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. 2016 Aug 4;12(8):e1005773.
doi: 10.1371/journal.ppat.1005773. eCollection 2016 Aug.

Plant-Mediated Effects on Mosquito Capacity to Transmit Human Malaria

Domonbabele F D S Hien  1 , Kounbobr R Dabiré  1 , Benjamin Roche  2 , Abdoulaye Diabaté  1 , Rakiswende S Yerbanga  1 , Anna Cohuet  3 , Bienvenue K Yameogo  1 , Louis-Clément Gouagna  3 , Richard J Hopkins  4 , Georges A Ouedraogo  5 , Frédéric Simard  3 , Jean-Bosco Ouedraogo  1 , Rickard Ignell  6 , Thierry Lefevre  1   3
Affiliations

Plant-Mediated Effects on Mosquito Capacity to Transmit Human Malaria

Domonbabele F D S Hien et al. PLoS Pathog. .

Abstract

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Effect of sugar treatment on the early development of P. falciparum, and on the survival and fecundity of malaria-exposed Anopheles coluzzii.
(a) Infection rate (± 95% CI), expressed as the proportion of mosquitoes exposed to an infectious blood meal and harboring at least one oocyst in their midgut, over 4 replicates and using a total of 7 gametocyte carriers. Numbers in brackets indicate the total number of mosquitoes dissected 7 days post infection (dpi) for each sugar treatment. Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (b) Infection intensity (± se), expressed as the mean number of developing oocysts in the guts of infected females, over 4 replicates and using a total of 7 gametocyte carriers. Numbers in brackets indicate the total number of infected mosquitoes for each sugar treatment. Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (c) Survivorship of malaria-exposed mosquitoes for each sugar treatment over 4 replicates and using a total of 7 gametocyte carriers. Survival was recorded twice a day from 1 to 7 dpi. (d) Egg incidence (± 95% CI) of malaria-exposed mosquitoes, expressed as the proportion of mosquito females carrying fully matured eggs inside their ovaries on 7 dpi for each sugar treatment and infection status.
Fig 2
Fig 2. Effect of sugar treatment on the sporozoite index and EIP.
(a) Sporozoite index (± 95% CI), expressed as the proportion of mosquitoes exposed to an infectious blood meal and having disseminated sporozoites in their head/thoraces, over 2 replicates and using a total of 4 gametocyte carriers. Numbers in brackets indicate, for each sugar treatment, the total number of mosquitoes analyzed with PCR on 14 days post infection (dpi). Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (b) Survivorship of malaria-exposed mosquitoes for each sugar treatment over 2 replicates, and using a total of 4 gametocyte carriers. Survival was recorded twice a day from 1 to 14 dpi. (c) Sporozoite index (± 95% CI) over time and using a total of 2 gametocyte carriers. *p<0.05; **p < 0.01, NS: non-significant difference between sugar treatment
Fig 3
Fig 3. Effects of sugar treatment and infection status on mosquito longevity.
Bars show the mean adult longevity ± 1 SE of uninfected control, exposed-uninfected and infected mosquitoes held on one of four sources of sugar. Numbers in brackets indicate, for each sugar treatment, the total number of mosquitoes monitored.
Fig 4
Fig 4. Theoretical difference in the distribution of outbreak sizes among plant sugars.
(a) Epidemiological outcomes predicted by the model for each plant species considered in isolation, and (b) in a community perspective. In urban areas (upper panel), Thevetia neriifolia is relatively more abundant than Barleria lupilina and Lannea microcarpa. Four configurations with various relative abundances were considered: (i) a scenario of no diversity whereby T. neriifolia—the dominant plant—represents 100% of the feeding opportunities, (ii) a scenario of 60% T. neriifolia, 30% B. lupilina and 10% L. microcarpa, (iii) a scenario of 60–20–20%, and (iv) a scenario of equal feeding opportunities on each plant species. In rural areas (lower panel), L. microcarpa is relatively more abundant than T. neriifolia and B. lupilina. The same configurations as for urban areas were considered using this ranking. Outbreak size is the proportion of humans that has been infected at the end of the transmission season after one infectious human was introduced into the population. The box plots indicate the median (large horizontal bars), the 25th and 75th percentiles (squares), the minimum and maximum values (whiskers) and outliers (circles).
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Publication types

Grants and funding

The work was funded by the ANR grant 11-PDOC-006-01 to TL (http://www.agence-nationale-recherche.fr). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.