Tree Physiology 17, 473--477
© 1997 Heron Publishing----Victoria, Canada
Carbon dioxide gas exchange of cembran pine (Pinus cembra) at the
alpine timberline during winter
GERHARD WIESER
Forstliche Bundesversuchsanstalt, Rennweg 1, A-6020 Innsbruck, Austria
Received March 7, 1996
Summary Winter CO2 gas exchange of the last three flushes
of cembran pine (Pinus cembra L.) was studied under ambient
conditions at the alpine timberline, an ecotone with strong
seasonal changes in climate. During the coldest months of the
year, December to March, gas exchange was almost completely
suppressed and even the highest irradiances and temperatures
did not cause a significant increase in net photosynthesis
compared to spring and fall. In general, daily CO2 balance was
negative between December and March except during extended warm periods in late winter. However, because twig
respiration was also reduced to a minimum during the December--March period, daily carbon losses were minimal. Total
measured carbon loss during the winter months was small,
equalling the photosynthetic production of one to two warm
days in spring or summer when average air temperature was
above 6 °C.
Keywords: carbon balance, photosynthesis, respiration.
Introduction
Evergreen conifers are the most common woody plants at the
alpine timberline, an ecotone with strong seasonal changes in
climate. Short growing seasons alternate with resting periods.
In a 10-year set of growth analysis experiments, Kronfuβ
(1994) showed that, at high altitudes, cembran pine (Pinus
cembra L.) has an average extension growth period of about
110 days during the warm summer months of May to August.
During the winter, low temperature is the main factor determining the duration and intensity of dormancy (Havranek and
Tranquillini 1995).
Seasonal variation in net photosynthesis and respiration at
the alpine timberline has been attributed to the prevailing
temperature. In the fall, frequent frosts cause a decline in net
photosynthesis of cembran pine that does not recover until
temperatures rise in spring (Cartellieri 1935, Pisek and
Winkler 1958, Tranquillini 1959, 1979).
Despite the many studies on gas exchange in conifers, there
have been few in situ measurements of gas exchange on mature
trees during winter dormancy (Havranek and Tranquillini
1995). Gas exchange at the alpine timberline has been investigated using cut twigs under laboratory conditions (Cartellieri
1935, Pisek and Winkler 1958), but there is little information
on seasonal variations in gas exchange of conifers at the alpine
timberline, especially during the winter months. Therefore, I
examined seasonal changes in gas exchange of a subalpine
cembran pine in situ under field conditions and estimated its
CO2 balance during the winter season.
Materials and methods
Study site and plant material
Measurements were made on a mature, 12-m high cembran
pine tree growing in a podsol on a south-west slope at 1950 m
a.s.l. near the Klimahaus Research Station on Mt. Patscherkofel (47° N, 11° E) near Innsbruck, Austria. Measurements
were made from December 9, 1993 to April 21, 1994 and from
November 2, 1994 to May 22, 1995, the beginning of bud
break. The field site is characterized by a cool subalpine
climate with low soil temperatures, a possibility of frost in all
months and a continuous snow cover from October until May.
Climate and gas exchange measurements
An aluminum platform provided access to the top of the tree.
An LI-190 PAR quantum sensor (Li-Cor, Inc., Lincoln, NE)
and a Skye SKH 2013 air temperature/humidity sensor (Skye
Instruments, Powys, U.K.) were installed on a horizontal aluminum rod about 1 m to the side of the top of the tree. Soil
temperatures were measured with copper constantan thermocouples at depths of 2, 15 and 50 cm.
The CO2 gas exchange of the last three flushes was measured continuously by means of a temperature-controlled chamber (Walz, Effeltrich, Germany) on sun-exposed branches
approximately 2 m from the top of the tree. Temperature in the
chamber was controlled and followed ambient air temperature.
Atmospheric humidity inside the chamber was monitored with
a capacitive humidity sensor (Vaisala, Helsinki, Finland). All
of the pneumatic tubing was heated and insulated. The shoot
in the chamber was changed every 7 to 8 weeks. Snow was not
removed artificially from the chamber after snow fall.
Actual needle temperature on the sun-exposed side was
measured with copper constantan thermocouples, one inside
the chamber and one outside. Thermocouple junctions, 0.1 mm
474
WIESER
in diameter, were formed into soldered loops of approximately
1.5 mm diameter, slipped over the needles and gently crimped
in place. Copper constantan thermocouples were also used to
measure stem temperatures 5 cm below the stem surface, 1.5 m
aboveground.
During winter, the chamber tracked ambient conditions
fairly well. The mean temperature difference between needles
inside and outside the chamber was close to zero (Figure 1).
Mean maximum overheating of needles in the chamber was
2.3 °K and mean maximum undercooling was −1.1 °K compared to needles outside the chamber; and the absolute maximum difference was +6.8 °K and −3.2 °K, respectively
(Figure 1). The observed differences in temperature between
needles inside the chamber and needles outside the chamber
were within the range found in pine needles within one branch
(author’s unpublished observations).
All data were recorded with a Campbell CR10 data logger
(Campbell Scientific Ltd., Shepshed, U.K.), programed to record the 10-minute means of measurements taken every minute. All CO2 gas exchange parameters were calculated
according to von Caemmerer and Farquhar (1981) and related
to needle dry weight. Specific leaf area was 61.3 cm2 gdw−1.
Analysis of data was based on half-hour means.
Results
Although the winter climate at the alpine timberline on Mt.
Patscherkofel is characterized by low temperatures, air temperatures did not remain continuously below 0 °C in any winter
month, in either 1993--94 or 1994--95 (Figure 2, and also see
Figure 7). The lowest half-hour mean temperature recorded
during the study was −19.2 °C on January 5, 1995 and the
highest half-hour mean temperature recorded was 14.8 °C on
May 6, 1995 (Figure 2). In both winters, snow cover persisted
from early December until the end of April. Under the snow,
soil temperatures in the top 2-cm layer were always above
−3.8 °C, and at depths below 15 cm soil temperatures never
dropped below 0.2 °C.
Figure 1. Observed daily mean and range in the difference between the
temperature of cembran pine needles inside (TNch) and outside
(TNamb ) the gas exchange chamber from December 9, 1993 to April
21, 1994.
Figure 2. Time course of meteorological data, photon flux density
(PFD), air temperature (Tair ), snow depth (Snow), stem temperature
5 cm below the stem surface, 1.5 m aboveground (Tstem ) and CO2 gas
exchange (Pn) of current-year to two-year-old needles of cembran pine
between November 2, 1994 and May 22, 1995. All data, except snow
depth, are shown as half-hour means.
During the winter, net photosynthesis and nighttime respiration were almost completely suppressed (Figure 2). The decline in CO2 gas exchange started in November as a
consequence of shorter days, lower irradiance and near-freezing temperatures. Recovery of photosynthesis began in spring
in response to the diminishing occurrence of frost and higher
air and stem temperatures (Figure 2).
Of all environmental variables examined, daily maximum
net photosynthesis was best correlated with minimum stem
temperature of the previous night, in both the fall and spring
(Figure 3). Seasonal changes in CO2 gas exchange were correlated with ambient light and temperature conditions at the
timberline site. In general, photosynthetic rates were negligible during the winter months (December to March) even at
the highest irradiances (Figure 4) and temperatures (Figure 5)
when compared with photosynthetic rates during the spring
and fall. Furthermore, at a given temperature, respiration during the night was substantially lower in winter than in spring
and autumn, indicating a decline in total respiration rate to the
maintenance rate (Figure 6).
Metabolic activity increased during long-lasting warm periods
in late winter. For example, in March 1994, which was unusually mild, respiration increased and net photosynthetic rates
reached up to 30% of summer values (Figure 7) during a period
TREE PHYSIOLOGY VOLUME 17, 1997
WINTER CO2 GAS EXCHANGE OF SUBALPINE CEMBRAN PINE
Figure 3. Maximum daily net photosynthesis (Pn,max ) in relation to the
previous night minimum stem temperature 5 cm below the stem
surface, 1.5 m aboveground in fall (d) and in spring (s).
Figure 4. Means of net photosynthesis (Pn) at different ranges of
irradiance (PFD) for current-year to two-year-old needles of cembran
pine. Data were selected according to the following climatic conditions: vapor pressure deficit ≤ 8 Pa kPa −1; air temperature ≥ 5 °C in
November, April, May, but ≥ 2 °C during December to March. Each
data point is the mean of 10 to 50 half-hour mean values based on
diurnal courses during the investigation period 1994--1995. Vertical
bars represent the standard error of the mean.
when maximum daily air temperatures were high and minimum night temperatures were above zero.
Monthly photosynthetic production was negative from December through February in both years. Although the period
of negative photosynthetic production normally extended to
April (e.g., for the winter 1994--1995 (Figure 2)), photosynthetic production was positive for the unusually mild month of
March 1994 (Table 1). In general, total carbon loss of the
foliage during the winter was less than 32 mg gdw−1.
Discussion
Variation in net photosynthesis of cembran pine tracked seasonal changes in climate at the alpine timberline. In late
autumn and early winter, CO2 exchange permanently de-
475
Figure 5. Means of net photosynthesis (Pn) at different ranges of air
temperatures (T) for current-year to two-year-old needles of cembran
pine. Data were selected according to the following climatic conditions: vapor pressure deficit ≤ 8 Pa kPa −1, photon flux density ≥ 500
µmol m −2 s −1. Each data point is the mean of 10 to 50 half-hour mean
values based on diurnal courses during the investigation period 1994-1995. Vertical bars represent the standard error of the mean.
Figure 6. Means rates of nighttime respiration (Rnight ) over different
ranges of air temperatures (T) for current-year to two-year-old needles
of cembran pine. Each data point is the mean of 20 to 80 half-hour
mean values based on diurnal courses during the investigation period
1994--1995. Vertical bars represent the standard error of the mean.
creased. This decline coincided with shorter days and temperatures below 0 °C. These same factors also cause the development of frost resistance and cellular alterations during pre-dormancy (Holzer 1958, Senser and Beck 1979, Havranek and
Tranquillini 1995). Near-freezing temperatures during frost
hardening of pines alter chlorophyll organization (Öquist and
Strand 1986) as well as pigment composition (Ottander et al.
1995) and chlorophyll fluorescence (Nagele 1989, Ottander
et al. 1995, Westin et al. 1995).
Several studies have shown that short periods of apparently
favorable conditions following a severe frost do not result in
CO2 uptake in trees at the alpine timberline (Tranquillini 1957,
Pisek and Winkler 1958, Tranquillini 1979), leading Tranquillini (1979) to conclude that winter dormancy in trees at the
alpine timberline is particularly rigid and long lasting. Al-
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476
WIESER
Figure 7. Time course of meteorological data, photon flux density
(PFD), air temperature (Tair ), snow depth (Snow), stem temperature
5 cm below the stem surface, 1.5 m aboveground (Tstem ) and CO2 gas
exchange (Pn) of current-year to two-year-old needles of cembran pine
between December 9, 1993 and April 21, 1994. All data, except snow
depth, are shown as half-hour means.
though daily CO2 balance was negative between December
and March, I observed an increase in gas exchange, with
photosynthetic rates reaching up to 30% of summer values
Table 1. Monthly carbon balance (mg gdw−1) of the last three flushes
of cembran pine during the winter of 1993--1994 and 1994--1995.
Month
1993--1994
1994--1995
November
December
January
February
March
April
May
Total carbon loss
-−11.90
−10.42
−8.74
93.00
41.76
-−31.06
43.80
−5.88
−6.62
−1.75
−8.18
72.72
351.17
−22.43
during an extended warm period in March 1994 when minimum air temperatures were above zero, and soil, stem and
branches were not frozen. Similarly, in February 1993 at the
same study site, I measured photosynthetic rates in Norway
spruce needles that increased as much as 15% of summer
values following several days of thaw with nighttime temperatures just below freezing (author’s unpublished observations).
In central alpine valleys, where the duration of the winter
suppression in gas exchange is shorter than at high altitudes,
winter photosynthetic rates of up to 30 and 50% of summer
values have been recorded in Norway spruce (Zöschg 1988)
and Scots pine (Meusburger 1988), respectively. Positive net
photosynthesis during favorable days in midwinter has also
been shown for Scots pine in central Sweden at 150 m a.s.l
(Troeng and Linder 1982) as well as in young red spruce grown
in Vermont at 104 m a.s.l. (Schaberg et al. 1995). However,
when branches were transferred from the field to optimum
conditions in the laboratory during the winter, photosynthetic
capacity did not recover to summer values (Pisek and Winkler
1958, Schwarz 1971), suggesting that photosynthetic capacity
during winter is suppressed not only by low temperatures but
also by an endogenous factor that is not lost when the branches
are excised. This suggestion is consistent with chlorophyll
fluorescence measurements (Nagele 1989).
The transition to winter dormancy was accompanied by a
change in the temperature response of respiration. At a given
ambient temperature, twig respiration was substantially lower
during winter than in spring and autumn, and thus reduced
carbon loss during the long subalpine winter. Similarly, stem
respiration of cembran pine was also found to be low during
winter compared with summer values (Havranek 1981). However, in May, when buds began to expand and were about
1.5 cm in length, there was an increase in twig respiration
probably because of a strong demand for carbohydrates in the
developing buds (cf. Sprugel et al. 1995).
At the alpine timberline, winter dormancy begins to break in
spring. Full recovery of photosynthesis occurred after the air
and stem temperatures had increased and the aboveground
tissue had thawed. Furthermore, in spring, a reorganization of
cell structures (Holzer 1958, Senser and Beck 1979) and pigment composition (Ottander et al. 1995) has been observed.
At the alpine timberline, monthly carbon balance of cembran pine twigs was negative for three to four months. The total
measured carbon loss of the twigs during the winter months
was only 22--31 mg CO2 per gram needle dry weight, which is
equal to the photosynthetic production of one to two warm
days in summer or spring, when average air temperature is
above 6 °C. This estimate of total carbon loss was more than
10 times lower than the value determined for cembran pine by
Tranquillini (1959). However, Tranquillini’s estimate was
based on the temperature respiration relationship measured
during the summer, which would be equivalent to the temperature respiration relationship estimated for May in this study,
which was significantly displaced on the y-axis above values
measured during the winter. The measured CO2 balance of
cembran pine was also less than the value of 140 mg CO2 per
gram of photosynthetically active tissue calculated for bristle-
TREE PHYSIOLOGY VOLUME 17, 1997
WINTER CO2 GAS EXCHANGE OF SUBALPINE CEMBRAN PINE
cone pine on the basis of gas exchange rates measured under
controlled temperatures in the field and temperature data
(Schulze et al. 1967).
During the leafless period from October to April, whole-tree
respiration of a European larch at the timberline was calculated
to be only 2.3% of its annual photosynthetic carbon gain
(Havranek and Tranquillini 1995). Similarly, continuous gas
exchange measurements during winter in Switzerland demonstrated that the monthly CO2 balance of mature Norway spruce
shoots was slightly negative between December and March in
trees growing at 1600 m a.s.l., whereas it was positive in trees
growing in the valley in all months (Häsler 1991). Even in the
boreal zone, CO2 balance of Scots pine was negative only from
December to February (Troeng and Linder 1982).
In conclusion, in response to the long and severe winters at
the alpine timberline, CO2 gas exchange and twig respiration
of forest trees were severely reduced, presumably reflecting an
acclimation to the low temperatures that are characteristic of
the region. Although winter dormancy is reported to be particularly rigid and long lasting (Tranquillini 1979), I observed
that net photosynthesis can become significant during extended warm periods in late winter. Total carbon loss by the
foliage throughout the winter was minimal, equalling the photosynthetic production of one to two warm days in spring or
summer. I conclude that these adaptations of gas exchange
contribute to the survival of conifers at the alpine timberline.
Acknowledgment
I thank Th. Gigele for excellent technical assistance during both
winters of investigation.
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