Impact of the intensity of infection in birds on Plasmodium development within Culex pipiens mosquitoes

Abstract

Abstract Background In vector-borne diseases, invertebrate hosts are exposed to highly variable quantities of parasites during their blood meal. This heterogeneity may partly explain the overdispersed distribution of parasites within the vector population and the variability in the extrinsic incubation period (EIP) of the parasite. Indeed, the quantity of parasites ingested is often considered as a good predictor of the quantity of parasites that will develop within the vectors, as well as the speed at which they will develop (i.e. EIP). However, density-dependent processes can influence the relationship between parasite burden in the vertebrate host and in vectors, making this relationship unclear at times. Methods Here, we used an avian malaria system to investigate whether the proportion of red blood cells infected by sexual and/or asexual stages of Plasmodium relictum influences the intensity of infection and the EIP within vectors. For this purpose, we experimentally infected 12 birds in order to generate a range of infection intensity. More than 1000 mosquitoes took a blood meal on these hosts, and the development of Plasmodium within the vectors was followed for more than 20 days. Results Our study reveals a negative relationship between the intensity of infection in birds and the time until 10% of mosquitoes become infectious (EIP10). A period of only 4 days was sufficient to detect sporozoites in at least 10% of mosquitoes fed on the most infected hosts. However, the number of sporozoites did not vary significantly according to the vertebrate host intensity of infection, but was positively correlated to the oocyst burden (parasitic stage preceding the sporozoite stage). Conclusions While the quantity of ingested parasites had no impact on oocyst and sporozoite burden in infectious mosquitoes, the EIP10 was affected. Studies have demonstrated that small changes in the EIP can have a significant effect on the number of mosquitoes living long enough to transmit parasites. Here, we observed a difference of 4–6 days in the detection of the first sporozoites, depending on the intensity of infection of the bitten vertebrate host. Considering that a gonotrophic cycle lasts 3–4 days, the shortened EIP may have significant effects on Plasmodium transmission. Graphical Abstract

Keywords

• Aggregated distribution
• Avian malaria
• Extrinsic incubation period
• EIP
• Transmission
• Overdispersion