Ecology: a prerequisite for malaria elimination and eradication

* Existing front-line vector control measures, such as insecticide-treated nets and residual sprays, cannot break the transmission cycle of Plasmodium falciparum in the most intensely endemic parts of Africa and the Pacific * The goal of malaria eradication will require urgent strategic investment into understanding the ecology and evolution of the mosquito vectors that transmit malaria * Priority areas will include understanding aspects of the mosquito life cycle beyond the blood feeding processes which directly mediate malaria transmission * Global commitment to malaria eradication necessitates a corresponding long-term commitment to vector ecolog

The impact of low erythrocyte density in human blood on the fitness and energetic reserves of the African malaria vector Anopheles gambiae

Background Anaemia is a common health problem in the developing world. This condition is characterized by a reduction in erythrocyte density, primarily from malnutrition and/or infectious diseases such as malaria. As red blood cells are the primary source of protein for haematophagous mosquitoes, any reduction could impede the ability of mosquito vectors to transmit malaria by influencing their fitness or that of the parasites they transmit. The aim of this study was to determine the impact of differences in the density of red blood cells in human blood on malaria vector (Anopheles gambiae sensu stricto) fitness. The hypotheses tested are that mosquito vector energetic reserves and fitness are negatively influenced by reductions in the red cell density of host human blood meals commensurate with those expected from severe anaemia. Methods Mosquitoes (An. gambiae s.s.) were offered blood meals of different packed cell volume(PCV) of human blood consistent with those arising from severe anaemia (15%) and normalPCV (50%). Associations between mosquito energetic reserves (lipid, glucose and glycogen)and fitness measures (reproduction and survival) and blood meal PCV were investigated. Results The amount of protein that malaria vectors acquired from blood feeding (indexed by haematin excretion) was significantly reduced at low blood PCV. However, mosquitoes feeding on blood of low PCV had the same oviposition rates as those feeding on blood of normal PCV, and showed an increase in egg production of around 15%. The long-term survival of An. gambiae s.s was reduced after feeding on low PCV blood, but PCV had no significant impact on the proportion of mosquitoes surviving through the minimal period required to develop and transmit malaria parasites (estimated as 14 days post-blood feeding). The impact of blood PCV on the energetic reserves of mosquitoes was relatively minor. Conclusions These results suggest that feeding on human hosts whose PCV has been depleted due to severe anaemia does not significantly reduce the fitness or transmission potential of malaria vectors, and indicates that mosquitoes may be able exploit resources for reproduction more efficiently from blood of low rather than normal PCV

Larval habitats of Anopheles gambiae s.s. (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites

<p>Abstract</p> <p>Background</p> <p>The origin of highly competent malaria vectors has been linked to productive larval habitats in the field, but there isn't solid quantitative or qualitative data to support it. To test this, the effect of larval habitat soil substrates on larval development time, pupation rates and vector competence of <it>Anopheles gambiae </it>to <it>Plasmodium falciparum </it>were examined.</p> <p>Methods</p> <p>Soils were collected from active larval habitats with sandy and clay substrates from field sites and their total organic matter estimated. <it>An. gambiae </it>larvae were reared on these soil substrates and the larval development time and pupation rates monitored. The emerging adult mosquitoes were then artificially fed blood with infectious <it>P. falciparum </it>gametocytes from human volunteers and their midguts examined for oocyst infection after seven days. The wing sizes of the mosquitoes were also measured. The effect of autoclaving the soil substrates was also evaluated.</p> <p>Results</p> <p>The total organic matter was significantly different between clay and sandy soils after autoclaving (P = 0.022). A generalized liner model (GLM) analysis identified habitat type (clay soil, sandy soil, or lake water) and autoclaving (that reduces presence of microbes) as significant factors affecting larval development time and oocyst infection intensities in adults. Autoclaving the soils resulted in the production of significantly smaller sized mosquitoes (P = 0.008). Autoclaving clay soils resulted in a significant reduction in <it>Plasmodium falciparum </it>oocyst intensities (P = 0.041) in clay soils (unautoclaved clay soils (4.28 ± 0.18 oocysts/midgut; autoclaved clay soils = 1.17 ± 0.55 oocysts/midgut) although no difference (P = 0.480) in infection rates was observed between clay soils (10.4%), sandy soils (5.3%) or lake water (7.9%).</p> <p>Conclusion</p> <p>This study suggests an important nutritional role for organic matter and microbial fauna on mosquito fitness and vector competence. It shows that the quality of natural aquatic habitats of mosquito larvae may influence malaria parasite transmission potential by <it>An. gambiae</it>. This information can be important in targeting larval habitats for malaria control.</p

Towards a sterile insect technique field release of Anopheles arabiensis mosquitoes in Sudan: Irradiation, transportation, and field cage experimentation

<p>Abstract</p> <p>Background</p> <p>The work described in this article forms part of a study to suppress a population of the malaria vector <it>Anopheles arabiensis </it>in Northern State, Sudan, with the Sterile Insect Technique. No data have previously been collected on the irradiation and transportation of anopheline mosquitoes in Africa, and the first series of attempts to do this in Sudan are reported here. In addition, experiments in a large field cage under near-natural conditions are described.</p> <p>Methods</p> <p>Mosquitoes were irradiated in Khartoum and transported as adults by air to the field site earmarked for future releases (400 km from the laboratory). The field cage was prepared for experiments by creating resting sites with favourable conditions. The mating and survival of (irradiated) laboratory males and field-collected males was studied in the field cage, and two small-scale competition experiments were performed.</p> <p>Results</p> <p>Minor problems were experienced with the irradiation of insects, mostly associated with the absence of a rearing facility in close proximity to the irradiation source. The small-scale transportation of adult mosquitoes to the release site resulted in minimal mortality (< 6%). Experiments in the field cage showed that mating occurred in high frequencies (i.e. an average of 60% insemination of females after one or two nights of mating), and laboratory reared males (i.e. sixty generations) were able to inseminate wild females at rates comparable to wild males. Based on wing length data, there was no size preference of males for mates. Survival of mosquitoes from the cage, based on recapture after mating, was satisfactory and approximately 60% of the insects were recaptured after one night. Only limited information on male competitiveness was obtained due to problems associated with individual egg laying of small numbers of wild females.</p> <p>Conclusion</p> <p>It is concluded that although conditions are challenging, there are no major obstacles associated with the small-scale irradiation and transportation of insects in the current setting. The field cage is suitable for experiments and studies to test the competitiveness of irradiated males can be pursued. The scaling up of procedures to accommodate much larger numbers of insects needed for a release is the next challenge and recommendations to further implementation of this genetic control strategy are presented.</p

Malaria mosquito control using edible fish in western Kenya: preliminary findings of a controlled study

<p>Abstract</p> <p>Background</p> <p>Biological control methods are once again being given much research focus for malaria vector control. This is largely due to the emerging threat of strong resistance to pesticides. Larvivorous fish have been used for over 100 years in mosquito control and many species have proved effective. In the western Kenyan highlands the larvivorous fish <it>Oreochromis niloticus </it>L. (Perciformes: Cichlidae) (formerly <it>Tilapia nilotica</it>) is commonly farmed and eaten but has not been previously tested in the field for malaria mosquito control.</p> <p>Methods</p> <p>This fish was introduced into abandoned fishponds at an altitude of 1,880 m and the effect measured over six months on the numbers of mosquito immatures. For comparison an untreated control pond was used. During this time, all ponds were regularly cleared of emergent vegetation and fish re-stocking was not needed. Significant autocorrelation was removed from the time series data, and t-tests were used to investigate within a pond and within a mosquito type any differences before and after the introduction of <it>O. niloticus</it>. Mulla's formula was also used on the raw data to calculate the percentage reduction of the mosquito larvae.</p> <p>Results</p> <p>After <it>O. niloticus </it>introduction, mosquito densities immediately dropped in the treated ponds but increased in the control pond. This increase was apparently due to climatic factors. Mulla's formula was applied which corrects for that natural tendency to increase. The results showed that after 15 weeks the fish caused a more than 94% reduction in both <it>Anopheles gambiae s.l</it>. and <it>Anopheles funestus </it>(Diptera: Culicidae) in the treated ponds, and more than 75% reduction in culicine mosquitoes. There was a highly significantly reduction in <it>A. gambiae s.l</it>. numbers when compared to pre-treatment levels.</p> <p>Conclusion</p> <p>This study reports the first field trial data on <it>O. niloticus </it>for malaria mosquito control and shows that this species, already a popular food fish in western Kenya, is an apparently sustainable mosquito control tool which also offers a source of protein and income to people in rural areas. There should be no problem with acceptance of this malaria control method since the local communities already farm this fish species.</p

Modelling the impact of vector control interventions on Anopheles gambiae population dynamics

<p>Abstract</p> <p>Background</p> <p>Intensive anti-malaria campaigns targeting the <it>Anopheles </it>population have demonstrated substantial reductions in adult mosquito density. Understanding the population dynamics of <it>Anopheles </it>mosquitoes throughout their whole lifecycle is important to assess the likely impact of vector control interventions alone and in combination as well as to aid the design of novel interventions.</p> <p>Methods</p> <p>An ecological model of <it>Anopheles gambiae sensu lato </it>populations incorporating a rainfall-dependent carrying capacity and density-dependent regulation of mosquito larvae in breeding sites is developed. The model is fitted to adult mosquito catch and rainfall data from 8 villages in the Garki District of Nigeria (the 'Garki Project') using Bayesian Markov Chain Monte Carlo methods and prior estimates of parameters derived from the literature. The model is used to compare the impact of vector control interventions directed against adult mosquito stages - long-lasting insecticide treated nets (LLIN), indoor residual spraying (IRS) - and directed against aquatic mosquito stages, alone and in combination on adult mosquito density.</p> <p>Results</p> <p>A model in which density-dependent regulation occurs in the larval stages via a linear association between larval density and larval death rates provided a good fit to seasonal adult mosquito catches. The effective mosquito reproduction number in the presence of density-dependent regulation is dependent on seasonal rainfall patterns and peaks at the start of the rainy season. In addition to killing adult mosquitoes during the extrinsic incubation period, LLINs and IRS also result in less eggs being oviposited in breeding sites leading to further reductions in adult mosquito density. Combining interventions such as the application of larvicidal or pupacidal agents that target the aquatic stages of the mosquito lifecycle with LLINs or IRS can lead to substantial reductions in adult mosquito density.</p> <p>Conclusions</p> <p>Density-dependent regulation of anopheline larvae in breeding sites ensures robust, stable mosquito populations that can persist in the face of intensive vector control interventions. Selecting combinations of interventions that target different stages in the vector's lifecycle will result in maximum reductions in mosquito density.</p

Effects of co-habitation between Anopheles gambiae s.s. and Culex quinquefasciatus aquatic stages on life history traits

<p>Abstract</p> <p>Background</p> <p>The effective measures for the control of malaria and filariasis vectors can be achieved by targeting immature stages of anopheline and culicine mosquitoes in productive habitat. To design this strategy, the mechanisms (like biotic interactions with conspecifc and heterospecific larvae) regulating mosquito aquatic stages survivorship, development time and the size of emerging adults should be understood. This study explored the effect of co-habitation between <it>An. gambiae </it>s.s. and <it>Cx. quinquefasciatus </it>on different life history traits of both species under different densities and constant food supply in the habitats of the same size under semi-natural conditions.</p> <p>Methods</p> <p>Experiments were set up with three combinations; <it>Cx. quinquefasciatus </it>alone (single species treatment), <it>An. gambiae </it>s.s. alone (single species treatment); and <it>An. gambiae </it>s.s. with <it>Cx. quiquefasciatus </it>(co-habitation treatment) in different densities in semi field situation.</p> <p>Results</p> <p>The effect of co-habitation of <it>An. gambiae </it>s.s. and <it>Cx. quinquefasciatus </it>was found to principally affect three parameters. The wing-lengths (a proxy measure of body size) of <it>An. gambiae </it>s.s. in co-habitation treatments were significantly shorter in both females and males than in <it>An. gambiae </it>s.s single species treatments. In <it>Cx. quinquefasciatus</it>, no significant differences in wing-length were observed between the single species and co-habitation treatments. Daily survival rates were not significantly different between co-habitation and single species treatments for both <it>An. gambiae </it>s.s. and <it>Cx. quinquefasciatus</it>. Developmental time was found to be significantly different with single species treatments developing better than co-habitation treatments. Sex ratio was found to be significantly different from the proportion of 0.5 among single and co-habitation treatments species at different densities. Single species treatments had more males than females emerging while in co-habitation treatments more females emerged than males. In this study, there was no significant competitive survival advantage in co-habitation.</p> <p>Conclusion</p> <p>These results suggest that co-habitation of <it>An. gambiae </it>s.s. and <it>Cx. quinquefasciatus </it>in semi-natural conditions affect mostly <it>An. gambiae </it>s.s. body size. Hence, more has to be understood on the effects of co-habitation of <it>An. gambiae </it>s.s. and <it>Cx. quinquefasciatus </it>in a natural ecology and its possible consequences in malaria and filariasis epidemiology.</p

The transmission potential of malaria-infected mosquitoes (An.gambiae-Keele, An.arabiensis-Ifakara) is altered by the vertebrate blood type they consume during parasite development

The efficiency of malaria parasite development within mosquito vectors (sporogony) is a critical determinant of transmission. Sporogony is thought to be controlled by environmental conditions and mosquito/parasite genetic factors, with minimal contribution from mosquito behaviour during the period of parasite development. We tested this assumption by investigating whether successful sporogony of Plasmodium falciparum parasites through to human-infectious transmission stages is influenced by the host species upon which infected mosquitoes feed. Studies were conducted on two major African vector species that generally are found to differ in their innate host preferences: Anopheles arabiensis and An. gambiae sensu stricto. We show that the proportion of vectors developing transmissible infections (sporozoites) was influenced by the source of host blood consumed during sporogony. The direction of this effect was associated with the innate host preference of vectors: higher sporozoite prevalences were generated in the usually human-specialist An. gambiae s.s. feeding on human compared to cow blood, whereas the more zoophilic An. arabiensis had significantly higher prevalences after feeding on cow blood. The potential epidemiological implications of these results are discussed