Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vectorpathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20°C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10°C) or constant temperature. A thermodynamic model predicted that at mean temperatures <18°C, DENV transmission increases as DTR increases, whereas at mean temperatures >18°C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.arbovirus | climate | vectorial capacity I ncidence, seasonal variation, and global distribution of vectorborne diseases are known to be influenced by climate (1). What is controversial is exactly how climatic factors-and thus climate change-impact the intrinsic transmission intensity of most vector-borne pathogens (1-5). Part of the problem derives from the interplay of multiple factors, such as spatial heterogeneity (6) or differing socioeconomic and demographic backgrounds (3, 7) that combine with climate to influence overall transmission dynamics. In addition, our ability to accurately define the impact of climatic factors on the risk of vector-borne disease is limited by poor understanding of the mechanistic link between environmental variables, such as temperature, and the vectorial capacity of insect vector populations (1,(8)(9)(10)(11)(12).Vectorial capacity captures key components of an insect's role in pathogen transmission, which is influenced by many environmental, ecological, behavioral, and molecular factors (13). Mathematically, it can be described by:where m is vector density per person, a is daily probability of a vector biting a human host, p is daily probability of vector survival, n is duration in days of the pathogen extrinsic incubation period (EIP) in the vector, and b is vector ...
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 ...
The incubation period for malaria parasites within the mosquito is exquisitely temperature-sensitive, so that temperature is a major determinant of malaria risk. Epidemiological models are increasingly used to guide allocation of disease control resources and to assess the likely impact of climate change on global malaria burdens. Temperature-based malaria transmission is generally incorporated into these models using mean monthly temperatures,
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.
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