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.Anopheles mosquitoes | climate change | diurnal temperature variability | ectotherms | Plasmodium malaria T he basic reproductive number (R 0 ), which defines the number of cases of a disease that arise from one case of the disease introduced into a population of susceptible hosts, is a key epidemiological metric providing essential information for understanding disease risk and for targeting resources for control. For malaria, R 0 is commonly described by the formula R 0 = ma 2 bce −pS /pr [note that this expression is also defined as (R 0 ) 2 ; ref. 1], where m is the vector:human ratio, a vector biting frequency, bc transmission coefficients defining vector competence, p daily vector survival rate, S the extrinsic incubation or development period of the parasite within the vector, and r the recovery rate of the vertebrate hosts from infection. Given that six of seven of these parameters relate in some way to mosquito abundance, biology, or physiology and that mosquitoes are small cold-blooded insects, it is clear that the transmission intensity of malaria will be strongly influenced by environmental temperature (2-6). Accordingly, the dynamics and distribution of malaria are expected to be extremely sensitive to climate change, although the nature and extent of the response remains highly controversial (7-15).The standard relationships describing the effects of temperature on malaria parasite and mosquito life history derive largely from laboratory studies conducted under constant temperature conditions (e.g., ref. 2 and references therein) and tend to use ...
Ectotherms are considered to be particularly vulnerable to climate warming. Descriptions of habitat temperatures and predicted changes in climate usually consider mean monthly, seasonal or annual conditions. Ectotherms, however, do not simply experience mean conditions, but are exposed to daily fluctuations in habitat temperatures. Here, we highlight how temperature fluctuation can generate ‘realized’ thermal reaction (fitness) norms that differ from the ‘fundamental’ norms derived under standard constant temperatures. Using a mosquito as a model organism, we find that temperature fluctuation reduces rate processes such as development under warm conditions, increases processes under cool conditions, and reduces both the optimum and the critical maximum temperature. Generalizing these effects for a range of terrestrial insects reveals that prevailing daily fluctuations in temperature should alter the sensitivity of species to climate warming by reducing ‘thermal safety margins’. Such effects of daily temperature dynamics have generally been ignored in the climate change literature.
Using a rodent malaria model, we found that exposure to surfaces treated with fungal entomopathogens following an infectious blood meal reduced the number of mosquitoes able to transmit malaria by a factor of about 80. Fungal infection, achieved through contact with both solid surfaces and netting for durations well within the typical post-feed resting periods, was sufficient to cause >90% mortality. Daily mortality rates escalated dramatically around the time of sporozoite maturation, and infected mosquitoes showed reduced propensity to blood feed. Residual sprays of fungal biopesticides might replace or supplement chemical insecticides for malaria control, particularly in areas of high insecticide resistance.
Parasite transmission generally exhibits some form of positive density dependence. Thus, as population density increases, so too does the per capita risk of becoming infected. Under such circumstances, natural selection should favor individuals that use cues associated with population density to determine the optimal allocation of resources to disease resistance mechanisms. As a consequence, individuals experiencing crowded conditions are predicted to be more resistant to parasites and pathogens than those experiencing low-density conditions. This phenomenon (termed ''density-dependent prophylaxis'') [Wilson, K. & Reeson, A. F. (1998) Ecol. Entomol. 23, 100 -101] is predicted to be particularly prevalent in outbreak pest species and in species exhibiting density-dependent phase polyphenism, such as the desert locust, Schistocerca gregaria. Here we show that, as predicted, desert locusts reared under crowded conditions are significantly more resistant than solitary locusts to the entomopathogenic fungus, Metarhizium anisopliae var. acridum, a key natural disease of acridids and an important agent in locust and grasshopper biocontrol. Moreover, enhanced pathogen resistance in crowded locusts is associated with elevated antimicrobial activity, but not with any difference in thermal preferences or behavioral fever response. These results have implications for understanding the development and biocontrol of locust plagues.
We demonstrate how variable temperatures, mediated by host thermoregulation and behavioural fever, critically affect the interaction between a host (the desert locust, Schistocerca gregaria) and a pathogen (the fungus Metarhizium anisopliae var. acridum). By means of behavioural thermoregulation, infected locusts can raise their body temperatures to fever levels. The adaptive value of this behaviour was examined using three thermal regimes wherein maximum body temperatures achievable were: (i) below, or (ii) at normally preferred temperatures, or were (iii) unrestricted, allowing heightened fever temperatures. All infected locusts ultimately succumbed to disease, with median survival times of 8, 15 and 21 days post-infection, respectively. Crucially, only those locusts able to fever produced viable offspring. This represents, to our knowledge, the first demonstration of the adaptive value of behavioural fever following infection with a naturally occurring pathogen. By contrast, although normal host thermoregulation moderately reduced pathogen reproduction (by 35%), there was no additional negative effect of fever, resulting in an asymmetry in the fitness consequences of fever for the host and the pathogen. The dependency of the host-pathogen interaction upon external abiotic conditions has implications for how virulence and resistance are treated both theoretically and in the management of pests and diseases.
Temperature is an important determinant of malaria transmission. Recent work has shown that mosquito and parasite biology are influenced not only by average temperature, but also by the extent of the daily temperature variation. Here we examine how parasite development within the mosquito (Extrinsic Incubation Period) is expected to vary over time and space depending on the diurnal temperature range and baseline mean temperature in Kenya and across Africa. Our results show that under cool conditions, the typical approach of using mean monthly temperatures alone to characterize the transmission environment will underestimate parasite development. In contrast, under warmer conditions, the use of mean temperatures will overestimate development. Qualitatively similar patterns hold using both outdoor and indoor temperatures. These findings have important implications for defining malaria risk. Furthermore, understanding the influence of daily temperature dynamics could provide new insights into ectotherm ecology both now and in response to future climate change.
Previous studies have suggested that Plasmodium parasites can manipulate mosquito feeding behaviours such as probing, persistence and engorgement rate in order to enhance transmission success. Here, we broaden analysis of this ‘manipulation phenotype’ to consider proximate foraging behaviours, including responsiveness to host odours and host location. Using Anopheles stephensi and Plasmodium yoelii as a model system, we demonstrate that mosquitoes with early stage infections (i.e. non-infectious oocysts) exhibit reduced attraction to a human host, whereas those with late-stage infections (i.e. infectious sporozoites) exhibit increased attraction. These stage-specific changes in behaviour were paralleled by changes in the responsiveness of mosquito odourant receptors, providing a possible neurophysiological mechanism for the responses. However, we also found that both the behavioural and neurophysiological changes could be generated by immune challenge with heat-killed Escherichia coli and were thus not tied explicitly to the presence of malaria parasites. Our results support the hypothesis that the feeding behaviour of female mosquitoes is altered by Plasmodium, but question the extent to which this is owing to active manipulation by malaria parasites of host behaviour.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.