Tree Physiology 28, 113–122
© 2008 Heron Publishing—Victoria, Canada
Leaf gas exchange of understory spruce–fir saplings in relict cloud
forests, southern Appalachian Mountains, USA
KEITH REINHARDT1 and WILLIAM K. SMITH1,2
1
Department of Biology, Wake Forest University, Winston-Salem, NC 27109-7325, USA
2
Corresponding author ([email protected])
Received February 9, 2007; accepted June 10, 2007; published online October 15, 2007
Summary The southern Appalachian spruce–fir (Picea
rubens Sarg. and Abies fraseri (Pursh) Poir.) forest is found
only on high altitude mountain tops that receive copious precipitation ( > 2000 mm year –1) and experience frequent cloud
immersion. These high-elevation, temperate rain forests are
immersed in clouds on ~65% of the total growth season days
and for 30–40% of a typical summer day, and cloud deposition
accounts for up to 50% of their annual water budget. We investigated environmental influences on understory leaf gas exchange and water relations at two sites: Mt. Mitchell, NC
(MM; 35°45′53″ N, 82°15′53″ W, 2028 m elevation) and
Whitetop Mtn., VA (WT; 36°38′19″ N, 81°36′19″ W, 1685 m
elevation). We hypothesized that the cool, moist and cloudy
conditions at these sites exert a strong influence on leaf gas exchange. Maximum photosynthesis (Amax ) varied between 1.6
and 4.0 µmol CO2 m – 2 s –1 for both spruce and fir and saturated
at irradiances between ~200 and 400 µmol m – 2 s –1 at both sites.
Leaf conductance (g) ranged between 0.05 and 0.25 mol m – 2
s –1 at MM and between 0.15 and 0.40 mol m – 2 s – 1 at WT and
was strongly associated with leaf-to-air vapor pressure difference (LAVD). At both sites, g decreased exponentially as
LAVD increased, with an 80–90% reduction in g between 0
and 0.5 kPa. Predawn leaf water potentials remained between
–0.25 and –0.5 MPa for the entire summer, whereas late afternoon values declined to between –1.25 and –1.75 MPa by late
summer. Thus, leaf gas exchange appeared tightly coupled to
the response of g to LAVD, which maintained high water status, even at the relatively low LAVD of these cloud forests.
Moreover, the cloudy, humid environment of these refugial forests appears to exert a strong influence on tree leaf gas exchange and water relations. Because global climate change is
predicted to increase regional cloud ceiling levels, more research on cloud impacts on carbon gain and water relations is
needed to predict future impacts on these relict forests.
Keywords: cloud immersion, ecophysiology, Fraser fir, red
spruce, southern Appalachians, water relations.
Introduction
The southern Appalachian spruce–fir (Picea rubens Sarg.–
Abies fraseri (Pursh) Poir.) forest is confined to seven high al-
titude mountaintop areas in the southern Appalachians, located between southwestern Virginia and southern North
Carolina (Oosting and Billings 1951, Ramseur 1960, White
1984). These forest islands are remnants of a larger spruce–fir
forest that dominated the landscape in the late Pleistocene
(Delcourt and Delcourt 1984) and currently occupy about 26.5
kha (Nicholas et al. 1992). Because of their high elevation
(> 1400 m) and SW-to-NE orientation, copious precipitation
(> 2000 mm year – 1, distributed evenly throughout the year)
and cool temperatures (6.5 °C annual mean, 13.5 °C growing
season mean (May–September)), these areas are frequently
immersed in clouds for 30–40% of a typical day during the
growth season (May–September) and immersion of some duration occurs on ~65% of all days (Vogelmann et al. 1968,
Smathers 1982, Saxena and Lin 1990, Mohnen 1992, Joslin
and Wolfe 1992, Weathers et al. 1995, Baumgardner et al.
2003). Interception of water from clouds accounts for between
25 and 50% of the annual water budget of these forests
(Mohnen 1992).
The recent decline of the southern Appalachian spruce–fir
forest has been attributed to a variety of factors, including
acidic deposition, climate change, logging, fires and pests
such as the balsam woolly adelgid (Adelges piceae
(Ratzeburg)) (White 1984, McLaughlin et al. 1987, 1991,
Bruck and Robarge 1988, Busing et al. 1988, Johnson and
Fernandez 1992, Schier and Jensen 1992, White and Cogbill
1992). Evidence for this decline includes decreased diameter
growth, increased adult mortality rates, reduced photosynthesis and changes in community composition and ecosystem dynamics (McLaughlin et al. 1987, Bruck and Robarge 1988,
Busing et al. 1988, McLaughlin et al. 1991). Recent studies
have indicated that current rates of regeneration may be insufficient to sustain spruce and fir as the dominant canopy trees
(Pauley and Clebsch 1990, Nicholas et al. 1992, Johnson and
Smith 2005).
Most studies evaluating spruce–fir decline in the southern
Appalachians have focused on population biology, emphasizing long-term changes in species distribution and community
structure. Few studies have evaluated the ecophysiology of
Picea rubens and Abies fraseri to determine the conditions
necessary for the establishment, growth and survival of these
species (McLaughlin et al. 1990, 1991, Johnson and Smith
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REINHARDT AND SMITH
2005, 2006). Moreover, the ecophysiological effects of clouds
on any forest tree species have rarely been assessed (see for example Bruijnzeel and Veneklaas 1998, Letts and Mulligan
2005, Motzer et al. 2005).
We investigated environmental influences on the gas exchange physiology of understory Fraser fir and red spruce
trees at two sites in the southern Appalachian mountains
(Mt. Mitchell, NC and Whitetop Mtn. VA). Because these sites
are often beneath or immersed in clouds during the growing
season (Saxena and Lin 1990, Mohnen 1992, Baumgardner et
al. 2003), we hypothesized that the humid, cloudy environment would exert a strong influence on photosynthetic carbon
and water relations. Specifically, it was predicted that photosynthetic performance of these species would be adapted to
low, diffuse light and leaf conductance to CO2 would be relatively high because of little water restriction and low leafto-air-vapor pressure deficit (LAVD). In view of the apparently strong association of this forest type with cloud immersion, changes in cloud patterns in response to climate change
may have a marked effect on the survival of these forests.
Materials and methods
Study sites
Study sites were located in forests dominated by spruce at
Whitetop Mountain and spruce–fir at Mt. Mitchell in Jefferson
National Forest and Mt. Mitchell State Park, respectively (Figure 1). Whitetop Mountain (WT; 36°38′19″ N, 81°36′19″ W,
1685 m elevation) and Mt. Mitchell (MM; 35°45′53″ N,
82°15′54″ W, 2028 m elevation) are covered by northern hardwood and spruce or spruce–fir forests, with the conifers dominant at the highest elevations (typically above 1585 and
1700 m for WT and MM, respectively; Table 1). Sites were selected as representative of the stand structure of spruce–fir
forests (Rheinhardt 1984, Rheinhardt and Ware 1984, Bruck
and Robarge 1988, Goelz et al. 1999). Mean total leaf area was
1757 mm2 for WT spruce, 1982 mm2 for MM spruce and
Figure 1. Study site locations: Mt. Mitchell, NC and Whitetop Mtn.,
VA.
Table 1. Site characteristics. Annual precipitation based on 30-year
means. Summer period is May 1–September 30, 2006.
Coordinates
Elevation (m)
Annual precipitation (mm)
Summer precipitation (mm)1
Summer cloudiness (% days)
Summer cloudiness (% hours)
1
Mt. Mitchell
Whitetop Mtn.
35°45′53″ N,
82°15′54″ W
2030
1890
650
55
29
36°38′19″ N,
81°36′19″ W
1685
1500
530
61
28
In September, MM received over 300 mm of rain while WT received only 100 mm.
4245 mm2 for MM fir for the 5.0 cm shoots placed in the gas
exchange cuvette. Mean needle density was 2.0 (mm shoot)– 1
at WT. At MM, mean needle density was 1.44 (mm shoot)– 1
for fir and 1.90 (mm shoot)– 1 for spruce.
Leaf gas exchange and micrometeorology of understory
trees were monitored during the summer of 2006 (May–September). One 25 × 25 m understory plot was established at
each site that included tree age classes ranging from young
seedlings (< 5 years old) to mature, old-growth trees
(> 200 years old), as well as a canopy gap (~10 m2 ). Slope azimuth was west-southwest (~240°) at WT and southwest
(~233°) at MM; slope angles ranged from ~2 to 5° at both sites.
Microclimatology
Instruments were centrally located within each study plot and
simultaneously recorded photosynthetic photon flux (PPF;
0.3–0.7 µm wavelengths), air temperature (Tair ), humidity,
precipitation and leaf wetness during an entire growth season.
At both sites, the instruments were placed at the edge of an interior canopy gap and were positioned at a height of 1 m. We
measured PPF every 30 min with LI-190 PAR sensors (Li-Cor,
Lincoln, NE) connected to voltage amplifiers (Model UTA,
EME Systems, Berkeley, CA) and HOBO data loggers (H8
4-channel logger, Onset Computer Corp., Bourne, MA). Additional measurements of PPF were made during photosynthetic
measurements with a handheld LI-190 PAR sensor positioned
according to the natural inclination and azimuth of the main
axis of the measured shoot tips. Air temperature and humidity
were measured every 30 min with a HOBO Pro Series
RH/Temp data logger (Onset Computer Corp.). Precipitation
was continuously recorded with a HOBO R3 data logging rain
gauge at a height of 1 m. Leaf wetting was measured with a
HOBO weather station leaf wetness smart sensor connected to
a HOBO Micro Station data logger. Cloud immersion frequency was quantified by comparing PPF, leaf wetness and
relative humidity measurements with hourly pictures generated by a webcam at Mt. Mitchell State Park
(http://www.ils.unc.edu/parkproject/ webcam/webcam.html).
It was determined that the combined measurements of PPF
< 600 µmol m – 2 s – 1, relative humidity > 95% and leaf wetness
> 85% (for non-precipitating cloud immersion events)
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UNDERSTORY SAPLING LEAF GAS EXCHANGE
matched the visual discrimination of cloud immersion (cloud
ceiling below maximum canopy height) based on images generated by the webcam at Mt. Mitchell.
115
tures during the night and early morning, which may have resulted in xylem cavitation (Pittermann and Sperry 2003).
Statistics
Leaf gas exchange and water relations
At each site, leaf gas exchange and shoot xylem water potentials were measured monthly throughout the summer
(May–September) with a Li-Cor LI-6400 model portable photosynthesis system (Li-Cor, Lincoln, NE). Diurnal measurements were made at 0800, 1000, 1200, 1400 and 1600 h (solar
time; List 2000) on two days each month: May 18 and 21, June
20 and 28, July 18 and 19, August 17 and 18 and September 29
and 30. All gas exchange measurements were made on randomly selected understory trees (n = 10 for each species for
each measurement time and representing both sun- and
shade-adapted leaves) on previous-year shoots at mid-tree
height on trees 0.3–3.0 m tall. Initially, gas exchange data
were separated into two height classes of trees for comparison,
0.3–1.0 m and 1.0–3.0 m. However, the data were not significantly different and were therefore combined for analysis and
interpretation. Natural orientation of shoots was maintained
during measurements, and air temperature and relative humidity inside the leaf chamber were maintained within ± 5% of
ambient values. Most measurements were made during clear
sky conditions (no cloud immersion). However, during cloud
immersion, needles with surfaces wet from fog were blotted
with tissue paper immediately before measurement of gas exchange (Smith and McLean 1989, Brewer and Smith 1997).
Because needles may still have been wet after blotting, erroneous leaf conductance values were discarded and only leaf conductance and transpiration values obtained during dry-leaf
conditions were used in the analysis.
Net photosynthesis (Anet ) was calculated on a total leaf area
basis because of the high silhouette to projected area ratio of
the shoots of the understory plants (Smith et al. 1991). Daily
maximum photosynthesis (Amax ) was calculated by averaging
the five highest values. Seasonal Amax and PPF at saturation
were determined from analysis of light response curves with
Photosyn Assistant (Ver. 1.1.2 Dundee Scientific, Dundee,
U.K.). Leaf area inside the sample cuvette was estimated by
multiplying the total number of needles inside the cuvette by
the mean surface area of individual needles determined with a
microscope micrometer and electronic micrometer caliper
(model IP54, Fred V. Fowler Comp., Newton, MA). To relate
single needle areas to needle lengths, 20 needles per species at
both sites were measured for both smaller (< 1.0 m) and larger
trees (> 1.0 m).
Plant water status was estimated from shoot water potentials
(Ψ) measured with a Scholander-type pressure chamber
(Model 1000, PMS Instrument Comp., Corvallis, OR) on the
same trees for which gas exchange was measured (n = 10 for
each species) at 0600 h (predawn) and 1400 h on the same days
as the photosynthesis measurements. Samples were taken
from the previous-year shoots at mid-tree height. September
predawn Ψ measurements for WT trees were extremely low
and discarded because of below-freezing air and leaf tempera-
All data sets were tested for normality and equality of variance. Diurnal and monthly measurements of photosynthesis
and shoot water potentials were averaged by site and time of
measurement. Best-fit regression analysis was used to generate response curves of gas exchange parameters to environmental conditions. Effects of site and measurement date on
inter-specific differences in environmental and gas exchange
measurements were evaluated by multivariate analysis of variance. Monthly means were compared post hoc by comparing
the overlap of 95% confidence intervals, and significance was
determined at P < 0.05.
Results
Site microclimate
Diurnal PPF values ranged from 255 to 829 µmol m – 2 s – 1 at
MM and from 60 to 290 µmol m – 2 s – 1 at WT and were
15–46% (MM) and 3–15% (WT) of PPF measured at the top
of the canopy (P < 0.001; Figure 2a), with the difference
mostly explained by greater cloudiness at WT. Midday Tair was
between 5 and 11 °C in May, increased to about 20 °C in July
and decreased to 2–13 °C in late September and did not differ
between sites (P = 0.32; Figure 2b). Atmospheric vapor pressure deficits (VPD) were similar at MM and WT (P = 0.22),
ranging between 0.1 and 0.7 kPa (Figure 2c). Leaf-to-air vapor
pressure deficits were greater at WT than at MM throughout
the summer (P = 0.0008), averaging between 0.2 and 1.0 kPa
for all measurements except in June at MM (~1.2 kPa) (Figure 2d). At both sites, cloud immersion occurred on 55–61%
of all days, constituting about 28–29% of all daylight hours
(0800–1800 solar time) from May through September (Table 1).
Leaf gas exchange and water relations
Mean maximum photosynthesis was generally higher for WT
spruce compared with MM spruce and fir (P = 0.05). Maximum photosynthesis for WT spruce was 2.9 µmol m – 2 s – 1 in
May and increased to 4.1 µmol m – 2 s – 1 in July before decreasing to 2.0 µmol m – 2 s – 1 in September (Figure 3a). Maximum
photosynthesis of MM trees had a less pronounced seasonal
pattern, and fir Amax was greater than spruce Amax in all months
except May, ranging from 2.2 to 2.9 µmol m – 2 s – 1 (MM fir),
whereas Amax of MM spruce was between 1.6 and 2.6 µmol
m – 2 s – 1 (Figure 3a).
Transpiration (E) was higher in WT spruce than in MM fir
throughout the summer (1.2–1.4 mmol m – 2 s – 1 and
0.6–1.1 mmol m – 2 s – 1, respectively; P < 0.0001). Transpiration of MM spruce was comparable with that of WT spruce for
the first half of the summer and then similar to E of MM fir for
the second half of the summer (Figure 3b). Leaf conductance
(g) in WT spruce was about 0.26 mol m – 2 s – 1 in early summer,
decreased to about 0.12 mol m – 2 s – 1 in July and increased to
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116
REINHARDT AND SMITH
Figure 2. Microclimatology of sites on days of diurnal measurements
of photosynthetic gas exchange. Values are diurnal means of (a)
photosynthetic photon flux (PPF), (b) air temperature (Tair ) , (c) vapor pressure deficit (VPD) and (d) leaf to air vapor pressure deficit
(LAVD), except for air temperature (mean of air temperatures for
1100–1300 h). Symbols: 䊊 = WT site; 䊏 = MM site; 夹 = calculated
global PPF at top of canopy. Vertical bars for (a) are 90th (upper) and
10th (lower) percentiles. Vertical bars for (c) and (d) are 95% confidence intervals.
about 0.4 mol m – 2 s –1 in September (Figure 3c). Stomatal conductance was generally lower in MM fir than in WT spruce
and ranged from 0.05 to 0.25 mol m – 2 s –1 during the summer,
with the lowest values in June (P = 0.0001; Figure 3c). At MM,
g of spruce was similar to that of fir throughout the summer except in August when mean g was 0.10 mol m – 2 s –1 lower in
MM spruce (Figure 3c).
The ratio of internal to atmospheric CO2 concentration
( ci /ca ) was between 0.90 and 0.98 on all measurement days,
except in MM trees in June (ci /ca = 0.79 fir, 0.82 spruce) (Figure 3d). Intrinsic water-use efficiency (WUE, Anet /g) patterns
were the mirror image of ci /ca patterns. In WT trees, WUE was
essentially constant throughout the summer (< 10 µmol CO2
mol –1 H2O for all measurement days) and lower than that for
MM species, which had higher WUE in June (37–47 µmol
CO2 mol –1 H2O), declining to about 9–18 µmol CO2 mol – 1
Figure 3. Mean of (a) maximum photosynthesis (Amax ), (b) transpiration (E), (c) leaf conductance (g), (d) the ratio of internal CO2 to atmospheric CO2 (ci /ca ) and (e) intrinsic water-use efficiency (WUE,
Anet /g) on days of diurnal measurement. Symbols: 䊊 = WT spruce;
䊐 = MM spruce; 䊏 = MM fir. Vertical bars are 95% confidence intervals.
H2O later in the summer (Figure 3e).
Net photosynthesis and PPF had similar diurnal patterns
(Figure 4). The general pattern for both species at MM was a
peak in Anet in midmorning followed by a midday depression
and another peak in late afternoon (Figure 4). However, Anet of
WT spruce was greatest during midday (Figure 4).
Predawn shoot Ψ at both sites varied little during the summer, starting at a mean value of –0.25 MPa in May at both sites
and decreasing to –0.65 MPa for MM trees and –0.55 MPa for
WT trees by September (Figure 5a). Mean summer predawn
Ψ at WT (–0.70 MPa) was significantly less than mean Ψ at
MM (–0.45 MPa; P = 0.001). Afternoon Ψ showed a more
seasonal pattern, declining from –0.45 MPa in May to
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UNDERSTORY SAPLING LEAF GAS EXCHANGE
–1.5 MPa in July at both sites before rebounding to –1.0 MPa
(WT) and –1.25 MPa (MM) in August, followed by a decrease in September to –1.25 MPa (WT) and –1.8 MPa (MM)
(Figure 5b). Mean summer afternoon ΨMM (–1.2 MPa) was
less than mean ΨWT (–1.0 MPa; P = 0.005).
Photosynthesis and water relations versus environmental
conditions
Photosynthetic rates of both spruce and fir were strongly correlated with PPF (P < 0.0001 for all; Figure 6). Maximum Anet
derived from light response curves was about 2.5, 2.0 and
3.5 µmol m – 2 s –1 for MM fir, MM spruce and WT spruce, respectively, and saturated at PPFs between 200 and 400 µmol
m – 2 s –1 at both sites (Figures 6a–c). Leaf conductance had a
strong response to LAVD. At both sites, g decreased exponentially as LAVD increased (P < 0.0001 for all; Figure 7), with
the sharpest decline occurring at LAVDs between 0 and
0.5 kPA. No values greater than 2.0 kPA were measured for
LAVD.
117
Intrinsic WUE increased from about 1 to more than 36 µmol
CO2 mol – 1 H2O for WT spruce and to over 70 µmol CO2 mol – 1
H2O for MM fir as LAVD increased from 0.0 to 2.0 kPa (Figure 8a) and as leaf temperature (Tl) increased from 5 to 30 °C
(Figure 8b). Photosynthesis and transpiration were not significantly associated with either Tl or LAVD and leaf conductance
was little affected by Tl (data not shown).
Discussion
The southern Appalachian spruce–fir temperate rain forests
are frequently immersed in clouds (Braun 1964, Smathers
1982, Saxena and Lin 1990, Cogbill and White 1991, Mohnen
1992, Baumgardner et al. 2003). Our study investigated the influence of the moist, humid and often cloudy environment of
these mountaintop forests on leaf gas exchange and water relations of understory trees, a potential factor in determining the
altitudinal and geographic distribution of this relic forest type.
(Siccama 1974, Smathers 1982, Cogbill and White 1991).
Microclimatology
Mean daily PPF was relatively low because of daily
orographic cloud formation (Figures 2a and 4). These incident
irradiances are lower than those reported for similar
understory forest sites, for example, mean monthly irradiance
is > 600 µmol m –2 s – 1 for Wyoming spruce–fir (Broderson et
al. 2006) and 900–1300 µmol m –2 s – 1 for mid-elevation New
England spruce–fir (Richardson et al. 2004); however, they
are similar to irradiances reported for moist conifer forests
(Johnson and Smith 2006, Urban et al. 2007) and tropical
montane cloud forests (Letts and Mulligan 2005). Furthermore, the ratio of direct PPF (µmol m – 2 s – 1 ) to potential global
radiation (W m – 2 ) (diffuse index) was quite low compared
Figure 4. Diurnal measurements of net photosynthesis (Anet ) and
photosynthetic photon flux (PPF) for Mt. Mitchell (MM) and
Whitetop Mtn. (WT) sites. Symbols: 䊐 = MM spruce; 䊏 = MM fir;
䊊 = WT spruce; and 夹 = PPF. Error bars are 95% confidence intervals.
Figure 5. Mean water status measured on days with diurnal measurements of photosynthetic gas exchange. Values are means of shoot water potential measurements (Ψ) for (a) predawn (~0630 h) and (b)
afternoon (1400–1430 h). Symbols: 䊊 = WT spruce; and 䊏 = MM
spruce and fir. Error bars are 95% confidence intervals.
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Figure 6. Net photosynthesis
(Anet ) and corresponding
photosynthetic photon flux (PPF)
measured for Mt. Mitchell (MM)
and Whitetop Mtn. (WT) spruce
and fir. Response curves for (a)
MM fir, (b) MM spruce and (c)
WT spruce were created by combining all measurements obtained
throughout the summer study period. All light response curves
were determined using the fitted
equation Anet = a(1 – e – bPPF),
where a and b are fitted constants.
with other studies (Letts and Mulligan 2005, Urban et al.
2007), varying between 0.11 and 0.52 for WT and between
0.13 and 0.24 for MM.
These southern Appalachian forest sites are much more humid compared with many other in North America continental
conifer forests, because of the frequent cloudiness, and low air
and leaf temperatures combine to keep VPD and LAVD low
throughout the summer (Figures 2c, 2d and 7). For example,
summer VPDs in this study (0.1–0.8 kPa) are substantially
less than those of 1.0–6.0 kPa typically reported for western
conifer forests (Carter et al. 1988, Goulden et al. 1997, Day
2000, Grossnickle et al. 2005, Broderson et al. 2006), but similar to VPDs of 0–2.75 kPa found in boreal spruce–fir forests
(Arain et al. 2003, Pejam et al. 2006, Urban et al. 2007) and
tropical montane cloud forests (Letts and Mulligan 2005,
Motzer et al. 2005).
A consequence of such humid and cloudy conditions was
frequent leaf wetness. The high humidity, nightly wetting and
frequent cloud immersion events resulted in considerable leaf
wetness throughout most daylight hours (mean leaf wetness of
solar day = 54–96%), with both adaxial and abaxial surfaces
of leaves wet during cloud immersion events.
Ecophysiology
Although our results are consistent with previous light and wa-
ter studies on spruce and fir trees (e.g., Lamhamedi and
Bernier 1994, Alexander et al. 1995, Fredeen and Sage 1999,
Day 2000, Rayment et al. 2002, Bigras 2005), some significant
differences may exist. Unlike previous studies investigating
environmental controls on conifer photosynthesis (Fredeen
and Sage 1999, Day 2000, Arain et al. 2003, Bigras 2005,
Grossnickle et al. 2005, Pejam et al. 2006), photosynthesis in
spruce and fir in the southern Appalachians does not appear to
be tightly coupled with leaf conductance (P = 0.11 for both
species and sites, r 2 < 0.16 for all; data not shown) and both parameters appeared to have different environmental responses.
Photosynthesis was strongly correlated with irradiance (Figure 6), whereas g was most strongly associated with LAVD
(Figure 7). Previous studies have cited photosynthetic light
saturation points for spruce and fir ranging from 200 to
1000 µmol m – 2 s – 1, with most values between 400 and
600 µmol m – 2 s – 1 (Lamhamedi and Bernier 1994, Alexander
et al. 1995, Goulden et al. 1997, Day 2000, Johnson and Smith
2005). Our results suggest even lower light saturation points
for P. rubens and A. fraseri of between 200 and 400 µmol m – 2
s – 1 (Figures 6a–c; similar to Johnson and Smith 2006). Numerous studies have shown that photosynthetic saturation values in this PPF range may be optimal for carbon capture because of the associated lower Tl, decreased transpirational water usage and reduced risk of photoinhibition (Hollinger et al.
Figure 7. Changes in leaf conductance (g) versus leaf-to-air vapor
pressure deficit (LAVD) for Mt.
Mitchell (MM) and Whitetop
Mtn. (WT) spruce and fir. Response curves for (a) MM fir, (b)
MM spruce and (c) WT spruce
were created by combining all gas
exchange measurements obtained
throughout the study. All regressions are hyperbolic decay equations, g = ab(b + LAVD) – 1,
where a and b are fitted constants.
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Figure 8. Changes in intrinsic water-use efficiency (WUE, Anet /g)
versus (a) leaf-to-air vapor pressure deficit (LAVD) and (b) leaf temperature (Tl). WUE versus LAVD regressions are linear, and WUE
versus Tl regressions are cubic: WUE = yo + aT l + bT l2 + cT l3, where
yo is the y-intercept a, b and c are fitted constants. All regressions are
significant (P < 0.0001). Symbols: 䊊 = WT spruce; 䊐 = MM spruce;
䊏 = MM fir; solid line = MM fir regression; gray line = MM spruce regression; dotted line = WT spruce regression.
119
haps this explains the genetic divergence of Fraser fir from balsam fir (Abies balsamea (L.) Mill.) (Delcourt and Delcourt
1984, White and Cogbill 1992, Clark et al. 2000). About
10,000 years ago, a post-glacial warming trend coincided with
a shift in spruce and fir distribution from much of eastern
North America to more northern locations and mountain tops
in the southeast USA (Delcourt and Delcourt 1984, White and
Cogbill 1992). By as early as 8000 years ago, southern
montane spruce–fir forests were fragmented from northern
populations and gene exchange among populations was prevented (Jacobs et al. 1984).
The ci /ca ratio remained high in both species (> 0.90 on most
measurement days), and water-use efficiencies were extremely low at low LAVDs (< 1.0 µmol CO2 mol – 1 H2O at <
0.1 kPa), with maximum values of about 72 and 36 µmol CO2
mol – 1 H2O for MM and WT trees, respectively (Figure 8). The
humid, cloudy conditions and low Anet allowed for consistently
high internal CO2 concentration, even during periods of active
photosynthesis, as has been reported in other temperate rain
forests (e.g., Tissue et al. 2005). Similarly, the intrinsic WUE
values reported here are lower, overall, than intrinsic WUE
values reported for western North American conifers (about
40 –160 µmol CO2 mol – 1 H2O) as well as temperate and tropical evergreen trees in Australia (37–85 and 18–96 µmol CO2
mol – 1 H2O, respectively; Cunningham 2005, Grossnickle et al.
2005). In addition, the relative magnitude of change (> 7900%
and 4100% for MM and WT, respectively) between maximum
and minimum intrinsic WUE values was much greater than
previously reported. For example, Grossnickle et al. (2005)
found that intrinsic WUE was relatively stable for western red
cedar (Thuja plicata Donn) across a broad VPD range, changing by only 6–22%, whereas Cunningham (2005) reported
modest increases in the range of 0.3–37%. These WUE characteristics apparently resulted from the sensitivity of g to
LAVD. The frequently humid and low-light conditions, combined with the moist soil conditions, presumably allow the
stomata of spruce and fir trees at our study sites to remain open
without causing excessive water loss.
Inter-site and interspecific comparisons
1994, Goulden et al. 1997, Germino and Smith 2000, Gu et al.
2002, Rocha et al. 2004, Min 2005, Motzer et al. 2005, Urban
et al. 2007). Furthermore, the more homogeneous light environment decreases the acclimation period of understory plants
to penetrating light (Chazdon and Pearcy 1986), and an increase in the blue/red light ratio during cloudy conditions has
been shown to increase photosynthetic rate (Urban et al.
2007).
We found a strong association between g and LAVD in both
species. Leaf conductance decreased exponentially as LAVD
increased, with a major reduction in g (80–90%) at an LAVD
of ~0.5 kPA (Figures 8d–f). The strong association between g
and LAVD, combined with the low PPF and LAVD recorded
during the study, reflect a forest system where gas exchange is
strongly influenced by the temperature and water regimes
characteristic of this cloudy mountaintop environment. Per-
Before the start of our study, we noted that MM receives almost 1900 mm year –1 of precipitation compared with just over
1500 mm year –1 for WT (Perry 2002, State Climate Office of
North Carolina 2006). We hypothesized that there would be a
similar differential in cloud immersion, which might cause
differences in gas exchange physiology between the sites.
However, no differences were seen in cloud immersion events
or precipitation during the study, except in September, when
MM received over 300 mm of rain and WT received only
~100 mm (Table 1). Nonetheless, photosynthesis in spruce
was significantly higher at WT than at MM on most measurement days (Figure 3a) despite lower PPF and Tair and higher
LAVD (Figure 2). Perhaps long-term climate differences (not
observed during our single summer of observations) have resulted in genetic differentiation in the photosynthetic capacity
of these mountain-top populations, although red spruce ap-
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REINHARDT AND SMITH
pears to have low genetic variability (DeHayes and Hawley
1992, White and Cogbill 1992, Schaberg 2000).
Forest stand structure differed between sites. The MM fir
was infested with the balsam woolly adelgid (Adelges piceae
(Ratzeburg)) pest introduced in the 1950s, resulting in high
mortality (40–90%) of adult trees (Eagar 1984, Pauley and
Clebsch 1990, Nicholas et al. 1992). Additionally, extensive
logging occurred up to the summit of MM before the 1950s
(White 1984). Thus, the MM spruce–fir forest is currently
young, a grading of second-growth fir forest intermixed with
old growth spruce trees. In contrast, the WT spruce forest is
classified as unlogged old growth (Rheinhardt and Ware
1984). These differences in forest age and disturbance regimes
may have influenced nutrient cycling (Johnson et al. 1991,
Johnson and Fernandez 1992), Ca2+ leaching from the soil
(Joslin et al. 1988, Johnson and Fernandez 1992) and incident
sunlight, resulting in differences in gas exchange.
In conclusion, the southern Appalachian spruce–fir forest
ecosystem is a relict forest found at only seven mountaintop
sites that are moist, cool and frequently immersed in clouds.
Although precipitation was low throughout most of the study
(15–45% of the long-term means), total precipitation was over
600 mm, cloud immersion occurred on about 55–61% of all
days and evidence of drought was absent. In support of this
were the high shoot water potentials that occurred throughout
the summer. In contrast, Anet was most strongly associated with
incident irradiance that matched unusually low light saturation
points for photosynthesis in both species (200–400 µmol m – 2
s – 1 ). Despite low apparent water stress, g was strongly and inversely exponentially coupled to LAVD, resulting in constant
and low Amax, E and WUE. Thus, it appears that the cloud-immersed, humid environment may strongly influence leaf gas
exchange, acting to maximize photosynthetic carbon gain at
low E. Because global climate change is predicted to increase
cloud ceiling heights (decreased cloud immersion) in the next
century (Still et al. 1999, Foster 2001, Richardson et al. 2003),
with the potential for major changes in temperature and humidity regimes, the long-term survival of these relic spruce–fir
forests is uncertain.
Acknowledgments
This research was supported by a grant from the William and Flora
Hewlett Foundation to WKS. We thank the Jefferson and George
Washington National Forest (Mt. Rogers National Recreation Area
District) and Mt. Mitchell State Park for permission to conduct field
research. We thank Simon Hallsberg and Steven Pennington for assistance with field data collection and laboratory assistance, and we are
grateful to Dr. Daniel Johnson and Dr. Robert Browne for discussion
and insightful comments.
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