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Published in final edited form as: Curr Biol. 2014 Jan 9;24(2):217–221. doi: 10.1016/j.cub.2013.12.022

Plasmodium falciparum-infection Increases Anopheles gambiae Attraction To Nectar Sources and Sugar Uptake

Vincent O Nyasembe a, Peter EA Teal b, Patrick Sawa a, James H Tumlinson c, Christian Borgemeister a,d, Baldwyn Torto a,*
PMCID: PMC3935215  NIHMSID: NIHMS555072  PMID: 24412210

Summary

Plasmodium parasites are known to manipulate the behaviour of their vectors so as to enhance transmission [1–4]. From an evolutionary standpoint, behaviour 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 [5, 6]. However, it is unknown if this vector manipulation also affects vector-plant interaction and sugar uptake. Here, we show that the attraction of Anopheles gambiae s.s. to plant odours increased by 30% and 24% following infection with 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 revealed an increased sugar uptake at oocyst-stage which 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 behaviour manipulation of An. gambiae by P. falciparum to enhance transmission. We conclude that the nectar seeking behaviour 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.

Keywords: Plasmodium falciparum, Anopheles gambiae, oocyst, sporozoite, Parthenium hysterophorus, Ricinus communis, Bidens pilosa

Results

Experimental infection

Three- to five-day old mosquitoes were fed on either non-gametocytic blood (uninfected group) or P. falciparum gametocyte-positive blood (infected group) using membrane feeders. Three experimental infections were achieved with an average infection rate of 53.73% (geometric mean oocyst density± SEM = 8.17 ± 1.97, n = 360). No oocyst was detected in the mid-gut of the uninfected group of An. gambiae.

P. falciparum-infection increases An. gambiae attraction to nectar sources

Olfactory cues play an important role in the location of nectar sources by An. gambiae [7]. We studied olfactory responses of uninfected and P. falciparum-infected An. gambiae to three nectar sources, Parthenium hysterophorus (Asteraceae), Ricinus communis (Euphorbiacea) and Bidens pilosa (Asteraceae). A general linear model taking into account the infection rate and density was used to analyse the data. Our results revealed that parasite infection altered nectar seeking behaviour of An. gambiae. In the dual choice olfactory responses, there was an overall preference for odours from the three nectar sources by both uninfected and Plasmodium-infected An. gambiae. Infection with P. falciparum increased nectar source attraction by 30% (0.42 – 0.86 CI, P < 0.01) at oocyst stage and 24% (0.48 – 0.99 CI, P < 0.01) at sporozoite stage compared to uninfected An. gambiae of corresponding ages. In terms of odour preference, significant differences were also detected among the three nectar sources at oocyst (F(2, 56) = 17.94, P < 0.001) and sporozoite- (F(2, 56) = 6.35, P < 0.05) stages of the parasite development (Fig. 1).

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

Figure 1

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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. falciparum-infection increases An. gambiae probing on nectar sources

Nectar feeding is preceded by landing and probing activity on floral and extra-floral parts of the plant. We conducted a no-choice probing assay to study the effect of P. falciparum infection on probing activity of An. gambiae on the three nectar sources. Similarly, a general linear model taking into account the infection rate and density was used to analyse the data. Overall, infection with both oocyst- and sporozoite-stages of P. falciparum increased probing activity of An. gambiae by 77% (0.38 – 5.87 CI, P < 0.001) and 80% (0.44 – 6.87 CI, P < 0.001), respectively, on the three nectar sources. Significant differences in probing activity was also detected between the three nectar sources (F(2, 80) = 55.78, P < 0.01) with P. hysterophorus having the highest number of An. gambiae probing (PR = 1.66, 1.2023702 – 2.349070 CI, P <0.01) followed by R. communis (PR = 1.27, 0.8815493 – 1.793855 CI) while B. pilosa was the least attractive (PR = 1). However, there was no significant interaction between nectar source and infection status (Fig. 2).

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

Figure 2

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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.

P. falciparum-infection alters An. gambiae sugar uptake and energy reserves

As evidence of actual plant probing, we analysed both uninfected and Plasmodium-infected An. gambiae for total sugar content using hot anthrone test following probing assays. Overall, the infection with oocyst-stage of P. falciparum significantly increased the amount of sugar uptake by An. gambiae from the different nectar sources (F(1, 24) = 14.69, P < 0.001), with An. gambiae obtaining the highest sugar amount from P. hysterophorus when infected (P < 0.05) (Fig.3). On the contrary, sugar uptake was significantly compromised at the sporozoite stage (F(1, 24) = 14.75, P < 0.001). The uptake of sugar in uninfected An. gambiae was higher from each of the three nectar sources than their sporozoite-infected counterparts, with a significant difference in the amount of sugar uptake detected among those probing on R. communis (P <0.01).

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

Figure 3

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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.

In addition, we tested for the effect of P. falciparum infection on glycogen and lipid reserves after 7 days (oocyst-stage) and 12 days (sporozoite) post infection. Our results show that infection with both oocyst- and sporozoite-stages of the parasite did not significantly affect the glycogen reserves but the sporozoite stage severely depleted lipid reserves (uninfected = 0.61; infected = 0.39; P < 0.001) (Fig. 4).

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

Figure 4

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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.

Discussion

Our results clearly indicate that infection with P. falciparum alters the behaviour of An. gambiae towards the three nectar sources. Both dual choice olfactometer and probing assays showed a marked increase in plant attraction and acceptance at oocyst and sporozoite stages of the parasite development, suggesting either physiological adjustment in An. gambiae due to the infection resulting in change in behaviour or behaviour manipulation of the vector by the parasite. Behaviour manipulation by malaria parasites on their host vectors has been reported for various Plasmodium species in vertebrate host-vector interactions, in which sporozoite-stage Plasmodium-infected mosquitoes were found to be highly attracted to their vertebrate host [1, 4, 8, 9]. Also, Plasmodium-infected vertebrate hosts have been reported to be more attractive to uninfected mosquitoes than uninfected hosts [3, 10]. Although nectar feeding is known to play a critical role in the survival of malaria vectors [11, 12], this is the first study to demonstrate possible physiological adjustment of P. falciparum-infected An. gambiae and/or behaviour manipulation by P. falciparum of the vector towards nectar sources. Increased vertebrate host attraction of malaria vectors confers evolutionary advantage to the parasite as it increases hostvector contact, thus enhanced chances of transmission [1, 6, 13]. On the other hand, increased vertebrate host attraction during non-transmissible stages of the parasite would be disadvantageous to the parasite since vertebrates are physically aggressive hence the high risk of untimely vector mortality [5, 14]. This suggests that in the evolutionary arms race, the selective pressure on An. gambiae appears to favour their plant nectar feeding during the non-infective stages of the parasite development, thus reducing feeding-associated vector mortality.

Our results further point to increased sugar uptake by infected An. gambiae at oocyst stage of the parasite while at the sporozoite stage, the sugar uptake was compromised. These results corroborate previous findings [15, 16], but they also underpin the important mechanisms involved in the possible vector manipulation by the parasite. While the increased sugar uptake at the oocyst-stage of the parasite can be explained by either the adjustment by An. gambiae to compensate for the energy deficit created by the parasite infection, or the parasite manipulation to increase sugar intake for its own metabolism and for improved vector survival [15], the reduced sugar uptake at the sporozoite stage is not in tandem with the observed increase in probing activity. The invasion of the salivary glands of the vector by the sporozoite-stage of the parasite has been linked to reduced apyrase activity with resultant increase in probing time [8, 13, 17]. Sporozoite infection has also been associated with difficulties in taking complete blood meals, with resultant persistent attempts to initiate new blood uptake [2]. Further evidence also points to altered levels of a number of proteins in the head of An. gambiae following infection with sporozoite stage of Plasmodium berghei. These include the synapse-associated proteins which could potentially affect the olfactory system [18]. Whichever the case, this is expected to confer transmission advantage to the parasite as many sporozoites are transferred to new vertebrate hosts with every feeding attempt. Therefore, we suggest that the observed increase in plant probing activity accompanied by reduced sugar uptake could possibly be an extrapolated effect of reduced apyrase activity or an altered olfactory system or both, resulting in impaired ability to imbibe on plant nectars and/or increased plant attraction.

Given that most parasitic infections exert energetic costs to their host vectors [19, 20], with resultant loss of reproductive potential and reduced lifespan [21–25], it is possible that the malaria vector’s quest for increased probing is to meet its own metabolic demands and that of the growing oocyst. Studies on the effect of Plasmodium infection on vector longevity are conflicting, with majority showing vector survival is unaffected, but some showing reduced vector survival [24]. Selection for Plasmodium-vector interactions that favour vector survival over reproduction has been suggested [5, 26] but more studies are needed to fully understand the effect of parasite infection on the energetic budget of mosquito vectors [6]. Zhao et al. [27] recently demonstrated increased survival of P. berghei-infected An. gambiae and An. stephensi compared to uninfected mosquitoes when they are subjected to starvation. They attributed this to decreased carbohydrate catabolism accompanied by enhanced expression of insulin-like peptides that lead to higher glycogen accumulation. Our study further demonstrates no effect on glycogen reserves of An. gambiae following infection with P. falciparum though the infected vectors had slightly higher glycogen reserves at the oocyst stage than their uninfected counterparts. These results further point to possible vector manipulation by the parasite to ensure sufficient energy supply, hence sustained vector survival that ensures completion of the sporogonic cycle, or physiological adjustment by the vector to parasite infection. However, further studies need to be carried out to fully understand the effect of P. falciparum infection on the vector energetic reserves.

The reduced lipid level, particularly at the sporozoite stage is noteworthy. Lipids have been implicated in Plasmodium-mosquito interactions [28]. While our study serves to shed more light into possible involvement of lipids in these Plasmodium-vector interactions, more studies are needed to further elucidate their role in the outcome of such interactions. It is possible that lipid reserves are depleted by the parasites’ invasion of the mid-gut epithelial cells either through destructive migratory activity or through formation of capsules around the oocyst stages [29]. Alternatively, the observed depletion of lipid reserves at the sporozoite stage of infection could be explained by the fact that developing oocysts normally sequester lipids for their structural development [28].

Rivero and Ferguson [15] alluded to a possible protective role played by high sugar intake which increases the ability of An. stephensi to synthesize nitric oxide, a defence molecule in its immune response. The observed increase in sugar uptake at oocyst stage further strengthens this argument given that this is the most virulent stage of the parasite in the mosquito vector [30, 31]. However, substantive studies on the metabolic pathway involving sugar uptake in P. falciparum-infected An. gambiae are needed to verify this possibility. Overall, these studies highlight a possible co-evolutionary relationship between the malaria parasite and its vector which results in minimal damage to both.

Conclusions

In conclusion, our findings highlight the influence of P. falciparum on nectar seeking behaviour of An. gambiae, which is similar to the previous results found for the parasite-infected vectors seeking a vertebrate host for a blood meal. In both cases, it appears that the nectar seeking behaviour is governed by the physiological adjustment by the vector to a P. falciparum invasion or the parasite’s need to advance its transmission while minimizing vector mortality. These results suggest evolutionary behaviour modification that is advantageous for both survival of the vector and parasite transmission. This study exemplifies the need to understand the mechanisms underlying vector-parasite interactions in malaria systems which is of paramount importance for disease control.

Supplementary Material

01

Highlights.

  • Plasmodium-infected Anopheles gambiae responds more strongly to nectar odours

  • Plasmodium-infected Anopheles gambiae probe more strongly on nectar sources

  • Plasmodium-infected Anopheles gambiae have higher plant sugar uptake

  • Plasmodium falciparum infection depletes lipid reserves of Anopheles gambiae

Acknowledgements

We are grateful to all the staff at the icipe Mbita and Duduville campuses who provided support without which our research would not have been possible. Special thanks are extended to Woodbridge A. Foster for critical review of the manuscript and Daisy Salifu for assistance with the statistical analysis. We also appreciate the technical assistance from George Omweri of icipe’s St Jude clinic in Mbita, Tom Guda and his team of vector competence unit and the staff at the insectary unit at Mbita and Onesmus Wanyama, Milka Gitau and Richard Ochieng’ at icipe Duduville. We thank Simon Mathenge (formerly of the Botany Department, University of Nairobi) for help in identification of plants. This study was funded in part by Centre for Medical, Agricultural, and Veterinary Entomology, U.S. Department of Agriculture and by the U.S. National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases (NIAID) grant R01A1077722 to Woodbridge A. Foster. VON was supported by icipe and the World Federation of Scientists. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Footnotes

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Author contributions

Conceived and designed the experiments: VON PEAT JHT CB BT. Performed the experiments: VON PS BT. Analysed the data: VON BT. Wrote the paper: VON PEAT PS JHT CB BT. All authors approved the final version for submission.

Supplemental Information

Supplemental Information contains Supplemental Experimental Procedures and supplemental references.

Competing Interests: The authors have declared that no competing interests exist.

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Supplementary Materials

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