Although An. funestus are among the most important vectors of malaria in Africa, little is known regarding their larval ecology and development. This crucial gap needs an urgent solution, but is perpetuated by the inability of most mosquito biologists to create laboratory colonies of this vector species. Understanding the basic environmental parameters that influence mosquitoes breeding and oviposition can improve the planning, development and deployment of new interventions to control malaria transmission [27]. This study identified and characterized larval habitats of An. funestus in south-eastern Tanzanian villages of Ulanga and Kilombero districts, where this mosquito species now mediates more than four fifths of ongoing malaria infections [4, 6].
The study examined more than 100 potential habitats across six villages, and identified three main habitat types. First were small water wells with well-defined edges and were spring fed, some of which were also used by locals as domestic water sources (Fig. 4b). These habitats were often occupied by multiple species of the An. funestus group, and in some cases, they were shaded by large trees. The second type of habitat was medium-sized ponds, for which the central part retained water for all or most of the year. These habitats often had surface vegetation (Fig. 4a) and were occupied by multiple other Anopheles species such as An. arabiensis. Third was the riverside habitats consisting of the slow-moving waters on the rivers or river tributaries, also with vegetation (Fig. 4c). These habitats were mostly found at altitudes above 400 m above sea level, unlike the other two habitats which were more common at lower altitudes below 300 m. In summary, An. funestus in this area appears to prefer permanent and semi-permanent aquatic habitats with stagnant or slow-moving waters, emergent vegetation e.g. algae on swamp surfaces, clear waters at depths exceeding 50 cm and nearness to human dwellings.
Recent entomological surveys have demonstrated that the lower altitude areas have higher An. arabiensis densities than An. funestus while the higher altitude areas have more An. funestus than An. arabiensis [5, 6, 28–30]. However, it has also been shown that An. funestus dominates malaria transmission across the valley in both the areas where its densities are lower and areas where its densities are higher than those of An. arabiensis [4, 6]. A separate epidemiological survey of human malaria infections has also demonstrated correlations between malaria parasite prevalence in all age groups and proportional abundance of An. funestus (Swai et al., unpublished). Villages with the highest densities An. funestus also had the highest malaria burden (Swai et al., unpublished). The data generated from this habitat characterization study is therefore particularly important in the ongoing efforts for malaria prevention and will form a basis for future control efforts.
The findings from this study that An. funestus prefer permanent or semi-permanent habitats characterized by emergent vegetation is concurrent with past evidence from earlier investigations in Kenya [20, 21, 31]. Although this current study did not assess seasonality of An. funestus larvae densities in the different habitats, the observed preference of permanent and semi-permanent water bodies explains the known seasonality of its adult densities in the same study villages as observed in recent entomological surveys [4, 30]. The adult densities of An. funestus tend to peak after the rains just before the dry seasons begin, and are sustained by the large permanent water bodies [20]. Although no detailed studies have been done in this area targeting An. funestus aquatic habitats, early accounts by Gillies and DeMeillon [9], as well as limited surveys done nearly fifty years ago in Ifakara area (which neighbors the current study site) already suggested an association between the late peaks in An. funestus densities and the large perennial habitats [32].
Although there was no clear statistical association, the An. funestus habitats had depths greater than 50 cm and were located within 100 m from the human dwellings. This is likely due to the anthropophagic nature of these mosquitoes [33], and further explains the importance of this species in malaria transmission in these areas. Other Anopheles species such as An. gambiae, which breed in open sunlit stagnant water pools [9, 20, 34] are also highly anthropophagic and generally occur near human habitations [35]. The ability of An. funestus to breed in the river waters is not unique to Tanzania, but has also been demonstrated in other places such as coastal Kenya [9, 21], and may be due to the higher levels of aeration and dissolved oxygen in such waters. Additional investigations are therefore required to further examine these details. A similar ecological niche has been described for An. pseudopunctipennis in South America, which was successfully controlled by clearing the river waters of the algal blooms [36]. While it is unclear whether clearing the identified habitats of emergent vegetation would be suitable for control of An. funestus in Tanzania, it will be important to investigate it as a potential environmentally-friendly approach, in which community members could be engaged to achieve effective disease prevention. Besides, it will be important to ascertain the importance of these habitat types across multiple sites and settings. For instance, in one area in the north of Tanzania, Dida et al., [37] found no mosquito larvae near the main rivers, suggesting the dominant malaria vectors may be breeding elsewhere in such settings.
Understanding the physicochemical characteristics of mosquito larval habitats is also important in understanding their overall ecological needs, and assessing options for manipulation. In this study, it is possible that the physicochemical parameters might have been influenced by agricultural practices and pesticide use, which are prevalent in the valley (Matowo et al., unpublished). Emerged adult mosquitoes from these aquatic habitats might become more resistant towards the insecticides having the same chemical formula used in mosquito vector control [35, 38, 39]. Here we found that the most prolific habitats were located at higher altitudes, perhaps less affected by agricultural insecticidal deposits [40, 41], than the floor of the valley. Nonetheless, the mosquito species from the same study villages are known to be already strongly resistant to insecticides used for public health, including pyrethroids and carbamates (Pinda et al., unpublished), a situation potentially related to widespread use of pesticides in both agriculture and public health. Similar to other studies on Anopheles mosquitoes, the An. funestus habitats in this study area had weak acidity pH [39, 42]. The main habitats had pH ranging from 6.5 to 6.7, turbidity from 26.6 to 54.8 NTU and total dissolved solids from 60.5 to 80.3 mg/L, all of which are similar to most observations of habitats of Anopheles mosquitoes in previous studies [43, 44]. Some of An. funestus mosquitoes were collected from the habitats with moderate concentration of nitrate, indicating the possibility that they use it as a source of nutrients during larval development as earlier described [39].
Overall, this study has provided the basic description of An. funestus habitats in rural south-eastern Tanzanian districts of Ulanga and Kilombero. The effective control measures for this species should consider understanding their behavior and ecology including characteristics of their aquatic habitats so that can be targeted during their immature stages. Given the rarity of the An. funestus habitats and the observed characteristics, these habitats fit the description of being fixed, few and findable. Future studies should therefore investigate potential of using larviciding or larval source management to improve malaria control in settings where An. funestus dominate.