Background
Female
Anopheles mosquitoes can carry
Plasmodium protozoan parasites, some of which transmit to humans. The majority of malaria caused by
Plasmodium falciparum and
Plasmodium vivax occurs in Africa. Between 2010 and 2017, there was a noticeable decline in malaria deaths and cases [
1]. However, the decline has slowed in recent years, and in the most recent years, there has been an increase in the number of cases [
2]. The presence of the most effective vectors, such as
Anopheles gambiae,
Anopheles arabiensis, and
Anopheles funestus is the main reason for the high rate of malaria transmission in Africa [
3]. Other locally important malaria vectors include
Anopheles melas, Anopheles merus, Anopheles moucheti, and
Anopheles nili [
3].
In Ethiopia,
P. falciparum and
P. vivax are the predominant malaria parasites. The country contributed 9% of the
P. vivax malaria cases globally in 2017 [
1]. Although there are many
Anopheles species in Ethiopia, only a few are known to transmit malaria.
Anopheles arabiensis, one of the
An. gambiae complexes are primarily responsible for transmitting malaria in the country [
4,
5]. In the 1930s, Italian malariologists identified the “
An. gambiae” complex as the main vector of malaria in Ethiopia [
6,
7]. Ethiopian Malaria Eradication Service, in collaboration with Jolivet, identified 31
Anopheles species in 1963 and documented the predominance of “
An. gambiae” (probably
An. arabiensis) [
7].
Anopheles gambiae remained the most common and prominent malaria vector even after extensive malaria vector control interventions were adopted in the 1960 and 1970s [
7,
8]. Several recent studies have demonstrated similar contributions to malaria transmission and the dominance of the same species despite decades of malaria control efforts [
4,
8‐
11].
Anopheles arabiensis shows flexible resting and feeding behaviour, as it rests and bites indoors and outdoors and feeds on humans and animals based on the hosts’ availability [
12]. This behavioural plasticity complicates malaria control and elimination programmes [
13]. Despite the plasticity of feeding and resting behaviour, insecticide-treated nets (ITN) and indoor residue spraying (IRS) have been widely used to control this species [
14].
Anopheles mosquito species diversity and behaviour will likely alter due to these interventions [
15‐
17]. For instance, a shift towards outdoor biting and resting vectors could result from interventions that target indoor feeding and resting vectors [
13,
15]. Behavioural resistance, such as avoiding insecticides on bed nets and walls, may reduce the efficacy of IRS and ITNs [
16]. Several reports have documented the outdoor and early-night human biting behaviour of
An. arabiensis in Ethiopia [
10,
17]. Integrated interventions may be necessary to target changes in vector species and their behaviour.
Several studies have been conducted to describe the species composition, feeding and resting habits, and infection rates of malaria mosquitos in various malaria-endemic areas [
4,
10,
11]. Nevertheless, it has yet to be explored if these malaria control interventions affected the diversity of malaria vector species, their geographic distribution, or infection rates. Therefore, studying the species distribution and their role in malaria transmission is critical for making evidence-based decisions. The current study assessed the composition of the
Anopheles mosquito species and their relative contribution to malaria transmission in southern Ethiopia.
Discussion
Eight Anopheles species, namely An. arabiensis, An. parensis, An. pharoensis, An. pretoriensis, An. demeilloni, An. kingi, An. tenebrosus and An. sergentii, were identified in southwest Ethiopia. Anopheles arabiensis was the most common and primary malaria vector in the region. There were no documented cases of Anopheles stephensi in the region.
Anopheles arabiensis was the region’s most widely distributed and predominantly vectoring
P. falciparum malaria. Many years ago, O’Connor [
26] documented 34
Anopheles species in Ethiopia. Among these
Anopheles species recorded at that time,
An. gambiae (presumably
An. arabiensis) was the dominant and primary malaria vector in wide geographic areas. Several studies have also shown that
An. arabiensis contribution as a primary vector in different parts of the country [
5,
10,
11]. Despite implementing a wide range of vector control interventions for decades, the species remained the dominant malaria vector in the region. For example, the
P. falciparum CSP infection rate of
An. arabiensis was 0.36%, comparable to the CSP rate of 0.77% reported from Gambella in 1994 [
27]. Krafsur reported a somewhat higher CSP rate (1.87%) of the same species from Gambella in 1977, although the method was a microscopic dissection of salivary glands [
6]. Using the HLC technique, the
P. falciparum CSP rate of
An. arabiensis was 0.5% in Sille, southern Ethiopia [
28]. In the Central Rift Valley of Ethiopia, a CSP rate of
An. arabiensis was 1.18% from the CDC light traps [
29]. The
P. falciparum CSP rate of
An. arabiensis from CDC light traps, as used in the current investigation, was 0.3% in the south-central and southwest Ethiopia [
4,
30,
31]. This implies that
An. arabiensis does not respond well to the current malaria vector control interventions. To effectively eliminate malaria in the country, it is necessary to use additional tools to control the species [
32,
33]. For example, interventions such as larval source management can be used to target the aquatic stages of malaria and other vectors [
34]. Toxic bait traps could be used to control mosquitoes seeking hosts outdoor [
32], while animal-based interventions can address the problem related to zoophagic mosquitoes [
35].
A challenge with
An. arabiensis is its plasticity in feeding and resting habits. For example, the species’ anthropophagic, zoophagic, and outdoor and indoor resting behaviour has been documented in Ethiopia [
12,
36,
37]. These adaptive characteristics allow the species to avoid interventions mainly targeting those that rest and feed indoors.
The majority of
An. funestus group was identified as
An. parensis. Similarly,
An. funestus group from Jimma was analysed and verified as
An. parensis using the PCR technique [
38], suggesting that
An. parensis is the predominant species of
An. funestus group in the region. During the 1930 and 1960s, the
An. funestus group was prevalent and widespread in Ethiopia [
39]. However, none of the 339
An. funestus group mosquitoes from Zwai and Awasa tested positive for sporozoite [
39]. In contrast, Krafsur reported a sporozoite rate of 1.23% in Gambella using PSCs in 1977 [
8]. However, identifying the specific species within the group was challenging due to the limited identification tools available. It’s worth noting that
An. funestus s.s. tends to bite and rest indoors, making it a potential candidate for DDT IRS, as seen in East African countries [
39]. Following the widespread use of DDT IRS, the outdoor biting and resting species
An. rivulorum substituted the primary vector
An. funestus s.s. in East Africa [
40]. This species was not identified at the current study sites. During the 1960s, the IRS projects carried out in southern Africa resulted in the elimination of the same species [
41]. This suggests that indoor-based intervention methods could be effective in reducing malaria vectors if the vectors are completely resting and biting indoors. However, in the presence of opportunistic feeders like
An. arabiensis, the current interventions may need to be revised to achieve the intended objective of malaria control and elimination.
In this study, after a detailed analysis of the sequence, a single
Anopheles mosquito specimen was confirmed to be
An. sergentii. Two species of
An. sergentii have been documented in Africa:
An. sergentii sergentii, found in several countries, and
An. sergentii macmahoni, mainly found in East Africa, including Ethiopia [
42]. Adult
An. sergentii macmahoni are rarely found indoors in human dwellings and typically feed on animals [
3].
Anopheles sergentii sergentii is an important malaria vector in the Saharan belt, spanning from northern Africa to the Middle East [
3]. The species is morphologically related to
An. parensis,
An. funestus,
An. demeilloni and
An. cameroni [
43]. It was also grouped under
An. demeilloni in the report of “Phylogeny and Classification of
Anopheles” [
44]. It is important to note that although the primers of the
An. funestus group amplify
An. sergentii, it is insufficient evidence to classify it as a member of the
An. funestus group. However, the results from sequencing suggest that the two species share the gene of interest used to identify species in the
An. funestus group. Therefore, it is crucial to provide detailed information on the degree of species divergence and percentage relationship by comparing the sequence of the species of interest with the sequence of the species obtained from GenBank [
45] in addition to primer amplification. By comparing
COI sequences from GenBank, it is evident that the current species belongs to
An. sergentii and does not belong to
An. funestus group.
The cross-sectional method used in this study has limitations because it cannot account for monthly and seasonal variations in species composition, which could lead to an incomplete list of species. Additionally, no confirmatory molecular test or boiling was performed on CSP ELISA positive samples, which could have led to false positives. However, the positive samples were repeated using the ELISA assay.
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