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).