Temperature impacts the transmission of malaria parasites byAnopheles gambiaeandAnopheles stephensimosquitoes

Abstract

<jats:p>Transmission of malaria and other vector-borne diseases (VBDs) is greatly influenced by environmental factors, especially temperature, due to the ectothermic nature of insect and arthropod vectors. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically non-linear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites, Plasmodium falciparum and Plasmodium vivax, by two malaria vector species, Anopheles gambiae and Anopheles stephensi. We model the non-linear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, egg to adult survival, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito-parasite combinations assessed in this study. The main differences are found at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (An. stephensi) and between mosquitoes carrying P. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g., An. stephensi and An. gambiae both with P. falciparum). Using prevalence data from Africa and Asia, we show that the transmission suitability metric S(T) calculated from our mechanistic model is an important predictor of malaria prevalence. We mapped risk to illustrate the areas in Africa and Asia that are suitable for malaria transmission year-round based temperature. The wider thermal range of transmission by An. stephensi for both malaria parasites allows for a greater geographic potential for malaria spread. This study could be useful in planing preventive strategies for areas where malaria outbreaks might occur.</jats:p>

Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential

“… Data points extracted from Villena et al . [ 61 ] were fit to a quadratic function using the nls function in R as described in Mordecai et al . [ 30 ].…”

Scaling effects of temperature on parasitism from individuals to host–parasite systems

“…Moreover, in the mosquito -parasite systems, which tended to have high population-level parasitism Topt (Fig. 2), biting rate-a driver of host contact-usually has one of the highest optimal temperatures of all measured traits (Mordecai et al 2013(Mordecai et al , 2017(Mordecai et al , 2019Shocket et al 2018aShocket et al , 2020Villena et al 2020). These empirical systems are in line with our model results that show that transmission-related traits with high thermal optima can somewhat shift thermal optima of R0 away from that of individual-level parasitism, though not to such an extent that population-level parasitism will peak at the same temperature as the transmission-related traits (Fig.…”

“…We sought out systems for which measures of host performance (e.g., lifetime reproduction), individual-level parasitism (e.g., parasite burden, parasite reproduction within the host, time spent infected), and population-level parasitism (e.g., R0, prevalence) were documented across temperatures, allowing us to identify Topt for each of these measures. While not an exhaustive list, we identified thirteen systems that matched these requirements (Table 1): four mosquito -virus systems (Mordecai et al 2013;Shocket et al 2018a;Tesla et al 2018;Mordecai et al 2019;Shocket et al 2020), four mosquito -malaria parasite systems (Villena et al 2020), two Daphnia -parasite systems (D. magna -O. colligata, Kirk et al 2018Kirk et al , 2020D. dentifera -M. bicuspidata, Shocket et al 2018), two amphibian -B. dendrobatidis (Bd, the causative agent of chytridiomycosis) systems (Cohen et al 2017), and one crab -rhizocephalan barnacle parasite system (E. depressus -L. panopaei; Gehman et al 2018).…”

Solar geoengineering could redistribute malaria risk in developing countries

“…More recent work suggests this may be deeply interlinked with vector biology, and that the lower critical temperatures of P. vivax may in fact be largely driven by the An. stephensi mosquito in south Asia (44); comparatively less is known about P. vivax in the Americas.…”

“…The copyright holder for this preprint this version posted October 25, 2020. ; https://doi.org/10.1101/2020.10.21.20217257 doi: medRxiv preprint studies since have proposed adjustments to these limits, based on further mathematical modifications of the R0(T) model (e.g., the inclusion of daily thermal variation through an integral process), but we chose to stay with these estimates as the most similar to the experimental limits that have been observed for transmission (which has been seen as low as 16°C). For Plasmodium vivax in southern Asia, we used a more recent estimate by (44), which assumes that transmission by An. stephensi occurs between 15.7°C and 32.5°C.…”