Ecological significance of leaf trichomes as diffusion resistance
As we demonstrated that the leaf trichomes in M. polymorphasubstantially influenced the leaf heat balance both in the field conditions and in the simulation analyses. This means that the indirect effects on the photosynthetic and transpiration rates through changing leaf temperature cannot be ignored (Figure 1).
The photosynthetic rates were increased by leaf trichomes only at the high-elevational sites and decreased at the other lower-elevational sites (Figure 4h). This different trend is mainly due to the non-linear response of photosynthetic rates to temperature (Figure 8). In cold alpine environments the increase in leaf temperature with leaf-trichome resistance can increase the activity of photosynthetic enzymes; thus, the leaf trichomes can increase the photosynthetic rate (Meinzer &Goldstein, 1985; Parkhurst & Loucks, 1972; Parkhurst, 1976). On the other hand, in warm low-elevational environments, the increase in leaf temperature dose not increase or even decreases the photosynthetic rate (Parkhurst & Loucks, 1972; Parkhurst, 1976) due to enhanced respiration as well as photorespiration (Hofstra & Hesketh, 1969; Long 1991).
The increase in the whole-day carbon gain with the leaf trichomes seem to be modest (+0.8%) for the large amount of leaf trichomes (up to 45% of leaf mass). In the model simulation, since we used the environmental variations during summer season on the island of Hawaii (in September), the effect of leaf trichomes on the carbon gain can be even greater at lower-temperature conditions (Figure 8) during a winter season: monthly mean temperature in the 2400 site ranges from 7.0 °C in February to 10.6 °C in August (Giambelluca et al., 2014). Because the pubescent leaves at the high-elevational site have long lifespan (ca. six years; Amada et al., 2017), such marginal carbon gain may accumulate and recover the large carbon investment in trichomes throughout the leaf lifespan. Moreover, the increased leaf temperature might also increase the photosynthesis through other physiological processes including leaf developments and hydraulic traits which is strongly depend on leaf temperature (Sack, Melcher, Zwieniecki, & Holbrook, 2002; Sack, Streeter, & Holbrook, 2004).
The leaf trichomes consistently decreased rather than increased the whole-day water-use efficiency (WUE) at all elevational sites (Figure 5g) across a range of trichome thickness (0.05-1 mm; Figure 6g); therefore, the hypothesis that leaf trichomes as diffusion resistance play a role in higher WUE (Bickford, 2016; Johnson, 1975; Kenzo et al., 2008; Ripley et al., 1999; Wuenscher, 1970) cannot be supported inM. polymorpha . This is mainly due to the strong-irradiance conditions in Hawaii (Figure 4b) and also due to the differences in temperature dependence between the photosynthetic rate and the transpiration rate (Figure 1b-c). The strong irradiance increases the heat gain of leaves, under which the sensible-heat flux is greatly suppressed by leaf trichomes; thus, further increases leaf temperature. Moreover, relative increase in the transpiration rates is faster than that of the photosynthetic rates with increase in leaf temperature (Figure 1 and 8). A similar logic can be applied to effects of leaf size on WUE through boundary-layer resistance, that is, larger leaves with greater boundary-layer resistance decrease WUE under strong-irradiance dry conditions (Parkhurst & Loucks, 1972; Okajima et al., 2012). Therefore, leaf trichomes cannot contribute to drought tolerance through increasing diffusion resistance if both direct and indirect effects are considered.
Since leaf trichomes are observed in the wide range of plant taxa (Ichie et al., 2016; Johnson, 1975), we also explore the roles of leaf trichomes for more anisohydric plants than M. polymorpha (Table 3; Cornwell et al., 2007; Amada et al., 2017). Our sensitivity analyses show that leaf trichomes can increase WUE for anisohydric leaves located in low-temperature conditions or for leaves located in low-irradiance conditions (Figure 8h,i). However, these leaf traits and environmental conditions are not the conditions where pubescent plants are found. Stomatal behavior tends to be conservative in the stressful environments where pubescent plants often exist, such as arid areas, strong-irradiative areas, high-elevational areas, windswept conditions, and dry seasons (Agrawal et al., 2009; Aronne & De Micco, 2001; Ehleringer, 1981; Ichie et al., 2016; Johnson, 1975; Moles et al., 2020; Smith & Nobel, 1977; Tsujii et al., 2016). Indeed, WUE itself is much greater in more isohydric leaves than in anisohydric leaves (Figure 8g,h,i, and S11); thus, stomatal regulation is more effective to improve WUE than increases leaf-trichome resistance. In a tropical forest, trees exposed to the strong irradiance (canopy trees and gap plants) tend to have greater trichome density than understory or subcanopy trees (Ichie et al., 2016). Therefore, we do not consider the diffusion resistance as the primary function of leaf trichomes against dry stresses even in other pubescent plant species.
Leaf trichomes may have other functions in relation to drought tolerance (Johnson 1975; Bickford, 2016) such as defense against herbivores to avoid extra water loss (Amada et al., 2020) and promoting condensation on leaf surface either to decrease water loss (e.g., Konrad et al ., 2015) or to uptake water from dew on leaf surface (e.g., Ohrui et al., 2007). Amada et al. (2020) suggested that leaf trichomes inM. polymorpha can impede gall formation of specialist psyllids that increases water stress in leaves. Moreover, leaf trichomes inM. polymorpha often get wet even in the coldest and driest alpine areas (Amada, unpublished data), which may improve leaf water status. To understand the extreme variation of leaf trichomes in M. polymorpha , still some further work may be needed to evaluate ecological significance of multifunctional leaf trichomes against various environmental stresses (Sack & Buckley, 2020).