Seasonal Variations of Nocturnal, Endophagous and Anthropophagous Anopheles Species of Rural Communities in Abia State, Nigeria
Transmission of human malaria requires contacts between vectors of malaria, Anopheles spp. and human hosts. In the present study, the abundance of nocturnal and endophagous anthropophagous anophelines species in Umuchieze and Uturu, rural communities in Abia State, Southeast, Nigeria, was investigated using all-night human-bait indoor insecticide spray sheet catches method for two consecutive years. Catch was made once a week in each community. A total of 500 adult mosquitoes (all female anophelines) was captured, 170 (34.00%) in Umuchieze Community and 330 (66.00%) in Uturu. Three Anopheles species: Anopheles gambiae, Anopheles funestus and Anopheles moucheti were found in the studied communities except in Umuchieze Community where Anopheles moucheti was never caught. Anopheles gambiae was dominant in both study communities with the species relative abundance of 55.29 and 51.82% recorded in Umuchieze and Uturu Communities, respectively. The relative abundances of various prevalent Anopheles species were higher during rainy season than the dry season. This periodic occurrence of the important malaria vectors explains periodicity of malaria epidemiology in the study communities. The high abundance rates of nocturnal and endophagous anthropophagous anophelines recorded in the two communities predispose inhabitants of the areas to incessant contact with the human malaria vectors resulting in the study areas being malaria endemic.
Received: June 28, 2012;
Accepted: August 25, 2012;
Published: November 08, 2012
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
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.
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).
|| Nocturnal and endophagous anthropophagous Anopheles
species composition for year 2005 and 2006
|NC: Number caught, RA: Relative abundance per Community
|| Monthly abundance of nocturnal and endophagous anthropophagous
anophelines found in Umuchieze for Year 2005 and 2006
|NC: Species number caught, PA: Percentage abundance
|| 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.
|| 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.
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
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).
1: Abdoon, A.M.M.O. and A.M. Alshahrani, 2003. Prevalence and distribution of Anopheline mosquitoes in malaria endemic areas of Asia region, Saudi Arabia. Eastern Mediterr. Health J., 9: 240-247.
PubMed | Direct Link |
2: Aigbodion, F.I. and M.A. Anyiwe, 2005. Mosquitoes and the environment: Some economic costs of Malaria in Nigeria. Niger. J. Entomol., 22: 93-107.
3: Anosike, J.C., C.O.E. Onwuliri, B.E.B. Nwoke and I.N.S. Dozie, 2003. Laboratory Investigation of the infection rates of Anopheles gambiae and Anopheles funestus in the transmission of Wuchereria bancrofti. Niger. J. Parasitol., 24: 143-148.
Direct Link |
4: Coetzee, M., M. Craig and D. le Sueur, 2000. Distribution of African malaria mosquitoes belonging to the Anopheles gambiae Complex. Parasitol. Today, 16: 74-77.
CrossRef | Direct Link |
5: Cohuet, A., F. Simard, C.S. Wondji, C. Antonio-Nkondjio, P. Awono-Ambe and D. Fontenille, 2004. High malaria transmission intensity due to Anopheles funestus (Diptera: Culicidae) in a village of savannah-forest transition area in Cameroon. J. Med. Entomol., 41: 901-905.
6: Diallo, D.A., A. Habluetzel, N. Cuzin-Ouattara, I. Nebie, E. Sanogo, S.N. Cousens and F. Esposito, 1999. Widespread Distribution of Insecticide-Impregnated Curtains reduces child mortality, prevalence and intensity of malaria infection and malaria transmission in rural Burkina Faso. Parassitologia, 41: 377-381.
7: Fontenille, D. and L. Lochouarn, 1999. The complexity f the malaria vectorial system in Africa. Parasitologia, 41: 267-271.
8: Gadzama, N.M., 1983. Mosquito vectors of the sahel savanna and environmental development. Ann. Borno, 1: 99-104.
Direct Link |
9: Gillet, J.D., 1972. Common African Mosquitoes and their Medical Importance. William Heinemann Medical Books Ltd., London, UK., Pages: 106
10: Guillet, P., 2001. Insecticide-treated nets in Africa: Where do we stand. Afr. Health, 23: S22-S24.
11: Horsfall, W.R., 1962. Medical Entomology: Arthropods and Human Diseases. Ronald Press Company, New York, USA., Pages: 467
12: Igbozurike, M., 1986. The Isuikwuato-Okigwe Region. Kato Press, Owerri, Nigeria, Pages: 248
13: Jambou, R., L. Ranaivo, L. Raharimalala, J. Randrianaivo and F. Rakotomanana et al., 2001. Malaria in the highlands of Madagascar after five years of indoor spraying of DDT. Trans. R. Soc. Trop. Med. Hyg., 95: 14-18.
14: Kalu, K., F.O. Nduka and P.E. Etusim, 2007. Qualitative Study of Anopheles species in Konduga Lake Area of Borno State, Nigeria. Anim. Res. Int., 4: 673-676.
Direct Link |
15: Kalu, K.M., N.A. Obasi, F.O. Nduka, V.O. Nwaugo and I.A. Onuabuchi, 2012. Abundance of nocturnal, endophagous and anthropophilic Anopheles species in relation to human malaria transmission in an urban and a rural community of Abia State, Nigeria. J. Entomol.
Direct Link |
16: Le Menach, A., F.E. McKenzie, A. Flahault and D.L. Smith, 2005. The unexpected importance of mosquito oviposition behaviour for malaria: Non-productive larval habitats can be sources for malaria transmission. Malaria J., 4: 23-23.
17: Service, M.W., 1997. Mosquito (Diptera: Culicidae) Dispersal-the long and short of it. J. Med. Entomol., 34: 579-588.
18: Service, M.W., 1993. Mosquito Ecology: Field Sampling Methods. Elsevier Applied Science, London, pp: 32-67
19: Sharma, V.P., 1999. Current scenario of malaria in India. Parasitologia, 41: 349-353.
20: Shililu, J.I., C.M. Mbogo, J.T. Gunter, C. Swalm and J.L. Regens et al., 2003. Spatial distribution of Anopheles gambiae and Anopheles funestus and malaria transmission in Suba district, Western Kenya. Int. J. Trop. Insect Sci., 23: 187-196.
21: Wanji, S., T. Tanke, S.N. Atanga, C. Ajonina, T. Nicholas and D. Fontenille, 2003. Anopheles species of the Mount Cameroon: Biting habits, feeding behaviour and entomological inoculation rates. Trop. Med. Int. Health, 8: 643-649.
CrossRef | PubMed | Direct Link |