4. Considering the combined effects of temperature and humidity
on transmission
The optimal regulation of both body temperature and water balance is
crucial for organismal performance and fitness (Bradshaw 2003). Due to
the fundamental relationship that exists between temperature and the
amount of moisture the air can hold (Fig. 3), variations in both
relative humidity and temperature will alter the degree of moisture
stress ectothermic organisms, like mosquitoes, experience. For a given
amount of atmospheric moisture, warmer temperatures result in higher
saturation vapor pressures that reduce relative humidity and increase
vapor pressure deficit (Fig. 3). Depending on the ambient temperature,
variation in relative humidity can exacerbate or buffer the negative
effects of higher temperature on mosquito fitness and pathogen
transmission. The current manner in which thermal performance of
vector-borne pathogen transmission is conceptualized and empirically
measured does not explicitly account for these effects. Even when
relative humidity is held constant, increases in temperature will
increase the vapor pressure deficit and the evaporative stress an adult
mosquito experiences. Thus, it is currently unclear if the thermal
maximum of a given trait, which is typically an upper lethal limit
(Chown & Nicolson 2004), is really being driven by temperature effects
on metabolic function or rather is a function of dehydration and water
stress on the organism. Understanding the physiological mechanisms
underpinning mosquito responses to these abiotic constraints will be
critical for predicting how transmission will shift with future
anthropogenic change (Chown & Gaston 2008; Deutsch et al. 2008;
Pörtner & Farrell 2008; Dillon et al. 2010).
We utilize a trait-based approach that leverages a widely used relativeR0 model (Mordecai et al. 2013, 2017,
2019; Murdock et al. 2017; Shocket et al. 2018a, 2020;
Tesla et al. 2018; Ryan et al. 2020b; Wimberly et
al. 2020; Villena et al. 2022) to present a framework that
outlines the manner in which variation in relative humidity could
influence the thermal performance of vector-borne pathogen transmission
(Figs. 4 & 5). Overall, we anticipate that variation in relative
humidity could result in significant shifts in the qualitative shape of
the temperature-trait relationship and cause these effects to vary with
mosquito traits. Drawing from the literature on other ectotherms,
insects, and what little we do know for mosquitoes, we outline several
hypotheses for how variation in relative humidity may affect the thermal
performance of mosquito and pathogen traits (Table 2). We anticipate
variation in relative humidity will be important throughout the mosquito
life cycle, with the largest effects at temperatures that approach the
upper thermal limit (Tmax ) for a given trait,
with little to no effect of variation in relative humidity on the
predicted thermal minimum (Tmin ) (Table 2). This
hypothesis is based on the observation that for a given change in
relative humidity, the corresponding change in vapor pressure deficit
and evaporative stress will be greater at higher temperatures (Figs. 3
& 4). How variation in relative humidity affects the predicted thermal
optimum (Topt ) of a given trait will be somewhat
dependent on the specific trait as well as the magnitude of the effect
at warmer temperatures.
The nature and magnitude of the effects of relative humidity and
temperature variation on mosquito and pathogen traits important for
transmission could differ depending on mosquito life stage. One way in
which relative humidity and temperature interact to affect developing
mosquitoes is through the evaporation rate of larval habitat, which is
also determined by the size and surface area of the larval habitat and
rate of water replenishment (Juliano & Stoffregen 1994). A second type
of interaction could involve altering some intrinsic factor of the
larval environment such as surface tension, microbial growth, or solute
concentration (Juliano & Stoffregen 1994; Pérez-Díaz et al.2012). Causal evidence from semi-field experiments shows negative
effects of high relative humidity at temperatures near or above the
predicted thermal optimum for Aedes albopictus (Mordecai et
al. 2017; Murdock et al. 2017) on larval survival and the
probability of adult emergence (Murdock et al. 2017). One
possibility is that both temperature and water vapor in the atmosphere
will affect the surface tension of aquatic larval habitats. Warm
temperatures and high humidity may cause larval habitats to have too
little surface tension, while cool and dry larval environments may have
too high surface tension (Singh & Micks 1957; Pérez-Díaz et al.2012), negatively affecting the ability of larval mosquitoes to breath,
access nutrients, and emerge from the pupal stage. In all likelihood,
both types of effect could be important in the field. Thus, the effects
of relative humidity on the rate of evaporation relative to larval
development or shifts in intrinsic conditions of larval habitats could
have substantial effects on the thermal performance curves for both
mosquito development rate (MDR ), the probability of egg to adult
survival (pEA ), and consequently the intrinsic growth rate of
mosquito populations.
Once adults emerge from the larval environment, variation in relative
humidity could potentially increase or decrease the predicted upper
thermal limit for adult traits that are critical for mosquito population
dynamics and transmission (Fig. 4, Table 2). For example, decreases in
relative humidity at warm temperatures could decrease mosquito survival
(by increasing the per capita daily mortality rate (μ)) via
increasing desiccation stress (Mayne 1930; Gaaboub et al. 1971;
Lyons et al. 2014). This, in turn, will decrease the temperatures
at which mosquitoes can survive to become infected and to transmit
vector-borne pathogens. Evidence from other insect systems (Shelford
(1918); Edney & Barrass (1962); Chown & Nicolson (2004); Yu et
al. (2010)) would predict that decreases in relative humidity at warm
temperatures could also decrease the per capita daily biting rate
(a) and production of eggs (EFD) by altering mosquito
activity and blood feeding due to shifts in behavior (e.g., utilization
of specific habitats, times of day, or times of season; Dow & Gerrish
(1970); Gaaboub et al. (1971); Provost (1973); Canyon et
al. (1999); Drakou et al. (2020)) and physiological responses
(e.g., decreased metabolic rate) to increase desiccation resistance or
tolerance (Chown & Davis 2003; Marron et al. 2003). However, the
evidence that does exist for mosquitoes suggests decreases in relative
humidity can actually increase biting rates on hosts (e.g., Culex
pipiens, Ae. aegypti, An. quadramaculatus; Hagan et
al. (2018)). It remains unclear if this pattern would persist in the
field for mosquito species that utilize sugar sources for hydration and
nutrition, because nectar-feeding mosquitoes can increase sugar feeding
behavior when environmental conditions are dry (Fikrig et al.2020).
Finally, we also anticipate that the development of mosquito-borne
pathogens and parasites, and potentially mosquito susceptibility to
infection, should be affected by variation in relative humidity under
different ambient temperature conditions based on physiological
acclimation responses (Beitz 2006; Liu et al. 2016). Aquaporin
water channels allow organisms to rapidly move water (aquaporins) or
water and glycerol (aquaglyceroporins) across cellular membranes to
promote cellular function. Mosquitoes utilize aquaporins and
aquaglyceroporins to minimize water loss in desiccating environments
(Liu et al. 2011) and to maintain glycerol concentrations to
stabilize proteins when mosquitoes are exposed to high heat (Tatzelet al. 1996; Diamant et al. 2001; Deocaris et al.2006; Liu et al. 2016). The physiological responses of mosquitoes
to optimally thermo- and hydro-regulate under sub-optimal temperature
and relative humidity environments could also have consequences for the
energy available to developing pathogen (Liu et al. 2016).