Warmer temperatures reduce the vectorial capacity of malaria mosquitoes

Abstract

The development rate of parasites and pathogens within vectors typically increases with temperature. Accordingly, transmission intensity is generally assumed to be higher under warmer conditions. However, development is only one component of parasite/pathogen life history and there has been little research exploring the temperature sensitivity of other traits that contribute to transmission intensity. Here, using a rodent malaria, we show that vector competence (the maximum proportion of infectious mosquitoes, which implicitly includes parasite survival across the incubation period) tails off at higher temperatures, even though parasite development rate increases. We also show that the standard measure of the parasite incubation period (i.e. time until the first mosquitoes within a cohort become infectious following an infected blood-meal) is incomplete because parasite development follows a cumulative distribution, which itself varies with temperature. Including these effects in a simple model dramatically alters estimates of transmission intensity and reduces the optimum temperature for transmission. These results highlight the need to understand the interactive effects of environmental temperature on multiple host-disease life-history traits and challenge the assumptions of many current disease models that ignore this complexity.

Climate, environmental and socio-economic change: weighing up the balance in vector-borne disease transmission

“…A series of studies investigating the effect of DTR on parasite development and transmission have shown that DTRs increase rate processes (speed up parasite development) at low mean temperatures and decrease rate processes at higher temperatures [85][86][87][88]; thus, using mean temperatures in disease models will underestimate transmission at cooler temperatures and overestimate at warmer temperatures. In addition to DTR affecting parasite development, temperature also has an impact on the proportion of mosquitoes carrying infectious sporozoites, with mosquitoes maintained at higher temperatures demonstrating a lower prevalence of sporozoites in the salivary glands [89]. Thus, at high temperatures, despite a decrease in parasite development time, fewer mosquitoes become infectious and able to transmit the parasite.…”

“…Combining data for these two species to estimate vital rates would not necessarily generate realistic inference. Furthermore, data and research are particularly needed to better understand the influence of environmental factors on key parameters such as the EIP [89], vector competence [94,113], biting behaviour and interactions with infection [118,119], because these have been very under-researched to date.…”

“…Modelling of how the EIP of P. falciparum is expected to vary over time and space across Africa (depending on DTR) was considered in [87]. It was shown in [89] that vector competence tails off at higher temperatures, even though parasite development rate increases. Using a model that incorporates empirically derived nonlinear thermal responses of Anopheles vectors, Mordecai et al [91] predict that the optimal temperature for malaria transmission is 258C (and that it significantly decreases beyond 288C).…”

Capacity of mosquitoes to transmit malaria depends on larval environment

“…To estimate vector competence (b, proportion of infectious bites on a susceptible host that lead to an infected host), we used the proportion of mosquitoes with sporozoites disseminated in the salivary glands. This is a standard approximation and assumes that if a mosquito has sporozoites in the salivary glands, it will likely transmit during feeding [3,4,46].…”

“…Any variation in environment that affects relevant aspects of vector biology could result in a change in transmission risk via effects on vectorial capacity [4][5][6][7][8]. Recent work shows that changes in temperature (both means and diurnal fluctuation) and rainfall events can have substantial effects on the transmission potential of malaria [7,[9][10][11].…”