Attractive Toxic Sugar Baits (ATSB) are used in a “lure-and-kill” approach for management of the malaria vector Anopheles gambiae, but the active chemicals were previously unknown. Here we collected volatiles from a mango, Mangifera indica, juice bait which is used in ATSBs in Tanzania and tested mosquito responses. In a Y-tube olfactometer, female mosquitoes were attracted to the mango volatiles collected 24–48 h, 48–72 h and 72–96 h after preparing the bait but volatiles collected at 96–120 h were no longer attractive. Volatile analysis revealed emission of 23 compounds in different chemical classes including alcohols, aldehydes, alkanes, benzenoids, monoterpenes, sesquiterpenes and oxygenated terpenes. Coupled GC-electroantennogram (GC-EAG) recordings from the antennae of An. gambiae showed robust responses to 4 compounds: humulene, (E)-caryophyllene, terpinolene and myrcene. In olfactometer bioassays, mosquitoes were attracted to humulene and terpinolene. (E)-caryophyllene was marginally attractive while myrcene elicited an avoidance response with female mosquitoes. A blend of humulene, (E)-caryophyllene and terpinolene was highly attractive to females (P < 0.001) when tested against a solvent blank. Furthermore, there was no preference when this synthetic blend was offered as a choice against the natural sample. Our study has identified the key compounds from mango juice baits that attract An. gambiae and this information may help to improve the ATSBs currently used against malaria vectors.

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Behavioural and Electrophysiological Responses of Female Anopheles gambiae Mosquitoes to Volatiles from a Mango Bait

In an era of big data, the availability of satellite-derived global climate, terrain, and land cover imagery presents an opportunity for modeling the suitability of malaria disease vectors at fine spatial resolutions, across temporal scales, and over vast geographic extents. Leveraging cloud-based geospatial analytical tools, we present an environmental suitability model that considers water resources, flow accumulation areas, precipitation, temperature, vegetation, and land cover. In contrast to predictive models generated using spatially and temporally discontinuous mosquito presence information, this model provides continuous fine-spatial resolution information on the biophysical drivers of suitability. For the purposes of this study the model is parameterized for Anopheles gambiae s.s. in Malawi for the rainy (December–March) and dry seasons (April–November) in 2017; however, the model may be repurposed to accommodate different mosquito species, temporal periods, or geographical boundaries. Final products elucidate the drivers and potential habitat of Anopheles gambiae s.s. Rainy season results are presented by quartile of precipitation; Quartile four (Q4) identifies areas most likely to become inundated and shows 7.25% of Malawi exhibits suitable water conditions (water only) for Anopheles gambiae s.s., approximately 16% for water plus another factor, and 8.60% is maximally suitable, meeting suitability thresholds for water presence, terrain characteristics, and climatic conditions. Nearly 21% of Malawi is suitable for breeding based on land characteristics alone and 28.24% is suitable according to climate and land characteristics. Only 6.14% of the total land area is suboptimal. Dry season results show 25.07% of the total land area is suboptimal or unsuitable. Approximately 42% of Malawi is suitable based on land characteristics alone during the dry season, and 13.11% is suitable based on land plus another factor. Less than 2% meets suitability criteria for climate, water, and land criteria. Findings illustrate environmental drivers of suitability for malaria vectors, providing an opportunity for a more comprehensive approach to malaria control that includes not only modeled species distributions, but also the underlying drivers of suitability for a more effective approach to environmental management.

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Leveraging big data for public health: Mapping malaria vector suitability in Malawi with Google Earth Engine.

The field of mosquito chemical ecology has shifted focus over the past five years, driven by the recognition that odour-mediated behaviours are regulated by distinct chemical codes, that is, odour blends emanating from the natural environment. As a research community, we have shifted from our anthropocentric focus to include other behaviours, including plant seeking and oviposition site seeking, in order to develop new tools to combat residual malaria in the wake of the increased insecticide and behavioural resistance in mosquitoes across sub-Saharan Africa. In this short review, we will outline the progress made, and the future directions, in understanding blend recognition and chemical parsimony, and their implications for preadaptation of the odour coding system in malaria mosquitoes.

Malaria mosquito chemical ecology

Understanding the ecology of larval malaria and lymphatic filariasis mosquitoes in a changing environment is important in developing effective control tools or programmes This study characterized the breeding habitats of Anopheles mosquitoes in rural communities in different ecological zones in Ghana during the dry and rainy seasons The spatio-temporal distribution, species composition, and abundance of larval Anopheles mosquitoes in breeding habitats were studied in five locations in three ecological zones of Ghana These were Anyakpor (coastal savannah area), Duase (forest area), and Libga, Pagaza, and Kpalsogu (Sahel savannah area) Larvae were collected using standard dippers and were raised in the insectary for identification Out of a total of 7984 mosquito larvae collected, 2152 (2726%) were anophelines and were more abundant in the rainy season (7082%) than in the dry season (2918%) The anophelines comprised 2128 (9888%) An gambiae sl, 16 (074%) An rufipes, and 8 (037%) An pharoensis In the coastal savannah and forest zones, dug-out wells were the most productive habitat during the dry (159 larvae/dip and 147 larvae/dip) and rainy seasons (1128 larvae/dip and 205 larvae/dip) Swamps and furrows were the most productive habitats in the Sahel savannah zone during the dry (025 larvae/dip) and rainy (214 larvae/dip) seasons, respectively Anopheles coluzzii was the most abundant sibling species in all the ecological zones Anopheles melas and An arabiensis were encountered only in the coastal savannah and the Sahel savannah areas, respectively Larval habitat types influenced the presence of larvae as well as larval density (p < 0001) The land-use type affected the presence of Anopheles larvae (p = 0001), while vegetation cover influenced larval density (p < 005) The most productive habitats were dug-out wells in the coastal savannah and forest zones, and furrows from irrigated canals in the Sahel savannah zone Anopheles coluzzii was the predominant vector species in all the ecological zones The abundance of Anopheles breeding habitats and larvae were influenced by anthropogenic activities Encouraging people whose activities create the larval habitats to become involved in larval source management such as habitat manipulation to stop mosquito breeding will be important for malaria and lymphatic filariasis control

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Larval habitat diversity and Anopheles mosquito species distribution in different ecological zones in Ghana

Despite global intervention efforts, malaria remains a major public health concern in many parts of the world. Understanding geographic variation in malaria patterns and their environmental determinants can support targeting of malaria control and development of elimination strategies. We used remotely sensed environmental data to analyze the influences of environmental risk factors on malaria cases caused by Plasmodium falciparum and Plasmodium vivax from 2014 to 2017 in two geographic settings in Ethiopia. Geospatial datasets were derived from multiple sources and characterized climate, vegetation, land use, topography, and surface water. All data were summarized annually at the sub-district (kebele) level for each of the two study areas. We analyzed the associations between environmental data and malaria cases with Boosted Regression Tree (BRT) models. We found considerable spatial variation in malaria occurrence. Spectral indices related to land cover greenness (NDVI) and moisture (NDWI) showed negative associations with malaria, as the highest malaria rates were found in landscapes with low vegetation cover and moisture during the months that follow the rainy season. Climatic factors, including precipitation and land surface temperature, had positive associations with malaria. Settlement structure also played an important role, with different effects in the two study areas. Variables related to surface water, such as irrigated agriculture, wetlands, seasonally flooded waterbodies, and height above nearest drainage did not have strong influences on malaria. We found different relationships between malaria and environmental conditions in two geographically distinctive areas. These results emphasize that studies of malaria-environmental relationships and predictive models of malaria occurrence should be context specific to account for such differences.

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Remote sensing of environmental risk factors for malaria in different geographic contexts

Understanding the ecology of exophilic anophelines is a key step toward developing outdoor control strategies to complement existing indoor control tools against malaria vectors. This study was conducted to assess the movement pattern of exophilic Anopheles mosquitoes between blood meal sources and resting habitats, and the landscape factors dictating their resting habitat choice. Resting clay pots were placed at 5 m, 25 m, 50 m, 75 m and 100 m away from isolated focal houses, radiating from them in four directions. The locations of the clay pots represent heterogeneous land cover types at a relatively fine spatial scale in the landscape. The effect of the landscape characters on the number of both female and male anophelines caught was modelled using zero-inflated negative binomial regression with a log link function. A total of 420 Anopheles mosquitoes (353 females and 67 males) belonging to three species; Anopheles arabiensis, Anopheles pharoensis, and Anopheles tenebrosus were caught in the resting clay pots, with An. arabiensis being the dominant species. Canopy cover, distance from the house, and land cover type were the significant landscape characters influencing the aggregation of resting mosquitoes. Both the count and binary models showed that canopy cover was the strongest predictor variable on the counts and the presence of Anopheles mosquitoes in the clay pots. Female Anopheles were most frequently found resting in the pots placed in banana plantations, and at sampling points that were at the greater distances (75 m and 100 m) from the focal house. This study showed that exophilic Anopheles mosquitoes tend to rest in shaded areas some distance away from human habitation. These findings are important when targeting mosquitoes outdoors, complementing the existing effort being made to control malaria vectors indoors.

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Shady business: understanding the spatial ecology of exophilic Anopheles mosquitoes

Plasmodium parasites manipulate the interaction between their mosquito and human hosts. Patients infected with gametocytes attract anopheline mosquitoes differentially compared to healthy individuals, an effect associated with an increased release of attractive volatile cues. This odour-driven manipulation is partly mediated by the gametocyte-specific metabolite, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), which induces increased release of select aldehydes and terpenes from red blood cells and results in the enhanced attraction of host-seeking mosquitoes, which are vectors of malaria. This study investigates the effect of the HMBPP-induced volatiles on the attraction of wild Anopheles mosquitoes to humans under field conditions. The efficacy of the HMBPP-induced odour blend to attract Anopheles was evaluated in a 4 × 6 Latin rectangular study design indoors using baited Suna traps. Furthermore, to assess the efficacy of the HMBPP-induced odour blend in (1) augmenting the attractiveness of human odour, and (2) attracting Anopheles mosquitoes in the absence of human odour, a two-choice assay using host decoy traps (HDTs) was used and evaluated using binomial generalized regression. Traps baited with the HMBPP-induced odour blend attracted and caught both Anopheles arabiensis and Anopheles pharoensis females in a dose-dependent manner in the presence of background human odour, up to 2.5 times that of an unbaited trap. Given a choice between human odour and human odour laden with the HMBPP-induced odour blend, mosquitoes differentially preferred traps augmented with the HMBPP-induced odour blend, which caught twice as many female An. arabiensis. Traps baited with the HMBPP-induced odour blend but lacking the background of human odour were not effective in attracting and catching mosquitoes. The findings of the present study revealed that the HMBPP-induced odour blend, when augmented with human body odour, is attractive to anopheline mosquitoes and could be used as a complementary vector control tool along with existing strategies.

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Plasmodium falciparum gametocyte-induced volatiles enhance attraction of Anopheles mosquitoes in the field.

Hotspots constitute the major reservoir for residual malaria transmission, with higher malaria incidence than neighbouring areas, and therefore, have the potential to form the cornerstone for successful intervention strategies. Detection of malaria hotspots is hampered by their heterogenous spatial distribution, and the laborious nature and low sensitivity of the current methods used to assess transmission intensity. We adopt ecological theory underlying foraging in herbivorous insects to vector mosquito host seeking and modelling of fine-scale landscape features at the village level. The overall effect of environmental variables on the density of indoor mosquitoes, sporozoite infected mosquitoes, and malaria incidence, was determined using generalized linear models. Spatial analyses were used to identify hotspots for malaria incidence, as well as malaria vector density and associated sporozoite prevalence. We identify household occupancy and location as the main predictors of vector density, entomological inoculation rate and malaria incidence. We propose that the use of conventional vector control and malaria interventions, integrated with their intensified application targeting predicted hotspots, can be used to reduce malaria incidence in endemic and residual malaria settings.

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Malaria hotspots explained from the perspective of ecological theory underlying insect foraging

Odour-based tools targeting gravid malaria vectors may complement existing intervention strategies. Anopheles arabiensis are attracted to, and stimulated to oviposit by, natural and synthetic odours of wild and domesticated grasses associated with mosquito breeding sites. While such synthetic odour lures may be used for vector control, these may have limited efficacy when placed in direct competition with the natural source. In this study, workflows developed for plant-feeding pests was used to design and evaluate a chimeric odour blend based on shared attractive compounds found in domesticated grass odours. Variants of a synthetic odour blend, composed of shared bioactive compounds previously identified in domesticated grasses, was evaluated sequentially in a two-choice olfactometer to identify a ratio-optimized attractive blend for malaria vectors. During this process, blends with ratios that were significantly more attractive than the previously identified synthetic rice blend were compared to determine which was most attractive in the two-choice olfactometer. To determine whether all volatile components of the most attractive blend were necessary for maximal attraction, subtractive assays were then conducted, in which individual components were removed for the most attractive blend, to define the final composition of the chimeric blend. Binary logistic regression models were used to determine significance in all two-choice assays. The chimeric blend was then assessed under field conditions in malaria endemic villages in Ethiopia, to assess the effect of dose, trap type, and placement relative to ground level. Field data were analyzed both descriptively and using a Welch-corrected t-test. A ratio-optimized chimeric blend was identified that significantly attracted gravid An. arabiensis under laboratory conditions. In the field, trap captures of An. arabiensis and Anopheles pharoensis were dependent on the presence of the lure, trap type (CDC, BG Sentinel and Suna traps), placement relevant to ground level, with low release rates generally luring more mosquitoes. The workflow designed for the development of chimeric lures provides an innovative strategy to target odour-mediated behaviours. The chimeric lure identified here can be used in existing trapping systems, and be customized to increase sustainability, in line with goals of the Global Vector Control Response Group.

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Yared Debebe

Papers

Shady business: understanding the spatial ecology of exophilic Anopheles mosquitoes

Plasmodium falciparum gametocyte-induced volatiles enhance attraction of Anopheles mosquitoes in the field.

Malaria hotspots explained from the perspective of ecological theory underlying insect foraging

Development of a chimeric odour blend for attracting gravid malaria vectors.