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      Establishment of a self-propagating population of the African malaria vector Anopheles arabiensis under semi-field conditions

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          Abstract

          Background

          The successful control of insect disease vectors relies on a thorough understanding of their ecology and behaviour. However, knowledge of the ecology of many human disease vectors lags behind that of agricultural pests. This is partially due to the paucity of experimental tools for investigating their ecology under natural conditions without risk of exposure to disease. Assessment of vector life-history and demographic traits under natural conditions has also been hindered by the inherent difficulty of sampling these seasonally and temporally varying populations with the limited range of currently available tools. Consequently much of our knowledge of vector biology comes from studies of laboratory colonies, which may not accurately represent the genetic and behavioural diversity of natural populations. Contained semi-field systems (SFS) have been proposed as more appropriate tools for the study of vector ecology. SFS are relatively large, netting-enclosed, mesocosms in which vectors can fly freely, feed on natural plant and vertebrate host sources, and access realistic resting and oviposition sites.

          Methods

          A self-replicating population of the malaria vector Anopheles arabiensis was established within a large field cage (21 × 9.1 × 7.1 m) at the Ifakara Health Institute, Tanzania that mimics the natural habitat features of the rural village environments where these vectors naturally occur. Offspring from wild females were used to establish this population whose life-history, behaviour and demography under semi-field conditions was monitored over 24 generations.

          Results

          This study reports the first successful establishment and maintenance of an African malaria vector population under SFS conditions for multiple generations (> 24). The host-seeking behaviour, time from blood feeding to oviposition, larval development, adult resting and swarming behaviour exhibited by An. arabiensis under SFS conditions were similar to those seen in nature.

          Conclusions

          This study presents proof-of-principle that populations of important African malaria vectors can be established within environmentally realistic, contained semi-field settings. Such SFS will be valuable tools for the experimental study of vector ecology and assessment of their short-term ecological and longer-term evolutionary responses to existing and new vector control interventions.

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          Most cited references65

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          Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction.

          A ribosomal DNA-polymerase chain reaction (PCR) method has been developed for species identification of individuals of the five most widespread members of the Anopheles gambiae complex, a group of morphologically indistinguishable sibling mosquito species that includes the major vectors of malaria in Africa. The method, which is based on species-specific nucleotide sequences in the ribosomal DNA intergenic spacers, may be used to identify both species and interspecies hybrids, regardless of life stage, using either extracted DNA or fragments of a specimen. Intact portions of a mosquito as small as an egg or the segment of one leg may be placed directly into the PCR mixture for amplification and analysis. The method uses a cocktail of five 20-base oligonucleotides to identify An. gambiae, An. arabiensis, An. quadriannnulatus, and either An. melas in western Africa or An. melas in eastern and southern Africa.
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            Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya

            Background High coverage of insecticide-treated bed nets in Asembo and low coverage in Seme, two adjacent communities in western Nyanza Province, Kenya; followed by expanded coverage of bed nets in Seme, as the Kenya national malaria programme rolled out; provided a natural experiment for quantification of changes in relative abundance of two primary malaria vectors in this holoendemic region. Both belong to the Anopheles gambiae sensu lato (s.l.) species complex, namely A. gambiae sensu stricto (s.s.) and Anopheles arabiensis. Historically, the former species was proportionately dominant in indoor resting collections of females. Methods Data of the relative abundance of adult A. gambiae s.s. and A. arabiensis sampled from inside houses were obtained from the literature from 1970 to 2002 for sites west of Kisumu, Kenya, to the region of Asembo ca. 50 km from the city. A sampling transect was established from Asembo (where bed net use was high due to presence of a managed bed net distribution programme) eastward to Seme, where no bed net programme was in place. Adults of A. gambiae s.l. were sampled from inside houses along the transect from 2003 to 2009, as were larvae from nearby aquatic habitats, providing data over a nearly 40 year period of the relative abundance of the two species. Relative proportions of A. gambiae s.s. and A. arabiensis were determined for each stage by identifying species by the polymerase chain reaction method. Household bed net ownership was measured with surveys during mosquito collections. Data of blood host choice, parity rate, and infection rate for Plasmodium falciparum in A. gambiae s.s. and A. arabiensis were obtained for a sample from Asembo and Seme from 2005. Results Anopheles gambiae s.s. adult females from indoor collections predominated from 1970 to 1998 (ca. 85%). Beginning in 1999, A. gambiae s.s decreased proportionately relative to A. arabiensis, then precipitously declined to rarity coincident with increased bed net ownership as national bed net distribution programmes commenced in 2004 and 2006. By 2009, A. gambiae s.s. comprised proportionately ca. 1% of indoor collections and A. arabiensis 99%. In Seme compared to Asembo in 2003, proportionately more larvae were A. gambiae s.s., larval density was higher, and more larval habitats were occupied. As bed net use rose in Seme, the proportion of A. gambiae larvae declined as well. These trends continued to 2009. Parity and malaria infection rates were lower in both species in Asembo (high bed net use) compared to Seme (low bed net use), but host choice did not vary within species in both communities (predominantly cattle for A. arabiensis, humans for A. gambiae s.s.). Conclusions A marked decline of the A. gambiae s.s. population occurred as household ownership of bed nets rose in a region of western Kenya over a 10 year period. The increased bed net coverage likely caused a mass effect on the composition of the A. gambiae s.l. species complex, resulting in the observed proportionate increase in A. arabiensis compared to its closely related sibling species, A. gambiae s.s. These observations are important in evaluating the process of regional malaria elimination, which requires sustained vector control as a primary intervention.
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              Mosquito sugar feeding and reproductive energetics.

              Sugar feeding is a fundamental characteristic of mosquito life. Most evidence indicates frequent ingestion by both sexes and all ages of mosquitoes of plant sugar, usually as floral and extrafloral nectar and honeydew. Energetically, sugar and blood are interchangeable; females of some species have evolved independence from one or the other, but most need blood to develop eggs and sugar to survive, to fly, and to enhance reproduction. Mosquitoes' commitment to sugar is further illustrated by a wealth of behavioral, structural, and physiological specializations for finding, feeding on, and processing it. Blood and sugar feeding activities are antagonistic and mutually exclusive, owing to conflicting demands, yet they support the same goals and often share the same activity period. The rules by which females make food-choice decisions have been inadequately explored, and we still lack convincing evidence that sugar availability in nature varies sufficiently to affect mosquito populations.
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                Author and article information

                Journal
                Malar J
                Malaria Journal
                BioMed Central
                1475-2875
                2010
                8 December 2010
                : 9
                : 356
                Affiliations
                [1 ]Biomedical and Environmental Thematic Group, Ifakara Health Institute, Box 53, Ifakara, Tanzania
                [2 ]Wageningen University and Research Centre, Wageningen, The Netherlands
                [3 ]Division of Infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, F4-217, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
                [4 ]K&S Consulting, Kalkestraat 20 6669 CP Dodewaard, The Netherlands
                [5 ]Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, G12 8QQ, Glasgow, UK
                Article
                1475-2875-9-356
                10.1186/1475-2875-9-356
                3017536
                21143870
                529fdf3d-81ab-4d91-9fa7-0a7758ec9dff
                Copyright ©2010 Ng'habi et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<url>http://creativecommons.org/licenses/by/2.0</url>), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 2 August 2010
                : 8 December 2010
                Categories
                Research

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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