Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:

Tree Physiology 17, 187--194
© 1997 Heron Publishing----Victoria, Canada

Seasonal air and soil temperature effects on photosynthesis in red
spruce (Picea rubens) saplings
PAUL A. SCHWARZ,1 TIMOTHY J. FAHEY1 and TODD E. DAWSON2
1

Department of Natural Resources, Fernow Hall, Cornell University, Ithaca, New York 14853, USA

2

Section of Ecology and Systematics, Corson Hall, Cornell University, Ithaca, New York 14853, USA

Received January 23, 1996

Summary Net photosynthesis and stomatal conductance
were measured in ten red spruce (Picea rubens Sarg.) saplings,
growing near Ithaca, New York, throughout the early spring and
late-fall growing periods. Gas exchange and daily minimum
and maximum soil and air temperatures were also measured.

Linear regression analysis showed that rates of net photosynthesis were positively correlated with both minimum daily soil
and air temperatures but that minimum soil temperature was a
better predictor of net photosynthesis. Moreover, net photosynthesis was more sensitive to changes in soil temperature than
to changes in air temperature, and photosynthesis was approximately twice as sensitive to temperature changes during the fall
than during the spring.
Keywords: air temperature, climatic change, gas exchange,
seasonal effects, temperature sensitivity.

Introduction
Evergreen coniferous trees growing in temperate climates become frost hardened and dormant during part of the winter
(Levitt 1980, Kozlowski et al. 1991, Havranek and Tranquillini
1995). While dormant, they may show an almost total cessation of gas exchange (but see Schaberg et al. 1995). However,
the evergreen habit affords the potential for year-round net
photosynthesis. Furthermore, climatic change resulting in
warmer winters may permit temperate conifers to continue
photosynthesizing later in the fall and to begin photosynthesizing earlier in the spring, thereby extending their growing
season. In the northeastern United States and eastern Canada,
red spruce (Picea rubens Sarg.) is an important evergreen
coniferous species in many montane and low-elevation forests
(Blum 1990). The present study was undertaken to assess the

possible influence of climatic warming on winter photosynthesis in red spruce by documenting the relationships between
photosynthetic rates and soil and air temperatures during the
spring and fall.
Previous studies of conifers native to western North America
have demonstrated significant reductions in gas exchange rates
on days following nights with near-freezing or sub-freezing air
temperatures (e.g., Fahey 1979, Kaufmann 1982, Smith et al.
1984), and other field and laboratory studies have shown that

low air temperatures can significantly limit gas exchange in
conifers (e.g., Smith 1985, DeLucia 1987, DeLucia and Smith
1987, Carter et al. 1987). In addition, several studies have
demonstrated the role of low soil temperatures in limiting gas
exchange in conifers (DeLucia 1986, DeLucia and Smith
1987, Carter et al. 1987, Day et al. 1989, 1990, 1991, Lippu
and Puttonen 1991).
Although recent observations of gas exchange in red spruce
at low temperatures have been conducted in conjunction with
studies of the species’ cold tolerance and susceptibility to
winter injury (Fincher et al. 1989, DeHayes 1992, Fincher and

Alscher 1992, L’Hirondelle et al. 1992, Amundson et al. 1993,
Eamus 1993, Hadley et al. 1993), no systematic examination
of the relative importance of air and soil temperatures in
influencing photosynthesis of red spruce during spring and fall
has been reported. Moreover, most studies of conifer gas exchange have focused on a single period during the growing
season. In this study, we examined both the beginning and the
end of the growing season. We hypothesized that gas exchange
responses of red spruce to temperature differs between the fall
and spring growing periods. In fall, air and soil temperatures
decline in tandem, and subsequently trees undergo winter
hardening. In spring, the presence of a snowpack may effectively decouple air and soil temperatures resulting in a more
complex suite of cues leading to springtime recovery of gas
exchange. The nature of these different temperature responses
will be important in determining the effects of climatic change
on a species’ performance.

Materials and methods
Site description and plant material
In April 1992, ten 7-year-old red spruce saplings were randomly selected from an even-aged plantation growing near
Cornell University, Ithaca, New York. The stand was established in 1987 with 2-year old, greenhouse-grown seedlings

from a South Range, Nova Scotia provenance collected in
1985 (Alscher et al. 1989). The plantation contained approximately 100 saplings planted in three rows in an east--west
orientation. Rows were approximately 2.1 m apart, and spac-

188

SCHWARZ, FAHEY AND DAWSON

ing within rows was approximately 0.9 m. Saplings were
between one and two meters tall.
Temperature measurements
For the first two sampling periods of the study (spring and fall
1992), calibrated thermistors were installed at four depths in
the soil profile (1, 5, 10, and 20 cm) beneath the canopy of
three of the saplings. Soil temperature measurements were
made between 0800 and 0900 h on each day of gas exchange
sampling, and it was assumed that these measurements approximated the minimum overnight soil temperatures. Minimum and maximum air temperatures for the preceding 24-h
period were also recorded each morning with a Taylor min-max thermometer located in a weather shed at the site.
During the second year of the study (spring and fall 1993),
a Campbell CR10 data logger (Campbell Scientific, Inc.,

Logan, UT) was installed to automate the collection of air and
soil temperatures. Copper-constantan thermocouples were installed at soil depths of 1, 5, and 10 cm beneath the canopy of
the same saplings measured during the previous year. An
additional sensor measured air temperature and relative humidity. The data logger was programed to scan each sensor
every 60 s, to calculate sample averages every 15 min, and to
calculate 24-h minimum and maximum temperatures for each
of the sensors.
Gas exchange measurements
Gas exchange was measured in situ on a single shoot selected
from the south side of each of the ten saplings. The measurements were made with an LI-6200 Portable Gas Exchange
System (Li-Cor, Inc., Lincoln, NE) equipped with a 0.25-liter
cuvette. The rate of CO2 depletion was measured over a 20-s
interval after orienting the shoot normal to the direction of the
sun. The same shoot from each of the saplings was used for all
of the measurements during the sampling period. In a few
cases, however, a shoot was accidentally damaged or broken,
in which case a nearby shoot (usually on the same branch) was
selected to take its place.
Two gas exchange sampling schedules were followed. Diurnal sampling sessions were scheduled periodically to measure
net photosynthetic rate and stomatal conductance at hourly

intervals on each of the three trees where the thermistors or
thermocouples were located. These sampling sessions were
used to characterize the diurnal pattern of gas exchange in the
saplings. A total of six diurnal sessions during the two spring
sampling periods and five sessions during the fall periods
suggested that daily maximum photosynthesis and stomatal
conductance occurred in the afternoon over a broad time period (1300--1600 h). Subsequent sampling sessions, during
which all ten saplings were measured, were scheduled during
these times. Sampling sessions were scheduled on sunny or
partly cloudy days in an attempt to minimize the variation in
irradiance. However, on four occasions over the two years, the
sky became cloudy during a sampling session and irradiances
were substantially reduced. In addition, late in the fall 1993
sampling period irradiances were reduced because of low sun
angles.

Leaf areas for individual shoots were measured with a LiCor LI-3100 portable area meter. The shoot from each sapling
was harvested at the end of the sampling period and then
brought to the laboratory where the needles were stripped off
and the projected leaf area measured. Three measurements

were made for each shoot and a sample mean was used to
calculate net photosynthetic rate and stomatal conductance on
a projected needle area basis.
Data analyses
Sample means were computed for each of the following gasexchange-related variables for each sampling session: daily
maximum net photosynthesis (Anet ), stomatal conductance
(gs), photosynthetically active radiation (PAR), and intercellular CO2 concentration (Ci). Sample means were also computed
for 24-h minimum and maximum soil temperatures at each of
the sampled depths. Atmospheric vapor pressure deficit (VPD)
at the time of the 24-h maximum air temperature was calculated for the two sampling periods (spring and fall 1993) for
which the necessary relative humidity data were available.
Pearson product-moment correlation coefficients were computed between average daily maximum Anet and average PAR,
24-h maximum and minimum air temperatures, and average
24-h maximum and minimum soil temperatures at each soil
depth. Minimum air temperature (minTair ), average minimum
soil temperature measured at 5 cm depth (min5Tsoil ), and average minimum soil temperature measured at 10 cm depth
(min10 T soil ) were selected as independent variables in a multiple linear regression analysis because each variable had a
substantive correlation coefficient in all four sampling periods.
These three variables were also believed to represent best the
thermal conditions within the canopy and rooting environments of the saplings. Combinations of the three variables

were used to construct least squares linear regression equations
to predict daily maximum Anet. In every case, adding more than
one independent variable to the regression equation resulted in
a nonsignificant slope coefficient and a reduction in the adjusted r 2 value. The likely explanation for this result is the
strong linear association among the three temperature variables. Subsequently, a simple least squares linear regression
was computed using only average min 5Tsoil and another using
only minTair . Although the regressions were based on time
series data, a lack of autocorrelation in the residuals was
verified by a Durbin-Watson test. For each regression, three
sets of linear contrasts were computed to examine differences
between the spring and fall sampling periods for both the slope
coefficient (β) and the intercept (α). Because the data failed to
meet the assumption of homogeneity of variance among the
four sampling periods, t-statistics were computed that incorporated the variance estimate for each sampling period. The
estimated degrees of freedom for each of the comparisons were
computed using Satterthwaite’s equation (Snedecor and Cochran 1980, p 228).

PHOTOSYNTHESIS IN PICEA RUBENS SAPLINGS

Results

Air and soil temperature
There was considerable day-to-day fluctuation in both 24-h
minimum and maximum air temperatures (Figures 1a, 1b, 2a,
and 2b) and in 24-h minimum soil temperature. The time series
showed trends of gradually increasing temperature during the
two spring sampling periods and gradually decreasing temperature during the two fall sampling periods. Exceptions to
this general pattern were the air temperature data for the spring
1993 sampling, which showed little overall trend. Subfreezing
nights were common throughout the spring of 1992 but occurred only once during spring 1993. There were frequent
overnight frosts and steadily declining daytime temperatures
during the fall sampling periods of both years.
Soil temperature tracked changes in air temperature, but the
day-to-day fluctuation in soil temperature measured within the

189

rooting zone (at a depth of 10 cm) was less than the fluctuation
at the soil surface (at a depth of 1 cm). In spring 1992, soil
temperature remained above freezing throughout the measurement period, whereas in 1993, soil surface temperatures
dropped below 0 °C on several occasions during April before

warming significantly in May. Throughout the four sampling
periods, soil temperatures in the rooting zone were usually 1 to
2 °C higher than surface temperatures, and minimum surface
soil temperatures were usually 3 to 6 °C higher than minimum
air temperatures, except for spring 1993 when the average
temperature difference was less than 1 °C .
Net photosynthesis
Seasonal patterns in peak, daily gas exchange rates during the
four sampling periods are shown in the top half of Figures 1a,
1b, 2a, and 2b. Gas exchange rates were measured between
early April and late May on 17 days during spring 1992 and 16

Figure 1. Average daily maximum net photosynthesis (Anet ), stomatal conductance (gs), intercellular CO2 concentration (Ci ), photosynthetically
active radiation (PAR), daily minimum and maximum air temperature (Tair ), and daily minimum soil temperature at 1 cm and 10 cm depths
(Tsoil ) during spring 1992 (a) and spring 1993 (b). Error bars are ± 1 SD. Note: the two soil depths were chosen to display the range of soil
temperatures; the temperature at 5 cm was used in the analyses (see text).

190

SCHWARZ, FAHEY AND DAWSON

Figure 2. Average daily maximum net photosynthesis (Anet ), stomatal conductance (gs), intercellular CO2 concentration (Ci ), photosynthetically
active radiation (PAR), daily minimum and maximum air temperature (Tair ), and daily minimum soil temperature at 1 cm and 10 cm depths
(Tsoil ) during fall 1992 (a) and fall 1993 (b). Error bars are ± 1 SD. Note: the gs value marked by an asterisk (fall 1992) was probably the result of
an instrument or measurement error (see Wong et al. 1979, 1985).

days during spring 1993. Fall measurements were begun in late
September. In 1992, measurements ended in mid-November
when average daily maximum net photosynthesis (Anet)
reached approximately 0 µmol m −2 s −1 (a total of 19 days of
measurements), whereas in 1993, measurements were made on
22 days because Anet was positive until well into December.
During the two fall periods, peak rates of photosynthesis occurred early in the sampling period (late September and early
October), whereas the pattern was less clear during the spring
periods. In spring 1992, the peak occurred midway through the
sampling period in mid-April, whereas in 1993 the peak occurred toward the end of the sampling period (mid- to lateMay). During the spring 1992 sampling period, average daily
maximum Anet was consistently higher than the rates during the
spring 1993 sampling period and both fall periods. In both fall
periods, Anet declined steadily and there were short-term reduc-

tions in gas exchange that corresponded with overnight frost
events.
Overall, average daily maximum Anet ranged from nearly
0 µmol m −2 s −1 in late fall to over 10 µmol m −2 s −1 in mid-April
1992. The patterns of Anet, stomatal conductance (gs), and
intercellular CO2 concentration (Ci) varied considerably
among trees. This variation was consistent within sampling
periods and among sampling periods.
Functional relationship between temperature and Anet
Daily maximum Anet and the various temperature variables
were highly correlated. The association between average daily
maximum Anet and average PAR was not as strong as the
association between Anet and temperature (Table 1); however,
the spring 1992 coefficient for PAR appears to be anomalous.
The fall data displayed stronger correlations than the spring

PHOTOSYNTHESIS IN PICEA RUBENS SAPLINGS
Table 1. Pearson product-moment correlation coefficients calculated
between average daily maximum Anet and various environmental factors: PAR, photosynthetically active radiation; maxTair /min Tair , maximum/minimum daily air temperature during the preceding 24 h; VPD,
atmospheric vapor pressure deficit at time of maxTair ;
max 1 Tsoil /min1 Tsoil , maximum/minimum daily soil temperature
measured at a soil depth of 1 cm during the preceding 24 h;
max 5 Tsoil /min5 Tsoil , maximum/minimum daily soil temperature
measure at a soil depth of 5 cm during the preceding 24 h;
max 10 Tsoil /min 10 Tsoil , maximum/minimum daily soil temperature
measured at a soil depth of 10 cm during the preceding 24 h.
Variable

PAR
maxTair
minTair

VPD
max 1 Tsoil
min 1 Tsoil
max 5 Tsoil
min 5 Tsoil
max 10 Tsoil
min 10 Tsoil

Spring

Fall

1992

1993

1992

1993

−0.065
−0.145
0.498
n.a.
n.a.
0.205
n.a.
0.180
n.a.
0.137

0.570
0.115
0.545
0.315
0.335
0.696
0.548
0.728
0.603
0.734

0.487
0.704
0.665
n.a.
n.a.
0.719
n.a.
0.697
n.a.
0.680

0.746
0.834
0.836
0.474
0.861
0.902
0.928
0.953
0.938
0.956

data, and the 1993 data displayed stronger linear relationships
than the 1992 data. This latter observation may be explained in
part by the improved accuracy of the environmental data that
were collected in 1993 compared with 1992. In particular, the
continuous monitoring of temperatures by the data logger may
have resulted in more reliable measurements of minimum and
maximum temperatures, especially at the various soil depths.
Summaries of the regressions for each of the four sampling
periods (Table 2) illustrate that min 5Tsoil was a significant
predictor of daily maximum Anet (P < 0.005) in all but the
spring 1992 sampling period, explaining 50 to over 90% of the
variation in average daily maximum net photosynthesis in the
other sampling periods.

191

Minimum Tair was a significant predictor of Anet (P < 0.005)
only during the two fall sampling periods, and it explained
only 30 to 70% of the variation. The regression summaries
indicate that the least squares regression model fits the fall data
better than the spring data and that the model fits the 1993 data
better than the 1992 data. None of the environmental variables
provided a significant linear relationship for the spring 1992
data, and scatter plots of average daily maximum Anet and other
variables did not suggest other functional relationships.
Although the regression slope coefficient for soil in spring
1992 (Table 2) was similar to the one in 1993, the regression
itself was not significant. Moreover, the magnitude and range
of measurements in 1992 were considerably higher than those
during the same period in 1993. The measurements were also
considerably higher than published values for many conifers
(Teskey et al. 1995). This discrepancy suggested a potential
calibration problem with the LI-6200, and the unit was subsequently re-calibrated by Li-Cor, Inc. Given these uncertainties, the spring 1992 data were removed from further analyses.
There was a significant, positive linear relationship between
average minimum Tsoil measured at 5 cm depth and average
daily maximum Anet and between minimum Tair and average
daily maximum Anet (Table 3). Furthermore, the results suggest
that the linear relationship with minimum Tsoil was significantly different between the spring 1993 sampling period and
the two fall periods, and that the relationship between the two
fall periods for both predictors was not significantly different.
In contrast, no seasonal differences were observed for the
relationship between Anet and minimum Tair .

Discussion
Both minimum air and soil temperatures appeared to influence
the pattern of photosynthesis during the spring and fall. During
fall, short-term reductions in daily maximum Anet that were
superimposed on a trend of steadily declining gas exchange
(Figures 2a and 2b) were associated with overnight frost events
and are consistent with the results of others (Fahey 1979,

Table 2. Linear, least squares regression summary for: daily max Anet = intercept (α) + slope (β) (minT).
Season

Spring 1992

Spring 1993

Fall 1992

Fall 1993

Regression

Predictor variable

coefficient

min 5 Tsoil

β

minTair

Value

P-value

0.121

n.s.

r

2

Value

P-value

0.205

0.059

5.891
0.078

< 0.001
0.054

1.231

0.001

0.167

0.002

1.938
0.126

< 0.001
< 0.001

1.416

< 0.001

0.032

α
β

5.184
0.112

0.003
0.003

α

0.987

< 0.001

β

0.241

< 0.001

0.248

0.530

0.297

0.486

α
β

0.049
0.239

n.s.
< 0.001

α

0.162

0.098

r2

0.442

0.908

0.699

192

SCHWARZ, FAHEY AND DAWSON

Table 3. Linear contrasts among regression slope and intercept coefficients. Coefficients were compared based on the t-test, computed using
unequal variance assumptions and degrees of freedom calculated by Satterthwaite’s approximation.
min 5 Tsoil

minTair

Linear contrast

Coefficient

P-value

Coefficient

P-value

1(Spring 93) -- 1/2(Fall 92 + Fall 93)

α
β
α
β
α
β

≈ 0.005
< 0.005
n.s.
n.s.
< 0.025
< 0.001

α
β
α
β
α
β

< 0.1
< 0.1
< 0.025
n.s.
< 0.001
< 0.001

0(Spring 93) + 1(Fall 92) -- 1(Fall 93)
1/3(Spring 93 + Fall 92 + Fall 93)

Smith et al. 1984, DeLucia 1987). Together with the strong
relationships between Anet and Tsoil in the fall sampling periods,
these results suggest a simple model of environmental regulation of photosynthesis: the gradual decline in Anet may be
driven by root-zone soil temperature, whereas short-term reductions are associated with overnight freezing. Such a model
is consistent with the observations of DeLucia and Smith
(1987) and Carter et al. (1987) who indicated that, for Rocky
Mountain Engelmann spruce (Picea engelmannii (Parry)), low
soil temperatures are more limiting to net photosynthesis and
stomatal conductance than low air temperatures only when air
temperatures are above freezing. However, maximum Tsoil was
also highly correlated with fall Anet (Table 1), suggesting that
a model for red spruce photosynthetic performance under
declining temperatures may be more complex than the simple
model proposed above. In addition, maximum Tair was
strongly correlated with Anet during the two fall sampling
periods (Table 1). This is likely to be related to the fact that
maximum daily air temperatures during the fall measurement
periods (15--30 °C) (Figures 2a and 2b) were in the optimal
range for photosynthesis in conifers (Belous 1986, as cited in
Teskey et al. 1995, p 114).
The regulation of Anet in red spruce during the spring appears
to be more complex than during the fall, and the results of the
present study do not provide a clear picture of environmental
controls. Although air and soil temperatures were significant
predictors of Anet , in spring 1993, possible effects of sub-freezing nights were not demonstrated because only one overnight
frost occurred during the sampling period. This may explain,
in part, the weaker relationship between minimum Tair and
Anet that was observed during the spring 1993 sampling period
compared with the spring 1992 sampling period (Figure 1b).
Moreover, in spring 1992, the pattern of daily maximum Anet
differed greatly from the pattern in 1993 with the highest
photosynthetic rates observed early in the spring (Figure 1a).
In a laboratory study, DeLucia (1986) reported sharp declines in photosynthesis in Engelmann spruce seedlings after
soil temperatures dropped below 8 °C. In another laboratory
study, Day et al. (1991) reported sharp reductions in Anet in
loblolly pine (Pinus taeda L.) seedlings when soil temperatures dropped below 10 °C, and Lippu and Puttonen (1991)
reported significant reductions in Anet in Scots pine (Pinus
sylvestris L.) seedlings in an 8 °C soil temperature treatment

relative to a 12 °C treatment. Moreover, both DeLucia (1986)
and Day et al. (1991) reported an overall curvilinear response
in Anet to changes in soil temperature, but the response was
linear when soil temperature fell below 10 °C. In the present
study, minimum subsurface soil temperatures during the two
fall sampling periods and the spring 1993 period were generally below 10 °C, and the data for these three periods suggest
a linear response of Anet to minimum soil temperature.
The high degree of covariance between air and soil temperatures in our field study makes it difficult to separate the effects
of these factors on gas exchange in spring and fall. In general,
minimum soil temperature explained more of the variation in
average daily maximum Anet than did minimum Tair (Table 2).
In addition, the steeper slope coefficients (β) in the regression
equations with average minimum soil temperature suggest that
Anet was more sensitive to changes in minimum soil temperature than to changes in minimum air temperature. A unit
change in minimum soil temperature resulted in an Anet response that was 50 to 90% greater than the photosynthetic
response from a similar change in minimum air temperature.
This sensitivity suggests that, during both the fall cooling
period and the spring warming period (1993), minimum soil
temperature may not only be a better predictor of daily maximum Anet than minimum Tair , but that photosynthesis may be
more limited by minimum soil temperature than by minimum
air temperature. Jurik et al. (1988) also concluded that soil
temperature was a better predictor of Anet than air temperature
during the springtime recovery of photosynthesis in white pine
(Pinus strobus L.). Thus, after accounting for the effects of
sub-freezing nights, it would seem that models of environmental control of fall (and probably spring) net photosynthesis
in conifers in cold temperate regions should focus on soil
temperatures.
We found a significant difference in the photosynthetic
response of red spruce to changes in temperature between the
spring and fall periods. The linear contrasts in Table 3 indicate
that the difference between the spring 1993 slope estimate for
minimum Tsoil (the predictor variable) and the average of the
two fall estimates was highly significant (P < 0.005). However,
the difference between the spring 1993 slope estimate for
minimum Tair and the average of the two fall estimates was not
significant (P < 0.1). Furthermore, although the regression
equation between Anet and minimum Tsoil for spring 1992 was

PHOTOSYNTHESIS IN PICEA RUBENS SAPLINGS

not significant, the slope estimate for spring 1992 was similar
to the estimate for spring 1993 (Table 2). Because of the
uncertainties in the spring data, these results are tentative;
however, they suggest that the sensitivity of net photosynthesis
to changes in soil temperature during the spring was approximately half of that during the fall. This result is consistent with
the hypothesis that the photosynthetic response of red spruce
to temperature differs between the fall and spring.
The simplest regression-type model, based solely on Tair and
T soil , may be inadequate for predicting the photosynthetic response of red spruce to changes in the spring warming and fall
cooling periods of the growing season. In particular, the sensitivity of Anet to changes in temperature depends on the particular physiological mechanisms that may constrain Anet during
these periods, and these constraints probably differ between
spring and fall. Changes in chloroplast thylakoid structure,
chlorophyll content, photosynthetic enzyme activity, and electron transport (see reviews by Öquist 1983, Havranek and
Tranquillini 1995, Teskey et al. 1995 and references therein)
are associated with winter hardening, and although the relationships among these physiological changes is unclear, it is
believed that these changes in combination with stomatal closure are largely responsible for the winter decline in net photosynthesis (Öquist 1983, Havranek and Tranquillini 1995,
Teskey et al. 1995). Limitations to the springtime recovery of
photosynthesis, on the other hand, have been associated with
photoinhibition (Lundmark et al. 1988, Ottander and Öquist
1991, Strand and Lundmark 1995), insufficient soil water
associated with soil thawing (Fahey 1979, Smith 1985, Jurik
et al. 1988, Day et al. 1990), root hormones and mycorrhizal
activity (Havranek and Tranquillini 1995). Thus, an improved
model of photosynthetic sensitivity to temperature will depend
on experimental work to isolate the relevant mechanisms and
to describe their seasonal dependence on air and soil temperatures. Finally, although warmer air and soil may delay the onset
of winter hardening and hasten springtime recovery, the significance of extending the growing season must be assessed in
terms of whole-plant responses and overall carbon balance.

Acknowledgments
The senior author gratefully acknowledges the support and assistance
of the staff at the Boyce Thompson Institute Research Field, especially
C. Tutton. In addition, the author thanks M. Stover, C. Williams, R.
Sladek, and S. Schwarz for their help in the field and also C. McCulloch for his advice on statistical analysis.

References
Alscher, R.G., R.G. Amundson, J.R. Cumming, S. Fellows, J. Fincher,
G. Rubin, P. Van Leuken and L.H. Weinstein. 1989. Seasonal
changes in the pigments, carbohydrates and growth of red spruce as
affected by ozone. New Phytol. 113:211--224.
Amundson, R.G., R.J. Kohut, J.A. Laurence, S. Fellows and L.J.
Colavito. 1993. Moderate water stress alters carbohydrate content
and cold tolerance of red spruce foliage. Environ. Exp. Bot.
33:383--390.

193

Blum, B.M. 1990. Picea rubens Sarg. red spruce. In Silvics of North
America: 1. Conifers. Eds. R.H. Burns and B.H. Honkala. Agric.
Handbook 654. U.S. Department of Agriculture, Forest Service,
Washington, DC, pp 250--259.
Carter, G.A., W.K. Smith and J.L. Hadley. 1987. Stomatal conductance in three conifer species at different elevations during summer
in Wyoming. Can. J. For. Res. 18:242--246.
Day, T.A., E.H. DeLucia and W.K. Smith. 1989. Influence of cold soil
and snowcover on photosynthesis and leaf conductance in two
Rocky Mountain conifers. Oecologia 80:546--552.
Day, T.A., E.H. DeLucia and W.K. Smith. 1990. Effect of soil temperature on stem sap flow, shoot gas exchange and water potential
of Picea engelmannii Parry during snowmelt. Oecologia 84:474-481.
Day, T.A., S.A. Heckathorn and E.H. DeLucia. 1991. Limitations of
photosynthesis in Pinus taeda L. (loblolly pine) at low soil temperatures. Plant Physiol. 96:1246--1254.
DeHayes, D.H. 1992. Winter injury and developmental cold tolerance
in red spruce. In The Ecology and Decline of Red Spruce in the
Eastern United States. Eds. C. Eager and M.B. Adams. SpringerVerlag, New York, pp 296--337.
DeLucia, E.H. 1986. Effect of low root temperature on net photosynthesis, stomatal conductance and carbohydrate concentration in
Engelmann spruce (Picea engelmannii Parry ex Engelm.) seedlings. Tree Physiol. 2:143--154.
DeLucia, E.H. 1987. The effect of freezing nights on photosynthesis,
stomatal conductance, and internal CO2 concentration in seedlings
of Engelmann spruce (Picea engelmannii Parry). Plant Cell Environ. 10:333--338.
DeLucia, E.H. and W.K. Smith. 1987. Air and soil temperature limitations on photosynthesis in Engelmann spruce during summer. Can.
J. For. Res. 17:527--533.
Eamus, D. 1993. Assimilation and stomatal conductance responses of
red spruce to midwinter frosts and the constituent ions of acid mist.
Tree Physiol. 13:145--155.
Fahey, T.J. 1979. The effect of night frost on the transpiration of Pinus
contorta ssp. latifolia. Oecol. Plant. 14:483--490.
Fincher, J. and R.G. Alscher. 1992. The effect of long-term ozone
exposure on injury in seedlings of red spruce (Picea rubens Sarg.).
New Phytol. 120:49--59.
Fincher, J., J.R. Cumming, R.G. Alscher, G. Rubin and L. Weinstein.
1989. Long-term ozone exposure affects winter hardiness of red
spruce (Picea rubens Sarg.) seedlings. New Phytol. 113:85--96.
Hadley, J.L., R.G. Amundson, J.A. Laurence and R.J. Kohut. 1993.
Physiological response to controlled freezing of attached red spruce
branches. Environ. Exp. Bot. 33:591--609.
Havranek, W.M. and W. Tranquillini. 1995. Physiological processes
during winter dormancy and their ecological significance. In Ecophysiology of Coniferous Forests. Eds. W.K. Smith and T.M.
Hinckley. Academic Press, New York, pp 95--124.
Jurik, T.W., G.M. Briggs and D.M. Gates. 1988. Springtime recovery
of photosynthetic activity of white pine in Michigan. Can. J. Bot.
66:138--141.
Kaufmann, M.R. 1982. Evaluation of season, temperature and water
stress effects on stomata using a leaf conductance model. Plant
Physiol. 69:1023--1026.
Kozlowski, T.T., P.J. Kramer and S.G. Pallardy. 1991. The physiological ecology of woody plants. Academic Press, New York, 657 p.
Levitt, J.D. 1980. Responses of plants to environmental stresses, 2nd
Edn. Volume I: Chilling, Freezing, and High Temperature Stresses.
Academic Press, New York, 497 p.

194

SCHWARZ, FAHEY AND DAWSON

L’Hirondelle, S.J., J.S. Jacobson and J.P. Lassoie. 1992. Acidic mist
and nitrogen fertilization effects on growth nitrate and reductase
activity and frost hardiness of red spruce seedlings. New Phytol.
121:611--622.
Lippu, J. and P. Puttonen. 1991. Soil temperature limitations on gas
exchange in 1-year-old Pinus sylvestris (L.) seedlings. Scand. J.
For. Res. 6:73--78.
Lundmark, T., J.-E. Hällgren and J. Hedén. 1988. Recovery from
winter depression of photosynthesis in pine and spruce. Trees
2:110--114.
Öquist, G. 1983. Effects of low temperature on photosynthesis. Plant
Cell Environ. 6:281--300.
Ottander, C. and G. Öquist. 1991. Recovery of photosynthesis in
winter-stressed Scots pine. Plant Cell Environ. 14:345--349.
Schaberg, P.G., R.C. Wilkinson, J.B. Shane, J.R. Donnelly and P.F.
Cali. 1995. Winter photosynthesis of red spruce from three Vermont
seed sources. Tree Physiol. 15:345--350.
Smith, W.K., D.R. Young, G.A. Carter, J.L. Hadley and G.M.
McNaughton. 1984. Autumnal stomatal closure in six conifer species of the Central Rocky Mountains. Oeologia 63:237--242.

Smith, W.K. 1985. Environmental limitations on leaf conductance in
Central Rocky Mountain conifers, USA. In Establishment and
Tending of Subalpine Forests: Research and Management. Eds.
H. Turner and W. Tranquillini. Proc. 3rd IUFRO Workshop. Eidg.
Anst. Forstel Versuch. 270:95--101.
Snedecor, G.W. and W.G. Cochran. 1980. Statistical methods, 7th Edn.
Iowa State University Press, Ames, Iowa, 507 p.
Strand, M. and T. Lundmark. 1995. Recovery of photosynthesis in
1-year-old needles of unfertilized and fertilized Norway spruce
(Picea abies (L.) Karst.) during spring. Tree Physiol. 15:151--158.
Teskey, R.O., D.W. Sheriff, D.Y. Hollinger and R.B. Thomas. 1995.
external and internal factors regulating photosynthesis. In Resource
Physiology of Conifers. Eds. W.K. Smith and T.M. Hinckley. Academic Press, New York, pp 105--140.
Wong, S.C., I.R. Cowan and G.D. Farquhar. 1979. Stomatal conductance correlates with photosynthetic capacity. Nature 282:424--426.
Wong, S.C., I.R. Cowan and G.D. Farquhar. 1985. Leaf conductance
in relation to rate of CO2 assimilation. Plant Physiol. 78:830--834.