Seasonal Variations of Nocturnal, Endophagous and Anthropophagous Anopheles Species of Rural Communities in Abia State, Nigeria

INTRODUCTION

The roles of insects in the incidence and transmission of human diseases have been recognized from antiquity (Sharma, 1999). The tropical areas of the world are more than blessed with an abundance of insect vectors (Service, 1997; Horsfall, 1962). Of all the insect vectors mosquitoes are the most important single disease vectors in the tropics (Abdoon and Alshahrani, 2003) and are of immense public health importance. Man-biting mosquitoes transmit from infected to uninfected humans the disease-causing agents (parasites) of several serious diseases, including malaria, filariasis, yellow fever, dengue and encephalitis.

Anopheles is the best known genus of mosquitoes and has noxious species that are vector-hosts of malaria (Abdoon and Alshahrani, 2003), filariasis (Anosike et al., 2003) and a host of other locally named human diseases (Gillet, 1972) in the tropical and temperate parts of the world. Malaria takes the pride of place as the outstanding human disease in which some 300-500 million people the world over are at risk (Wanji et al., 2003). Anopheles mosquitoes are of species complexes with each sympatric population varying in capacity to transmit malaria parasites (Cohuet et al., 2004). Fontenille and Lochouarn (1999) have discussed the complexity of malaria vectorial systems in Africa, with different species involved in transmission in different bio-geographical zones.

The principal vectors of malaria in Nigeria are Anopheles gambiae and Anopheles funestus which are widespread. Anopheles arabiensis is restricted to the western part of the country and Anopheles squamosus to the northern part and the coastal zones of the southern part. Anopheles moucheti and Anopheles ziemani play a secondary role in the transmission of malaria in southeastern and northern parts and their relative importance may vary from one bio-ecological zone to another (Kalu et al., 2007; Gadzama, 1983).

Female adults of all mosquitoes require at least a blood meal for the maturation of each batch of eggs. Whereas some species are zoophagous, others are anthropophagous. Different Anopheles species exhibit marked preference for feeding in particular habitats. Most female Anopheles is nocturnal and indoor feeders, feeding and resting inside human habitations. These nocturnal and endophagous anthropophagous Anopheles species are often important vectors of human malaria parasites, Plasmodium species (Fontenille and Lochouarn, 1999; Le Menach et al., 2005).

Umuchieze and Uturu which are rural areas in Abia State of Nigeria, can be considered as communities of hyperendemic malaria. Malaria parasitaemia studies recently revealed prevalence rates of 72.58% (225 out of 310) and 74.19% (230 out of 310) in inhabitants of the areas, respectively (Kalu et al., 2012). Despite these high incidences of malaria in the communities, no research has been carried out on malaria transmission and on the roles played by different vectors at different seasons of the year. Nigeria is characterized by several bio-geographical zones and the national programme for malaria control under the Roll-Back Malaria Initiative requires information on the malaria transmission from all the bio-geographical zones of the country. This study reports on work carried out in two rural communities of Abia State, South-Eastern Nigeria on the abundance of nocturnal and endophagous anthropophagous Anopheles species during two seasons of the year.

MATERIALS AND METHODS

Study areas: The present study was carried out in Umuchieze and Uturu, rural communities in Abia State, South-Eastern Nigeria. The areas are located in the same bio-geographical region as well as belong to the same climatological regime. The vegetation in Umuchieze and Uturu is ordinarily considered part of tropical rain forest which is the dominant natural vegetation in most parts of south eastern Nigeria. The economic trees of the rainforest community are extremely numerous but the oil palm appears to be the most important. Thus, most of the areas are generally covered by oil palm.

The communities have tropical climate. The mean daily maximum air temperature ranges from 28-35°C and mean minimum temperature ranges from 19-24°C. The areas have a long rainy season that starts in late March and ends in late October with maximum rainfall in August and September. The dry season commences in early November and terminates in March. Mean relative humidity ranges from 80 to 85% and above during the rainy season but drops to 60% or lower during the dry season (Igbozurike, 1986).

Umuchieze (5°42'23" N, 7°10'35"E) is a rocky area located in Umunneochi Local Government Area of Abia State. Extensive stone mining activities by quarry mining companies created and abandoned some quarry pits in the community. The pits later became filled with water as rains progressed. Though the water-filled abandoned quarry pits serve the community various purposes, they may be potential breeding habitats for vectors of malaria parasites.

Uturu (5°51'22"N, 7°30'54"E) is a community in Isuikwuato Local Government Area of Abia State. The Abia State University main campus is cited in the community. Two streams, namely, Ihiku and Atuma, provide all year round drinking water to the inhabitants of the area. These stream over flow their banks during the rainy season. They are likely to provide all year round breeding places for vectors of malaria parasites in the community.

Mosquito collection: The study was carried out in 2 successive years, from January 2005 to December 2006. Four houses (2 per study community) were randomly selected as sampling sites. Adult mosquitoes were caught in all-night human-bait indoor insecticide spray sheet, as described by Service (1993).

Mosquitoes were collected in an empty bedroom selected from each sampling site. The researcher opened the bedroom door and window from 6:00 p.m. (18:00 h) Nigerian time to the time of collection of mosquitoes, covered the floor with a white sheet and allowed himself/herself to be bitten by mosquitoes in the bedroom from 9:00 p.m. (21:00 h) Nigerian time to the collection time. Catches were carried out between 10:00 p.m. (22:00 h) and 2:00 a.m. (02:00 h) Nigeria time using an insecticide spray contained in an aerosol can (RAID brand). Catch in each site was made once in a week throughout the 24 months of the study. Paper cups internally padded with soft tissue paper were used to store the collected mosquitoes before identification.

Identification of mosquitoes: The morphological identification of different species of Anopheles approach described by Gillet (1972) was used to identify collected mosquitoes.

Data analysis: Chi-square statistic was used to compare Anophelines abundance while student t-test was used to test research hypothesis that sought the significance differences of species. The significance was fixed at <0.05.

RESULTS

Anopheles mosquitoes: nocturnal and endophagous anthropophagous species, distribution and abundance: In total, 500 Anopheles, all females, were collected: 170 (34.00%) in Umuchieze and 330 (66.00%) in Uturu (Table 1), between early January, 2005 and late December, 2006. Three nocturnal and endophagous anthropophagous Anopheles species were identified: A. gambiae, A. funestus and A. moucheti. Anopheles moucheti was rare and found only in Uturu (Table 3).

Table 1:	Nocturnal and endophagous anthropophagous Anopheles species composition for year 2005 and 2006

NC: Number caught, RA: Relative abundance per Community

Table 2:	Monthly abundance of nocturnal and endophagous anthropophagous anophelines found in Umuchieze for Year 2005 and 2006

NC: Species number caught, PA: Percentage abundance

Table 3:	Monthly abundance of nocturnal and endophagous anthropophagous anophelines found in Uturu for year 2005 and 2006

NC: Number captured, SPA: Species percentage abundance

A. gambiae was the dominant species with overall relative abundance of 53.00% (n = 265). The species common to both study communities were significantly more abundant in Uturu (χ², p>0.05).

There were monthly and seasonal variations in species abundance in both study areas. Monthly data on prevalence and abundance of Anopheles species in each study area are presented in Table 2 and 3. Anopheles population was established in April in both communities and their abundance increased progressively from month to month thereafter until a population peak was reached in the month of September during the present study period. Population drops were recorded in October and November.

Table 4:	Seasonal abundance of anopheles species found in Umuchieze and Uturu communities for year 2005 and 2006

RA: Relative abundance

In Umuchieze, the vectors were not found from January to March as well as in November, while they were absent in Uturu only from January to March. However, Anopheles were scarce in the months of November and December in Uturu community during which period the relative abundance of the vectors was 7.20% (36 of 500). The monthly abundance of A. gambiae, the predominating species, was significantly higher (χ², p<0.05) in Uturu than Umuchieze.

Anopheles were abundantly captured during the rainy season. Out of the 500 Anopheles collected during the study period 454 (90.80%) and 46 (9.20%) were caught during the rainy and dry seasons, respectively (Table 4). All the three species were found from April which was the onset of rainy season, to late October, the end of rainy season. The various species were found in small numbers at the onset of rains. Abundance of the anophelines increased progressively as the rains intensified. Species population densities reached a climax in September in both study communities followed by a drop in their abundance in October. In all, 251 (50.20%) A. gambiae, 138 (37.60%) A. funestus and 65 (13.00%) A. moucheti were collected during the rainy season (Table 4). Anophelines were scarce during dry season in the study areas. They were found in low population only in November and December, being completely absent from January to March of the study period (Table 4). A total of 14 (2.80%) A. gambiae, 24 (4.80%) A. funestus and 8 (1.60%) A. moucheti were captured during the dry season.

DISCUSSION

The main endophagous and nocturnal anthropophagous Anopheles species in some rural areas of Abia State, Nigeria are A. gambiae, A. funestus and A. moucheti. These results confirm the confinement of A. gambiae complex to the forested areas of Africa (Coetzee et al., 2000). A. gambiae and A. funestus may be the major vectors of malaria in these study areas as they are well known as efficient vectors of malaria in other areas of Africa and Madagascar (Shililu et al., 2003; Jambou et al., 2001). The presence of A. moucheti in Uturu community and its probable implication in malaria transmission is noteworthy; A. moucheti has only rarely been found in Nigeria and its relative abundance of 22.12% (73 of 330) in this study area is relatively high. Data on the malaria transmission potential of A. moucheti in the region are lacking. However, being endophilic and anthropophilic species it should be considered an important malaria vector there. The present finding may be the baseline information about the prevalence of the species in the eastern part of Nigeria. Moreover, Ihiku and Akiyi streams which are located in the proximity of the study sites in Uturu, possess features favourable for breeding of A. moucheti and thus, might be the breeding places for the species.

Both larval and adult stages of Anopheles mosquitoes are influenced by their immediate environments, the influence of which leads to variations in the prevalence and abundance of the vector species (Aigbodion and Anyiwe, 2005). Results of the present study conform to this fact. The occurrence and abundance of Anopheles encountered during the period of this study varied from community to community, monthly and seasonally. All the three Anopheles species were found in Uturu, while only two of them: A. gambiae and A. funestus, occurred in Umuchieze community. The relative abundance of these two species was higher in Uturu than Umuchieze. The greater species richness and abundance recorded in Uturu than Umuchieze might be attributed to the fact that environmental conditions favourable for breeding and survival of adult anophelines were more abundant in one study area than the other.

The Anopheles species encountered during this study were abundantly found during the rainy season (April-October), scarce during early dry season (November and December) and completely absent in the other months of the dry season (January-March). Pronounced variations in monthly abundance of Anopheles species were observed in both study areas. Anopheles mosquitoes were established in early April in both communities and the abundance of the species increased as rainfall intensified. A population peak of A. gambiae and A. funestus was observed in September in Umuchieze, while the species were most abundant in September and October, respectively, in Uturu. A. moucheti, found only in Uturu had population peaks in May and September but was absent from December through January to March. The presence of A. gambiae and A. funestus in dry months of November and December in Uturu indicates that the species breed in natural and permanent water bodies. Ihiku and Akiyi streams, each situated at a distance less than 0.50 km away from the sampling sites, might be the breeding places for the species.

The seasonal variations in the vectors abundance in both study locations may probably be due to the fact that some Anopheles species display variations in their biting behaviour according to time of the year, being more endophagous during the rainy season and exophagous during the dry season (Wanji et al., 2003). Climate operates directly in determining the seasonal availability of breeding places for mosquitoes (Service, 1997). The low species abundance in November (in Umuchieze) and December (in Uturu) might be due to setting in of climatic factors detrimental to survival of Anopheles, while the complete absence of Anophelines from December (in Umuchieze) and January (in Uturu) to March might be due to lack of rainfall as well as the disappearance of their breeding places through evaporation. On the other hand, the malaria vectors might have hibernated during the dry months because climate operates directly in determining the requirement for their hibernation and aestivation (Service, 1997).

The findings of the present study have certain interesting implications for transmission of human malaria and control of the vectors of malaria parasites in the study areas and Abia State in general: All the Anopheles species recorded are efficient vectors of human malaria in Africa (Fontenille and Lochouarn, 1999); A. gambiae which is the most noxious and most efficient malaria vector in Africa (Gillet, 1972) was the most abundant species in both Umuchieze and Uturu communities; high population densities of the prevalent Anopheles species in these areas predispose the inhabitants to incessant contact with the vectors; and the vectors were more abundantly found during rainy season in the study areas.

This study shows that Umuchieze and Uturu are rural areas inhabited by the major and efficient vectors of malaria in Africa and are expected to be areas of high malaria transmission intensity. The abundance of Anopheles species, their highly anthropophagous behaviour and their biting humans when they are asleep in the night indicate the necessity of introducing vector control measures in the area and other malaria endemic areas of Abia State as one of the strategies of fighting malaria. Each vector control needs to focus on providing an effective personal protection for the most susceptible age groups at least, against vector contact rather than aiming at reducing the potential for transmission at the community level. The most appropriate vector control option in the study areas could be the use of insecticide treated bed net (ITN) as these tools are currently the most effective and practical vector control option in areas where malaria is highly transmitted (Guillet, 2001; Diallo et al., 1999).