Discussion
This study provides the first unambiguous experimental proof that leaf
hairs reduce the boundary layer conductance for heat transfer between
leaves and the air (g bh). Our approach was
carefully designed to exclude all potentially confounding influences: we
inferred g bh in bald patches and in otherwise
identical hairy patches from the time constant for cooling following
transient radiative heating, accounted for differences in leaf surface
conductance to water vapor and leaf heat capacity, and ensured that the
radiative environments of each patch were identical and constant over
time. Cooling was faster and boundary layer conductance was greater in
the bald patch than in the hairy patch in nearly all experiments, by 2.4
to 38.7% (means within species). This finding could not be attributed
to differences in stomatal conductance or other components of energy
balance between patches. Our results thus validate the hypothesis that
leaf hairs slow convective heat exchange between leaves and air.
Several previous studies have examined the effects of leaf hairs on leaf
energy balance or gas exchange, though none was able to directly
quantify the effect of hairs on boundary layer conductance in intact
leaves in isolation from potential confounding factors. Benz and Martin
(2006) found no correlation between trichome cover and gas exchange
rates across 12 Tillandsia species, and concluded that hairs had
negligible influence on boundary layer conductance; yet, other factors
that differed across the 12 species may have confounded the observed
differences in gas exchange rates. Wuenscher (1970b) observed higher
leaf temperatures and lower transpiration rates in shaved versus
unshaved leaves of Verbascum thapsus , and attributed these
differences to a 90-fold increase of boundary layer resistance by hairs.
However, Parkhurst (1976) reassessed Wuenscher’s results and concluded
that hair removal would likely have increased boundary layer resistance
two-fold at most, and suggested a role for cuticular or epidermal damage
caused by hair removal; differences in stomatal conductance may also
have played a role. Ripley et al (1999) measured surface conductance to
water vapor by gas exchange before and after removal of hairs fromArctotheca populifolia leaves, and inferred that the hairs
generated a resistance of around 0.2 m2 s
mol-1; however, as in Wuenscher’s (1970) study, those
results could have been influenced by other unobserved changes in leaf
surface vapor transport caused by hair removal. Woolley (1964) observed
a substantial reduction in wind speed near the surface (both above and
within the hair layer) of hairy soybean leaflets as compared to shaved
leaflets, which is consistent with an increase in the effective boundary
layer thickness and a reduction in g bh.
Measurements of water loss were more ambiguous: variability obscured any
effect of hairs in excised, living leaflets, whereas shaving increased
transpiration rate by 21% in leaflets that had been killed by boiling.
Meinzer and Goldstein (1985) simulated effects of hairs on energy
balance in Espletia timotensis by assuming hairs entrained a
layer of still air equal to their depth and that hairs did not affect
absorptance; their simulations reasonably matched observations of
greater leaf temperatures in hairy as compared to partially-shaved
leaves. Amada et al. (2021) observed lower in situ leaf
temperatures in shaved versus hairy leaves of Metrosideros
polymorpha ; having verified that surface conductances to water vapor
did not differ between the two treatments, the authors attributed the
result to reduction in g bh, and thus in
convective cooling. That result could also have arisen from effects of
leaf hairs on radiation absorption, although hairs in M.
polymorpha are light in color and thus probably reduced radiation
absorption rather than the converse.
In the present study, we directly quantified g bhitself in hairy and bald leaf patches, and eliminated all factors that
could have confounded the results of previous studies described above:
(1) We eliminated the confounding influence of differences in light
absorption by using dynamic IR thermography rather than steady-state
temperature to infer differences in g bh, which
enabled us to estimate g bh per se despite
any differences in light absorption. (2) We eliminated the confounding
influence of differences in leaf size and shape between bald and hairy
leaves by choosing adjacent bald and hairy patches identical in size and
position relative to the leading edge of the leaf, and ensured identical
wind speeds by measuring both patches simultaneously in the same air
stream. (3) We eliminated the confounding effects of transplanting hair
layers or boiling leaves by measuring only intact leaves from which
hairs had been either left in place or removed. (4) We eliminated the
confounding influence of differences in stomatal conductance by
measuring surface vapor conductance directly in each patch with a
porometer immediately before measurements and incorporating those data
into our inference of g bh. Surface conductance
was very low in general, but was marginally lower on average in bald
patches than in hairy patches, ruling out evaporative cooling as a
general explanation for faster cooling in bald patches.
Our results do not appear to confirm the theoretical prediction that
hairs add a resistance, r h, proportional to the
depth of the hair layer (d h). While hair depth
and theoretical r h varied nearly 6-fold across
species in this study (from 0.04 to 0.80 m2 s
mol-1 for r h), our experimental
estimates of r h – based on observed differences
in g bh between bald and hairy patches – were
unrelated to theoretical predictions (Fig 7), although they spanned a
similar range. The experimental estimates also depended sensitively on
the value of an unknown parameter: the ratio (β ) between the
boundary layer resistances at the adaxial and abaxial surfaces in the
absence of hairs. It may seem reasonable to assume β ≈ 1.
However, in three of our study species (MAGR, OLEU and SOLY), the edges
of each leaf had a slight downward curl that may have slightly sheltered
the abaxial surface from wind, which could have increased boundary layer
resistance at that surface independent of hairs, making β less
than 1.0. A similar effect was reported by Grace and Wilson (1976), who
found lower wind speeds just behind the downward-curled leading edge of
the abaxial surface in Populus × euramericana . β< 1 would bring the results for r h in
OLEU and MAGR closer to the theoretical predictions: observed and
theoretical r h would match at β = 0.47 for
MAGR and β = 0.67 for OLEU (Fig S4). In summary, our data suggestr h is at best weakly related to hair layer depth,
but is probably on the same order of magnitude as theoretical
predictions based on hair layer depth.
Our results also initially appear inconsistent with modeling by
Schreuder et al. (2001), which suggested that leaf hairs mayenhance g bh by promoting turbulence near
the leaf surface. However, turbulence was predicted to emerge only above
a critical windspeed that depended on trichome height; e.g., for 2.5 cm
leaves with 500 µm trichomes, the critical windspeed was 2.18 m
s-1, and the critical windspeed increased as trichome
height decreased and leaf size increased. In our experiments, wind speed
was below 2 m s-1 in most experiments, trichomes were
shorter than 300 µm in all species except SOLY (Table 2), and leaves
were >> 2.5 cm wide except in OLEU. Thus, our
data neither contradict nor confirm the predictions of Schreuder et al.
(2001). It is interesting to note, however, that the largest deviation
between theoretical and experimental estimates ofr h in this study was in SOLY, which also had the
longest trichomes by far. The fact that experimentalr h was less than half the theoretical prediction
for SOLY, regardless of what value of β we assumed, may hint at
promotion of turbulence by tall hairs as proposed by Schreuder et al.
(2001).
We could not rigorously scale up our estimates ofg bh from the patch scale to whole leaves – the
estimates reproted here refer only to the individual patches of leaf
measured within each experiment – for three reasons. First, we could
not locate patches at a constant distance from the leaf edge across
experiments, due to the difficulty of finding leaf patches that we could
successfully shave without damaging the leaf. Second, it was impossible
to remove hairs from entire leaves in most cases. Third, our results did
not validate the estimate of hair-layer resistance from hair-layer
depth; had they done so, then we could have concluded that the effect of
hairs is independent of leaf size, in which case we could merely add a
calculated hair-layer resistance to predictions from existing models ofg bh in relation to leaf size and wind speed. For
example, prior theory predicts that g bh is
proportional to the square root of the ratio of wind speed
(v w, m s-1) to leaf size
(d l, m), thus: g bh ≈
0.267(v w/d l)0.5, where g bh is a whole-leaf (two-sided) value in
mol m-2 s-1 (Gates, 1968; Nobel,
1975). In the context of that theory, the range of % decreases ing bh that we observed (means of 2.4 to 39% across
species) correspond to the effect, predicted by the theory, of a 4.9 –
93% increase in leaf size or a 4.6 – 48% decrease in wind speed. An
important caveat is that our data apply only to leaf patches located 2
– 6 mm from the leading edge of a leaf. Given that the wind speed at a
given position above the leaf surface declines progressively with
distance from the leaf edge (e.g., Grace and Wilson, 1976), the boundary
layer resistance in the absence of hairs likewise increases with
distance from the leaf edge, which would make hair-layer resistance a
smaller proportion of the total resistance in locations farther from the
leaf edge. Thus, had we located patches farther from the leaf edge, we
may have found smaller percent increases in boundary layer
resistance due to hairs.
Authors have speculated for decades about how leaf hairs affect
photosynthesis (A ) and transpiration (E ) via boundary
layer conductance. Hairs have a wide range of reported effects on gas
exchange (e.g., Ehleringer and Mooney, 1978; Baldocchi et al., 1983;
Ripley et al., 1999), but it is typically difficult to disentangle the
effect mediated by g bh from other effects of
hairs, such as on radiation balance. For example, a seminal study by
Ehleringer and Mooney (1978) reported large suppression of both Aand E by hairs in Encelia farinosa as compared to its
close hairless relative E. californica , though these effects were
largely driven by increased reflectance due to hairs; photosynthesis
rates were similar with or without hairs after correcting for
differences in light absorption, indicating little or no effect of hairs
on boundary layer resistance. Amada et al. (2017) found small
differences in gas exchange rates in M. polymorpha , consistent
with the small (< 10%) increases in total CO2or H2O transport resistance due to trichomes predicted
from the thickness of the trichome layer. Our modeling suggests theg bh-mediated effects of hairs on gas exchange
should depend sensitively on conditions. A hair-layer resistance of 0.1
m2 s mol-1 – roughly the value we
estimated for OLEU – would change instantaneous WUE by -1.7% to +2.9%
depending on conditions, according to our model. For example, hairs
would increase WUE by nearly 2% at a stomatal conductance of 0.5 mol
m-2 s-1 or by 1.5% at a PPFD of 250
µmol m-2 s-1, or decrease WUE by
1.5% in a 1 mm leaf at 10oC (Fig 8). Generally, hairs
should tend to improve WUE when stomatal conductance, air temperature or
VPD is high or when PPFD is subsaturating. Hairs should influence WUE to
a greater degree in small leaves, though the direction of the effect
depends on air temperature.