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Seasonal mosquito larval abundance and composition in Kibwezi, lower eastern Kenya.

Introduction

Mosquito larval habitats are the locations where many important life-cycle processes take place: oviposition, larval development, adult emergence, resting, swarming and mating (1). Effective control of malaria through vector management requires information on the distribution and abundance of vectors in the targeted areas. Mosquito larval control is a potentially important target in malaria vector control. Source reduction through modification of larval habitats was the key to malaria eradication efforts in the United States, Italy, and Israel (2). The suppression and even eradication of malaria from vast areas has been attributed to effective large-scale programmes to kill the immature Anopheles species vectors or reduce the amount of suitable habitat for them in proximity to vulnerable human populations (3-6). The appropriate management of larval habitats during the dry season may help suppress vector densities and consequently, malaria transmission. However, our understanding of anopheline larval ecology in Africa is insufficient and this affects the design and implementation of larval control.

National malaria control efforts in Kenya, as in most African countries, focus on case management and the use of insecticide-treated bednets (7). Currently in Kenya, there is a scaling-up of insecticide-treated bednets access and use to pregnant women and children under the age of five years (8). Domestic vector control interventions against adult mosquitoes in the form of insecticide-treated bednets (9) or indoor residual spraying (10), combined with improved access to effective diagnosis and treatment, have enormous potential to Roll Back Malaria and constitute the primary means to achieve the Abuja targets (11). However, even these highly effective interventions are insufficient to eliminate malaria transmission from most endemic parts of Africa (12,13).

Understanding the factors that regulate the size of mosquito populations is considered fundamental to the ability to predict transmission rates and for vector population control (14,15). Larval habitats are important determinants of adult distribution and abundance. Although the transient habitats of An. gambiae may not be a reasonable target for vector control, an understanding of the dynamics and productivity of larval habitats is required, if efforts to model and predict adult abundance are to succeed. To control mosquitoes, whether adults or larvae, it is crucial to understand the relevant ecology of the target species. This requires the study of not only the fluctuations of the adult populations, but also the factors affecting larval abundance and distribution. While considerable progress towards understanding the aquatic stages of An. gambiae sensu lato has been made in recent years (16-23), systematic research on the larval ecology of the main malaria vectors in Africa is still limited and often represents short data collection periods, frequently considering mosquito-infested habitats only. In contrast, more intensive larval ecology studies evaluating and acknowledging options for larval vector control have been conducted in central and southern America on various malaria vectors in the last decade (24-30).

During the rainy season, areas of rain-dependent agriculture have provision of ideal aquatic habitats that support high density of diverse mosquito species including vectors of malaria, filariasis and a number of arbovirus. Thus, there is an urgent need to address the problem of mosquito-borne diseases in these areas in order to reduce the risk of massive public health problems and economic loss due to sickness. Such a goal can only be achieved through integrated control of the diverse mosquito species occurring in these areas. Most of the work done in Kibwezi previously described different aspects of malaria including immunological responses in children under five years of age (31), asymptomatic malaria and nutritional inadequacies (as indicated by stunting) (32), and anti-malarial use (33). Malarial infection reported at the clinical facilities in the area is exclusively due to Plasmodium falciparum. There is no active malaria control programme in the area, and no epidemiological or entomological studies of malaria have been conducted previously. Although this area has been described as seasonal malaria transmission (31-34), and mosquito is major problem especially during both long and short rains, no effort has been made to describe the mosquito species composition. The objective of this study was to describe mosquito aquatic habitats, to determine larval abundance, species composition, and habitat types found in Kasayani village of Kibwezi division.

Material & Methods

Study village: The study was done in Kasayani village which lies at 37[degrees]36'44" E and 2[degrees]30'15" S. This village is in Kibwezi division and is 250 km east of Nairobi City. Kasayani village lies approximately 20 km north of Kibwezi town off the Kibwezi-Kitui Road and the University of Nairobi College of Arid and Range Management is situated at the northern end of this village.

The main physiography of the area is generally flat with very few sections of undulating ground especially where erosion has been rife. The village has an inclination of [+ or -] 1.22 and it is 1200 m above sea level on a very flat expanse of land. It receives rainfall within two seasons of the year--between March and May, and November and December. Mean annual temperatures range from 27-30 and 18-27[degrees]C maximum and minimum respectively. There are high evapo-transpiration and percolation rates, thus during rains, water is quickly lost to the atmosphere and to the ground respectively. However, there are some pools of water collection in some areas which last for a longer period of time. The mean annual rainfall is 500 mm.

The agricultural activities in this area include horticulture (including growing of kales (Brassica oleracea), tomatoes (Solanum lycopersicum), mangoes (Mangifera indica) and hot pepper (Capsicum spp), livestock farming (cattle, goats and sheep mostly by free range husbandry) and subsistence farming (including growing of maize (Zea mays), peas (Pisum sativum) and beans (Pisum sativum) mainly using the rain water.

Habitat type description: Larval habitats which were found within 2 km from the Kasayani village market center were sampled. This included: water reservoir tanks which were mainly rectangular in shape constructed with bricks and cement. They are mainly used to store water during construction and after they are converted to harvest rainwater. They are mainly open and about one meter high. Puddles were mainly small pools of water measuring <0.5 m in length and were mainly found within homesteads. Tyre tracks were mainly found along Kibwezi-Kitui Road. These were tyre marks found on the road as a result of the vehicles using this road. Temporary pools were mainly found on two valleys one on the upper side and other on the lower side of the village. The temporary pools were measuring >0.5 m in length.

Larval sampling: A cross-sectional larval sampling in December 2006 to generate stage-specific estimates of Anopheles and culicine larval densities and diversity was done. Further a second round of sampling was done in March 2007 in which all the habitats were re-visited. December is the peak of the rainy season in this area while March is the peak of dry season. Samples were taken using standard dipping techniques with a plastic dipper (BioQuip Products, Inc. California, U.S.A.). From each habitat type 2-10 dips were taken and the mosquito larvae collected and sorted to the sub-families as either anopheline or culicine. The anopheline and culicine larvae were grouped according to instars as early (L1 and L2), late (L3 and L4) and pupae. The late instars were preserved in 75% ethanol and identified morphologi cally (35,36).

Data analysis: Statistical analysis was done using SPSS software (Version 15.0 for Windows, SPSS Inc., Chicago, IL). The mosquito larvae were grouped as per sub-family and instars and summed for each larval habitat. Variation in larval densities between habitats was compared by Student t-test. One-way analysis of variance (ANOVA) was used to compare the differences in the number of mosquito larvae in different habitats. Where significant differences were detected in ANOVA, the means were separated by Tukey test highly significant difference. Variation in diversity of habitat types was compared using chi-square test. Statistical analyses were done using log transformed ([log.sub.10] n + 1) larval counts to normalize the data. Results were considered significant at p < 0.05.

Results

The habitat types found during this survey included water reservoir tanks (n = 3), puddles (n = 8), tyre tracks (n = 2) and temporary pools (n = 11) (Table 1). All these habitats were found to be dry at the second round of mosquito sampling. Further, observation showed that puddles, tyre tracks and temporary pools had very turbid water while water reservoir tanks had clear water. Tanks were found within the homesteads and were mostly used to harvest rainwater during the rainy season but they were all concrete and open. Temporary pools were located at the lower parts of two valleys found transversing the village. One-way ANOVA showed that there was no significant variation in Anopheles larval densities ([F.sub.(1,3)] = 1.399, p = 0.272) in the habitats whereas the tanks had significantly higher densities for culicine than other habitat types ([F.sub.(1,3)] = 10.736, p < 0.001). A total of 2660 mosquito larvae were collected, of which 2140 (80.45%) were culicines, 503 (18.91%) were Anopheles and 17 (0.64%) were pupae. For culicines, 1787 (83.5%) were categorized as early instars and 353 (16.5%) as late instars while in the Anopheles 425 (84.49%) were classified as early and 78 (15.51%) as late instars. Only 17 pupae were collected during this survey and they were predominantly found in water storage tanks. The density of early instars was 5.46-fold (t = 2.65, df = 1, p = 0.03) higher than late instars for Anopheles while it was relatively similar for culicines where the early instars were 5.21 higher than late instars (t = 1.83, df =1, p = 0.008).

During the sampling, six mosquito species were collected which included Anopheles gambiae complex 16.24% (n = 70), An. funestus 1.16% (n = 5), An. coustani 0.70% (n = 3), Culex quinquefasciatus 42.46% (n = 183), Cx. duttoni 6.26% (n = 27) and Ae. aegypti 33.18% (n = 143) (Table 2). Anopheles gambiae and Cx. quinquefasciatus were collected in all the habitat types while Ae. aegypti were found only in water reservoir tanks. Anopheles funestus and An. coustani were found only in puddles and pools while Cx. duttoni were found in water reservoir tanks, puddles and pools. Chi-square analysis indicated that anopheline and culicine larvae were more likely to coexist in the same habitats than would be expected by chance alone ([chi square] = 46.208, p < 0.01).

Discussion

This is the first entomological study in this study area which sought to understand the ecologies of mosquito larvae and mosquito species composition in this area. This study found Anopheles and Culex mosquito species together in the habitats. The habitats which were sampled in this study were formed after the onset of rains.

The habitats which were sampled during the study period included pools, puddles, tanks and tyre tracks. Most of the An. gambiae larvae were collected in temporary pools and puddles. Anopheles mosquitoes have been shown to frequently occur in small temporary pools, such as pits, tyre tracks, and animal footprints (17,18,37,38). In general, larval predation of mosquitoes is less prevalent in temporary habitats than it is in large, permanent habitats (39,40). Because small and sunlit habitats have higher water temperatures, mosquito larval-pupal developmental time may be shortened if the warmer habitat produces more food resources. Culicine larvae were collected in diverse habitat types but were predominantly collected in tanks (water reservoir containers). The Culex mosquitoes breed in a wide range of habitats although they have been able to exploit same habitats as Anopheles mosquitoes. Culex quinquefasciatus is predominantly associated with urban areas but occurring also in rural. This Cosmo-tropical urban mosquito Cx. quinquefasciatus preferentially breeds in organically rich water. With both anopheline and culicine larvae occurring in similar habitats, there is a need to have larval control programmes targeting all the habitats available in this area. This would ensure maximum reduction of mosquitoes consequently significantly reducing the risk of mosquito-borne diseases. A potentially important target of malaria vector control is the immature stages of anopheline mosquitoes (4,6). Source reduction through modification of larval habitats has been an important tool for malaria eradication efforts in the United States, Israel, and Italy (2). Recently, WHO has issued a Global Framework for Integrated Vector Management (IVM), stressing the importance of evidence-based combinations of vector control methods (41).

Our study collected important vectors for malaria, filariasis and haemorrhagic fevers. These vectors included An. gambiae, An. funestus (malaria), Cx. quinquefasciatus (filariasis and yellow fever) and Ae. aegypti (haemorrhagic fevers). Malaria has been documented as a predominant mosquito-borne disease in this area (31-33,42). Recently, an outbreak of Rift Valley Fever (RVF) was detected in late 2006 in the Garissa District of the north-eastern Province of Kenya and subsequently spread into other districts of Kenya and into Tanzania in early 2007, where it has caused considerable morbidity and mortality in both human and domestic ruminant populations (43). Rift valley fever virus (RVFV) has been responsible for numerous outbreaks of severe disease in ruminants in sub-Saharan Africa over the past 70 years (44), and those outbreaks have been associated with excessive rainfall in sub-Saharan Africa (45). Presence of some vectors incriminated in the transmission of RVFV, dengue fever, yellow fever and other haemorrhagic fevers exposes the inhabitants of this area to high risk of infection in the event of an outbreak. The transmission of malaria has been described in this area as seasonal (7,33,34) where higher number of cases are seen in December and in April coinciding with the peaks of long and short rains. Nevertheless, none of other mosquito-borne diseases has been described in the area despite the presence of their vectors. This calls for the public health advisory teams in this area to be alert especially during the rainy season and intensify the mosquito control campaign utilizing the integrated vector management approaches.

There is need for further entomological studies to describe the adult mosquito populations including their feeding, resting behaviours and role in disease transmission especially malaria which is the main mosquito-borne disease. Due to logistic problems we could not further analyze the An. gambiae Complex by polymerase chain reaction to their sibling species. In conclusion anopheline and culicine mosquitoes in these areas breed in temporary pools, puddles, tyre tracks and water reservoir tanks. The mosquito species present in this area predisposes the inhabitants of this area to the risk of infections of mosquito-borne diseases. This calls for an accelerated campaign of mosquito control in this area especially during the rainy season encompassing the integrated vector management approaches.

Acknowledgement

We would like to thank James Wauna, Peter Barasa and Enock Mpanga for technical assistance. This paper has been published with the permission from the Director of the Kenya Medical Research Institute.

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Joseph M. Mwangangi (a), Ephantus J. Muturi (b) & Charles M. Mbogo (a)

(a) Department of Entomology, Center for Geographic Medicine Research Coast, Kenya Medical Research Institute, Kilifi, Kenya; (b) Department of Medicine, William C. Gorgas Center for Geographic Medicine, Alabama, U.S.A.

Corresponding author: Joseph M. Mwangangi, Department of Entomology, Center for Geographic Medicine Research Coast, Kenya Medical Research Institute, P.O. Box 428--80108, Kilifi, Kenya.

E-mail: jmwangangi@kilifi.kemri-wellcome.org

Received: 20 June 2008 Accepted in revised form: 3 November 2008
Table 1. Mosquito larval abundance in the different
habitat types in Kasayani village

Habitat n * Anopheles Culicine Pupae
type

 Early Late Early Late
 instars instars instars instars

Tanks 3 81 10 1221 289 11
 ([dagger])
Puddles 8 97 19 231 18 2
Tyre tracks 2 26 6 30 4 0
Pools 11 221 43 305 42 4
Total 24 425 78 1787 353 17

* Number of habitats sampled; ([dagger]) Water reservoir tanks

Table 2. Species diversity in each habitat type

Habitat An. An. An.
type gambiae funestus coustani

Tanks 10 0 0
Puddles 17 1 1
Tyre tracks 6 0 0
Pools 37 4 2
Total 70 5 3

Habitat Cx. Cx. Ae.
type quinque- duttoni aegypti
 fasciatus

Tanks 140 6 143
Puddles 3 15 0
Tyre tracks 4 0 0
Pools 36 6 0
Total 183 27 143
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Author:Mwangangi, Joseph M.; Muturi, Ephantus J.; Mbogo, Charles M.
Publication:Journal of Vector Borne Diseases
Article Type:Report
Geographic Code:6KENY
Date:Mar 1, 2009
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