Aspects of spatial and habitat ecology of multiple Anopheles species (Diptera: Culicidae): malaria vectors in the highlands and foothills of Ecuador

摘要

The resurgence of malaria in highland regions of Africa, Oceania and recently in SouthAmerica underlines the importance of the study of the ecology of highland mosquito vectors ofmalaria. Since the incidence of malaria is limited by the distribution of its vectors, the purpose ofthis PhD thesis was to examine aspects of the ecology of Anopheles mosquitoes in the Andes ofEcuador, South America. A historical literature and archival data review (Chapter 2) indicatedthat Anopheles pseudopunctipennis transmitted malaria in highland valleys of Ecuador prior to1950, although it was eliminated through habitat removal and the use of chemical insecticides.Other anopheline species were previously limited to low-altitude regions, except in a fewunconfirmed cases. A thorough larval collection effort (n=438 attempted collection sites) in allroad-accessible parts of Ecuador except for the lowland Amazon basin was undertaken between2008 - 2010 (Chapter 3). Larvae were identified morphologically and using molecular techniques(mitochondrial COl gene), and distribution maps indicated that all five species collected(Anopheles albimanus, An. pseudopunctipennis, Anopheles punctimacula, Anopheles oswaldois.l. and Anopheles eiseni) were more widespread throughout highland regions than previouslyrecorded during the 1940s, with higher maximum altitudes for all except An. pseudopunctipennis(1541 m, 1930 m, 1906 m, 1233 m and 1873 m, respectively). During larval collections, tocharacterize species-specific larval habitat, a variety of abiotic and biotic habitat parameters weremeasured and compared between species-present and species-absent sites using chi-square testsand stepwise binary logistic regression analyses (Chapter 4). An. albimanus was significantlyassociated with permanent pools with sand substrates and An. pseudopunctipennis with graveland boulder substrates. Both species were significantly associated with floating cyanobacterial mats and warmer temperatures, which may limit their presence in cooler highland regions.Anopheles punctimacula was collected more often than expected from algae-free, shaded poolswith higher-than-average calculated dissolved oxygen. Anopheles oswaldoi s.l., the speciesoccurring on the Amazonian side of the Andes, was associated with permanent, anthropogenichabitats such as roadside ditches and ponds. To address the hypothesis that human land usechange is responsible for the emergence of multiple highland Anopheles species by creatinglarval habitat, common land uses in the western Andes were surveyed for standing water andpotential larval habitat suitability (Chapter 5). Rivers and road edges provided large amounts ofpotentially suitable anopheline habitat in the western Andes, while cattle pasture also createdpotentially suitable habitat in irrigation canals and watering ponds. Other common land usessurveyed (banana farms, sugarcane plantations, mixed tree plantations, and empty lots) wereusually established on steep slopes and had very little standing water present. Using distributionand larval habitat data, a GIS-based larval habitat distribution model for the common westernspecies was constructed in ArcGIS v.l 0 (ESRI 2010) using derived data layers from fieldmeasurements and other sources (Chapter 6). The additive model predicted 76.4 - 97.9% of thefield-observed collection localities of An. albimanus, An. pseudopunctipennis and An.punctimacula, although it could not accurately distinguish between species-absent and speciespresentsites due to its coarse scale. The model predicted distributional expansion and/or shift ofone or more anopheline species into the following highland valleys with climate warming:Mira/Chota, Imbabura province, Tumbaco, Pichincha province, Pallatanga and Sibambe,Chimborazo province, and Yungilla, Azuay province. These valleys may serve as targeted sitesof future monitoring to prevent highland epidemics of malaria. The human perceptions ofmalaria and mosquitoes in relation to land management practices were assessed through an interview-based survey (n=262) in both highlands and lowlands, of male and female land ownersand managers of five property types (Chapter 7). Although respondents had a strongunderstanding of where the disease occurs in their own country and of the basic relationshipamong standing water, mosquitoes and malaria, about half of respondents in potential risk areasdenied the current possibility of malaria infection on their own property. As well, about half ofrespondents with potential anopheline larval habitat did not report its presence, likely due to ahighly specific definition of suitable mosquito habitat. Most respondents who are considered atrisk of malaria currently use at least one type of mosquito bite prevention, most commonly bednets. In conclusion, this interdisciplinary thesis examines the occurrence of Anopheles species inthe lowland transition area and highlands in Ecuador, from a historic, geographic, ecological andsociological perspective.