Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum

Abstract

Background Besides feeding on blood, females of the malaria vector Anopheles gambiae sensu lato readily feed on natural sources of plant sugars. The impact of toxic secondary phytochemicals contained in plant-derived sugars on mosquito physiology and the development of Plasmodium parasites remains elusive. The focus of this study was to explore the influence of the alkaloid ricinine, found in the nectar of the castor bean Ricinus communis, on the ability of mosquitoes to transmit Plasmodium falciparum. Methods Females of Anopheles gambiae and its sibling species Anopheles coluzzii were exposed to ricinine through sugar feeding assays to assess the effect of this phytochemical on mosquito survival, level of P. falciparum infection and growth rate of the parasite. Results Ricinine induced a significant reduction in the longevity of both Anopheles species. Ricinine caused acceleration in the parasite growth rate with an earlier invasion of the salivary glands in both species. At a concentration of 0.04 g l−1 in An. coluzzii, ricinine had no effect on mosquito infection, while 0.08 g l−1 ricinine-5% glucose solution induced a 14% increase in An. gambiae infection rate. Conclusions Overall, our findings reveal that consumption of certain nectar phytochemicals can have unexpected and contrasting effects on key phenotypic traits that govern the intensity of malaria transmission. Further studies will be required before concluding on the putative role of ricinine as a novel control agent, including the development of ricinine-based toxic and transmission-blocking sugar baits. Testing other secondary phytochemicals in plant nectar will provide a broader understanding of the impact which plants can have on the transmission of vector-borne diseases. Graphical abstract

Using an antimalarial in mosquitoes overcomes Anopheles and Plasmodium resistance to malaria control strategies

“…These results support the use of antimalarials in ATSB-like strategies to reduce residual malaria transmission carried out by mosquitoes that predominantly rest and feed outside and thereby avoid both LLINs and IRS. While current proposed ATSB designs rely on insecticidal ingredients [ 24 , 25 , 47 ], the use of antimalarials in sugar baits could act as a more specific and environmentally benign paradigm for this promising intervention should suitable antimalarial ingredients be identified [ 48 – 50 ]. Future studies to assay mosquito choice, repellency behavior, and total drug ingestion when both treated and untreated sugar sources are presented will be important to ensure any end product can compete with natural sugar-nectar sources.…”

Intervention reducing malaria parasite load in vector mosquitoes: no impact onPlasmodium falciparumextrinsic incubation period and the survival ofAnopheles gambiae

“…In addition, trade-offs between lifespan and fecundity are expected [63] and further studies based on a more complete picture of individual mosquitoes' fitness are still needed. However, to date several previous studies suggest that resisting the infection induced a reduced survival of mosquitoes, consistent with a cost of resistance, although high variance was found between assays [40,64,65].…”

“…In addition, trade-offs between lifespan and fecundity are expected [63] and further studies based on a more complete picture of individual mosquitoes’ fitness are still needed. However, to date several previous studies suggest that resisting the infection induced a reduced survival of mosquitoes, consistent with a cost of resistance, although high variance was found between assays [40,64,65]. Therefore, to better depict the interactions between malaria vectors and parasites, future studies, using the non-destructive detection of parasite at the mosquito individual level, will still be needed to examine possible associations between vector survival and fecundity and parasite load and EIP.…”

Antimalarials in mosquitoes overcome Anopheles and Plasmodium resistance to malaria control strategies

“…These results support the use of antimalarials in ATSB-like strategies to reduce residual malaria transmission carried out by mosquitoes that predominantly rest and feed outside and thereby avoid both LLINs and IRS. While current proposed ATSB designs rely on insecticidal ingredients (23, 24, 46), the use of antimalarials in sugar baits could act as a more specific and environmentally benign paradigm for this promising intervention should suitable antimalarial ingredients be identified (47–49). ATQ uptake via tarsal contact at 3- or 6-days post infection also significantly reduced oocyst growth, resulting in an appreciable reduction in the proportion of salivary gland sporozoite-positive mosquitoes.…”