Introduction

Leaf trichomes are known to influence various biophysical processes depending on their habitat conditions (Bickford, 2016; Johnson, 1975) such as increasing water‐use efficiency (WUE) through increasing vapor‐diffusion resistance (e.g., Kenzo, Yoneda, Azani, & Majid, 2008); maintaining leaf temperature above air temperature by decreasing sensible‐heat flux (e.g., Meinzer & Goldstein, 1985) or below air temperature by reflecting radiations (e.g., Ehleringer & Mooney, 1978); avoiding photoinhibition by increasing light reflectance (e.g., Skelton, Midgley, Nyaga, Johnson, & Cramer, 2012); promoting condensation on leaf surface either to decrease water loss (e.g., Konrad, Burkhardt, Ebner, & Roth‐Nebelsick, 2015) or to capture water from dew on leaf surface (e.g., Ohrui, et al. 2007). Leaf trichomes are often associated with drought tolerance because plants with densely pubescent leaves are often abundant in dry environmental conditions (Aronne & De Micco, 2001; Ehleringer & Mooney, 1978; Ichie, Inoue, Takahashi, Kamiya, & Kenzo, 2016; Johnson, 1975; Moles et al., 2020; Smith & Nobel, 1977) and because pubescent individuals have lower mortality than glabrous individuals after climatic drought events even within a species (Ando, Isagi, & Kitayama, 2020). In addition, plants with extremely dense trichomes are also often found in alpine regions (Hedberg, 1964; Meinzer & Goldstein, 1985), suggesting that the dense leaf trichomes could play some important roles in low‐temperature conditions as well.
Dense leaf trichomes, in theory, increase diffusion resistance (i.e., decrease diffusion conductance which is the inverse of resistance) to gas and heat fluxes on the lamina surface (called as “leaf-trichome resistance” in this study; Nobel, 2009; Schuepp, 1993), which may be associated with the adaptations to both dry and low-temperature conditions. An increase in diffusion resistance on gas fluxes including H2O and CO2 can reduce both transpiration rate and photosynthetic rate. When leaf temperature is fixed, the effect of diffusion resistance is larger on the transpiration rate than on the photosynthetic rate, leading to greater WUE (called as “direct effect” in this study; Figure 1; Flexus et al., 2013; Schuepp, 1993). Since in many species the density of leaf trichomes is higher on leaf lower surface, where stomata exist, than on the upper surface (e.g., Aronne & De Micco 2001; Roth, 1984), it has been believed for many years that this “direct” effect (possible higher WUE through a direct suppression of gas-exchange rates) is a major ecological advantage of leaf trichomes in dry conditions [reviewed in Bickford (2016), Johnson (1975), and Sayre (1920)]. While some previous studies supported this argument (Kenzo et al., 2008; Ripley, Pammenter, & Smith, 1999; Wuenscher, 1970), many other studies repeatedly demonstrated that the direct effect of leaf-trichome resistance on H2O diffusion is negligible because the leaf-trichome resistance is an order of magnitude smaller than stomatal resistance (Amada, Ichie, Onoda, & Kitayama, 2017; Benz & Martin, 2006; Ehleringer & Mooney, 1978; Johnson, 1975; Nobel, 2009; Sayre, 1920; Skelton, Midgley, Nyaga, Johnson, & Cramer, 2012).
The leaf-trichome resistance can indirectly increase rather than decrease the gas diffusion through increasing leaf temperature due to reduction in the sensible‐heat and the latent‐heat fluxes (called as “indirect effect” in this study; Figure 1) (Campbell & Norman, 2010; Jones, 2014). Higher leaf temperature increases the transpiration rate (Campbell & Norman, 2010; Gate, 1968; Jones, 2014) and also can increase the photosynthetic rate especially in plants grown at a low temperature (Meinzer & Goldstein, 1985; Parkhurst & Loucks, 1972; Parkhurst, 1976). This is the contrary to the above‐mentioned “direct effects” of leaf-trichome resistance on the gas exchanges. Whether leaf-trichome resistance increase or decrease the photosynthetic rate and the transpiration rate depends on the combination of the direct and indirect effects of diffusion resistance (called as “combined effects” in this study; Figure 1).
Relative importance of direct and indirect effects of leaf-trichome resistance, and the magnitude of their combined effects on the gas-exchange rates are subject to other leaf traits (e.g., leaf size, stomatal openness) and environmental conditions (e.g., air temperature, humidity, light intensity) (Jones 2014). Larger leaf width can increase the “boundary-layer resistance” (defined as diffusion resistance of boundary layer outside of trichome layer in this study), which reduces the fluxes of gas, latent heat and sensible heat, and low stomatal conductance directly reduces the fluxes of gas and latent heat (Campbell & Norman, 2010; Jones, 2014). Air temperature may influence the indirect effect rather than the direct effect though modulating leaf temperature that determines the photosynthetic rate and the transpiration rate. For example, at low air temperature conditions (e.g., in high-elevational areas), both the photosynthetic rate and the transpiration rate can be greatly increased by increased leaf temperature, while at high air temperature conditions (e.g., in low-elevational areas), only the transpiration rate can be increased by increased leaf temperature since the photosynthetic rate is saturated or even decreases at a higher temperature (Figure 1b-c). In addition, environmental variations occur not only among sites but also within a day (i.e., diurnal change) which may influence the direct and indirect effects of leaf-trichome resistance on the whole-day gas-exchange rates.
To examine the combined direct and indirect effects of leaf-trichome resistance on the gas-exchange rates across environmental gradients, we studied Metrosideros polymorpha , an endemic and dominant tree species in the Hawaii Islands, which has enormous variations in the amount of leaf trichomes across a wide range of habitat environments: elevation ranges from nearly 0 to 2500 m asl (treeline), mean annual temperature from 5 to 25°C, mean annual precipitation from a few hundreds to over 10,000 mm yr-1, and soil age from a few decades to over four million years (Cordell, Goldstein, Mueller‐Dombois, Webb, & Vitousek, 1998; Cornwell, Bhaskar, Sack, Cordell, & Lunch, 2007; Kitayama & Mueller‐Dombois, 1995). Leaf trichomes are mostly found on the lower surface of leaves (thus, the role of light reflectance is not likely) and their amount varies from 0 to ca 150 g m–2 (Joel, Aplet, & Vitousek, 1994; Tsujii, Onoda, Izuno, Isagi, & Kitayama, 2016). Glabrous individuals are often abundant in moderately wet areas, whereas pubescent individuals are more abundant in dry or high‐elevation areas (Tsujii et al., 2016; Vitousek, Aplet, Turner, & Lockwood, 1992). In particular, the individuals with the largest amount of leaf trichomes (up to 40% of leaf mass; Tsujii et al., 2016) can be found in dry alpine areas on Mauna Loa where the photosynthetic rate may be limited by low air temperature and drought (Hoof, Sack, Webb, & Nilsen, 2008; Tsujii et al., 2016). Although Amada et al. (2017) showed that the “direct” effects of leaf‐trichome resistance on WUE were negligible, they did not consider the “indirect” effects of leaf trichomes on gas exchanges through modulating leaf temperature. The “indirect” effect could be important especially in alpine areas where plants suffer from low temperature. In order to understand to what extent the leaf trichomes in M. polymorpha contribute to the carbon gain and WUE across the environmental gradient, it is necessary to examine both direct and indirect effects of the leaf‐trichome resistance on the daily photosynthetic rate and the daily transpiration rate as well as on instantaneous gas-exchange rates.
This study aims to examine the combined effects of leaf‐trichome resistance on gas exchanges across environmental gradients to obtain insights into ecological significances of the large variation in the amount of leaf trichomes in M. polymorpha . With this aim, we measured leaf morphological and physiological characteristics and monitored leaf temperature in field conditions across five elevational sites (100, 700, 1280, 1800, and 2400 m). Using the field-obtained values of morphological and physiological characteristics, we conducted model simulation analyses to quantify the combined effects of leaf‐trichome resistance on the photosynthetic rate and the transpiration rate. We address the following three questions in relation to the function of leaf trichomes in M. polymorpha : (I) do leaf trichomes increase leaf temperature in field conditions through increasing diffusion resistance? (II) does the leaf-trichome resistance increase or decrease the daily photosynthetic rate and the daily transpiration rate at each elevational site? (III) which leaf traits and environmental conditions significantly influence the combined effects of leaf-trichome resistance on the photosynthetic rate and the transpiration rate across the elevational gradient?