, aligns with human activities, indoors and outdoors, such as household chores, farming, and fetching water during which people are unprotected by ITNs. The findings are a piece of additional evidence to several recent findings of extended biting by malaria vectors in Africa [36, 80, 81]. In particular, they confirm the now seemingly ubiquitous patterns of An. funestus, the predominant vector in our study area, having extended morning to mid-morning biting activity [35, 36, 38, 82].

Analysis of indoor and outdoor biting rates also revealed significant differences between the species and between the nocturnal and diurnal time ranges. At night, just over half (54.5%) of An. arabiensis were caught outdoors, but this increased significantly to 80.4% indoors during the day. Similarly, An. funestus were primarily caught indoors both at night (57.1%) and during the day (69%). The greater percentages of indoor biting during the day are likely driven by temperature differences, with indoor areas being cooler than outdoors during the day. More importantly, these patterns suggest that while ITNs are effective in targeting indoor-biting mosquitoes at night, additional tools or approaches are needed to cover the fraction of biting that happens during the daytime indoors. The other main vector control tool, IRS is likely to continue being effective both day and night [31], most people do not use any personal protection against malaria vectors during the day. Moreover, the effectiveness of ITNs is absent during the day except in cases where the vectors remain fully susceptible, where community benefits arising from the mass mosquitocidal effects of ITNs might be impactful more [8, 10].

Another parameter examined was the physiological states and parity rates of the mosquitoes collected. A high proportion of unfed mosquitoes were found during the daytime, with more than 58% of day-biting and 72% of diurnal-biting mosquitoes being unfed. This likely reflects the host-seeking state at which the mosquitoes were collected during their diurnal and nocturnal activity cycles. The parity rates were generally high but were notably higher in daytime collections for An. arabiensis (82.57% indoors and 79.47% outdoors) compared to nighttime catches. For An. funestus, the parity rates were comparable between day and night. These high parity rates likely reflect the near absence of newly emerged unfed mosquitoes foraging indoors at these hours. More importantly, it suggests that many of these mosquitoes might had potentially been exposed to infective blood meals and survived more than one gonotrophic cycle, increasing the risk of malaria transmission. Indeed, higher parity rates are regularly reported for An. funestus compared to An. [33, 57–59], and in households far from aquatic habitats [84], but are more likely a result of our biased sampling design, which focused mostly in and around households. Additionally, Plasmodium-positive mosquitoes were detected in both day and night-time collections of An. arabiensis. These results imply that there is indeed an risk of malaria infections associated with these day-biting mosquitoes, irrespective of the small numbers collected during daytime and are in agreement with the results of a recent study from the Central African Republic [85].

Human behaviors and activities significantly contribute to exposure risk during different times of the day and night [25, 43, 86]. In this study, several activities, including farming, fetching water, and other livelihood tasks, were identified as having the potential to elevate the risk of mosquito bites during periods of high mosquito activity when people are not protected by ITNs. These findings correlate with previous observations in various settings, including East Africa [25, 43, 87], West Africa [64, 65], several other African settings [37, 72, 90], and the South Pacific [91]. This study showed overlaps between human activities and mosquitoes both indoors and outdoors, in the mornings and evenings. This overlap may contribute to significant human-vector contacts [72, 76, 89, 92, 93]. In the evenings, previous studies have reported multiple peri-domestic activities happening before people eventually go under their nets. These behaviors typically result in lower protective efficacy of ITNs, even in settings where ownership and use of ITNs are high [7, 37, 86, 94]. Unfortunately, community surveys also revealed a general lack of awareness about the risk posed by day-biting mosquitoes, which has implications for malaria prevention practices. Educating communities about the importance of protection during daytime activities and implementing strategies that extend protection beyond nighttime, such as daytime repellents or protective clothing, could therefore be critical in reducing malaria transmission.

The findings of this study highlight the limitations of current malaria control interventions that primarily target nocturnal and indoor-biting mosquitoes. The modest but significant daytime and outdoor biting activity observed necessitates a re-evaluation of vector control strategies to include measures that address mosquito activity throughout the entire 24-hour period. Compared to the 14.8% Anopheles biting observed in this study, earlier studies demonstrated that these fractions could reach 20–30% in some settings [23], further emphasizing the need to expand both the surveillance and control programs to include 24-hr cycles. Future research should investigate the full implications of this extended spectrum of biting on malaria risk in the villages and whether significant additional interventions are warranted. One way to address this is by careful re-evaluation of existing vector control tools. For example, while ITNs may be less effective on day-biting mosquitoes, IRS, by targeting resting mosquitoes at all times, can remain effective regardless of the biting patterns [95–97].

Indeed, a careful evaluation of the current interventions is essential for safeguarding at-risk populations and achieving the goal of malaria elimination, especially in regions with persistent transmission despite high ITN coverage. Integrating comprehensive entomological and human behavior data can inform more effective and responsive malaria control measures, ultimately enhancing the effectiveness of interventions and reducing the burden of malaria in endemic areas [25, 43, 86, 98] Interventions such as larval source management, which targets mosquitoes at their source could be highly effective as a complementary tool alongside ITNs and IRS [28]. Personal protection such as repellents or long-sleeved clothing and mosquito repellents are other options, although their consistent use in low-income settings might be low. Regarding ITNs, even though these are typically used at night, there is scope for ITNs or even untreated nets for young children and babies sleeping indoors during the day, as well as for any invalids or elderly people who spend most of their time indoors. Overall, the extended range of locations and times when biting exposure occurs highlights the need for interventions that can protect individuals both indoors and outdoors throughout the day, particularly in areas with high malaria transmission where outdoor activities are common

The study had several limitations that could potentially bias our findings. Firstly, it was conducted during the dry season, when adult Anopheles mosquito populations are typically low, and we could not estimate 24-hour patterns and malaria transmission risks during the wet season due to time and funding constraints. Moreover, in the dry season, people are more likely to spend time outdoors compared to the rainy season, which may likely have led to over-estimation of exposure to risk outdoors or underestimated exposure risk indoors Secondly, while molecular analysis was performed, it relied heavily on findings from previous studies in the region due to limited time and laboratory resources. Thirdly, for confidentiality, human behavior observations in the peri-domestic area were conducted in a subset of households with a literate volunteer, potentially missing observations in other households or when volunteers were unavailable. Finally, the study was limited to two villages, which may not represent the entire population or environment, restricting the generalizability of our findings.

We recommend comprehensive longitudinal studies with larger sample sizes to fully understand the role of day-biting in sustaining persistent malaria transmission and its implications for current vector control tools. Additionally, with increasing evidence of day-biting mosquitoes, it is recommended to include diurnal biting mosquitoes in routine entomological surveys to accurately estimate their contribution to persistent malaria transmission and inform the development and deployment of effective vector control interventions

This study provides important updates to our understanding of the biting patterns of the main malaria vectors, An. arabiensis and An. funestus, in rural southeastern Tanzania, highlighting substantial biting activity outside the protection of ITNs. While nocturnal biting remains predominant, with peaks from 7 pm to 11 pm for An. arabiensis and from 1 am to 3 am for An. funestus, this study has revealed considerable daytime biting activity, especially in the mornings and early evenings, coinciding with human activities. This broader biting spectrum suggests that current vector control strategies, which primarily target nocturnal behaviors, may be insufficient. The higher parity rates observed during daytime collections indicate the potential for significant malaria transmission risk during the day when people are not under ITNs. Therefore, complementary strategies are needed to holistically suppress vectors regardless of biting patterns, e.g. using larval source management or extend personal protection against mosquitoes active during these times, e.g. using repellents. Additionally, intensive health education and community engagement are crucial to raise awareness of the risks associated with daytime mosquito activity and to promote protective measures, ultimately contributing to more effective malaria control and elimination efforts. Finally, further studies are also required to better understand the extent of this extended biting and its implications for disease transmission and control.

Ethical considerations

Ethical clearance for this study was obtained from the Ifakara Health Institute Institutional Review Board (IHI/IRB/No.32-2023) and Medical Research Coordinating Committee (MRCC) at the National Institute for Medical Research Protocol ID: NIMR/HQ/R.8a/Vol.IX/3495). At the community level, permission to conduct the research activities within the selected villages was obtained from the local community leaders after explaining to them, the aim and procedures of the study. We also obtained separate written consent from heads of households selected for routine mosquito sampling and human behavior observations. The field mosquito collectors also provided written consent to participate in the study.

Acknowledgments

We thank village leaders and the local communities of Tulizamoyo and Minepa villages in Ulanga district for generously accepting to participate in this study. Our special thanks to Gerry. F. Killeen for his insights on how to calculate human exposure risk. We extend our sincere appreciation to Winnfrida Mponzi, Alex Limwagu, Frank M. Jackson, Dickson Msaky, Hereth Mahenge, Godfrey Katusi, Goodluck Malika, Rukiyah Mohammad, and the entire outdoor mosquito control (OMC) team at Ifakara Health Institute for their technical support and teamwork throughout the study period. We would like to express our heartfelt gratitude to our research assistants and the laboratory technicians, who spent sleepless nights recording human activities, conducting community interviews, collecting mosquitoes, and processing the samples. Last we convey our sincere appreciation to all fellow MSc Scholars of Public Health Research at Nelson Mandela African Institution of Science and Technology specifically, Ampuriire Patience, Amri S. Abas, Sperancia Coelestine, Fahad Mwakalebela, Aidi Lugenge, Allan Mtanga, Erick Killel, and Jelly Mseti for their support during the entire study period.

Funding

This work was supported in whole by the Bill & Melinda Gates Foundation [Grant No. INV-002138 and OPP1214408 awarded to Ifakara Health Institute]. Under the grant conditions of the Foundation, a Creative Commons Attribution 4.0 Generic License has already been assigned to the Author Accepted Manuscript version that might arise from this submission.

Availability of data and materials

The data supporting the findings of this study is available from the corresponding author upon receipt of official request.

Author contributions

Conceptualization CMM, FOO, BJM, HSN, and CN. CM and JJK carried out field data collection and laboratory procedures. CMM, YAM, and HSN conducted data analysis. CMM wrote the first draft and subsequent drafts of the manuscript with technical support from FOO, HSN, NFK, MFF, and BJM. CMM, HSN, and FOO wrote the final version of the manuscript. All authors have read, edited, and approved the published version of the manuscript

Consent for publication

Permission to publish this study was obtained from the National Institute for Medical Research, in Tanzania xxxxxx. Ref no.

Competing interests

The authors declare that they have no competing interests

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Analysis of the 24-Hour Biting Patterns and Human Exposures to Malaria Vectors in South-Eastern Tanzania

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Abstract

Background

Methods

Results

Conclusion

Figures

Background

Methods

Study area

Study design

Sampling and processing of adult mosquitoes

Observations of the behaviors and activities of household members in the peri-domestic area

Data analysis

Results

Mosquito catches indoors and outdoors during nighttime and daytime collections

24-Hr biting patterns of the main malaria vectors

Human exposure to mosquito bites indoors and outdoors

Routine household activities within the peri-domestic area

Results of the community survey: sociodemographic of study participants

Knowledge and perceptions about day-biting mosquitoes

A day in the respondent's life during wet and dry seasons

Discussion

Conclusions

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1