Environmental factors associated with the malaria vectors Anopheles gambiae and Anopheles funestus in Kenya

<p>Abstract</p> <p>Background</p> <p>The <it>Anopheles gambiae </it>and <it>Anopheles funestus </it>mosquito species complexes are the primary vectors of <it>Plasmodium falciparum </it>malaria in sub-Saharan Africa. To better understand the environmental factors influencing these species, the abundance, distribution and transmission data from a south-eastern Kenyan study were retrospectively analysed, and the climate, vegetation and elevation data in key locations compared.</p> <p>Methods</p> <p>Thirty villages in Malindi, Kilifi and Kwale Districts with data on <it>An. gambiae sensu strict</it>, <it>Anopheles arabiensis</it> and <it>An. funestus</it> entomological inoculation rates (EIRs), were used as focal points for spatial and environmental analyses. Transmission patterns were examined for spatial autocorrelation using the Moran's <it>I </it>statistic, and for the clustering of high or low EIR values using the Getis-Ord Gi* statistic. Environmental data were derived from remote-sensed satellite sources of precipitation, temperature, specific humidity, Normalized Difference Vegetation Index (NDVI), and elevation. The relationship between transmission and environmental measures was examined using bivariate correlations, and by comparing environmental means between locations of high and low clustering using the Mann-Whitney <it>U </it>test.</p> <p>Results</p> <p>Spatial analyses indicated positive autocorrelation of <it>An. arabiensis </it>and <it>An. funestus </it>transmission, but not of <it>An. gambiae s.s</it>., which was found to be widespread across the study region. The spatial clustering of high EIR values for <it>An. arabiensis </it>was confined to the lowland areas of Malindi, and for <it>An. funestus </it>to the southern districts of Kilifi and Kwale. Overall, <it>An. gambiae s.s</it>. and <it>An. arabiensis </it>had similar spatial and environmental trends, with higher transmission associated with higher precipitation, but lower temperature, humidity and NDVI measures than those locations with lower transmission by these species and/or in locations where transmission by <it>An. funestus </it>was high. Statistical comparisons indicated that precipitation and temperatures were significantly different between the <it>An. arabiensis </it>and <it>An. funestus </it>high and low transmission locations.</p> <p>Conclusion</p> <p>These finding suggest that the abundance, distribution and malaria transmission of different malaria vectors are driven by different environmental factors. A better understanding of the specific ecological parameters of each malaria mosquito species will help define their current distributions, and how they may currently and prospectively be affected by climate change, interventions and other factors.</p

Anopheles larval abundance and diversity in three rice agro-village complexes Mwea irrigation scheme, central Kenya

<p>Abstract</p> <p>Background</p> <p>The diversity and abundance of <it>Anopheles </it>larvae has significant influence on the resulting adult mosquito population and hence the dynamics of malaria transmission. Studies were conducted to examine larval habitat dynamics and ecological factors affecting survivorship of aquatic stages of malaria vectors in three agro-ecological settings in Mwea, Kenya.</p> <p>Methods</p> <p>Three villages were selected based on rice husbandry and water management practices. Aquatic habitats in the 3 villages representing planned rice cultivation (Mbui Njeru), unplanned rice cultivation (Kiamachiri) and non-irrigated (Murinduko) agro-ecosystems were sampled every 2 weeks to generate stage-specific estimates of mosquito larval densities, relative abundance and diversity. Records of distance to the nearest homestead, vegetation coverage, surface debris, turbidity, habitat stability, habitat type, rice growth stage, number of rice tillers and percent <it>Azolla </it>cover were taken for each habitat.</p> <p>Results</p> <p>Captures of early, late instars and pupae accounted for 78.2%, 10.9% and 10.8% of the total <it>Anopheles </it>immatures sampled (n = 29,252), respectively. There were significant differences in larval abundance between 3 agro-ecosystems. The village with 'planned' rice cultivation had relatively lower <it>Anopheles </it>larval densities compared to the villages where 'unplanned' or non-irrigated. Similarly, species composition and richness was higher in the two villages with either 'unplanned' or limited rice cultivation, an indication of the importance of land use patterns on diversity of larval habitat types. Rice fields and associated canals were the most productive habitat types while water pools and puddles were important for short periods during the rainy season. Multiple logistic regression analysis showed that presence of other invertebrates, percentage <it>Azolla </it>cover, distance to nearest homestead, depth and water turbidity were the best predictors for <it>Anopheles </it>mosquito larval abundance.</p> <p>Conclusion</p> <p>These results suggest that agricultural practices have significant influence on mosquito species diversity and abundance and that certain habitat characteristics favor production of malaria vectors. These factors should be considered when implementing larval control strategies which should be targeted based on habitat productivity and water management.</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

Shading by Napier Grass Reduces Malaria Vector Larvae in Natural Habitats in Western Kenya Highlands

Increased human population in the Western Kenya highlands has led to reclamation of natural swamps resulting in the creation of habitats suitable for the breeding of Anopheles gambiae, the major malaria vector in the region. Here we report on a study to restore the reclaimed swamp and reverse its suitability as a habitat for malaria vectors. Napier grass-shaded and non-shaded water channels in reclaimed sites in Western Kenya highlands were studied for the presence and density of mosquito larvae, mosquito species composition, and daily variation in water temperature. Shading was associated with 75.5% and 88.4% (P < 0.0001) reduction in anopheline larvae densities and 78.1% and 88% (P < 0.0001) reduction in Anopheles gambiae sensu lato (s.l.) densities in two sites, respectively. Shading was associated with a 5.7°C, 5.0°C, and 4.7°C, and 1.6°C, 3.9°C, and 2.8°C (for maximum, minimum, and average temperatures, respectively) reduction (P < 0.0001) in water temperatures in the two locations, respectively. An. gambiae s.l. was the dominant species, constituting 83.2% and 73.1%, and 44.5% and 42.3%, of anophelines in non-shaded and shaded channels, respectively, in the two sites, respectively. An. gambiae sensu stricto (s.s.) constituted the majority (97.4%) of An. gambiae s.l., while the rest (2.6%) comprised of Anopheles arabiensis. Minimum water temperature decreased with increasing grass height (P = 0.0039 and P = 0.0415 for Lunyerere and Emutete sites, respectively). The results demonstrate how simple environmental strategies can have a strong impact on vector densities

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

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 x 9.1 x 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 (&gt; 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

The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis

<p>Abstract</p> <p>Background</p> <p>This is the second in a series of three articles documenting the geographical distribution of 41 dominant vector species (DVS) of human malaria. The first paper addressed the DVS of the Americas and the third will consider those of the Asian Pacific Region. Here, the DVS of Africa, Europe and the Middle East are discussed. The continent of Africa experiences the bulk of the global malaria burden due in part to the presence of the <it>An. gambiae </it>complex. <it>Anopheles gambiae </it>is one of four DVS within the <it>An. gambiae </it>complex, the others being <it>An. arabiensis </it>and the coastal <it>An. merus </it>and <it>An. melas</it>. There are a further three, highly anthropophilic DVS in Africa, <it>An. funestus</it>, <it>An. moucheti </it>and <it>An. nili</it>. Conversely, across Europe and the Middle East, malaria transmission is low and frequently absent, despite the presence of six DVS. To help control malaria in Africa and the Middle East, or to identify the risk of its re-emergence in Europe, the contemporary distribution and bionomics of the relevant DVS are needed.</p> <p>Results</p> <p>A contemporary database of occurrence data, compiled from the formal literature and other relevant resources, resulted in the collation of information for seven DVS from 44 countries in Africa containing 4234 geo-referenced, independent sites. In Europe and the Middle East, six DVS were identified from 2784 geo-referenced sites across 49 countries. These occurrence data were combined with expert opinion ranges and a suite of environmental and climatic variables of relevance to anopheline ecology to produce predictive distribution maps using the Boosted Regression Tree (BRT) method.</p> <p>Conclusions</p> <p>The predicted geographic extent for the following DVS (or species/suspected species complex*) is provided for Africa: <it>Anopheles </it>(<it>Cellia</it>) <it>arabiensis</it>, <it>An. </it>(<it>Cel.</it>) <it>funestus*</it>, <it>An. </it>(<it>Cel.</it>) <it>gambiae</it>, <it>An. </it>(<it>Cel.</it>) <it>melas</it>, <it>An. </it>(<it>Cel.</it>) <it>merus</it>, <it>An. </it>(<it>Cel.</it>) <it>moucheti </it>and <it>An. </it>(<it>Cel.</it>) <it>nili*</it>, and in the European and Middle Eastern Region: <it>An. </it>(<it>Anopheles</it>) <it>atroparvus</it>, <it>An. </it>(<it>Ano.</it>) <it>labranchiae</it>, <it>An. </it>(<it>Ano.</it>) <it>messeae</it>, <it>An. </it>(<it>Ano.</it>) <it>sacharovi</it>, <it>An. </it>(<it>Cel.</it>) <it>sergentii </it>and <it>An. </it>(<it>Cel.</it>) <it>superpictus*</it>. These maps are presented alongside a bionomics summary for each species relevant to its control.</p

Malaria in Africa: Vector Species' Niche Models and Relative Risk Maps

A central theoretical goal of epidemiology is the construction of spatial models of disease prevalence and risk, including maps for the potential spread of infectious disease. We provide three continent-wide maps representing the relative risk of malaria in Africa based on ecological niche models of vector species and risk analysis at a spatial resolution of 1 arc-minute (9 185 275 cells of approximately 4 sq km). Using a maximum entropy method we construct niche models for 10 malaria vector species based on species occurrence records since 1980, 19 climatic variables, altitude, and land cover data (in 14 classes). For seven vectors (Anopheles coustani, A. funestus, A. melas, A. merus, A. moucheti, A. nili, and A. paludis) these are the first published niche models. We predict that Central Africa has poor habitat for both A. arabiensis and A. gambiae, and that A. quadriannulatus and A. arabiensis have restricted habitats in Southern Africa as claimed by field experts in criticism of previous models. The results of the niche models are incorporated into three relative risk models which assume different ecological interactions between vector species. The “additive” model assumes no interaction; the “minimax” model assumes maximum relative risk due to any vector in a cell; and the “competitive exclusion” model assumes the relative risk that arises from the most suitable vector for a cell. All models include variable anthrophilicity of vectors and spatial variation in human population density. Relative risk maps are produced from these models. All models predict that human population density is the critical factor determining malaria risk. Our method of constructing relative risk maps is equally general. We discuss the limits of the relative risk maps reported here, and the additional data that are required for their improvement. The protocol developed here can be used for any other vector-borne disease

Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years

BACKGROUND: Over the past 20 years, numerous studies have investigated the ecology and behaviour of malaria vectors and Plasmodium falciparum malaria transmission on the coast of Kenya. Substantial progress has been made to control vector populations and reduce high malaria prevalence and severe disease. The goal of this paper was to examine trends over the past 20 years in Anopheles species composition, density, blood-feeding behaviour, and P. falciparum sporozoite transmission along the coast of Kenya. METHODS: Using data collected from 1990 to 2010, vector density, species composition, blood-feeding patterns, and malaria transmission intensity was examined along the Kenyan coast. Mosquitoes were identified to species, based on morphological characteristics and DNA extracted from Anopheles gambiae for amplification. Using negative binomial generalized estimating equations, mosquito abundance over the period were modelled while adjusting for season. A multiple logistic regression model was used to analyse the sporozoite rates. RESULTS: Results show that in some areas along the Kenyan coast, Anopheles arabiensis and Anopheles merus have replaced An. gambiae sensu stricto (s.s.) and Anopheles funestus as the major mosquito species. Further, there has been a shift from human to animal feeding for both An. gambiae sensu lato (s.l.) (99% to 16%) and An. funestus (100% to 3%), and P. falciparum sporozoite rates have significantly declined over the last 20 years, with the lowest sporozoite rates being observed in 2007 (0.19%) and 2008 (0.34%). There has been, on average, a significant reduction in the abundance of An. gambiae s.l. over the years (IRR = 0.94, 95% CI 0.90–0.98), with the density standing at low levels of an average 0.006 mosquitoes/house in the year 2010. CONCLUSION: Reductions in the densities of the major malaria vectors and a shift from human to animal feeding have contributed to the decreased burden of malaria along the Kenyan coast. Vector species composition remains heterogeneous but in many areas An. arabiensis has replaced An. gambiae as the major malaria vector. This has important implications for malaria epidemiology and control given that this vector predominately rests and feeds on humans outdoors. Strategies for vector control need to continue focusing on tools for protecting residents inside houses but additionally employ outdoor control tools because these are essential for further reducing the levels of malaria transmission

Quantifying Heterogeneity in Host-Vector Contact: Tsetse (Glossina swynnertoni and G. pallidipes) Host Choice in Serengeti National Park, Tanzania

Identifying hosts of blood-feeding insect vectors is crucial in understanding their role in disease transmission. Rhodesian human African trypanosomiasis (r-HAT or ‘sleeping sickness’) caused by Trypanosoma brucei rhodesiense and transmitted by tsetse flies, is commonly associated with wilderness areas of east and southern Africa. Such areas hold a diverse range of species which form communities of hosts for disease maintenance. The relative importance of different wildlife hosts remains unclear. This study quantified tsetse feeding preferences in a wilderness area of great host species richness, Serengeti National Park, Tanzania, assessing tsetse feeding and host density contemporaneously. Glossina swynnertoni and G.pallidipes were collected from six study sites. Bloodmeal sources were identified through matching Cytochrome B sequences amplified from bloodmeals from fed flies to published sequences. Densities of large mammal species in each site were quantified, and feeding indices calculated to assess the relative selection or avoidance of each host species by tsetse. The host species most commonly identified in G. swynnertoni bloodmeals, warthog (94/220), buffalo (48/220) and giraffe (46/220), were found at relatively low densities (3-11/km2) and fed on up to 15 times more frequently than expected by their relative density. Wildebeest, zebra, impala and Thomson’s gazelle, found at the highest densities, were never identified in bloodmeals. Commonly identified hosts for G. pallidipes were buffalo (26/46), giraffe (9/46) and elephant (5/46). This study is the first to quantify tsetse host range by molecular analysis of tsetse diet with simultaneous assessment of host density in a wilderness area. Although G.swynnertoni and G.pallidipes can feed on a range of species, they are highly selective. Many host species are rarely fed on, despite being present in areas where tsetse are abundant. These feeding patterns, along with the ability of key host species to maintain and transmit T.b.rhodesiense, drive the epidemiology of r-HAT in wilderness areas