Influence of climate on malaria transmission depends on daily temperature variation

Abstract

Malaria transmission is strongly influenced by environmental temperature, but the biological drivers remain poorly quantified. Most studies analyzing malaria-temperature relations, including those investigating malaria risk and the possible impacts of climate change, are based solely on mean temperatures and extrapolate from functions determined under unrealistic laboratory conditions. Here, we present empirical evidence to show that, in addition to mean temperatures, daily fluctuations in temperature affect parasite infection, the rate of parasite development, and the essential elements of mosquito biology that combine to determine malaria transmission intensity. In general, we find that, compared with rates at equivalent constant mean temperatures, temperature fluctuation around low mean temperatures acts to speed up rate processes, whereas fluctuation around high mean temperatures acts to slow processes down. At the extremes (conditions representative of the fringes of malaria transmission, where range expansions or contractions will occur), fluctuation makes transmission possible at lower mean temperatures than currently predicted and can potentially block transmission at higher mean temperatures. If we are to optimize control efforts and develop appropriate adaptation or mitigation strategies for future climates, we need to incorporate into predictive models the effects of daily temperature variation and how that variation is altered by climate change.

Fig. 1.

Mean monthly temperature and mean monthly DTR throughout Africa for January, April, July, and October. Temperature surfaces were generated by interpolation using weather station data collected between 1960 and1990. For areas where data records were limited, such as in the Democratic Republic of the Congo, the time period was extended to 2000. The current geographical limits of malaria transmission are illustrated by the dotted lines.

Fig. 2.

Growth rate and dissemination of P. chabaudi malaria in An. stephensi mosquitoes under constant and fluctuating temperature regimens. Mosquitoes were kept at either constant temperatures (dashed red lines) or temperatures with a diurnal temperature fluctuation of ±6 °C (DTR = 12 °C; solid blue lines). Baseline mean temperatures were (A) 16 °C, (B) 18 °C, (C) 24 °C, and (D) 26 °C. The number of sporozoites per oocyst (circles, Left) describes parasite growth kinetics up to the point of first sporozoite release. Dissemination (squares, Right) describes the percentage of mosquitoes that were observed with mature sporozoites circulating in the hemocoel. Error bars equal the SEM. Drawings of oocysts are generated by the Centers for Disease Control and Prevention (http://www.dpd.cdc.gov/dpdx/HTML/Malaria.htm).

Fig. 3.

Interaction plot of the development time and survival of the immature stages of An. stephensi under constant compared with fluctuating temperature regimens. (A) Development time (days, solid lines) and survival (percentage, dashed lines) of mosquito immatures until they reached the adult stage at a constant 20 °C and at a mean temperature of 20 °C but with a diurnal temperature fluctuation of ±6 °C (DTR = 12 °C). (B) Data from an equivalent experiment at 27 °C. Results are given for three different larval densities (■, 0.5, ▲, 1, and •, 2 larvae/cm²). Error bars equal the SEM.

Fig. 4.

Cumulative percent survival and gonotrophic cycle length of female An. stephensi mosquitoes under constant and fluctuating temperature regimens. (A) Survival at constant 18 °C (dashed red line) compared with survival at a mean temperature of 18 °C but with a diurnal temperature fluctuation of ±6 °C (DTR = 12 °C; closed blue line). (Inset) The percentage of mosquitoes that completed the gonotrophic cycle on a given day (on the x axis) at constant 18 °C (red bars) compared with completion at a mean temperature of 18 °C but with a diurnal temperature fluctuation of ±6 °C (DTR = 12 °C; blue bars). (B) Data from equivalent experiments at 24 °C. Error bars equal the SEM.