Impact of sugarcane irrigation on malaria vector Anopheles mosquito fauna, abundance and seasonality in Arjo-Didessa, Ethiopia

Irrigation-based agriculture has been largely promoted to alleviate poverty and improve economic growth in Africa [1]. However, existing evidence shows that irrigation might increase the risk of vector-borne diseases such as malaria [2‐5]. Man-made environmental modifications and expansion of unplanned water development schemes could enhance mosquito breeding and sustain malaria transmission [2‐5]. In Ethiopia, where malaria is a major cause of morbidity and hospital admissions [6], irrigation activities may contribute to increased risk of the disease. Irrigations can enhance malaria transmission by increasing the number and diversity of mosquito-breeding habitats (e.g., poorly managed irrigation canals and canal seepages) that can increase vector composition, density and longevity. This can ultimately increase risk of malaria and extend the duration of malaria transmission in irrigation areas in Ethiopia where the disease is seasonal and unstable [7‐9].

Previous studies indicate higher malaria risk close to dam and irrigation schemes compared to communities living further away [9‐11]. In northern Tanzania, a 4-fold increase in the density of Anopheles arabiensis and risk of malaria was documented in rice irrigation fields than in non-irrigated savannah villages [11]. In Ghana, higher larval and adult anopheline densities were observed in irrigated areas compared to non-irrigated areas in the rainy and dry seasons [12]. Similarly, in Ethiopia, villages practicing irrigated agriculture were shown to have increased malaria vector abundance [13], risk of malaria infection [14] and mosquito density [9, 10] compared to non-irrigated villages. However, some studies indicate that irrigated sugarcane cultivation resulted in water pooling but did not produce more vectors [11]. In general, unlike areas where malaria is stable, irrigation practices in areas of unstable malaria could affect vector abundance and lead to increased transmission [2].

Although several studies reported an increase in mosquito density and malaria transmission associated with rice irrigation [2], little is known about the impact of sugarcane irrigation on malaria transmission in Africa [11]. Available data from cross-sectional studies failed to depict trends of temporal malaria vector dynamics at least in the two major seasons: dry and wet. Studies that evaluate the impact of sugarcane irrigation on malaria mosquito dynamics are scarce in Ethiopia despite the country’s unprecedented expansion in irrigation practices.

Thus, it was deemed necessary to evaluate the current impact of sugarcane irrigation on vector distribution, abundance and seasonality pattern in a way to suggest vector control interventions and inform public health professionals [15]. Furthermore, knowledge of the dynamics and behaviour of local Anopheles mosquitoes may help devise control tools to achieve malaria elimination goal [16]. This study aimed to assess the impact of Arjo-Didessa sugarcane irrigation on species composition, seasonality and abundance of Anopheles mosquitoes. The study tests the hypothesis that irrigation increases mosquito abundance both during the dry and wet seasons of the year.

Sugarcane irrigation activities, in Arjo-Dedissa area of southwestern Ethiopia, were associated with increased Anopheles species diversity, abundance and density during dry and wet seasons. Interestingly, An. amharicus was recorded in sugarcane irrigated areas in the present study. Indeed, irrigation provided suitable breeding grounds for malaria vector mosquitoes in the area and increased mosquito species composition and abundance. This could emanate from the availability of several and suitable Anopheles species breeding microhabitats as a result of the uninterrupted sugarcane irrigation activity. Six Anopheles species were found in the irrigated sugarcane plantation areas while only four species were collected in the non-irrigated areas. This could explain the relevance of sugarcane irrigation schemes in supporting breeding of diverse Anopheles species. Similar studies from Ethiopia [13] and elsewhere in Africa [20‐22] suggest that irrigation agricultural practices influence Anopheles species diversity. The presence of such diversified malaria-transmitting Anopheles species might influence the risk of malaria transmission and affect vector control efforts in the irrigation scheme. However, data on sporozoite rate would be required to confirm the increased malaria risk in areas with increased vector density since elevated vector abundance does not necessary translate into increased disease risk.

Occurrence and distribution of An. amharicus in irrigation schemes was recorded for the first time in this study. Anopheles amharicus was reported for the first time in Ethiopia by Hunt et al. [23] about 18 km east of the present study area [24]. Although much is unknown about the geographic distribution of this species in Ethiopia [24], its co-existence with An. arabiensis in the present study indicate that these two species might have similar breeding habitat and ecologic preferences. Changes in microclimate and increased water ponding resulting from diversified habitat types, such as irrigation canals, hippo trench and man-made pools, might favour breeding and distribution of An. amharicus in the irrigated clusters.

The two secondary malaria vectors in Ethiopia, An. pharoensis and An. funestus group [25, 26], were also recorded in the study area, predominantly from the irrigated clusters. Similarly, these two vector species were linked with irrigation practices in Central Ethiopia [9]. A study in northern Tanzania indicate that An. funestus group was increased following introduction of irrigation schemes [11]. The study showed that semi-permanent ponds formed due to poorly maintained water systems were the main breeding habitats of An. funestus around irrigation schemes. The occurrence of diverse Anopheles species both in the dry and wet seasons in the irrigated clusters indicated that irrigation created conducive breeding grounds for diverse Anopheles species throughout most of the year. Anopheles funestus has become a common mosquito species in areas with water resources development in Ethiopia [9, 10].

This study clearly shows that Anopheles species were more abundant in the irrigated clusters than in the non-irrigated clusters both in the dry and wet seasons. Higher abundance of An. gambiae s.l. (primarily comprising An. arabiensis), the major malaria vector, in the irrigated villages shows the role of sugarcane irrigation in increasing mosquito densities that might affect the potential risk of malaria transmission. Poorly managed irrigation creates sunlit water lodging that favour An. arabiensis breeding [27]. Previous studies documented An. arabiensis predominating in irrigated fields in Ethiopia [9, 13, 28, 29], northern Tanzania [11] and Ghana [12]. A previous study in Ethiopia also showed that an increase in canal water release to be associated with an increase in larval density of An. arabiensis [30]. Another study noted that An. arabiensis gravid females to be more attracted to sugarcane pollen-associated volatile sweet attractants [31] which might be the reason for the greater abundance of this species in the sugarcane irrigated fields in the present study. Overall, as vector abundance is one of the direct predictors for malaria transmission; this study suggested a high risk of malaria transmission around the irrigated fields unless proper vector intervention strategies are implemented.

In the present study, Anopheles mosquito density was generally higher outdoors than indoors, which could compromise the effectiveness of indoor-based vector interventions (long-lasting, insecticidal nets (LLINs) and indoor residual spray (IRS)). In agreement to this finding, an outdoor-biting activity of anophelines was also documented in southwestern Ethiopia [32]. This could be attributed to the intensive use of insecticide-based indoor vector control strategies (IRS and LLINs) in the area that might gradually change the mosquito feeding and resting behaviour from indoor to outdoors. Kibret and Wilson [33] noted an increasing trend of outdoor-feeding An. arabiensis in central Ethiopia due to extensive use of indoor insecticide-based vector interventions. In addition, presence of cattle and other animals in the vicinity that serve as an alternative source of mosquito blood meal might also contribute to the outdoor feeding tendency of anopheline mosquitoes in the study area. A targeted larval source management in the irrigated fields could help reduce vector density/abundance both indoors and outdoors [34]. Irrigation schemes should therefore consider additional vector management strategies to mitigate malaria vector breeding in such settings.