Matthew B. Thomas

Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti

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 vector–pathogen 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.

Influence of climate on malaria transmission depends on daily temperature variation

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.

Understanding the link between malaria risk and climate

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, yet temperatures fluctuate throughout the diurnal cycle. Here we use a thermodynamic malaria development model to demonstrate that temperature fluctuation can substantially alter the incubation period of the parasite, and hence malaria transmission rates. We find that, in general, temperature fluctuation reduces the impact of increases in mean temperature. Diurnal temperature fluctuation around means >21°C slows parasite development compared with constant temperatures, whereas fluctuation around <21°C speeds development. Consequently, models which ignore diurnal variation overestimate malaria risk in warmer environments and underestimate risk in cooler environments. To illustrate the implications further, we explore the influence of diurnal temperature fluctuation on malaria transmission at a site in the Kenyan Highlands. Based on local meteorological data, we find that the annual epidemics of malaria at this site cannot be explained without invoking the influence of diurnal temperature fluctuation. Moreover, while temperature fluctuation reduces the relative influence of a subtle warming trend apparent over the last 20 years, it nonetheless makes the effects biologically more significant. Such effects of short-term temperature fluctuations have not previously been considered but are central to understanding current malaria transmission and the consequences of climate change.

Coping with crowds: Density-dependent disease resistance in desert locusts

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.

How to make evolution-proof insecticides for malaria control.

The evolution of resistance to insecticides by mosquitoes is a major threat to ongoing malaria control programs and plans for global eradication. Evolutionary theory suggests a practical solution.

Can fungal biopesticides control malaria

Recent research has raised the prospect of using insect fungal pathogens for the control of vector-borne diseases such as malaria. In the past, microbial control of insect pests in both medical and agricultural sectors has generally had limited success. We propose that it might now be possible to produce a cheap, safe and green tool for the control of malaria, which, in contrast to most chemical insecticides, will not eventually be rendered useless by evolution of resistance. Realizing this potential will require lateral thinking by biologists, technologists and development agencies.

Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness

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.

Frontiers in climate change–disease research

The notion that climate change will generally increase human and wildlife diseases has garnered considerable public attention, but remains controversial and seems inconsistent with the expectation that climate change will also cause parasite extinctions. In this review, we highlight the frontiers in climate change–infectious disease research by reviewing knowledge gaps that make this controversy difficult to resolve. We suggest that forecasts of climate-change impacts on disease can be improved by more interdisciplinary collaborations, better linking of data and models, addressing confounding variables and context dependencies, and applying metabolic theory to host–parasite systems with consideration of community-level interactions and functional traits. Finally, although we emphasize host–parasite interactions, we also highlight the applicability of these points to climate-change effects on species interactions in general.

Temperature variation makes ectotherms more sensitive to climate change

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.

PREDICTING THE ECONOMIC IMPACT OF AN INVASIVE SPECIES ON AN ECOSYSTEM SERVICE

Quantifying the impact of alien invasive species on ecosystem services is an essential step in developing effective practices and policy for invasive species management. Here we develop a stochastic bioeconomic model that enables the economic impact of an invasive pest to be estimated before its arrival, based on relatively poorly specified ecological and economic parameters. We developed the model by using a hypothetical invasion of the varroa bee mite (Varroa destructor) into Australia and the negative flow-on effects that it would have on pollination by reducing honey bee populations, giving rise to a loss of pollination services, reduced crop yields, and additional production costs. If the mite were to continue to be prevented from entering the country over the next 30 years, we estimate that the economic costs avoided would be U.S.