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?