How does the dengue vector mosquito Aedes albopictus respond to global warming?

How global warming potentially influences vector-borne diseases has prompted great concerns from both the general public and ecological scientists [1, 2]. Dengue fever, known as the most prevalent mosquito-borne epidemic, generates 50–100 million cases per year and is constantly growing with the expansion of urban residence, increased air travel and the growth of global population [2–5]. In addition to human-induced factors, the observed global warming trend plays a potential role in the generation and transmission of the disease [6]. The complex interplay between global warming and dengue viruses has been a subject of debate yet to be fully understood; one critical component in the long chain of transmission events is the altered population dynamics of the vector, Aedes albopictus, commonly known as the Asian Tiger mosquito [7–10]. Understanding how Ae. albopictus responds to global warming underscores the need to develop effective strategies to mitigate and control dengue and other mosquito-borne epidemics.

Ae. albopictus is native to the humid tropics of Southeast Asia [11]. With an increasing pace of globalization, the mosquito expanded its habitat to other continental regions, including East Asia, Europe, Africa, the Middle East and the Americas [6, 9, 11]. With an observed warmer global pattern in the last several decades, Ae. albopictus has geographically shifted from its original habitats [12, 13]. Specifically, the presence of the mosquito surged in certain high-latitude temperate areas, such as central north-western European and Balkan countries [14, 15]. The emergence was attributed to the rising local temperature, giving rise to more conductive habitats and lengthened activity periods that allowed for an improved rate of success in overwintering [14]. In addition, field observations confirmed a decline in the density of the species in areas with a recorded dry and warm summer, such as southern Spain and Sardinia [14]. This decline was explained by the rising temperature rendering the previously favored habitats less suitable [14, 16]. These contrasting responses displayed a potential geographical shift due to changes in mosquito habitats and behaviors as a result of warmer temperatures. These empirical studies further provided evidence for predicting the regional sustainability of the mosquito and controlling their infestation in areas of prevalence.

A step forward to accommodate these observations is to identify the climatic conditions that affect Ae. albopictus growth. In most world regions, temperature plays a dominating role in the development of the species, along with precipitation and photoperiod [17]. There has been a long tradition in biological research on the relationship between climatic factors and population dynamics of Ae. albopictus, using controlled laboratory experiments [18–20]. It is generally accepted that moderate-to-high temperatures expedite selected stages of the development, while shortening the lifespan of adult mosquitoes [21, 22]. These structured relationships have been incorporated in temperature-driven empirical models to demarcate areas suitable for mosquito development under projected future warming scenarios [14].

One element missing in the discussion is how global warming affects the mosquitoes’ life cycle in terms of different growth stages. This issue is introduced by two existing gaps in the research on the climate-driven nature of the Ae. albopictus population. First, although many studies are able to identify the favorable conditions for development, the contingencies between growth stages are often overlooked. The complete life cycle of the Ae. albopictus is a chain of events differing in morphology and natural habitats. Existing studies using controlled experiments and statistical modeling are invariably centered on limited growth stages (e.g. larvae, pupae), while the intrinsic connections between stages are ignored. Secondly, although a wide discussion arises regarding the projection of climatic suitability for the growth of mosquito in the context of global warming [13, 14, 16, 20], the seasonality of development (i.e. the population variance on a seasonal basis) rendered by warming effects has received very little attention to date. This issue is of great importance as the global warming pattern is considerably uneven across four seasons, with the greatest warming effect at high-latitudes in winter [23, 24]. Thus, an emergent need is to develop a rigorous mathematical model that illuminates the seasonal and stage-specific relationship and thus provides evidence for excavating how the mosquito responds to the heterogeneity of global warming.

Based on a recently proposed mechanistic population model [25], this study examines the theoretical thermal reaction of Ae. albopictus adults over four seasons of a year. By incorporating a 35-year historical dataset into the model, the study identifies critical metrics about the mosquito development. This study aims to provide a tentative answer to the effects of seasonality on Ae. albopictus, while shedding light on the assessment of the epidemic vector’s sustainability in a regional context.

As an extension of the MPAD model, the paper provides a new perspective to examine how the mosquito Ae. albopictus responds to warming temperatures, a problem that raises both ecological and epistemological concerns. To accommodate former studies that established the thermal reaction norms using controlled experiments [42], this study is the first to explore the seasonality of warming effects on Ae. albopictus adults implemented in a mechanistic population model. One persisting issue in controlled experiments and field surveys is that monitoring mosquito adults is relatively difficult; and the larval/pupal surveillance may misrepresent the adult population abundance [43, 44]. To this end, the established MPAD model is able to simulate and elucidate the nature of the thermal reaction at each phase of the life cycle while providing corroborating evidence of how the seasonality affects the overall population abundance.

The historical pattern of global warming manifests temporal fluctuations, characterized by warmer winter temperatures at northern latitudes [23, 24, 45]. The effect of winter warming comes with an early arrival of both spring and winter, extending the favorable period for mosquitoes to grow, develop and reproduce [42]. This physiological response involves both altered life histories and thermal adaptations to seasonality [46]. For this reason, the simulation of the warming effect cannot be treated homogeneously in any effort to evaluate or predict impacts on mosquitoes of different global species or genera [47]. The designed seasonal warming patterns become necessary to evidence how seasonal warming impedes or promotes Ae. albopictus growth in an annual development cycle. The short-term temperature variance as exemplified in the paper has a marked influence on the life cycle of epidemic vectors beyond the effects of long-term climate change [48–53].

By incorporating the 35-year climate dataset into the model, we have observed that the different degrees of all-year warming had very contrasting influences on the population dynamics. A modest temperature rise generally aided in the development with respect to the all-year accumulative population abundance (Fig. 3e); this effect was possibly caused by the elongated development time period the warming temperature induced (Fig. 3a, b). This finding further corroborates the fact that the projected planetary temperature rise of less than 2 °C in the years to come [54] will likely facilitate the mosquito growth in most world regions and promote its expansion to areas that are currently unfavorable. However, as the temperature continued to rise, the summer growth was inhibited. The intervening effect could be explained by laboratory controlled experiments that the preferable temperature range for Ae. albopictus adults to survive is 15–30 °C and the temperature of natural eradication is over 36 °C [55]. Thus, the summer temperature increase even to a small extent will exponentially raise the mortality rate and cause the population to plummet. This trend is also evidenced by research on the species in tropics and subtropics that the annual population dynamics has two peaks and a trough in summer [56, 57].

We have also observed that the different seasonal warming patterns mediated the development process very differently. The change of population abundance in all seasons but summer is possibly induced by the effect on diapause, a state of the mosquito eggs being dormant in winter in response to adverse environmental conditions [17, 58]. Typically, when the temperature drops below 9.5 °C, Ae. albopictus eggs transition into diapause and become completely inactive [59]. As the simulations illustrate, spring warming breaks the dormancy of diapause eggs and allows them to hatch earlier; autumn warming slightly extends the favorable period for reproduction and delays the diapause. However, these warming effects rendered cannot carry over to the following year. This result is very likely the effect of winter when the mosquito fully ceases from development and survives in terms of diapause eggs [17]. In addition, winter warming shortens the period of diapause. These effects are also evident in the SW2 and SW3 warming patterns, as shown in Additional file 1.

Admittedly, this study is flawed in several aspects. First, the design of the simulations assumes that the increased degree of temperature over the warming period is uniform. This assumption deviates from the uncertainties involved in global warming that the temperature rise is historically uneven on a daily basis and is documented with regional complications [23, 54]. To address the issue, future research on simulating the influence of warming should account for the natural fluctuating temperatures derived from historical climate data or projected by regional climate models [60]. Secondly, although both temperature and precipitation have been incorporated, the warming effects discussed in the paper only include temperature. In an atmospheric context, the change of the temperature gradient could contingently alter other climatic factors, including precipitation and humidity [2]. The constituent elements of global warming as predicted by scenarios in the Representative Concentration Pathways [61] and stochastic climatic conditions [62] should both be considered in the simulation as a way to improve the rigor of the model. Thirdly, an overlooked facet in the analysis is the evolutionary adaptation of the mosquito to climate change as a long-term shift in weather conditions [63]. The mechanistic link between population abundance and temperature is mediated by evolutionary responses that allow the mosquito to genetically evolve and facilitate its adaptation to warmer weathers and higher degrees of desiccation [64, 65]. Future research on evaluating and projecting the climatic suitability should take a precautionary approach to examining the yearly difference in the life cycle under similar climatic conditions.

The rising presence and rapid expansion of dengue fever in the last few decades has raised considerable concerns about the nature and cause of the epidemic resurgence [66]. Although it is generally understood that global warming plays a potential role in increasing the incidence and geographical range of the disease [2], how climatic factors mechanistically alter the prevalence of the disease is a less elucidated territory with much complexity. In addition to human factors that increase vector-host interaction, the dengue transmission is dictated by the population dynamics of the vector Ae. albopictus mosquitoes. Our simulations with the 35-year climate data in a mathematical model show that the mosquito’s life cycle is sensitive to seasonal warming in different ways, where the development is inhibited by summer warming but is facilitated by both spring and winter warming. In this regard, the projected warming to a modest degree in future decades will most likely promote the growth and expansion of the species in high-latitude regions. Understanding this temperature-driven mechanism as one chain of the transmission events is critical to refining the thermal reaction norms of epidemic vectors under global warming as well as developing effective mosquito prevention and control strategies.