Field assessments in western Kenya link malaria vectors to environmentally disturbed habitats during the dry season

The World Health Organization estimates that 300 to 500 million people are diagnosed with malaria annually, causing 1.1 to 2.7 million deaths. Approximately 1 million of these deaths are among children in sub-Saharan Africa, where 90% of all malaria cases occur [1]. During the 1950's and 1960's, a coordinated world-wide effort succeeded in eliminating malaria transmission within countries with temperate climates, and dramatically reduced malaria transmission in many other countries. Since the collapse of this campaign, malaria has since resurged, surpassing pre-campaign infection rates in many places, and entering previously unaffected locations [2]. The global resurgence of malaria has been attributed to a number of factors: drug-resistant parasites, insecticide-resistant vectors, population shifts, war-damaged infrastructures, altered meteorological conditions, and drastic ecological transformation [1, 2].

The first recorded epidemic of malaria in the highlands of western Kenya occurred in 1918/19, with additional epidemics occurring periodically until 1950 [3]. These initial epidemics were associated with both population movements and progressive construction of roads and a railway through the highlands. With these human activities, new aquatic habitats were created, facilitating a gradual spread of parasites and vector mosquitoes into the highlands from the low-lying hyperendemic-disease areas [4]. Adoption of an extensive malaria control program [5] temporarily kept the highlands free from epidemics.

Since the 1980s, however, the incidence of highland malaria and frequency of epidemics have been increasing, with severe outbreaks in 1995, 1998/99, [6–9] and most recently in May through July, 2002. Fifteen districts are now considered epidemic-prone by the Kenyan government [10]. Climate changes have poorly predicted epidemics in the East African highlands [11–14]. Hay et al. [11] suggest that intrinsic population dynamics are more likely the cause of vector fluctuations. Investigators reviewing Kericho District tea plantation records [9, 15, 16] found no obvious change in average temperature or rainfall over the previous 20–30 years, stable tribal/ethnic composition in the study area, and a properly maintained health care system. These studies suggest a failure of medications was the most likely cause for the recurrence of malaria epidemics in the highlands. However, due to the retrospective approach, these studies were unable to investigate environmental/ecological changes in the highlands or evaluate the role of malaria vectors, as had been done for earlier epidemics [4].

Following the 2002 epidemic, this study was conducted to identify the ecological and socioeconomic variables affecting malaria vector densities and distributions. In this paper we connect specific man-made aquatic habitats present during the dry season with malaria vector larvae in western Kenya.

Our study shows that man-made larval habitats were the predominant (87.5%) source of malaria vectors in Mosocho Division during the dry season. In particular, the continuously disturbed, functional brick-making pits contained high densities of malaria-vectoring mosquitoes. PRAs revealed that small brick-making groups have developed into large-scale industries over the past two decades, and brick-making is now dispersed throughout the highlands in unfarmable wetlands. Because brick-making occurs predominantly in the dry season, it may aid in maintaining vector populations year-round.

Additionally, houses closest to brick-making pits had malaria vectors present within them. While the number of mosquitoes captured during a single transect of spray-catches was only one per house, this represents a real, if low, possibility of malaria transmission during the dry season at these locations. Thus brick-making areas may function as refugia for malaria parasites and their vectors over the dry season, facilitating spread of malaria when habitats become more plentiful in the wet season.

In this study we found emergent vegetation to be negatively associated with presence of malaria vectors in man-made habitats. This association may be a result of an association of both emergent vegetation and predator diversity with habitat age. In continually disturbed habitats (such as functional brick-making pits), the habitats are kept at a low stage of biological succession, possessing fewer species of both plants and animals. There may also be a direct effect of vegetation on the trophic dynamics in ground pools. In structurally simple habitats, intraguild predation has been shown to suppress the diversity of important predators [21–23]. Whether due to co-associated variables, direct effects, or some combination, there was a sizable 57% increase in predator taxa found in abandoned, vegetated pits and a >50% reduction of Anopheles larval densities. More research into the ecology of small aquatic pools will help clarify the interrelationships of these variables.

In ground pools, predators are typically thought to regulate the density of mosquito larvae [24, 25]. Predators may exert an effect by consuming larvae or through deterring oviposition into an otherwise suitable habitats[26]. During the dry season, disturbed, man-made habitats (such as functional brick-making pits and quarries) provide a developmental habitat in which Anopheles larvae escape the high degree of predation found in the natural environment. These habitats should be specifically targeted during larval control programs. With substantial socioeconomic motivation for brick-making in the highlands, traditional source reduction (eliminating standing water) is unsustainable, and larvicides should be employed. Further research is needed on the use of these habitats by mosquito larvae during the wet season.

The negative correlation between predator diversity and mosquito density suggests that pesticide application may exacerbate epidemics by decreasing predation pressure if used in natural habitats. Pesticide applications can be selectively harmful to larger predators such as dragonflies and large dytiscid beetles which take months to years to develop[27]. In contrast, larvicides have a smaller impact on rapidly developing insects such as mosquitoes, which can reach maturity in a week. Rapid recolonization of predator-free habitats by mosquitoes would lead to vector resurgence [8, 28]. Thus, targeting larvicide application to disturbed aquatic habitats should lead to a better mosquito control than treating all available habitats.

The social and economic benefits accompanying disease reduction through vector control was demonstrated in the Zambian copperbelt [29]. As the population density of the highlands of western Kenya grows, the social and economic costs of malaria are likely to grow as well, unless vector-centered interventions (including environmental management, larvicide application, and vector surveillance systems) are used to confront the disease.