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).