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      Sweet attraction: sugarcane pollen-associated volatiles attract gravid Anopheles arabiensis

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          Abstract

          Background

          Anopheles arabiensis is a key vector for the transmission of human malaria in sub-Saharan Africa. Over the past 10,000 years, humans have successfully cultivated grasses and altered the landscape, creating An. arabiensis favourable environments that contain excellent habitats for both larvae and adults. Sugarcane is the most expanding agricultural system in sub-Saharan Africa, and is linked to the increased threat of malaria in rural communities. The prolific production and wind dispersal of sugarcane pollen, together with standing pools of water, often provide, as a result of irrigation, a nutrient-rich environment for the offspring of gravid malaria mosquitoes.

          Results

          In the present study, sugarcane pollen-associated volatiles from two cultivars are shown to attract gravid An. arabiensis in a still air two-port olfactometer and stimulate egg laying in an oviposition bioassay. Through combined gas chromatography and electroantennographic detection, as well as combined gas chromatography and mass spectrometric analyses, we identified the bioactive volatiles and generated a synthetic blend that reproduced the full behavioural repertoire of gravid mosquitoes in the Y-tube assay. Two subtractive odour blends, when compared with the full blend, were significantly more attractive. These three and four-component subtractive blends share the compounds ( 1R)-(+)-α-pinene, nonanal and benzaldehyde, of which, ( 1R)-(+)-α-pinene and nonanal are found in the attractive odour blends from rice plants and maize pollen. In pairwise comparisons, the rice synthetic odour blend was more attractive to gravid mosquitoes than either of the pollen blends, whereas the pollen blends did not differ in attraction.

          Conclusions

          The attraction of gravid females to sugarcane pollen volatiles demonstrated in this study, together with the previously found grass-associated volatiles, raise the potential of developing a bioactive chimeric blend to attract gravid malaria mosquitoes. This is discussed in relation to the development of novel and cost-effective vector control measures.

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          Most cited references31

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          The practical importance of permanent and semipermanent habitats for controlling aquatic stages of Anopheles gambiae sensu lato mosquitoes: operational observations from a rural town in western Kenya.

          Control of aquatic-stage Anopheles is one of the oldest and most historically successful interventions to prevent malaria, but it has seen little application in Africa. Consequently, the ecology of immature afrotropical Anopheles has received insufficient attention. We therefore examined the population dynamics of African anopheline and culicine mosquitoes using operationally practicable techniques to examine the relative importance and availability of different larval habitats in an area of perennial malaria transmission in preparation for a pilot-scale larval control programme. The study was conducted in Mbita, a rural town on the shores of Lake Victoria in Western Kenya, over 20 months. Weekly larval surveys were conducted to identify the availability of stagnant water, habitat characteristics and larval densities. Adult mosquitoes were collected indoors at fortnightly intervals. Availability of aquatic habitats and abundance of mosquito larvae were directly correlated with rainfall. Adult mosquito densities followed similar patterns but with a time-lag of approximately 1 month. About 70% of all available habitats were man-made, half of them representing cement-lined pits. On average, 67% of all aquatic habitats on a given sampling date were colonized by Anopheles larvae, of which all identified morphologically were A. gambiae sensu lato. Natural and artificial habitats were equally productive over the study period and larval densities were positively correlated with presence of tufts of low vegetation and negatively with non-matted algal content. The permanence of a habitat had no significant influence on larval productivity. We conclude that A. gambiae is broadly distributed across a variety of habitat types, regardless of permanence. All potential breeding sites need to be considered as sources of malaria risk at any time of the year and exhaustively targeted in any larval control intervention.
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            Habitat characteristics of Anopheles gambiae s.s. larvae in a Kenyan highland.

            Anopheline larval habitats associated with a swamp, were examined in a highland area (1910 m elevation) of western Kenya. A significant association was found between occurrence of Anopheles gambiae Giles s.s. (Diptera: Culicidae) larvae and two factors, habitat size and vegetation type. Over 80% of An. gambiae s.s. larvae were found in small isolated pools, characterized by short plants, occurring in both swamp margins and roadside ditches. However, Anopheles gambiae s.s. was not found in habitats marked by papyrus and floating plants. The larval habitat of An. gambiae s.s. was characterized by warmer daytime temperatures of water, which were significantly affected by habitat size and plant size. The density of indoor resting An. gambiae s.s. was 0.22 per house and negatively associated with distance from the swamp. These results indicate that the practice of swamp cultivation, in populated areas of the African highlands, increases availability and enhances habitat conditions for the malaria vector.
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              Identifying the most productive breeding sites for malaria mosquitoes in The Gambia

              Background Ideally larval control activities should be targeted at sites that generate the most adult vectors, thereby reducing operational costs. Despite the plethora of potential mosquito breeding sites found in the floodplains of the Gambia River, about 150 km from its mouth, during the rainy season, only a small proportion are colonized by anophelines on any day. This study aimed to determine the characteristics of larval habitats most frequently and most densely populated by anopheline larvae and to estimate the numbers of adults produced in different habitats. Methods A case-control design was used to identify characteristics of sites with or without mosquitoes. Sites were surveyed for their physical water properties and invertebrate fauna. The characteristics of 83 sites with anopheline larvae (cases) and 75 sites without (controls) were collected between June and November 2005. Weekly adult productivity was estimated with emergence traps in water-bodies commonly containing larvae. Results The presence of anopheline larvae was associated with high invertebrate diversity (Odds Ratio, OR 11.69, 95% CI 5.61–24.34, p < 0.001), the presence of emergent vegetation (OR 2.83, 95% CI 1.35–5.95, p = 0.006), and algae (at borderline significance; OR 1.87, 95% CI 0.96–3.618, p = 0.065). The density of larvae was reduced in sites that were larger than 100 m in perimeter (OR 0.151; 95% CI 0.060–0.381, p < 0.001), where water was tidal (OR 0.232; 95% CI 0.101–0.533, p = 0.001), vegetation shaded over 25% of the habitat (OR 0.352; 95% CI 0.136–0.911, p = 0.031) and water conductivity was above 2,000 μS/cm (OR 0.458; 95% CI 0.220–0.990, p = 0.048). Pools produced the highest numbers of Anopheles gambiae adults compared with rice fields, floodwater areas close to the edge of the floodplain or close to the river, and stream fringes. Pools were characterized by high water temperature and turbidity, low conductivity, increased presence of algae, and absence of tidal water. Conclusion There are few breeding sites that produce a high number of adult vectors in the middle reaches of the river in The Gambia, whereas those with low productivity are larger in area and can be found throughout the rainy season. Even though risk factors could be identified for the presence and density of larvae and productivity of habitats, the results indicate that anti-larval interventions in this area of The Gambia cannot be targeted in space or time during the rainy season.
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                Author and article information

                Contributors
                sharon.hill@slu.se
                Journal
                Malar J
                Malar. J
                Malaria Journal
                BioMed Central (London )
                1475-2875
                21 February 2018
                21 February 2018
                2018
                : 17
                : 90
                Affiliations
                [1 ]ISNI 0000 0001 1250 5688, GRID grid.7123.7, Department of Zoological Sciences, , Addis Ababa University, ; Box 1176, Addis Ababa, Ethiopia
                [2 ]ISNI 0000 0000 8578 2742, GRID grid.6341.0, Disease Vector Group, Department of Plant Protection Biology, , Swedish University of Agricultural Sciences, ; Box 102, Sundsvägen 14, 230 53 Alnarp, Sweden
                [3 ]ISNI 0000 0004 1794 5158, GRID grid.419326.b, Behavioural and Chemical Ecology Department, , International Centre of Insect Physiology and Ecology, ; P. O. Box 30772, Nairobi, 00100 Kenya
                Author information
                http://orcid.org/0000-0002-6474-0214
                Article
                2245
                10.1186/s12936-018-2245-1
                5822481
                29466989
                cece548d-9ef2-4e08-80f8-c752e08ec491
                © The Author(s) 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 10 September 2017
                : 18 February 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100004441, Styrelsen för Internationellt Utvecklingssamarbete;
                Funded by: Organisation of Women in Science for the Developing World
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Infectious disease & Microbiology
                mosquitoes,attraction,stimulation,cultivars,pollen volatiles,gravid,oviposition

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