Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae s.s

Abstract

Background: Malaria transmission depends on vector life-history parameters and population dynamics, and particularly on the survival of adult Anopheles mosquitoes. These dynamics are sensitive to climatic and environmental factors, and temperature is a particularly important driver. Data currently exist on the influence of constant and fluctuating adult environmental temperature on adult Anopheles gambiae s.s. survival and on the effect of larval environmental temperature on larval survival, but none on how larval temperature affects adult life-history parameters.

Methods: Mosquito larvae and pupae were reared individually at different temperatures (23 ± 1°C, 27 ± 1°C, 31 ± 1°C, and 35 ± 1°C), 75 ± 5% relative humidity. Upon emergence into imagoes, individual adult females were either left at their larval temperature or placed at a different temperature within the range above. Survival was monitored every 24 hours and data were analysed using non-parametric and parametric methods. The Gompertz distribution fitted the survivorship data better than the gamma, Weibull, and exponential distributions overall and was adopted to describe mosquito mortality rates.

Results: Increasing environmental temperature during the larval stages decreased larval survival (p < 0.001). Increases of 4°C (from 23°C to 27°C, 27°C to 31°C, and 31°C to 35°C), 8°C (27°C to 35°C) and 12°C (23°C to 35°C) statistically significantly increased larval mortality (p < 0.001). Higher environmental temperature during the adult stages significantly lowered adult survival overall (p < 0.001), with increases of 4°C and 8°C significantly influencing survival (p < 0.001). Increasing the larval environment temperature also significantly increased adult mortality overall (p < 0.001): a 4°C increase (23°C to 27°C) did not significantly affect adult survival (p > 0.05), but an 8°C increase did (p < 0.05). The effect of a 4°C increase in larval temperature from 27°C to 31°C depended on the adult environmental temperature. The data also suggest that differences between the temperatures of the larval and adult environments affects adult mosquito survival.

Conclusions: Environmental temperature affects Anopheles survival directly during the juvenile and adult stages, and indirectly, since temperature during larval development significantly influences adult survival. These results will help to parameterise more reliable mathematical models investigating the potential impact of temperature and global warming on malaria transmission.

Figure 1

Experimental design. Larvae (640) reared at each temperature (23°C, 27°C, 31°C, 35°C) were allowed to develop into imagoes, and the adult females were kept at the same temperature at which they were reared as juveniles, or placed at one of the other two temperatures. None of the larvae reared at 35°C survived to adulthood, so no adults were maintained at that temperature.

Figure 2

Kaplan-Meier plots of An. gambiae larval (A) and adult (B) survival at different environmental temperatures. The 23°C temperature (blue) was set as the baseline against which survival at other temperature was compared; 27°C (red); 31°C (green); 35°C (yellow).

Figure 3

Kaplan-Meier plots of An. gambiae adult survival at different environmental temperatures having been reared as larvae at different temperatures. (3A). Adult survival curves at adult environmental temperature of 23°C. Larval temperature 23°C (blue) was set as the baseline against which survival at other larval temperatures was compared; 27°C (red); 31°C (green). (3B). Adult survival curves at adult environmental temperature 27°C. Larval temperature 23°C (blue) was set as the baseline against which survival at other larval temperatures was compared; 27°C (red); 31°C (green). (3C). Adult survival curves at adult environmental temperature 31°C. Larval temperature 23°C (blue) was set as the baseline against which survival at other larval temperatures was compared; 27°C (red); 31°C (green).