3. The effects of humidity on mosquito fitness, population dynamics, and pathogen transmission
Spatial and temporal variation in atmospheric moisture has important implications for an organism’s ability to hydroregulate (Box 1). Hydroregulation is defined as the suite of physiological and behavioral responses organisms utilize to regulate water balance and tolerate dehydrating environmental conditions (Chown & Nicolson 2004; Benoit 2010; Chown et al. 2011; Edney 2012; Lucio et al. 2013). The relationship between organismal fitness and optimal hydroregulation is complex, with significant costs to fitness (e.g., decreased survival and reproduction) occurring when organisms become dehydrated (Mitchell & Bergmann 2016; Anderson & Andrade 2017) or overhydrated (Chown & Nicolson 2004). Insects have a suite of adaptations to conserve water, like physiological changes in skin or cuticular permeability (Rajpurohitet al. 2008; Wu & Wright 2015), differential regulation of urine and feces production (Weihrauch et al. 2012; Durant & Donini 2019; Durant et al. 2021; Lajevardi et al. 2021), and behavioural changes in activity (Kühnholz & Seeley 1997; Ostwaldet al. 2016). Insects also can mitigate water loss by regulating water intake via changes in water utilization, food sources, and selection of specific habitats (Benoit 2010; Hagan et al. 2018; Bezerra Da Silva et al. 2019)). Finally, insects can also produce water via metabolic processes (Jindra & Sehnal 1990; Chown et al. 2011). Maintaining water balance is a particular challenge for blood-feeding (hematophagic) vectors (Kleynhans & Terblanche 2011; Chappuis et al. 2013), like mosquitoes (Edney 2012), where the act of taking a blood meal results in overhydration that requires specialized adaptations for the excretion of water, which in turn enhances susceptibility to desiccation overall (Benoit & Denlinger 2010).
Instead of measuring humidity directly (Box 1), many studies use related variables, like seasonal precipitation or land cover to predict mosquito population dynamics or pathogen transmission (Johansson et al.2009; Chaves & Kitron 2011; Soti et al. 2012; Chandy et al. 2013; Abdelrazec & Gumel 2017; Sang et al. 2017; Nosratet al. 2021). Mosquito-borne diseases generally peak during, or following, periods of highest rainfall (Karim et al. 2012; Chowdhury et al. 2018; Magombedze et al. 2018; McLaughlinet al. 2019). Rainfall can matter as a standalone variable, since standing water is essential for mosquitoes’ ontogenetic development. However, the effect of precipitation on mosquito population dynamics and disease transmission can operate through other factors that covary with precipitation, such as increased humidity and shifts in temperature that impact mosquito development rates, adult survival and reproduction, parasite development rates, and mosquito-human contact rates. The relationship between mosquitoes and precipitation is even more difficult to discern for mosquito species that develop in artificial, human watered containers, where complex interactions can occur between amount of rainfall and access to piped water (Hayden et al. 2010; Padmanabha et al. 2010; Schmidt et al. 2011; Stewart Ibarra et al. 2013; Brown et al. 2014; Lippi et al.2018). Similarly, measures of land cover such as the normalized difference vegetation index (NDVI) have been used to account for areas too dry for widespread mosquito habitat (Ryan et al. 2015). Ultimately, the use of these proxy measures obscures our understanding of how relative humidity and other environmental variables affect transmission, which in turn constrains our ability to predict how mosquito-borne pathogens will respond to future climate and land use change.
Several studies have demonstrated statistical associations between humidity and mosquito abundance, as well as vector-borne disease incidence and prevalence (Mayne 1930; Azil et al. 2010; Chenet al. 2010; Buckner et al. 2011; Karim et al.2012; Althouse et al. 2015; Lega et al. 2017; Asigau & Parker 2018; Davis et al. 2018; Jemal & Al-Thukair 2018; Dialloet al. 2019; Evans et al. 2019; Santos-Vega et al.2022). For example, the sizes of seasonal malaria epidemics in two cities in India exhibit a clear association with relative humidity (Fig. 2), with a higher correlation than for temperature or rainfall (Santos-Vega et al. 2016). A semi-mechanistic epidemiological model that incorporates this effect of relative humidity on the transmission rate parameter accurately predicts the temporal dynamics of the disease, including the multiyear cycles in the size of seasonal epidemics (Santos-Vega et al. 2016, 2022). Such predictions can inform mosquito control efforts and targeting prophylaxes. However, the underlying biology of the relationships that exist between humidity and these response variables are often assumed and based on a limited number of empirical studies (summarized in Table 1). Experimental work has thus far shown generally positive effects of increased relative humidity on mosquito survival and desiccation tolerance, production and development of eggs, and mosquito activity (up to 90% relative humidity). In contrast, biting rates exhibited increases when conditions are drier and the effect of humidity on vector competence is less clear (Table 1).
Despite the existing body of research, we still do not have a sufficient knowledge base for incorporating the effects of humidity into the current temperature-trait modeling framework. Results from observations studies cannot necessarily be extrapolated to new locations or into the future. Further, the effects of humidity on mosquito and pathogen fitness described by experimental / causation studies are of limited resolution, typically exploring a limited number of humidity levels and encompassing only a handful of mosquito species. The need to better incorporate humidity effects is not unique to vector-borne diseases, but parallels trends seen in the larger body of ecological work on the effects of climate variability and climate change on heat health in ectotherms (van Heerwaarden & Sgrò 2014; Gunderson & Stillman 2015). In the following section, we outline how variation in relative humidity interacts with temperature to change the thermal performance of ectothermic vectors and, consequently, pathogen transmission.