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. 2017 Mar 8;4(3):160969.
doi: 10.1098/rsos.160969. eCollection 2017 Mar.

The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk

Affiliations

The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk

Lindsay M Beck-Johnson et al. R Soc Open Sci. .

Abstract

Temperature is a key environmental driver of Anopheles mosquito population dynamics; understanding its central role is important for these malaria vectors. Mosquito population responses to temperature fluctuations, though important across the life history, are poorly understood at a population level. We used stage-structured, temperature-dependent delay-differential equations to conduct a detailed exploration of the impacts of diurnal and annual temperature fluctuations on mosquito population dynamics. The model allows exploration of temperature-driven temporal changes in adult age structure, giving insights into the population's capacity to vector malaria parasites. Because of temperature-dependent shifts in age structure, the abundance of potentially infectious mosquitoes varies temporally, and does not necessarily mirror the dynamics of the total adult population. In addition to conducting the first comprehensive theoretical exploration of fluctuating temperatures on mosquito population dynamics, we analysed observed temperatures at four locations in Africa covering a range of environmental conditions. We found both temperature and precipitation are needed to explain the observed malaria season in these locations, enhancing our understanding of the drivers of malaria seasonality and how temporal disease risk may shift in response to temperature changes. This approach, tracking both mosquito abundance and age structure, may be a powerful tool for understanding current and future malaria risk.

Keywords: age structure; delay-differential equations; malaria risk; mosquito population dynamics; seasonality; temperature fluctuation.

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Figures

Figure 1
Figure 1
Annual cycles of abundance from one mean temperature (26°C) with three different seasonal drivers. Annual cycles of adult mosquito abundance (orange solid lines), abundance of potentially infectious mosquitoes (dashed orange lines) and the temperature fluctuation (grey line or band). The abundance is number of mosquitoes per litre of larval habitat. (a) 12°C annual temperature range, (b) 8°C diurnal temperature range and (c) 8°C diurnal temperature range nested within a 12°C annual temperature range.
Figure 2
Figure 2
Annual cycles of abundance from four mean temperatures with the same seasonal driver (4°C annual temperature range). Annual cycles of adult mosquito abundance (solid lines), abundance of potentially infectious mosquitoes (dashed lines) and the temperature fluctuation (grey lines). The abundance is number of mosquitoes per litre of larval habitat. (a) Mean of 18°C, (b) mean of 22°C, (c) mean of 26°C and (d) mean of 30°C.
Figure 3
Figure 3
Comparison of the mean, median and variation across temperature fluctuation types and sizes. Panels (a) and (b) show the abundance of the potentially infectious adult population (number of mosquitoes per litre of larval habitat) predicted by the model driven by both the constant and all the fluctuating temperature drivers. Panel (a) shows results for a mean temperature of 18°C and panel (b) shows results for a mean temperature of 26°C. The x-axis is the temperature driver, where constant denotes constant temperature, D denotes a diurnal fluctuation and A denotes an annual fluctuation. The numbers along the x-axis (4, 8, 12 and 14) indicate the size of the temperature fluctuation around the mean temperature. For example, 4A, 8D refers to a 4°C annual and an 8°C diurnal fluctuation. The x-axis is arranged in order of increasing annual fluctuation. The box and whiskers show the total variation and the median for each fluctuation and the blue dots show the mean abundance.
Figure 4
Figure 4
Mean annual mosquito population dynamics, filtered by water availability. These plots show the model predictions for the potentially infectious mosquito population. The left y-axis corresponds to the mosquito population abundance (number of mosquitoes per litre of larval habitat) and the right y-axis corresponds with precipitation. The blue dashed line is the mean monthly precipitation and the horizontal green dotted line shows the 80 mm precipitation threshold. The mosquito population line has been colour coded to correspond with the availability of water. Recall that the model is not directly run with precipitation information, but is rather filtered once the temperature-dependent results are established. The red portions of the line correspond to populations in which the eggs were laid when precipitation was equal to or above the 80 mm per month threshold. The orange portions of the mosquito population line shows the populations where precipitation has fallen below the threshold but mosquitoes that were already in the potentially infectious class are surviving. The greyed out portion of the line shows what the population would do if water was available year round. The black horizontal time index bars at the top of the panels mark the beginning and end of the malaria season. The panels are (a) Birao; (b) Libreville; (c) Victoria Falls and (d) Xai-Xai.

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