Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake

Abstract

Plasmodium parasites are known to manipulate the behavior of their vectors so as to enhance transmission. From an evolutionary standpoint, behavior manipulation by the parasite should expose the vector to limited risk of early mortality while ensuring sufficient energy supply for both it and the vector. However, it is unknown whether this vector manipulation also affects vector-plant interaction and sugar uptake. Here, we show that the attraction of Anopheles gambiae s.s. to plant odors increased by 30% and 24% after infection with the oocyst and sporozoite stages of Plasmodium falciparum, respectively, while probing activity increased by 77% and 80%, respectively, when the vectors were infected with the two stages of the parasite. Our data also reveal an increased sugar uptake at the oocyst stage that decreased at the sporozoite stage of infection compared to uninfected An. gambiae, with depletion of lipid reserves at the sporozoite stage. These results point to a possible physiological adjustment by An. gambiae to P. falciparum infection or behavior manipulation of An. gambiae by P. falciparum to enhance transmission. We conclude that the nectar-seeking behavior of P. falciparum-infected An. gambiae appears to be modified in a manner governed by the vector's fight for survival and the parasite's need to advance its transmission.

Figure 1. Olfactometer responses of different stages of Plasmodium-infected Anopheles gambiae to intact plant odours

A: Oocyst stage; B: Sporozoites stage; uninfected, comprising blood-fed An. gambiae of corresponding ages to oocyst- and sporozoite-stage infected mosquitoes were used as controls; eight replicates of each experiment comprising 10 mosquito per mosquito group/plant were conducted; error bars indicate standard error of means; bars capped with * indicate difference between test and control for each plant species at P < 0.05.

Figure 2. Probing responses of different stages of Plasmodium-infected Anopheles gambiae on different plant species

A: Oocyst stage; B: Sporozoites stage; uninfected, comprising blood-fed An. gambiae of corresponding ages to oocyst- and sporozoite-stage infected mosquitoes were used as controls; eight replicates of each experiment comprising 10 mosquito per mosquito group/plant were conducted; error bars indicate standard error of means; bars capped with * indicate difference between test and control for each plant species at * P< 0.05, ** P< 0.01, *** P< 0.001.

Figure 3. Mean amount of total sugar content in oocyst- and sporozoite-stage Plasmodium-infected Anopheles gambiae

A: Oocyst stage; B: Sporozoites stage; the total sugar content was measured on day 7 (during oocyst stage of parasite development) and day 12 (sporozoite stage) post-infection for each group of mosquitoes probing on each plant species; uninfected, comprising blood-fed An. gambiae of corresponding ages to oocyst- and sporozoite-stage infected mosquitoes that probed on the three plant species were used as controls; error bars show the standard error of means, total number of each group of An. gambiae per plant species (n) = 40, bars capped with asterisk are significantly different from the corresponding controls at * P < 0.05, ** P < 0.01.

Figure 4. Mean amounts of glycogen and lipid content in oocyst- and sporozoite-stage Plasmodium-infected Anopheles gambiae

The total sugar content was measured on day 7 (during oocyst stage of parasite development) and day 12 (sporozoite stage) for each group of mosquitoes; uninfected, comprising blood-fed An. gambiae of corresponding ages to oocyst- and sporozoite-stage infected mosquitoes were used as controls; total number of each group of An. gambiae (n) = 120, bar capped with asterisk (*) is significantly different from the corresponding uninfected mosquito counterparts at P <0.05.