Background
A wide range of human and animal diseases are transmitted by mosquitoes and those diseases remain a major source of death worldwide [
1]. Malaria remains one of the most serious vector-borne diseases, affecting half of the world’s 7.4 billion people [
2]. The proliferation of mosquitoes is promoted not only by ecological changes due to human activities (deforestation, public works, construction of dams, rice paddies, irrigation), but also by environmental parameters (rainfall, temperature and relative humidity), which also play a fundamental role in the level of transmission and the epidemiology of diseases [
3,
4]. In intertropical Africa, malaria transmission is very heterogeneous due to eco-climatic variations [
5]. Currently, five species of the parasite of the
Plasmodium genus have been identified as responsible for malaria infection in humans [
6]. Among them
Plasmodium falciparum remains the most virulent species causing the deadly forms of malaria [
7]. The
Plasmodium species responsible for human malaria are mainly transmitted by primary vector species, such as
Anopheles gambiae sensu lato (s.l.),
Anopheles funestus group and
Anopheles nili group [
8,
9]. The existence of those different species complexes in an area represents a great challenge for malaria control programmes.
Anopheles nili group has a wide geographical distribution in most of tropical Africa [
10] and its preferential habitats are fast-flowing, upright-flowing streams, large rivers or dense shade along streams [
7]. It is a group that includes four species, including
An. nili sensu stricto (s.s.),
Anopheles carnevalei,
Anopheles somalicus and
Anopheles ovengensis [
8,
11].
In Benin, over the past two decades, the roles of
An. gambiae s.l. and
An. funestus group in the transmission of
P. falciparum in several regions of the country have been studied by several authors [
12‐
19]. Few of these studies have shown the presence of
An. nili group in the different surveyed areas. Moreover, none of them has demonstrated its involvement in malaria transmission in Benin. It is in this context that a large population of
An. nili group was collected during this cross-sectional survey conducted in the districts of Kérou and Péhunco located in the Atacora region. Thus, the possible involvement of this
Anopheles species in the transmission of
P. falciparum was investigated in the study area.
This study aims at providing information on vector species composition involved in malaria transmission in the areas of Kérou and Péhunco (northwestern Benin) where there is a lack of data.
Discussion
The study of malaria vectors in an area is a prerequisite not only to understand the epidemiology of the disease but also to implement a strategy for effective and targeted control of those vectors. In the current study, 12 mosquito species including 6 anophelinae were identified in the two surveyed districts. Among these 6
Anopheles species, two (
An. gambiae s.l. and
An. funestus group) have already been implicated in malaria transmission in Benin [
13,
17,
18]. During this cross-sectional study, they were found in both study districts but,
An. nili group was found only in Kérou. The three vector species (
An. gambiae s.l.,
An. funestus group and
An. nili group) identified in Kérou live in sympatry in this savannah zone. This finding is similar to those of several authors in West Africa [
30,
31].
In Péhunco and Kérou,
An. gambiae and
An. coluzzii are the only members of the
An. gambiae complex recorded with a predominance of
An. gambiae (96.43% and 78.43%, respectively, in Péhunco and Kérou). No species of
An. arabiensis was identified after PCR in both districts. This could be due to anthropogenic actions such as deforestation and urbanization that destroy its natural habitats causing its gradual disappearance in some areas of northern Benin as reported by Aïkpon et al. [
32] and Salako et al. [
33]. All the specimens of the
An. nili and
An. funestus groups identified by PCR were
An. nili s.s. and
An. funestus s.s. in the district of Kérou. These results corroborate those of Djouaka et al. [
19,
34] who found
An. funestus s.s. as the only species of the
An. funestus group in the areas of Pahou and Kpomè in southern Benin. The results are also similar to works by Carnevale et al. [
35], Dia et al. [
36] and Adja et al. [
31], who found
An. nili s.s. as the only species in forest zone respectively in Cameroon, Senegal and Côte d’Ivoire.
The number of
An. funestus group collected in both districts was low during the study period as was also reported by some authors in the area and around [
32,
37,
38]. This could be justified by the scarcity of breeding sites favorable to the development of this species. Moreover, contrary to
An. gambiae s.l.,
An. nili group was found to be exophagic (significantly higher biting activity outdoors compared to indoors) in Kérou. This low biting behaviour of
An. nili group inside the dwellings had also been reported in Nigeria [
39]. Kérou being a savanna area, this behaviour of
An. nili group confirms the results of other authors who have shown that savanna populations of
An. nili group are more exophagic and exophilic [
40,
41].
In Kérou, each inhabitant receives 5 bites of
An. nili group per night. This biting rate was significantly higher than the one of
An. funestus group and not negligible for just four nights of collection. This reflects the presence of breeding sites favorable to the development of this species in the area. In fact, Kérou is close to several rivers, and the water level of these rivers is kept high for a good part of the year by the rain. This flow of water contributes to the development of several permanent mosquito breeding sites. This could probably explain the high density of the populations of the
An. nili group in Kérou. As a result, in an area with multiple vectors, variation in ecological, spatial and temporal parameters directly influences the relative role of each species in malaria transmission [
42]. The biting rate of
An. gambiae s.l. was very high in Kérou (26.19 bites/human/night) and in Péhunco (4 bites/human/night) compared to the other species and allows this vector to maintain the transmission of malaria in both districts.
Another important aspect of the current study is the involvement of
An. nili group in malaria transmission in Benin. Indeed, the SI of
An. nili group was 1.25% in Kérou. This index is similar to that recorded by Carnevale et al. [
35] in Cameroon and lower than the one of Elissa et al. [
43] in Gabon and Adja et al. [
31] in Côte d’Ivoire. The sporozoite indexes of
An. gambiae s.l. in Kérou (1.7%) and Péhunco (0.9%) were lower than those reported by previous studies in different areas of Benin [
16,
33,
37]. This could be due to the low number of tested mosquitoes in the short collection period covered by the current study as compared to previous records which considered a longer time period.
This study also showed malaria transmission by different mosquito species in the Kérou district.
An. gambiae s.l. and
An. nili group share in the indoors and outdoors malaria transmission. In
An. funestus group where EIR has been observed indoors, no definitive conclusion can be drawn as to its participation in outdoor transmission since the collection period in this study is short. As previously found in several sites in Benin [
13‐
18],
An. gambiae s.l. also remains the primary vector of malaria transmission in Kérou (13.05 infected bites/human/month), followed by
An. nili group (1.87 infected bites/human/month) and
An. funestus group (0.94 bites/human/month).
The EIR by
An. gambiae s.l. in Kérou was higher than those reported in a longitudinal study by Salako et al. [
37] in similar bioecological areas (Kandi and Gogounou) in the department of Alibori, Benin. In Péhunco, each inhabitant receives 1.02 infected bites of
An. gambiae s.l. per month. The high transmission by
An. gambiae s.l. in Kérou compared to both
An. funestus group and
An. nili group may be due to its significantly higher physiological age compared to the one of the other mosquito species (p < 0.05). The small number of
An. funestus group collected in each district could explain its low level of malaria transmission. Findings of this study shows that no specimen of
An. nili group and
An. funestus group was collected indoors after PSC. This could be due to the low sampling of mosquitoes performed during our survey.
An. gambiae s.l. which was the most frequent vector in the two districts takes mostly its blood meal on humans, thus confirming its anthropophagic nature [
33].
Regarding the presence of resistance mechanisms in
An. gambiae s.l., the L1014F
Kdr mutation was found at very high frequencies in its two detected sibling species (
An. gambiae and
An. coluzzii) in the two districts. Contrary to the works of Gnanguenon et al. [
44], Yahouédo et al. [
45] and Akogbeto et al. [
33] in some locations of southern and northern Benin, no significant difference was noted between the allelic frequencies of the L1014F
kdr mutation of
An. gambiae and
An. coluzzii in Kérou and Péhunco. This result corroborates those of Salako et al. [
46] who also found no significant difference between the L1014F
kdr frequencies of
An. gambiae and
An. coluzzii in Djougou, Ségbana and Copargo, northern Benin. The trend was the same for the relatively low allelic frequencies of the G119S
ace-
1 mutation of
An. gambiae and
An. coluzzii of the two study districts. However, the highest allelic frequencies of the G119S
Ace-
1 mutation was recorded in
An. gambiae in each zone with values ranging from 5 to 7.3%. In
An. coluzzii, this frequency varied from 0% in Péhunco to 5% in Kérou.
Authors’ contributions
RAO, FT, GGP, RA and MCA designed the study. RAO, AF and CK performed the fields activities. RAO, AS and WS carried out the laboratory’s activities. RAO drafted the manuscript and analysed the data. MCA, MA, GGP, ADS, BA and RA critically revised the manuscript for intellectual content. All authors read and approved the final manuscript.