1. Introduction
Environmental changes potentially impacting the geographical ranges or local abundance of arthropod vectors transmitting infectious disease agents are among the important concerns linked to climate [
1,
2,
3,
4,
5,
6]. Associations reported in the literature show that climate-related variables can be used to predict local abundance and the potential for the expansion of arthropod vectors, such as mosquitoes or ticks [
7,
8,
9,
10]. Since field surveys are both costly and time consuming, remote sensing (RS) technology is increasingly used to estimate habitat suitability for a variety of vector species [
11,
12,
13,
14]. Temperature and rainfall are the weather parameters of special interest, because they impact both the distribution of suitable vector habitat and the potential for local vector proliferation. Although terrain elevation is strongly associated with temperature, urban heat islands might cause slight differences in the associations between vector abundance and climate parameters in studies conducted within urban environments. Thus, elevation is included among the variables of interest for this study.
Aedes aegypti (
Ae. aegypti), the primary mosquito vector of dengue and yellow fever viruses and an important vector of chikungunya virus to humans in urban settings, is most abundant in urban environments [
15].
Dengue is one of the most important mosquito-borne viral diseases in the subtropics and tropics, with one estimate of the global infection burden reaching approximately 390 million virus infections and nearly 100 million cases with disease manifestations per year, over three times that estimated by the World Health Organization [
16]. Although the presence and abundance of the mosquito vector is strongly influenced by the human peridomestic environment (e.g., access to water-holding containers serving as larval development sites and the potential for intrusion into homes to engage in indoor biting), these are also affected by meteorological variables, such as temperature, rainfall, humidity and solar radiation. Several studies have addressed the relationship between weather or climate variability and the incidence of dengue disease cases [
17,
18,
19,
20,
21,
22,
23,
24,
25,
26,
27,
28]. Such relationships, however, may be influenced by additional factors, such as the exposure of humans to mosquitos and the intensity of virus transmission [
29].
The strength of the association between RS-based climate parameters and vector abundance may be limited by the spatial resolution of the satellite products that are freely available and more commonly used [
7]. Environmental and socio-economic conditions can change drastically over distances of 10–100 m of meters; therefore, spatial models designed to estimate vector presence and abundance developed at the regional or state level cannot reliably be down-scaled for locally-relevant risk predictions. To develop models to predict vector presence and abundance at the local (community or neighborhood) scale using RS-based environmental inputs requires consistent monitoring of recent local environmental conditions with RS imagery that can distinguish the differences between adjacent communities or neighborhoods. The present study tests if three widely used RS-based environmental products are able to distinguish those differences at the local level, despite having spatial resolutions equal or larger than 90 m. Our motivation is to evaluate the potential for using RS-based environmental products that are freely-available to decision-makers in developing countries, to monitor the presence and abundance of
Ae. aegypti at the local scale. For a geographic transect of approximately 330 km by road, corresponding to an area of approximately 245 km (west-east) by 98 km (north-south) in central Mexico, we describe the associations between the presence and abundance of the pupal life stage of
Ae. aegypti and environmental conditions estimated from RS products, including land surface temperature (LST), rainfall, land surface properties and elevation.
4. Discussion
Associations between extreme weather events and mosquito outbreaks [
40,
41], as well as the weather-mediated seasonal dynamics of mosquito abundance [
42] have been reported in the literature for
Ae. aegypti. Although seasonal weather fluctuations can in large part explain intra-annual fluctuations in the abundance of
Ae. aegypti, studies conducted at the local scale and, therefore, under very similar weather conditions, have revealed differences in vector abundance among nearby urban locations [
42,
43,
44]. This likely reflects the effect of anthropogenic modifications in the urban environments that this mosquito prefers to inhabit [
42,
44]. Using a study design that takes advantage of a geographic transect with similar socio-economic conditions in the specific field survey areas, a previous cross-sectional analysis using this dataset for the abundance of
Ae. aegypti and
in situ weather data also reported significant associations between mosquito abundance and weather variables (temperature or rainfall) and elevation [
30]. The uniformity in socio-economic conditions in the specific study areas allows the opportunity to minimize the influence of the anthropogenic sources of variability, while at the same time studying elevation and weather variables at approximately the same point in time. The present study further capitalizes on such advantages by specifically focusing on testing the applicability of widely-used RS products to explore weather linkages with
Ae. aegypti abundance at the local scale.
Despite the relatively coarse spatial resolution of 1 km for nighttime LST and approximately 26 km for rainfall, strong correlations were found between data from the MYD11A1 product or 3B42 V7, respectively, and the local abundance of
Ae. aegypti pupae. Conversely, the results were not encouraging for daytime LST. Honório
et al. [
45] showed a positive linear relationship between mosquito abundance and ambient temperature within a range of 18 °C to 24 °C. The authors did not detect any variation in the abundance of
Ae. aegypti above this temperature threshold. Further, Eisen
et al. [
46] reported a positive linear relationship between water temperature and the development rate for immature
Ae. aegypti between 15 °C to 30 °C. In that study, lower developmental zero temperatures were estimated to be in the 10 °C to 14 °C range for eggs and immature
Ae. aegypti and the upper developmental zero temperatures in the 38 °C to 42 °C range. It is interesting to notice that in our study, the mean cluster level daytime LST ranged from 27.5 °C to 40.7 °C while the nighttime LST ranged from 7.8 °C to 24.2 °C, which included the range of positive correlation reported by Honório
et al. [
45] and partially overlapped with that reported by Eisen
et al. [
46]. Additional work is needed to assess the correlations between the abundance of
Ae. aegypti and RS data for a broader range of temperatures than examined in the present study, especially for the higher end temperatures. Similar to our results with RS data, positive linear relationships with nighttime LST, but not with daytime LST, were detected in malaria prediction models [
47].
As expected from the strong positive correlation between the abundance of
Ae. aegypti and night LST, there was also a strong, but negative, correlation between mosquito abundance and elevation. In general, a negative relationship is expected between elevation and temperature [
48]; in our case, however, this was detected only when considering night LST, but not when considering day LST. Indeed, daytime LST was only associated with nighttime LST and not associated with any other variable, including elevation. This may be related to more cloud cover during the daytime than at nighttime, as suggested by the lower mean number of cloud-free images available in the daytime LST data (6.8 images,
Figure 3) compared to 7.9 images available for nighttime LST data. The effect of minimum temperatures may be another contributing factor; Lozano-Fuentes
et al. [
30] identified the mean minimum daily temperature and the mean minimum daily winter temperature among the weather parameters with potential relevance for the biology of
Ae. aegypti. Although our study did not consider these specific parameters, it is possible that minimum temperatures (which occur in our night LST data) in general may play an important role in the biology of
Ae. aegypti.
Finally, a strong correlation has been reported between median family income and surface temperature during the daytime, with a much weaker correlation at nighttime [
49]. The specific areas (
i.e., neighborhoods within communities) used in this study were selected under the criteria of being urban low- to middle-income homes with small- to medium-sized yards. The study premises often harbored considerable vegetation, and it is known that leaf temperatures and other vegetative features are a major aspect related to urban temperature [
50]. Although, the possibility exists that income factors play a role in the differences detected between daytime and nighttime LST, such a possibility is not evident in our study, since many of our communities were small and not likely to influence the urban heat island effect as detected in a 1-km × 1-km grid box.
While it is possible to explain the positive correlation between RS estimated rainfall and the abundance of
Ae. aegypti in terms of more containers being filled with rain water (or some containers having a greater volume of water) and, thus, more potential larval development sites when it rains, this could be a casual association, due to the fact that the areas with higher temperature and lower elevation also typically have a higher rainfall. Indeed, rainfall and nighttime LST were weakly, but significantly and positively correlated. It also should be noted that the impact of rainfall on the presence of larval development sites for
Ae. aegypti is complicated by human water storage practices, with the importance of containers filled by rain
versus human action varying both among geographic areas and within the year in single locations. However, the results found in this study are consistent with those of Lozano-Fuentes
et al. [
30] using meteorological data from weather stations along the same transect. Additionally, our results are consistent with process-based life-cycle models of
Ae. aegypti; mosquito populations become largest when temperatures are warm and rainfall is abundant [
51,
52]. They are also consistent with studies indicating that dengue risk in humans is positively correlated with temperature and rainfall [
53], which is likely in part due to the impacts of temperature and rainfall on vector populations [
54,
55].
The apparent outlier of Rio Blanco and Orizaba depicted in
Figure 4 is also clear in table of Lozano-Fuentes
et al. [
30], when using data on both pupae and larvae. We found that in general, the relationship between
Ae. aegypti pupal abundance and temperature/rainfall is robust in the higher elevation regions (above ~1300 m ASL) and is weaker at lower elevations (below ~1300 m ASL). We believe the weaker relationship between temperature/rainfall and pupal abundance below ~1300 m in our study region is an indicator that once temperature and rainfall increase to a certain point, pupae are abundant no matter how much warmer or wetter it becomes;
i.e., the climate is ideal for immature
Ae. aegypti development anywhere in the warm, wet regions below ~1300 m. From a mathematical standpoint, this observation indicates that the relationship between pupal abundance and climate variability likely becomes more asymptotic below ~1300 m, so the linear fits shown in
Figure 4 may oversimplify what is in reality a non-linear relationship. However, for the purposes of our paper, in which we are simply trying to show that LST, rainfall and elevation are correlated with
Ae. aegypti pupal abundance, these linear fits are adequate. It may also be possible that the comparatively greater urban density of Orizaba and Rio Blanco (Rio Blanco is a dormitory city of Orizaba) may be more favorable for higher numbers of
Ae. aegypti, perhaps because of the sheer numbers of container habitats. In support of this conjecture, Coatepec has similar characteristics of elevation and temperature (although slightly lower rainfall) compared to Orizaba and Rio Blanco, but lower urban density; and it has also a lower presence and abundance of
Ae. aegypti pupae (
Table 1).
The findings of this study suggest the promise for future RS-based predictive models of
Ae. aegypti population fluctuations and other applications, such as dengue outbreak prediction [
56]. These results are even more promising when considering future remote sensing products with enhanced capabilities that may be available soon via new or planned NASA and/or partner missions. Of special note are the Visible Infrared Imaging Radiometer Suite (NPP-VIIRS), the Global Precipitation Measurement (GPM) mission and the Soil Moisture Active Passive (SMAP) mission. Carried onboard the Suomi National Polar-orbiting Partnership (NPP) satellite, the VIIRS sensor will use visible and infrared wavelengths to study land, atmosphere, ice and ocean. Besides LST, VIIRS will make observations on active fires, vegetation, ocean color, sea surface temperature and other surface features available to the scientific community [
57]. These observations will facilitate the study of climate change, clouds and aerosols; phytoplankton and sediment in the seas; forest cover and productivity; and changes in polar sea ice. The similarities between VIIRS and MODIS will provide continuity for monitoring programs conducted with MODIS. The Global Precipitation Measurement (GPM) mission will provide continuity to TRMM data to monitor precipitation and for other hydrological applications [
58]. Measuring soil moisture present at the Earth’s land surface, the Soil Moisture Active Passive (SMAP) mission will be critical to flood assessment and drought monitoring, as well as to the study of the global carbon balance [
59]. SMAP is expected to be another undertaking that will play an important role in the monitoring of environmental variables associated not just with vector transmitted diseases in general, but also, and especially, soil transmitted helminthes infections. Soil moisture is a critical determinant for the survival of helminth eggs in the soil [
60,
61,
62].
The application of the remotely-sensed products in this study was useful for identifying correlations between environmental variables and the presence and abundance of
Ae. aegypti. This finding is encouraging for using these products to identify areas most at risk of high pupal abundance at local scales on the order of 1-km. It is tempting to speculate that if these products work at the local scale for cities along our topographically complex transect in Mexico, they would work even better in areas where the topographic variability is comparatively smaller (and therefore, environmental variables do not vary as much in space), for example, in the southern part of the continental United States. However, since the abundance of
Ae. aegypti is also closely linked to the characteristics of the human environment, it is imperative to also consider the potential confounding effects of socioeconomic and human ecology (e.g., housing style, water storage,
etc.) factors associated with mosquito establishment and proliferation [
3,
63]. In addition to affecting mosquito abundance, socio-economic factors can play a role in the vulnerability of human inhabitants to dengue virus infection; for example, Hagenlocher
et al. [
63] constructed a composite index of socioeconomic vulnerability to dengue that included both indicators of susceptibility, as well as a lack of resilience.
An overarching goal, whether focusing on mosquito vector abundance, vector infection rates and the risk of virus transmission to humans, socioeconomic vulnerability or the risk for dengue epidemics, is to give public health professionals and the general public time to prepare for and attempt to prevent or mitigate disease outbreaks. For example, researchers have determined that the optimal lead time for dengue early warning for officials in Singapore would be three months in order to suppress an epidemic [
64], and global risk maps have been developed to estimate the risk of dengue in Europe [
65]. Better defining the linkages between environmental and climatic conditions and the incidence and geographic spread of mosquito vectors and dengue, together with the ability to use remotely-sensed observations to detect conditions signaling increased risk, would be of great value for future outbreak prediction and disease suppression.
