Anopheles arabiensis in Sudan: a noticeable tolerance to urban polluted larval habitats associated with resistance to Temephos

During the past 10 years many studies have stated that Anopheles species were adapted to polluted habitats in urban settings, the majority from African countries. Anopheles gambiae sensu stricto (s.s.) in urban settings in Nigeria are adapting to a wide range of water pollution [1].

In urban cities in Ghana, An. gambiae was found in polluted aquatic habitats and this, coupled with occurrence of insecticide resistance, is alarming [2]. In Yaoundé, Cameroon, the presence of An. gambiae in organically polluted sites has been confirmed [3]. Other studies such as in Pakistan and Sri Lanka indicated the adaptation of Anopheles gambiae sensu lato (s.l.) and Anopheles culicifacies to organically polluted water habitats [4, 5] and reported that rapid, unplanned urbanization is considered to favour adaptation of anophelines to various xenobiotics and the expansion of their niche to polluted habitats. Anopheles gambiae complex, which includes the major vectors in Africa, has the capacity to exploit different kinds of habitat that are created either directly or indirectly by humans. This is evidenced by its wide geographical distribution and its occurrence in a variety of micro- and macro-environmental conditions throughout tropical Africa, and that larvae were found in habitats organically polluted by rotting vegetation, human faeces, or oil [2, 6, 7].

Anopheles arabiensis, a sibling species of the An. gambiae complex, is a predominant malaria vector all over Sudan, covering arid and semi-arid areas of the country. It is the only malaria vector encountered in Khartoum State [8], the capital of Sudan, which have long been Sudan’s primary industrial, commercial and manufacturing hubs with very poor infrastructure that has many environmental consequences [9]. The present study documents, the presence of An. arabiensis larvae in polluted habitats in urban Khartoum, central Sudan, which further influenced its susceptibility to insecticides.

Until recently, urban development was generally believed to reduce the risk of vector breeding, and thus malaria transmission. However, millions of clinical episodes of malaria occur annually in urban areas, indicating that the epidemiology of this disease is changing [17, 18]. The findings of the present study, together with other studies on other anopheline mosquitoes, indicate a change of An. arabiensis breeding requirements in urban settings. This is in line with many studies which stated that Anopheles mosquitoes have adapted to new breeding sites created by urbanization [19]. Studies conducted in Accra, Ghana and Dar es Salaam in Tanzania, revealed the presence of An. gambiae s.l. in organically polluted water habitats, sewage ponds and in swamps extremely polluted with organic matter [4, 7].

Khartoum State in Central Sudan had a unique Khartoum Malaria-Free Initiative (KMFI), which was launched in 2002 by the State and the Federal Ministry of Health, in collaboration with WHO. The core intervention for KMFI was larval control through weekly application of Temephos and environmental management [20]. The continuous application of Temephos larvicide for more than 13 years might explain the development of resistance to Temephos. Anopheles arabiensis from polluted habitats was more tolerant to Temephos compared to An. arabiensis from non polluted habitats. This finding is in line with Kabula et al. [2] who suggested that the adaptation of An. gambiae s.s. to breed in polluted water may be influenced by their insecticide resistance status and vice versa. It is more likely that resistant gravid female choose the available polluted water as a last chance to lay its eggs when they have no choice during the hot dry season to find an alternative habitat which require more flying during an extreme harsh environmental condition. Aboud et al. [14] reported that the haplotype diversity within melanic populations of An. arabiensis was higher than within normal populations and better adapted to hot and arid environments. A high level of genetic diversity is often beneficial to a species as it provides more opportunities for adaptation when a species environment change and might explain the increased tolerance of the melanic form to Temephos insecticide.

The mean level of conductivity reported in this study increased 8.6 times compared to control site. Similar findings was obtained by Tene Fossog et al. [6] in Douala, Cameroon, for conductivity in non-polluted and polluted sites and by Awolola et al. [1] in Lagos, Nigeria. However, in Yaoundé, Cameroon, Antonio-Nkondjio et al. [3] recorded lower values of conductivity in rural and urban habitats. In the present study, the turbidity levels were similar to with the result recorded by Awolola et al. [1]. The simple definition of ‘turbidity’, which favours Anopheles larvae in a habitat might not be precise enough. This is because water which is turbid from particles not nutritious for Anopheles larvae could disfavour the growth and development of larvae and can be considered a limiting factor [21], while water turbid from food particles represents a very suitable habitat and may be useful for larval development. Some studies showed that An. arabiensis and An. gambiae s.s. larvae were associated with highly turbid water, with algae and little or no aquatic vegetation, while other studies recorded presence of algae and vegetation as limiting factors [22, 23]. This study reported that all water bodies (permenant or semi permenent) are potential larval habitats and help maintaing the vector populations during the hot dry season. [24] reported that permanence of a habitat had no significant influence on larval productivity and all potential breeding sites need to be considered as source of malaria risk at any time of the year. 

The study confirmed the presence of oil in polluted water but the values was lower compared to the values recorded by Awolola et al. [1] in Lagos, Nigeria, who found that the level of the three heavy metals (Fe, Cu, Pb) was more than twofold higher than those obtained from the control site. However, in this study concentrations of Pb (mg/l) and Cu (mg/l) were less by at least three times in comparison to the control site. The present study found that the mean of nitrate was 4.6 times compared to control site.

The findings of the present study together with other studies from sub-Saharan Africa and other parts of the world, indicates that An. gambiae complex is adapting to a wide range of water pollution in urban settings. Anopheles larvae are not restricted to clearly defined habitats. Therefore, all water bodies in an urban environment should be considered potential breeding places and must be a target for larval control. Further studies are need to be shown over time, during different seasons, in respect to other positive habitats from the total found in the area to estimate the extent of this adaptation in the targeted area.