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.