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.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 ...

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

“…1982; Paaijmans et al. 2010). Meanwhile, transmission rates (or infectivity) of pathogens shift linearly with host population density (Anderson and May 1981).…”

Increasing frequency of low summer precipitation synchronizes dynamics and compromises metapopulation stability in the Glanville fritillary butterfly

“…Most ecological studies related to climate change have analysed changes in species' geographical ranges [11][12][13][14] and abundances [11,13,15], where the driving forces are thought to be the mean values of climatic variables, typically some measure of temperature. Many recent theoretical [16], modelling [17,18], experimental [17,[19][20][21][22] and observational [23][24][25] studies indicate that climatic variability and climatic extremes may have a similar or even stronger impact than the respective mean values on species dynamics. Once again, however, these studies have generally examined the impact of environmental variation on the geographical ranges and mean abundances of species, whereas practically no studies have analysed the impact of climatic variability on more complex aspects of population dynamics, such as the amplitude or spatial synchrony of population dynamics.…”

Temporal variation in temperature determines disease spread and maintenance inParameciummicrocosm populations

“…This work highlights that both differences in mean and variance are important to consider when trying to understand how variation in environment influences the behaviour of natural systems. Recent theoretical analyses of Plasmodium dynamics [13] and a single generation study of its development in mosquitoes [23] advocate strongly that environmental variation is a key determinant for parasite epidemiology. However, experimental demonstration of the influence of a variable versus constant environment for long-term host -parasite dynamics is not yet established.…”