Date Published: August 4, 2016
Publisher: Public Library of Science
Author(s): Domonbabele F. d. S. Hien, Kounbobr R. Dabiré, Benjamin Roche, Abdoulaye Diabaté, Rakiswende S. Yerbanga, Anna Cohuet, Bienvenue K. Yameogo, Louis-Clément Gouagna, Richard J. Hopkins, Georges A. Ouedraogo, Frédéric Simard, Jean-Bosco Ouedraogo, Rickard Ignell, Thierry Lefevre, Kenneth D Vernick.
The ecological context in which mosquitoes and malaria parasites interact has received little attention, compared to the genetic and molecular aspects of malaria transmission. Plant nectar and fruits are important for the nutritional ecology of malaria vectors, but how the natural diversity of plant-derived sugar sources affects mosquito competence for malaria parasites is unclear. To test this, we infected Anopheles coluzzi, an important African malaria vector, with sympatric field isolates of Plasmodium falciparum, using direct membrane feeding assays. Through a series of experiments, we then examined the effects of sugar meals from Thevetia neriifolia and Barleria lupilina cuttings that included flowers, and fruit from Lannea microcarpa and Mangifera indica on parasite and mosquito traits that are key for determining the intensity of malaria transmission. We found that the source of plant sugar meal differentially affected infection prevalence and intensity, the development duration of the parasites, as well as the survival and fecundity of the vector. These effects are likely the result of complex interactions between toxic secondary metabolites and the nutritional quality of the plant sugar source, as well as of host resource availability and parasite growth. Using an epidemiological model, we show that plant sugar source can be a significant driver of malaria transmission dynamics, with some plant species exhibiting either transmission-reducing or -enhancing activities.
The ability of anopheline mosquitoes to transmit Plasmodium falciparum malaria is a complex phenotypic trait, determined by mosquito and parasite genetic factors, environmental factors, as well as the interaction between these factors [1–6]. A key environmental variable for host-parasite relationships is the availability and quality of food resources, which have been shown to influence host susceptibility, parasite infectivity and virulence, and ultimately disease dynamics . The influence of diet on infectious diseases is particularly apparent in tritrophic interactions involving herbivorous insects, their parasites and larval food plants . Such plant-mediated effects have often been attributed to either the direct toxic effect of plant secondary metabolites on parasite development , or differences in nutritional value that, in turn, affect host immunocompetence .
Feeding on different sources of natural plant-derived sugars can influence key traits that affect the capacity of mosquitoes to transmit malaria, including mosquito longevity and mosquito susceptibility to P. falciparum. When combined into an epidemiological model these effects have important consequences for malaria transmission. Compared to control mosquitoes fed on a 5% glucose solution, individuals fed on T. neriifolia showed a 30% decrease in malaria transmission. In contrast, mosquitoes fed on L. microcarpa and B. lupilina showed a 30% and 40% increase in transmission potential, respectively. Previous research has revealed the role of sugar in providing energy for flight, increasing mosquito survival and fecundity and decreasing biting rate on vertebrate hosts [12,23]. Our findings add a more direct effect of epidemiological importance by showing that plant-derived sugars can modulate mosquito-Plasmodium interactions.