Journal of Experimental Botany, Vol. 58, No. 15/16, pp.
4293–4306, 2007
doi:10.1093/jxb/erm313
This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER
Temperature dependency of bark photosynthesis in beech
(Fagus sylvatica L.) and birch (Betula pendula Roth.) trees
Christiane Wittmann and Hardy Pfanz*
Institute of Applied Botany, University of Duisburg-Essen, D-45117 Essen, Germany
Received 13 June 2007; Revised 25 October 2007; Accepted 29 October 2007
Abstract
Temperature dependencies of stem dark respiration
(Rd) and light-driven bark photosynthesis (Amax) of two
temperate tree species (Fagus sylvatica and Betula
pendula) were investigated to estimate their probable
influence on stem carbon balance. Stem Rd was found
to increase exponentially with increasing tempera-
tures, whereas Amax levelled off or decreased at the
highest temperatures chosen (35–40
C). Accordingly,
a linear relationship between respiratory and assimila-
tory metabolism was only found at moderate tempera-
tures (10–30
C) and the relationship between stem
Rd and Amax clearly departed from linearity at chilling
(5
C) and at high temperatures (35–40
C). As a result,
the proportional internal C-refixation rate also de-
creased non-linearly with increasing temperature.
Temperature response of photosystem II (PSII) photo-
chemistry was also assessed. Bark photochemical
yield (DF/Fm#) followed the same temperature pattern
as bark CO2 assimilation. Maximum quantum yield of
PSII (Fv/Fm) decreased drastically at freezing tempera-
tures (–5
C), while from 30 to 40
C only a marginal
decrease in Fv/Fm was found. In in situ measurements
during winter months, bark photosynthesis was found
to be strongly reduced. Low temperature stress in-
duced an active down-regulation of PSII efficiency as
well as damage to PSII due to photoinhibition. All in all,
the benefit of bark photosynthesis was negatively
affected by low (<5
C) as well as high temperatures
(>30
C). As the carbon balance of tree stems is
defined by the difference between photosynthethic
carbon gain and respiratory carbon loss, this might
have important implications for accurate modelling of
stem carbon balance.
* To whom correspondence should be addressed. E-mail: hardy.pfanz@uni-essen.de
ª 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which
permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Key words: Beech, birch, CO2 exchange, fluorescence, stem
photosynthesis, stem respiration, temperature response.
Introduction
Temperature may affect productivity of forest trees by
altering the balance between photosynthesis and respir-
ation, because these processes respond differently to
temperature changes (Maier et al., 1998). As temperature
is the driving force behind most physiological processes
that occur in a plant (Kramer and Kozlowski, 1979),
changes in temperature may also have markedly different
effects on the physiological processes that contribute to
stem carbon balance, namely stem respiration and bark
photosynthesis. Stem respiration makes an important
contribution to total ecosystem respiration. In a beech
forest in France, it was estimated that the annual CO2
efflux from aboveground woody tissues consumed 26% of
the annual gross primary production (Damesin et al.,
2002). In a tropical savanna ecosystem Cernusak et al.
(2006) estimated the annual aboveground woody tissue
CO2 efflux to be 275 g C m
2 ground year
1, or ;13%
of the annual gross primary production. Therefore, stem
respiration is regarded as an important factor in the
regulation of forest productivity and carbon storage (Ryan
et al., 1997). A recent study by Cavalleri et al. (2006)
further underlined the large contribution of small diameter
woody tissue CO2 efflux to total plant respiration. For
a tropical forest they found that small diameter stems
(<10 cm), only 15% of total woody biomass, accounted
for 70% of total woody tissue CO2 efflux from the forest.
In young stems, a non-negligible part of the respired CO2
is directly re-assimilated in the assimilatory bark tissues
during illumination, a process that has been termed ‘CO2
refixation’ or, alternatively, ‘bark photosynthesis’ (Foote
and Schaedle, 1978; Sprugel and Benecke, 1991). Bark
4294 Wittmann and Pfanz
photosynthesis allows young stems to compensate for 60–
90% of their respiratory carbon loss (Wittmann et al.,
2001; Pfanz et al., 2002) and equals growth respiration on
an annual basis (Damesin, 2003). For young beech trees,
Gansert (1994) found annual bark photosynthetic rates of
;24%. Kharouk et al. (1995) estimated the average bark
input to whole tree C balance of Populus tremula as 10–
15% during the mid-summer vegetative period. Thus,
besides stem respiration, bark photosynthesis is an
important and often overlooked component of stem and
even tree carbon balance.
All published carbon gain models use a temperature
response function (Harley and Tenhunen, 1991; Leuning,
1997; Dreyer et al., 2001). Nevertheless, despite numer-
ous studies that have shown the temperature response of
stem respiration (Maier et al., 1998; Stockfors, 2000; Zha
et al., 2004), only few studies (Cernusak and Marshall,
2000) have produced data sets for temperature depend-
ency of bark photosynthesis, although both processes are
clearly correlated with each other (Cernusak and Marshall,
2000; Aschan et al., 2001; Wittmann et al., 2005).
Furthermore, the temperature response of bark photosyn-
thesis among different tree species has not been com-
pared. This would enhance our ability to predict
individual tree function and competition between different
tree species under changing environmental conditions.
Therefore, the objectives of this study were: (i) to
examine the short-term temperature dependency of CO2
gas exchange [separated into dark respiratory (Rd) and
photosynthetic fluxes (Amax)] as well as photosystem II
(PSII) quantum yield (DF/Fm#) in stems of two temperate
tree species (Fagus sylvatica and Betula pendula) under
controlled environmental conditions; (ii) to examine
whether DF/Fm# in stems and leaves of both species
responds similarly to changes in temperature; and (iii) to
investigate the temperature dependency of Rd, Amax, and
DF/Fm# in stems under field conditions in order to
estimate possible acclimation effects.
Studies indicate that different species originating from
different habitats may have developed genotypic adjust-
ments to their evolutionary temperature environment
(Berry and Björkman, 1981; Read, 1990; Niinemets
et al., 1999). To assess the extent to which temperature
responses of stem Rd and Amax depend on species-specific
attributes reflecting evolutionary adaptation to species
temperature environment, experiments were conducted on
two deciduous trees (F. sylvatica and B. pendula), which
clearly differ in temperature and light requirements/
preferences and successional status. Both F. sylvatica
and B. pendula are widely distributed in Europe, but
F. sylvatica is less frost-tolerant than B. pendula (Otto,
1994); the native range of B. pendula extends further
north than that of F. sylvatica. With regard to the
successional status, F. sylvatica is a shade-tolerant climax
species growing in dense stands. Betula pendula is
a pioneer tree abundant in northern Europe. Pioneer trees
typically require gaps or clearings to establish a new
generation of seedlings that are exposed to high irradi-
ances, which support fast growth but also give rise to the
danger of photoinhibition (Robakowski, 2005). In con-
trast, late-successional species germinate and undergo
early development in the shade of forest canopies, often
under extremely low irradiance (Küppers et al., 1996).
Thus, the question was also asked of whether these
species-specific attributes alter Amax, Rd, and DF/Fm#
versus T response curves.
Materials and methods
Plant material
Laboratory and field experiments were performed during early
summer (June) on 6-year-old beech (F. sylvatica L.) and birch trees
(B. pendula Roth.), that were grown outside in plastic containers
under sufficient nutrition (Einheitserde Typ T, Balster, Germany)
and water supply, realized by periodic fertilization with Osmocote
(Bayer, Germany) and daily irrigation. The plants were exposed
to ambient temperatures. Mean monthly temperature recorded in
June at the weather station Essen Schuir (Essen, Germany),
located ;1500 m from the growing side of the plants, was 19.9
C.
Temperature treatment
For controlled environment observations, potted trees were trans-
ferred to the laboratory and were placed intact into a large climate
chamber (4.46 m34.83 m32.95 m; PVP GmbH, Willich, Ger-
many), which allows full control of temperature, relative humidity,
and light intensity. Plants were left to acclimate for 1 d under the
following conditions: air temperature, 20
C; relative humidity,
50%; and PAR, 600/0 lmol m
2 s
1 (day/night). Day and night
lengths were 15 h and 9 h, respectively. Thereafter, air temperature
was set to the desired value (–5, 5, 10, 15, 20, 25, 30, 35, 40, and
43
C) while relative humidity and PAR were kept constant. All
measurements were made as follows: chamber temperatures were
set to a constant value and the trees were left to temperature-adapt
for at least 60 min. Then the gas exchange and fluorescence
parameters were measured on the middle of the length of two intact
stems (1–2 years old; stem diameters ranged from 1.1 cm to
2.0 cm) of each tree (n¼5). In all cases, measurements
were performed inside the climate chamber on stems/leaves from
the outer sun-crown at a height of ;1.5 m and the whole plant
was exposed to the measurement temperature during this period.
This procedure avoided bias due to leaf/stem portion versus whole-
plant temperature control during measurement (Atkin et al., 2000;
Griffin et al., 2002).
As acclimation processes may affect the temperature responses of
photosynthesis (and respiration), for each temperature step a new set
of trees (n¼5) was collected from the field. Although acclimation
can be rapid, for example acclimation occurred within 2 d of
a temperature change in some species (Billings et al., 1971; Atkin
et al., 2000), time to full acclimation has been reported to be of the
order of 10 d or longer (Bolstad et al., 2003). These periods are
substantially longer than those used in the present experiments.
CO2 gas exchange measurements
Laboratory measurements: For gas exchange measurements 7 cm
long portions of 1- to 2-year-old stems were enclosed in a

transparent, stem cuvette allowing simultaneous measurements of
CO2 exchange by infrared gas analysis. The gas exchange system
operates with full control of CO2 concentrations, incident light
intensity, air temperature, and relative humidity inside the cuvette.
Stem temperature was measured with a thermocouple attached to
the outer stem surface. Light was supplied by an Osram Power Star
HQI-R lamp only to the upper part of the stem; comparable with
natural conditions. The stem segment was exposed to a flow of
400 ml min
1 of air. CO2 gas exchange between the stem and the
air was measured with a differential infrared gas analyser (Li 6400;
Li-Cor, Lincoln, NE, USA) under constant microclimatic conditions
(relative humidity 50%; constant temperature) and ambient CO2
(360 ppm). Both the climate chamber and the temperature-con-
trolled cuvette of the gas exchange system were set to equal values
during measurements.
Stem net CO2 flux may be considered as the sum of three terms:
stem or woody tissue respiration (+flux), bark photosynthesis
(–flux), and CO2 dissolved in the xylem sap (+flux, if diffusing
out, –flux, if transported away) (Cernusak and Marshall, 2000;
Pfanz et al., 2002; McGuire and Teskey, 2004; Bowman et al.,
2005; Cavalleri et al., 2006). Yet, when stem CO2 efflux before and
after cutting of young beech and birch stems was measured (for
a total of 4 h) under laboratory conditions, no significant differences
were found (data not shown). If CO2 dissolved in the xylem sap
mainly contributed to stem CO2 efflux, a change in efflux rates
should have occurred. Furthermore, longitudinal fluxes of respira-
tory CO2 in the transpiration stream were minimized by keeping
relative humidity constant, while changing temperature. Thus, the
assumption is made that observed CO2 efflux rates in the dark are
equivalent to stem respiratory CO2 production rates. In young
stems, live sapwood respiration rates are small in comparison with
respiration of cambial, cortical, and phloem cells (Linder and
Troeng, 1980; Matyssek and Schulze, 1988). The high surface to
volume ratio further minimizes the contribution of sapwood xylem
parenchyma cell respiration, thus the rate of dark CO2 efflux is
expected to reflect primarily cambial/cortical (phloem included)
respiration (Levy and Jarvis, 1998; Cavalleri et al., 2006; Wittmann
et al., 2006). Secondly, the assumption is made that the contribution
of CO2 dissolved in the xylem sap is minimized under the
measurement conditions applied (constant relative humidity), so
that maximum bark photosynthesis (Amax) is equivalent to:
Amax ¼ jRd
Rl j ð1Þ
where Rd is stem CO2 release in the dark and Rl is stem CO2 release
in the light. Rd was measured after a 60 min shading period.
Subsequently, Rl was determined after a 45 min period of light
exposure to saturating 600 lmol photons m
2 s
1 (see Wittmann
et al., 2001, 2005). Both rates (Rd, Rl) were expressed on a total
stem surface area, and the Amax was calculated as the absolute
value of the difference between Rd and Rl. It should be noted
that the above-named assumptions could be a source of bias, in
older and larger trees, where sapwood makes up >80% of the total
stem volume, as well as under dry and sunny (field) conditions,
when high rates of transpiration (and thus high sap velocities)
occur (Martin et al., 1994; McGuire and Teskey, 2002). At
high transpiration rates, a portion of the locally respired CO2
may be carried upward by the transpiration stream instead of
released through the bark (Negisi, 1979; Martin et al., 1994;
Maier and Clinton, 2006). The study of Wittmann et al. (2006)
supported the suggestion that rates of photorespiration are sup-
pressed by high CO2 levels in young stems of trees and that
mitochondrial stem respiration is similar in the light and in the
dark. Thus, photorespiration and inhibition of mitochondrial
respiration, as another reason for the divergence between Rd and Rl,
were neglected.
Temperature dependency of bark photosynthesis 4295
Relative CO2 refixation as a percentage of the dark respiration
rate was estimated as follows:
Relative refixation ð% of dark respirationÞ ¼ ½jRd
Rl j=Rd 3100 ð2Þ
Field measurements: Daily courses of CO2 gas exchange were
monitored on 6-year-old potted birch trees (see Plant material),
which were exposed for the whole year to ambient temperatures.
Seasonal patterns of stem Rd and Amax were determined from
diurnal (daytime) assays made during the summer vegetative period
(August) but also during winter (January). CO2 gas exchange
between the stem and the air was measured with a differential
infrared gas analyser (Li 6400; Li-Cor). Stem temperature was
measured with a thermocouple attached to the outer stem surface.
PAR was monitored in the chamber near the stem plane using a
miniature GaAsP sensor. For measurements of bark photosynthesis,
a transparent stem cuvette was used. For respiratory measurements,
cuvettes were surrounded with aluminium foil. Bark photosynthesis
at a given time was calculated according to Equation 1 as the
absolute value of the difference between CO2 efflux in the dark (Rd)
and under illumination with ambient light (Ramb).
Fluorescence measurements
Temperature response measurements: Fluorescence measurements
were made under ambient CO2 and constant microclimatic
conditions (relative humidity: 50%; 600 lmol photons m
2 s
1) by
means of a pulse amplitude-modulated fluorometer (PAM-2000;
Walz, Effeltrich, Germany), equipped with a 2030-B leaf clip
holder, featuring an integrated micro-quantum sensor and a thermo-
couple. The 0.8 s saturation pulse intensity was set to ;10 000
lmol m
2 s
1, an intensity that was found to be always saturating.
To determine accurately the fluorescence signal of a cylindrical
stem, a piece of non-fluorescing black paper with a rectangular
3 mm310 mm window was attached on the clip. During the
measurements this window was orientated along the stem axis; thus
only photon exchange between the plane, central part of the stem
and the instrument is considered. The outer bark temperature of the
investigated stems was measured by the thermocouple of the clip
holder directly attached to the stem surface; all temperatures
reported are thus stem surface temperatures (60.5
C).
All measurements were made as follows: trees were left to dark-
adapt for at least 60 min. After determination of maximum quantum
yield in dark-adapted material (Fv/Fm), the effective quantum yield
(DF/Fm#) of PSII was measured on two stems (1–2 years old) and
adjacent, fully developed leaves of each tree (n¼5) under an actinic
light intensity of 600 lmol photons m
2 s
1. As determined in
preliminary experiments, 600 lmol photons m
2 s
1 are saturating
for leaf and bark photosynthesis. These results corresponded to
observations in a number of tree species (Fagus crenata, Quercus
acutissima, Han and Suzaki, 1981; Populus tremuloides, Foote and
Schaedle, 1976; Acer rubrum, Coe and McLaughlin, 1980;
F. sylvatica, Populus tremula, Wittmann et al., 2001; B. pendula,
Wittmann et al., 2006); in all these species bark photosynthesis
saturated between 200 and 500 lmol PAR m
2 s
1. Chlorophyll
fluorescence parameters, maximum quantum yield (Fv/Fm), and
effective quantum yield (DF/Fm#) of PSII were calculated according
to Schreiber et al. (1994) and Genty et al. (1989).
Light response measurements: Additionally, instant light response
curves of the effective quantum yield (DF/Fm#) of PSII under
freezing (–5
C), chilling (5
C), and warm temperatures (20
C)
were obtained using the PAR curve program of the PAM. After
determination of maximum quantum yield in dark-adapted material
(60 min), a 5 min pre-irradiation period at moderate irradiance
4296 Wittmann and Pfanz
(120 lmol photons m
2 s
1) provided a stationary fluorescence is an entropy term, T (K) is leaf temperature, and R (0.008314 kJ
level of the samples. Then the ‘actinic light’ intensity was decreased mol
1 K
1) the gas constant. The whole temperature data set for
to 60 lmol photons m
2 s
1 for 5 min, before a saturation pulse Amax was fitted to Equation 3. To simplify the fitting procedure and
was applied to obtain the effective quantum yield (DF/Fm#) of PSII. make comparison of temperature responses easier, the entropy term
Within the following 20 min, irradiance was increased stepwise DS was held constant at 0.385 kJ K
1 mol
1. A similar approach is
with irradiation periods of 2 min and subsequent saturation pulses described in Harley et al. (1992). Equation 3 provided a function
until 1250 lmol photons m
2 s
1 was reached. closely fitting the data, and r2 of the non-linear regressions was
always >0.99 (cf. Fig. 1 for the fits).
The temperature dependence of dark respiration rates (Rd) is
Data analysis described by the Arrhenius equation:
Non-linear least-square regression was used to fit temperature
dependencies of bark photosynthesis (Amax) by (see also Harley Rd ¼ ec
DHa =RT ð4Þ
et al., 1992; Niinemets et al., 1999): where c ist the scaling constant, DHa (kJ mol ) is the activation
1

ec
DHa =RT energy, and R (0.008314 kJ mol
1 K
1) the gas constant. The
Amax ¼ ð3Þ whole temperature data set for Rd was fitted to Equation 4. The
1 þ eðDST
DHd Þ=RT Arrhenius equation gave excellent fits to the data with a minimum
where c is the scaling constant, DHa (kJ mol
1) is an activation r2 of 0.99 (cf. Fig. 1 for the fitted curves). Yet, the parameters c and
energy, DHd (kJ mol
1) is a deactivation energy, DS (kJ K
1mol
1) DHa of Equation 4 are not fitted independently, thus making it

4,0 4,0 8 8

bark photosynthesis (Amax) [µmol CO2 m-2 s-1]

bark photosynthesis (Amax) [µmol CO2 m-2 s-1]
dark respiration rate (Rd) [µmol CO2 m-2 s-1]

a b

dark respiration rate (Rd) [µmol CO2-2 s-1]

3,5 3,5 7 7

3,0 3,0 6 6

2,5 2,5 5 5
r2= 0.9914, P<0.0001 r2= 0.996, P<0.0001
2,0 2,0 4 4

1,5 1,5 3 3

1,0 1,0 2 2

0,5 0,5 1 1
r2= 0.9947, P<0.0001 r2= 0.9978, P<0.0001
0,0 0,0 0 0
-5 0 5 10 15 20 25 30 35 40 -5 0 5 10 15 20 25 30 35 40

100
c 100 d

80 80

60 60

40 40

20 20

r2= 0.9964, P<0.0001 r2= 0.9802, P=0.0004

0 0
-5 0 5 10 15 20 25 30 35 40 -5 0 5 10 15 20 25 30 35 40
stem surface-temperature [°C]

Fig. 1. Temperature response curves of dark respiration (Rd; filled circles), Amax (open circles; measured at saturating 600 lmol photons m
2 s
1),
and relative corticular refixation (% of Rd) of 1- to 2-year-old stems of Fagus sylvatica (a, c) and Betula pendula (b, d). Graphs (c) and (d) are
deduced from values of (a) and (b). Means 6SD; n¼10. The curves describe the Arrhenius fits to the whole data set (least-square fits to Equation 3
for Amax and Equation 4 for Rd), using parameter values shown in Table 1. In all panels, the correlation coefficients for non-linear regressions are
given.

difficult to compare the changes in the shape of the temperature
response curves. To eliminate the autocorrelation, the stem
respiration data were standardized with respect to the respiration
rate measured at 20
C as in Harley and Baldocchi (1995). Given
that the standardized rate, k, is equal to:
Rd ðTÞ ec
DHa =RT
¼ c
DH =R293 ¼ e R ð293
TÞ ;
DHa 1 1
k¼
Rd ð293Þ e a (activation energy) were 4560.82 kJ mol
1 for beech and
c is eliminated, and for each standardized rate ki, an estimate of
DHa independent of c was found as:
 
1 1
DHa ¼ Rlnðki Þ
;
293 T
Further, the whole standardized stem respiration data was fitted to
Equation 5 and the coefficient DHa (6SE) for the regression model
was computed.
As in carbon balance models, respiration rates are often
expressed in terms of Q10, temperature response of dark respiration
was additionally described by respiration–temperature response
functions of the form (see also Bolstad et al., 2003):
RdðTÞ ¼ RdðT0 Þ Q10
ðT
T0 Þ=10
where Rd(T) is the observed dark respiration rate at temperature T,
T0 is a reference temperature, and RdðT0 Þ and Q10 are estimated
coefficients. The Q10 may be interpreted as the ratio of respiration
measured over a 10
C span (see also Tjoelker et al., 1999;
Turnbull et al., 2001; Bolstad et al., 2003). The whole temperature
data set for Rd was fitted to Equation 7 and the coefficient Q10
(6SE) for the regression model was computed. Equation 7 provided
a function fitting the whole stem respiration data just as well as
Equation 4, and r2 of the non-linear regressions was always >0.99
(P <0.0001).
For statistical data analysis, the SigmaPlot 2001 software (SPSS
Inc., Chicago, IL, USA) was used. The significance of differences
between sets of data was checked by Student’s t-tests. To visualize
and plot the curve that best describes the shape and behaviour of the
data (‘curve fitting’) the ‘regression wizard’ of the program was
used. The coefficient of determination, a measure of how well the
regression model describes the data, is given in the figures.
Temperature dependency of bark photosynthesis 4297
Results
Temperature response of Rd and Amax
The temperature response of stem dark respiration of
F. sylvatica and B. pendula revealed a typical exponential
relationship (Fig. 1). Regression-based estimates of DHa
ð5Þ
4360.36 kJ mol
1 for birch trees. Regression-based
estimates of Q10 gave a value of 1.7560.01 for beech
and 1.8760.08 for birch stems.
In contrast, an exponential increase in light-saturated bark
ð6Þ
photosynthesis (Amax) with temperature was only found
from 5
C to 25
C, while at higher temperatures saturation
or even inhibition (40
C) of photosynthesis was obtained
(Fig. 1). Thus, the percentage of dark-respired CO2 that
was refixed within the bark chlorenchyma (¼relative
refixation) declined with increasing temperature (Fig. 1c, d).
At a common reference temperature of 20
C, stem Rd
and Amax were closely related to each other (Fig. 2). The
ð7Þ slope of the relationship between the two parameters was
0.68 for birch and 0.83 for beech stems. This suggests that
the photosynthetic bark chlorenchyma reduced dark
respiration rates under saturating illumination up to 68%
or 83%, respectively. The relationship between stem Rd
and Amax was clearly temperature dependent (Fig. 3).
At moderate values between 10
C and 25
C a linear
relationship [birch, r2¼0.98; beech, r2¼0.91; f(x)¼0.5x]
between both physiological processes was observed. If
additionally freezing (–5
C), chilling (5
C), and high
temperatures (35–40
C) were considered (Fig. 3), this
relationship clearly departs from a simple linear function
[ f(x)¼ax]. Consequently, the data set was expressed most
appropriately by a non-linear equation closely fitting the
data (r2 of the non-linear regressions was always >0.99;
cf. Fig. 3 for the fits). Furthermore, species differences in

1,0 2,2
a Fagus sylvatica b Betula pendula
bark photosynthesis (Amax)

bark photosynthesis (Amax)

2,0
[µmol CO2 m-2 s-1]

0,9
[µmol CO2 m-2 s-1]

1,8

1,6
0,8 1,4

1,2
0,7 1,0
Amax = 0.83 * Rd Amax = 0.68 * Rd
0,8
r2= 0.88 (P < 0.0001) r2= 0.89 (P < 0.0001)
0,6 0,6
0,8 0,9 1,0 1,1 1,0 1,5 2,0 2,5 3,0
dark respiration rate (Rd) at 20°C
[µmol CO2 m-2 s-1]

Fig. 2. The relationship between corticular photosynthesis and dark respiration (absolute value) in young stems (1- to 2-year-old) of Fagus sylvatica
(a) and Betula pendula (b) at 20
C. Measurements were performed under constant climatic conditions (20
C, 50–55% relative humidity, 600 lmol
photons m
2 s
1) and a controlled CO2 supply (360 ppm). In all panels, the function equations and correlation coefficients for non-linear regressions
are given. Data are derived from 10 individual measurements shown as mean values in Fig. 1.
4298 Wittmann and Pfanz
2,5 Table 1. Parameters used to describe temperature dependence
a Betula pendula of bark photosynthesis (Amax) of 1- to 2-year-old stems of Fagus
sylvatica and Betula pendula
2,0 30°C
All values have been determined from measured data via least-square
35°C
fits to equation 3 for Amax (cf. Fig. 1 for the fitted curves). c is the
40°C
scaling constant, DHa is an activation energy, DHd is a deactivation
energy, and DS is an entropy term. The coefficients for the regression
1,5 model 6SE are given. To simplify the fitting procedure, the entropy
20°C term DS was held constant at 0.385 kJ K
1mol
1.

Species Temperature Units

1,0
parameters

Fagus sylvatica c (Amax) 14.8363.00 –

0,5
DHa (Amax) 14.4363.00 kJ mol
1
10°C
DHd (Amax) 39.3367.91 kJ mol
1
bark photosynthesis [µmol CO2 m-2 s-1]

DS (Amax) 0.385 kJ K
1 mol
1

5°C Betula pendula c (Amax) 31.8760.87 –
0,0 -5°C r2= 0.998, P<0.0001
DHa (Amax) 76.5468.22 kJ mol
1
DHd (Amax) 115.965.48 kJ mol
1
0 2 4 6 8
DS (Amax) 0.385 kJ K
1 mol
1

1,50
b Fagus sylvatica
of bark photosynthesis during the summer vegetative
1,25
period (Fig. 4a, c) and the winter period (Fig. 4b, d)
showed that Amax clearly followed the daily temperature
35°C
40°C
and PAR course during the summer months (Fig. 4c, e),
30°C
1,00 reaching photosynthetic rates of up to 4 lmol CO2 m
2
20°C
s
1, while the values were almost zero during the winter
months (Fig. 4d, f). Even when illumination increased
0,75
stem surface temperatures from below zero to values of
15°C ;10
C for up to 6 h (12:00–18:00; Fig. 4b, d), bark
0,50 photosynthesis did not return to summer values.
10°C

Temperature response of PSII photochemistry

0,25 5°C
-5°C
0,00
0 1
dark respiration rate [µmol CO2 m-2 s-1]
Fig. 3. The relationship between corticular photosynthesis and dark
respiration (absolute value) in 1- to 2-year-old stems of Betula pendula
(a) and Fagus sylvatica (b) as measured at temperatures between –5
C
and 40
C. Data pairs are deduced from values of Fig. 1. Measurements
were performed under constant climatic conditions (at current tempera-
ture, 50–50% relative humidity) and a controlled CO2 supply
(360 ppm) before and after illumination with 600 lmol photons m
2
s
1. Means 6SE; n¼10 (see Fig. 1). In all panels, the correlation
coefficients for non-linear regressions are given.
temperature response of bark photosynthesis were recorded.
Estimates of the temperature coefficients DHd (deactivation
energy) and DHa (activation energy) differed significantly
(Table 1). A complete list of parameters used to describe
the temperature dependence of Amax is shown in Table 1.
Daily courses of Rd and Amax
To compare short- and long-term temperature responses,
the diurnal and seasonal patterns of Rd and Amax were
additionally monitored in the field. Typical daily courses
Differences between leaves and stems in the temperature
r2= 0.994, P<0.0001 response of PSII quantum yield were also assessed. Light-
adapted photochemical yield of stems (DF/Fm#; Fig. 5)
2 3
followed a similar temperature pattern to Amax (Fig. 1).
Yet, a clear difference with respect to leaves was found as
the temperature optimum of DF/Fm# (Topt) was 34
C in
stems and 28
C in leaves of birch (for beech 36
C and
30
C, respectively). Besides the difference in Topt, it was
evident that at high temperatures (>35
C) the reduction
in effective quantum yield of PSII was clearly higher in
leaves than in stems (Fig. 5). Accordingly, stems showed
a broader thermal optimum range and the decline in the
curve was comparatively flat (Fig. 5).
Compared with CO2 assimilation (Fig. 1) and light-
adapted photochemical yield (Fig. 5), the maximum
quantum yield of PSII (Fv/Fm) of stems and leaves was
relatively insensitive to temperature changes (Table 2).
Between 5
C and 30
C no significant differences in
Fv/Fm were found (Table 2). In contrast, freezing tempera-
tures (–5
C) resulted in a steep decrease in maximum
quantum yield of PSII of leaves and stems. High tempera-
tures (40
C) led only to a marginal decrease in Fv/Fm,
while a significant decrease occurred in leaves (Table 2).
To follow up the influence of low temperatures on bark
 Temperature dependency of bark photosynthesis 4299
summer winter
0,0 0,0
-1,0 a -1,0 b
-2,0 -2,0

[µmol CO2 m-2 s-1]

[µmol CO2 m-2 s-1]

-3,0 -3,0
-4,0
Rd or Rl
-4,0

Rd or Rl
-5,0 -5,0
-6,0 -6,0
-7,0 -7,0
-8,0 Rd -8,0 Rd
-9,0 Rl -9,0 Rl
-10,0 -10,0
08:00 10:00 12:00 14:00 16:00 18:00 20:00 08:00 10:00 12:00 14:00 16:00 18:00 20:00
time [hh:mm] time [hh:mm]

5,5 5,5
c d
4,5 4,5

bark photosynthesis
bark photosynthesis

[µmol CO2 m-2 s-1]

[µmol CO2 m-2 s-1]

3,5 3,5

2,5 2,5

1,5 1,5

0,5 0,5

-0,5 -0,5
08:00 10:00 12:00 14:00 16:00 18:00 20:00 08:00 10:00 12:00 14:00 16:00 18:00 20:00
time [hh:mm] time [hh:mm]

2000 40 2000 40
1800 e 35 1800 f 35
1600 1600
[µmol photons m-2 s-1]
[µmol photons m-2s-1]

30 30
temperature [°C]

temperature [°C]
1400 1400
25 25
1200 1200
20 20
PAR

PAR

1000 1000
15 15
800 800
10 10
600 600
400 5 400 5
200 0 200 0
0 -5 0 -5
08:00 10:00 12:00 14:00 16:00 18:00 20:00 08:00 10:00 12:00 14:00 16:00 18:00 20:00
time [hh:mm] time [hh:mm]

Fig. 4. Diurnal course of stem CO2 efflux in the dark (Rd), stem CO2 efflux in the light (Rl) (a, b), and corticular photosynthesis (|Rd–Rl|) (c, d). Stem
surface temperatures (grey rhombi; solid lines) and PAR (white rhombi; dotted lines) are shown in (e, f). Summer data (August) (a, c, e) and winter
data (January) (b, d, f). Measurements were performed in situ on 1-year-old stems of Betula pendula.

photosynthesis, the light response of DF/Fm# at warm an immediate alteration in the rate of Rd and Amax, with
(20
C), chilling (5
C), and freezing (–5
C) tempera- the extent of that alteration being determined by the
tures was also determined (Fig. 6). In both species a steep temperature coefficient of each process (Atkin et al.,
decline in DF/Fm# at 5
C and –5
C was observed. 2007). Temperature response of stem Rd revealed a typical
exponential relationship, with regression-based estimates
Discussion of Q10 that confirm observations in other woody species in
which Q10 values of stem dark respiration were between
Temperature response of Rd and Amax 1.6 and 2.3 (Sprugel and Benecke, 1991: 2–2.3; Damesin
Because photosynthesis (Amax) and respiration (Rd) are et al., 2002: 1.6–2.1; Edwards et al., 2002: 1.9–2.1).
temperature sensitive, a change in temperature results in Regression-based estimates of DHa (activation energy)
4300 Wittmann and Pfanz
0,6 0,6
Fagus sylvatica a Betula pendula b
0,5 0,5
0,1

0,4 0,4
0,03

0,3 0,3

0,2 0,2

0,1 0,1
5°C
6 °C
0,0 0,0

0 10 20 30 40 50 0 10 20 30 40 50
stem temperature [°C]

Fig. 5. Temperature response of effective quantum yield of PSII (DF/Fm#) of leaves (open circles) and 1- to 2-year-old stems (filled circles) of (a)
Fagus sylvatica and (b) Betula pendula. Measurements were performed with a chlorophyll fluorometer (PAM2000, Walz, Effelrich, Germany) at
light-saturating 600 lmol photons m
2 s
1. Values are means 6SE of 10 independent measurements.

were within the range of published values for Rd (Reddig Table 2. Temperature-dependent changes in dark-adapted
(maximum) quantum yield of PSII (Fv/Fm) of 1- to 2-year-old
and Gries, 1999). Temperature response of bark photo-
stems (S) and concomitant leaves (L) of Betula pendula and
synthesis was similar to that generally found in leaves Fagus sylvatica
(Kramer and Kozlowski, 1979; Larcher, 2001). At
Data are means 6SD (n¼10). The asterisks indicate statistically
a common reference temperature of 20
C and saturating significant differences between S and L (P <0.05).
illumination, photosynthetic bark chlorenchyma reduced
dark respiration rates by 68% or 83%, respectively Temperature Betula pendula Fagus sylvatica
(
C)
(Fig. 2). These results are in good agreement with previous Organ Fv/Fm Organ Fv/Fm
studies in which light-saturated bark photosynthesis was
found to compensate for 60–90% of the respiratory carbon –5 L 0.4560.03* L 0.4460.03*
S 0.3260.05* S 0.3060.04*
loss of young stems (Sprugel and Benecke, 1991; 5 L 0.7360.05 L 0.8060.07
Cernusak and Marshall, 2000; Aschan et al., 2001; S 0.7160.06 S 0.7860.06
Wittmann et al., 2001, 2005; Pfanz et al., 2002). Thus, 10 L 0.7760.02 L 0.8060.03
S 0.7760.03 S 0.7960.06
bark photosynthesis clearly supports stem carbon balance 20 L 0.7960.01 L 0.8160.03
at moderate temperatures. However, while stem dark S 0.7960.03 S 0.7960.05
respiration was found to increase exponentially with 30 L 0.7960.02 L 0.8160.04
S 0.8060.04 S 0.8060.02
increasing temperatures, bark photosynthesis levelled off 40 L 0.6960.03* L 0.7460.02*
or decreased at high temperatures (35–40
C). As a result, S 0.7660.05* S 0.7760.04*
the proportion of carbon that is refixed also declined
dramatically as the temperature increases (Fig. 1). Ac-
cordingly, a linear relationship between respiratory and temperatures this relationship departed from linearity in
assimilatory metabolism was only found at moderate stems (Fig. 3). This indicates that temperature sensitivity of
temperatures (10–30
C). This confirms findings by Amax differs from that of Rd under these conditions, with
Cernusak and Marshall (2000), Aschan et al. (2001), and the result that Rd/Amax is altered. One reason for this
Wittmann et al. (2007), who reported a linear relationship alteration may be that photosynthesis is particularly
between stem Rd and Amax at 20
C for Pinus monticola, sensitive to the rate of utilization or export of its products.
Populus tremula, and B. pendula stems. Rd and photosyn- If this is low (e.g. with reduced sink strength or at low
thesis are interdependent, with Rd relying on photosyn- temperatures which limit respiration) the rate of photosyn-
thate as substrate, whereas photosynthesis depends on thesis may become restricted by ‘feedback inhibition’ (see
Rd for the carbon skeletons and for the ATP required Stitt et al., 1987). Woodwell (1990) and Ryan et al.
for sucrose synthesis plus repair of photosynthetic proteins (1996) found that the Rd/Amax ratio increased with
(Krömer, 1995; Atkin et al., 2000, 2007; Padmasree et al., elevated temperature in leaves. According to Dewar et al.
2002). Consequently, Rd and Amax cannot diverge in- (1999), this reflects the transient dynamics of the plant
definitely, and homeostasis of Rd/Amax is often assumed pools (e.g. the non-structural carbohydrate and protein
(Gifford, 2003). Yet, at high (>35
C) and low (<5
C) pools), in which the turnover rates of labile C and starch

1,0
a Fagus sylvatica
0,8
0,6
0,4
0,2
0,0
0 200 400 600 800 1000 1200 1400
PAR [µmol photons m-2 s-1]
Fig. 6. Light response of effective quantum yield of PSII (DF/Fm#) obtained from 1- to 2-year-old stems of Fagus sylvatica (a) and Betula pendula
(b) under exposure to warm (20
C; filled triangles), chilling (5
C; open circles), and freezing (–5
C; filled circles) temperatures. Values are means
6SE of 10 independent measurements. Grey dashed lines indicate the maximum quantum yield of PSII (Fv/Fm).
are more temperature sensitive than photosynthesis. Conse-
quently, an imbalance between the underlying C fluxes
with increasing temperature is maintained. Similar reasons
may also explain why increases in temperature stimulated
stem Rd more than Amax.
There may be several physiological reasons for the
species-specific differences in temperature response of
Amax, but those reasons are difficult to assess, because of
the variety of contributing processes. In leaves, the cause
may originate from intrinsic differences in Rubisco
activase activity (Crafts-Brandner and Salvucci, 2000) or
part of the specific temperature responses may be related
to the thermal properties of the processes contributing to
CO2 diffusion and transport into the chloroplast (Dreyer
et al., 2001). Nevertheless, addressing those reasons in
stems will require further investigation before it can be
wholly understood.
Temperature response of PSII photochemistry
The relationship between quantum yield of PSII and
quantum yield for CO2 assimilation has been well
documented (Cheng et al., 2001). Linear relationships
have been reported in many species (Krall and Edwards,
1990, 1991; Cornic and Ghashghaie, 1991; Genty et al.,
1992; Maxwell et al., 1998) and it appears that this
relationship is conserved, as it holds across species
(Seaton and Walker, 1990) and is not affected by water
stress or elevated CO2 (Cornic and Ghashghaie, 1991;
Habash et al., 1995). Based on this relationship, T versus
DF/Fm# curves of leaves and stems were examined. Bark
photochemical yield (DF/Fm#) followed the same tempera-
ture pattern as bark CO2 assimilation, which reflects
a functional linkage between photochemistry and photo-
synthetic carbon reduction of stems. However, compared
with DF/Fm#, the maximum quantum yield of PSII
(Fv/Fm) of stems and leaves was relatively insensitive to
Temperature dependency of bark photosynthesis 4301
1,0
b Betula pendula
0,8
0,6 -5°C
5°C
20°C
0,4
0,2
0,0
0 200 400 600 800 1000 1200 1400
temperature changes. Between 5
C and 30
C no
significant differences in Fv/Fm were found (Table 2),
indicating a well-functioning PSII over a broad range of
temperatures. Manetas and Pfanz (2005) found compara-
ble Fv/Fm values for both species at room temperature.
However, at freezing temperatures, maximum quantum
yield of PSII (Fv/Fm) of leaves and stems decreased
drastically (–5
C, Table 2). It is suggested that the
observed drop in Fv/Fm reflects an active down-regulation
of Fv/Fm to avoid low temperature stress. However,
damage to PSII also cannot be excluded. According to
Solhaug and Haugen (1998), maximum quantum yield of
PSII in bark of P. tremula was considerably reduced
during winter. Since the reduction in Fv/Fm partly
depended on sun exposure and on phellem thickness, they
concluded that photoinhibition must be partly responsible
for the low Fv/Fm. The steep decline in the light response
curves of DF/Fm# at 5
C and –5
C reflects the
increasing stress resulting from low temperatures as the
light level is increased (Fig. 6). Under low temperature,
increased levels of photoinhibition (even under moderate
light levels) in leaves have been attributed to several
factors, including the reduced utilization of excitation
energy in carbon metabolism. This leads to an increased
proportion of reduced QA (primary quinone acceptor; the
first electron acceptor of PSII) in the steady state, which
results in an increase in excess excitation energy. Rates of
repair via D1 protein turnover can be severely reduced as
well (Krause, 1994). Furthermore, Fv/Fm of stems and
leaves declined at high temperatures (40
C; Table 2).
PSII is well known to be sensitive to high temperatures,
and it is often cited as the most heat-sensitive component
of photosynthesis in temperate species (Berry and Björk-
man, 1980; Havaux, 1992). Therefore, it is likely that
damage to PSII contributed to the inhibiton of leaf and
bark photosynthesis at these temperatures (Fig. 5).
4302 Wittmann and Pfanz
Differences in optimum temperature for
photosynthesis
Comparison of T versus DF/Fm# curves of leaves and
stems revealed that optimal bark photosynthesis occurred
at higher temperatures than leaf photosynthesis (Fig. 5).
C4 plants have a higher temperature optimum for
photosynthesis than C3 plants due to the operation of
a CO2-concentrating system that inhibits Rubisco oxygen-
ase activity (Berry and Björkman, 1980; Edwards and
Walker, 1983; Badger and Pfanz, 1995). Thus, it is
assumed that the comparably higher temperature optimum
of stems may hint at a C3–C4 intermediate pathway of
carbon fixation in the stem chlorenchyma, as recently
reported by Hibberd and Quick (2002) for herbaceous
plants. Phosphoenolpyruvate (PEP) carboxylase in tree
stems was found at ;10–23 times higher levels than in
leaves of C3 plants (Höll, 1973, 1974; Berveiller and
Damesin, 2005). Compared with Rubisco, PEP carboxyl-
ase is heat stable; Rubisco activase is actually the heat-
labile component of C3 photosynthetic reactions (Rubisco
between 20
C and 25
C; PEP carboxylase is optimally
active at ;37
C). The suggestion of C3–C4 intermediacy
should also show up in the carbon isotope discrimination
of photosynthetic stems. Indeed, Cernusak et al. (2001)
did observe a departure from the discrimination expected
for C3 photosynthesis at high refixation rates in
bark chlorenchyma of P. monticola. Another important
aspect is the high CO2 concentration in the refixing bark
tissues. In young stems of B. pendula, suppression of
photorespiration was attributed to high bark CO2 concen-
trations (618–1548 lmol CO2 mol
1; Wittmann et al.,
2006). These values are up to seven times higher than
those generally reported for C3 (240 lmol CO2 mol
1) or
C4 (200 lmol CO2 mol
1) leaves (Von Willert et al.,
1995). In leaves of C3 plants elevated CO2 concentrations
led to a suppression of photorespiration as well as a shift
of the photosynthetic optimum to higher temperatures
(Acock and Allen, 1985; Long, 1991; Bowes, 1993).
Furthermore, the greater heat capacity of stems may con-
tribute to the observed differences in temperature opti-
mum, but addressing those reasons in stems will require
further investigation before it can be wholly understood.
Several studies also demonstrated lower optimum tempera-
tures in species evolutionarily adapted to cooler environ-
ments (Berry and Björkman, 1980; Hällgren and Öquist,
1990). Betula pendula, the range of which extends further
north than that of F. sylvatica, is a pioneer tree that
typically requires gaps or clearings to establish a new
generation of seedlings that are exposed to high irradi-
ances. Yet, optimum temperatures for photosynthesis of
birch leaves and stems were always somehow lower than
those of beech trees. Across a wide range of species, foliar
frost resistance and optimum temperatures for photosyn-
thesis are inversely correlated (Read and Hope, 1989), and
it seems that species are unable to optimize the perform-
ance in either hot or cold environments. Thus, irrespect-
ive of differences between leaf and stem temperature
optimum for photosynthesis, the species-specific differ-
ences in optimum temperature of bark photosynthesis
may also manifest evolutionary adaptation to temperature
environment. Niinemets et al. (1999) reported similar
results for leaves of Tilia cordata and P. tremula.
Daily courses of bark photosynthesis in the field
In situ measurements on field-grown plants were generally
consistent with those made on plants in the chamber
studies. Bark photosynthesis clearly followed the daily
temperature and PAR course during the summer months
(mean monthly temperature recorded in August was
21.5
C), but values were strongly inhibited during the
winter months (mean monthly temperature recorded in
January was 2.6
C). Several authors suggested that
branches of deciduous trees might be able to photosynthe-
size even during the leafless period and that bark
photosynthesis is an important factor in the ability of
deciduous trees to survive in areas with long cold winters
(Pearson and Lawrence, 1958; Strain and Johnson, 1963;
Perry, 1971; Foote and Schaedle, 1976; Parker, 1978;
Pilarski, 2002). The present results call this assumption
into question. Foote and Schaedle (1976) found similar
seasonal patterns of bark photosynthesis on 5- to 7-year-
old aspen stems. Furthermore, Larcher and Nagele (1992)
conclusively demonstrated that the photosynthetic capac-
ity of 3- to 7-year-old stems of F. sylvatica is lowered in
winter, and that short-term rewarming treatments cannot
restore it to summer values. In contrast, the maximum
quantum yield of PSII in bark chlorenchyma of Scots pine
twigs, measured as Fv/Fm, was shown to be well pre-
served during winter, while Fv/Fm of Scots pine needles
was severely reduced (Ivanov et al., 2005). In leaves and
needles of evergreen woody plants, winter depression of
photosynthesis has been considered to be associated with
after-effects of freezing (Larcher, 1981; Öquist, 1983),
with changes in chloroplast structure and molecular
composition during winter (Senser et al., 1975), and with
processes of cold adaptation and photoinhibition (Strand
and Öquist, 1988). Similar processes might in pars or in
toto also explain the observed winter depression of bark
photosynthesis in stems of F. sylvatica and B. pendula.
Furthermore, it is well known that from autum to winter
the levels of soluble carbohydrate in stem tissues of trees
increase (Sakai and Larcher, 1987). The outcome of this is
that besides osmotic effects on photosynthetic activity, the
high sugar accumulation in the chloroplasts leads to
a potent feedback inhibition of photosynthesis (Foyer,
1988). Electron microscopic studies by Sagisaka et al.
(1990) further revealed that major cytological changes in
the cortical cells of deciduous trees began to occur in early

September in conjunction with the metabolic transition
from the growing to the wintering stage.
Conclusions
This study showed that the benefit of bark photosynthesis
is negatively affected by low (<5
C) as well as high
temperatures (>30
C). The carbon balance of trees is
defined by the difference between photosynthetic carbon
assimilation and the expenditure of fixed C by respiration;
it is therefore obvious that any shift in this balance
reduces the efficiency of stems/trees to convert photosyn-
thetically reduced C into new biomass. Temperatures
above 30
C lead to a sustained imbalance between stem
dark respiration and bark photosynthesis, because bark
photosynthesis declines at high temperatures, while
respiration increases exponentially. Consequently, the
proportion of carbon that is refixed also declines dramat-
ically as temperature increases and a higher amount of
CO2 is lost to the atmosphere. Even though it is difficult
to extrapolate from young saplings to mature trees, and
from short-term temperature change to long-term acclima-
tion, the possible implications for forest carbon balance
with increasing global temperatures are thought-provoking.
During winter, both gas exchange and fluorescence
measurements clearly indicated a reduction of stem carbon
assimilation. Thus, carbon acquisition capacity of stems
may be limited in winter by low temperatures (<5
C) due
to a drop in Fv/Fm and in summer by high temperatures
(>30
C). First evidence also suggests species-specific
differences in temperature response of bark photosynthesis
due to evolutionary adaptation to the temperature environ-
ment. Nevertheless, in the face of carbon balance, bark
photosynthesis could be important during the winter even
if its values are low, because respiration values are also
low during this period. Furthermore, the present data
suggest an important role for bark photosynthesis by
woody trees in maintaining a favourable carbon balance
during the late autumn and early spring, when leaf
photosynthesis of deciduous trees is decreasing or non-
existent, and stems are exposed to rather low temperatures
(;5–10
C).
Acknowledgements
We would like to thank Gudrun Friesewinkel, Sabine Kühr, and
Christa Kosch for technical assistance. Warm thanks also to Dr
Sabine Begall, Dipl. Umweltwiss. Sabine Flohr, and Janne
Mombour. Dr Francesco Loreto (CNR-Roma) is gratefully
acknowledged for helpful discussions.
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