Introduction
Leaf hairs, formally known as trichomes, are epidermal appendages on
average present in >50% of species in given ecosystems and
varying widely in morphology among and even within species
(Perez-Estrada et al., 2000). Leaf hairs are thought to provide several
functional roles. They provide mechanical protection against
phytophagous insects (Levin, 1973; Dalin et al., 2008), and some plant
species can produce leaf hairs with glandular secretion which also serve
a defensive purpose (Werker, 2000). Leaf hairs can also provide
protection from disease pressures such as downy mildew (Kortekamp and
Zyprian, 1999). Leaf hairs also influence energy balance and gas
exchange. The measured effect of hairs on leaf temperature varies, from
warming up to several degrees C (Woolley, 1964; Ehleringer and Mooney,
1978; Ripley et al., 1999; Peng et al., 2015) to cooling in summer and
warming in winter (Ehleringer and Mooney 1975). The overall effect of
hairs on water use efficiency (WUE, the ratio of net photosynthetic rate
to transpiration rate) differs across studies but is most commonly
reported to be positive (Ehleringer and Mooney, 1978; Ripley et al.,
1999). The influence of trichomes on leaf temperature and gas exchange
arises from effects on reflectivity and the boundary layer. Trichomes
can lower leaf absorptance to visible light (Wuenscher, 1970a; Holmes
and Keiller, 2002) and provide protection from photoinhibition,
ultraviolet radiation and overheating (Ehleringer and Mooney, 1978;
Karabourniotis et al., 1992; Karabourniotis et al., 1995; Ntefidou and
Manetas, 1996).
Trichomes are also thought to influence the diffusive exchange of heat
and mass across the leaf boundary layer – that is, the zone adjacent to
the leaf surface where wind speed is substantially reduced by friction
with the leaf surface, and in which transport is therefore dominated by
diffusion rather than by advection. Because diffusion is much slower
than advection at macroscopic scales (e.g., over distances
> ~21 µm at a wind speed of just 1 m
s-1), the boundary layer slows heat and gas exchange
between the leaf and air (Raschke, 1960; Grace and Wilson, 1976). It is
most often assumed that hairs increase the effective thickness of the
boundary layer by entraining a layer of relatively still air, and
thereby impede heat and mass transport, and that boundary layer
thickness relates to the height of the trichome canopy (Wuenscher,
1970a; Ehleringer and Mooney, 1978; Nobel, 2005). However, some have
speculated the converse, on the premise that hairs break up air flow and
thereby promote turbulence (Wolpert, 1962; Schreuder et al., 2001).
These contrary theoretical speculations on the influence of leaf
trichomes on the boundary layer, and potentially on gas exchange, have
have not been adequately tested experimentally. This may be partly
because leaf boundary layer conductance is perceived to be very large
relative to stomatal conductance (Nobel, 2005; Jones, 2014) and thus
relatively unimportant. Indeed, many models assume leaf and air
temperatures are always equal (Dong et al., 2017), which is equivalent
to assuming boundary layer conductance is infinite (resistance is zero),
so that leaf temperature is strongly coupled with air temperature. Yet
many studies have reported large leaf-air temperature differencesin situ (Leigh et al., 2017; Fauset et al., 2018; Guha et al.,
2018; Xu et al., 2020): e.g., ΔT (leaf minus air) = +5.1 ± 2.1oC (mean ± SD) for 68 Proteaceae species (Leigh et
al., 2017); –6 to +7 oC for three woody species in a
tropical dryland (Dong et al., 2017); +3.7 to + 4.7 oC
in wheat (Ehrler et al., 1978; Ayeneh et al., 2002); –4.1 to +4.1oC in almond canopies (Gonzalez-Dugo et al., 2012).
Leaf-air temperature difference is strongly influenced by boundary layer
conductance because it directly influences both convective heat exchange
and transpiration (and thus latent cooling).
Full resolution of precisely how trichomes affect the boundary layer has
not been achieved, because of the technical difficulty of estimating
boundary layer conductance experimentally in real leaves, rather than in
physical models of leaves. It is common, for example, to estimate
boundary layer conductance to water vapor in a gas exchange chamber
using a wet filter paper or other wet fabric surface, to represent a
leaf without an epidermis and thus without stomatal resistance (Monteith
and Unsworth, 2013). Another approach, based on using rigid, heated
metal plates, contributed to the validation of phenomenological
equations relating g bh to wind speed and to leaf
size (specifically, the characteristic dimension related to downwind
width) (Gates, 1968; Nobel, 1975; Schuepp, 1993; Brenner and Jarvis,
1995; Schlichting and Gersten, 2017). Another set of methods is based on
surface treating leaf surfaces with water or a water-impermeable
substance to modulate the contribution of evaporation to energy balance
(Impens, 1966; Impens et al., 1967; Linacre, 1972; De Parcevaux and
Perrier, 1973; Paw U and Daughtry, 1984). While potentially powerful,
each of those approaches is difficult to apply to the specific question
of how leaf hairs affect boundary layer conductance. The most direct
experimental test of this question was performed by Wuenscher (1970),
who examined how the removal of leaf hairs affected transpiration rate
in Verbascum thapsus . Although Wuenscher concluded that
hairs reduced boundary layer conductance, later reanalysis by Parkhurst
(1976) suggested that cuticular damage caused by shaving led to enhanced
transpiration and evaporative cooling, which confounded Wuenscher’s
results.
Dynamic thermography – heating a leaf and then measuring its rate of
cooling by convection (Jones, 2014) – can quantify boundary layer
conductance independent of the effect of hairs on light absorption.
Dynamic thermography using infrared cameras has recently been used
successfully to quantify both boundary layer conductance (Albrecht et
al., 2020) and stomatal conductance (Vialet-Chabrand and Lawson, 2019)
in intact leaves. Here we adapt and extend the approach of Albrechtet al . (2020) to quantify the influence of leaf hairs on boundary
layer conductance to heat (g bh; see Table 1 for a
list of symbols) in five broadleaved species, by measuring the time
constant for leaf cooling (τ ) after transient radiative heating
in leaf patches with hairs and without hairs and then inferringg bh from τ using a dynamic energy balance
model, accounting for stomatal conductances measured in each patch. We
hypothesized that leaf hairs will add a component of transport
resistance that is proportional to the depth of the hair layer, thereby
reducing g bh compared to an otherwise similar
leaf surface without leaf hairs.