Functional Ecology 2012, 26, 46–55
doi: 10.1111/j.1365-2435.2011.01934.x
Impact of clear and cloudy sky conditions on the vertical
distribution of photosynthetic CO2 uptake within a
spruce canopy
Otmar Urban1,*, Karel Klem1, Alexander Ač1, Katerˇina Havránková1, Petra Holišová1,
Martin Navrátil2, Martina Zitová1, Klára Kozlová1, Radek Pokorný1, Mirka Šprtová1,
Ivana Tomášková1, Vladimı´r Špunda1,2 and John Grace3
1
Global Change Research Centre, Academy of Sciences of the Czech Republic, Bělidla 4a, CZ-60300 Brno, Czech
Republic; 2Department of Physics, Faculty of Science, University of Ostrava, 30. dubna 22, CZ-701 03 Ostrava 1, Czech
Republic; and 3Institute of Atmospheric and Environmental Science, School of GeoSciences, University of Edinburgh,
The Kings Buildings, Edinburgh EH9 3JN, UK
Summary
1. Cloud cover affects carbon exchange between biota and the atmosphere. Recent studies have
demonstrated that an increase in the diffuse radiation fraction enhances the photosynthetic
efficiency of canopies. Although the exact mechanism behind this effect is not clear, a more even
distribution of light among leaves across the vertical profile of the canopy is considered to be the
most important cause of this difference.
2. To test this hypothesis, the net ecosystem production (NEP) of a Norway spruce forest
(30-year-old) was measured under cloudy and sunny skies by the eddy covariance method. In
parallel, measurements of the diurnal courses of gas exchange and chlorophyll fluorescence
parameters were made in the upper sun (5th whorl; 1-year-old needles), middle (8th and 10th
whorl; 1- and 2-year-old needles) and lower shade (15th whorl; >2-year-old needles) shoots.
3. The higher diffuse radiation fraction during cloudy days resulted in significantly higher ecosystem carbon uptake than at corresponding incident photosynthetic photon flux density on
sunny days. Our shoot-level data show that shoots from deep within the canopy contribute substantially to the overall carbon balance during cloudy days. But, although shade-adapted shoots
had a markedly positive carbon balance over a 24-h period on cloudy days, their performance
was impaired on sunny days contributing only a marginal or even negative carbon balance from
the middle and shaded parts of the canopy. The uppermost sun shoots contributed 78% of the
total carbon assimilated during a sunny day, but only 43% during a cloudy day.
4. In addition, afternoon depression of canopy NEP and CO2 assimilation rates of the uppermost shoots (5th and 8th whorl) occurred in response to irradiance on sunny days, characterized
by significant decreases in CO2 uptake and apparent quantum yield; however, this depression
did not occur under cloudy conditions. Stomatal and non-stomatal regulations of carbon
assimilation in the afternoon are discussed.
Key-words: afternoon depression of photosynthesis, daily course, diffuse ⁄ direct radiation,
eddy covariance, light response curve, light use efficiency, net ecosystem production, photorespiration, stomatal conductance
Introduction
The contribution of plants to the carbon cycle through photosynthetic assimilation relies on the absorption of radiant
energy. Solar energy reaches the Earth’s surface both as
*Correspondence author. E-mail: urban.o@czechglobe.cz
direct beams from the sun and in diffuse form after scattering in the atmosphere. The ratio of these two components
has undergone substantial variation during recent decades
with trends described as global ‘dimming’ and ‘brightening’
effects (e.g. Wild 2009). In general, cloud cover and aerosol
loading in the atmosphere lead to (i) reduced incident photosynthetic photon flux density (I), (ii) an increased ratio
2011 The Authors. Functional Ecology 2011 British Ecological Society
Vertical distribution of photosynthesis 47
between the diffuse and direct solar radiation fractions, (iii)
altered spectral composition of incident radiation and (iv)
subsequent changes in microclimatic parameters (e.g.
decreases in temperature and vapour pressure deficit). These
effects were reviewed in Gu et al. (2002). Thus, the sky conditions, not just the total incoming solar energy, may
influence photosynthesis of ecosystems.
Although cloud cover decreases primary productivity and
daily carbon sequestration, owing to the dramatic reduction
in total irradiance (Alton 2008), recent theoretical and observational studies have demonstrated that increases in the fraction of diffuse radiation enhances photosynthetic efficiency
and may, thus, intensify the net terrestrial carbon sink (Knohl
& Baldocchi 2008; Mercado et al. 2009). At canopy level, diffuse radiation on cloudy days enhances photosynthesis and
results in a significantly lower compensation irradiance
(Hollinger et al. 1994; Law et al. 2002; Urban et al. 2007) and
a higher apparent quantum yield (AQY) (Gu et al. 2003;
Niyogi et al. 2004; Still et al. 2009; Dengel & Grace 2010).
The specific mechanisms whereby diffuse light stimulates
canopy-level photosynthesis are still not well understood. The
suggested reasons for these differences are (i) more favourable
microclimatic conditions during cloudy periods, i.e. lower
temperature and vapour pressure deficit (D), resulting in
lower ecosystem respiration and sufficient stomatal conductance (GS), (ii) stimulation of photochemical reactions and
stomatal opening via an increase in the blue ⁄ red light ratio
and (iii) increased penetration of light into the canopy, and
thus a more even distribution of light among leaves (reviewed
in Gu et al. 2003; Urban et al. 2007; Knohl & Baldocchi 2008;
Still et al. 2009; Dengel & Grace 2010; Pingintha et al. 2010).
It is hypothesized that the nonlinear response between leaflevel or shoot-level CO2 assimilation rate and I is responsible
for the photosynthetic advantages of diffuse radiation over
direct beam radiation at the canopy level (Gu et al. 2003; Still
et al. 2009), as whole-canopy photosynthesis includes the
contribution of photosynthesis from sunlit and shaded leaves.
Sunlit leaves are often brightly illuminated and photosynthesize at saturating rates, which leads to a less efficient use of
irradiance than those of shaded leaves, whereas the assimilation rates of shaded leaves may be enhanced by additional
diffuse radiation reaching the lower parts of the canopy.
In addition, it is hypothesized that an excessive flux of
direct radiation and exposure to high tissue temperatures during hot sunny days may lead to significant down-regulation of
photosynthesis, evident as stomatal closure, photo-inhibition
of photo-chemical reactions and ⁄ or stimulation of photorespiratory CO2 efflux (Muraoka et al. 2000; Larcher 2003;
Franco, Matsubara & Orthen 2007; Stroch et al. 2010).
Within this hypothesis, down-regulation of carbon assimilation is expected in the upper-sunlit leaves during hot sunny
days with a shift in the main assimilation activity to the lower
parts of the canopy. To the best of our knowledge, a comprehensive study on how individual levels of a canopy contribute
to the whole ecosystem exchange of CO2 under direct and diffuse sky conditions is still lacking. Therefore, we investigated
this problem specifically within a Norway spruce (Picea abies)
canopy and compared the results during cloudy and sunny
days.
To test these hypotheses, net ecosystem production (NEP),
defined as the difference between ecosystem-level photosynthetic gain of CO2 and ecosystem respiratory loss of CO2
(Chapin et al. 2006), over the spruce forest was measured
under conditions of cloudy and sunny days by the eddy
covariance method. In parallel, measurements of the diurnal
courses of related physiological processes were made on
shoots at different levels in the canopy.
Materials and methods
SITE DESCRIPTION
The forest stand selected for this study is located at the experimental
research site Bı́lý Křı́ž (Beskydy Mountains, 4933¢N, 1832¢E, NE of
the Czech Republic, 908 m a.s.l.) and it forms a part of the CarboEurope-IP (http://www.carboeurope.org) and ICOS (http://www.icosinfrastructure.eu) networks. This area has a cool (annual mean air
temperature 6Æ7 C) and humid (annual mean relative air humidity
80%) climate with high annual precipitation (the average for
2000–2009 is 1374 mm).
The forest stand (6Æ2 ha) consists of P. abies (L.) Karst (99%) and
Abies alba Mill. (1%) planted on the slope (11–16) with SSW orientation (see details in Urban et al. 2007). At the time of the physiological
investigations, the stand density was 1428 trees ha)1 (hemi-surface
leaf area index c. 9Æ5 m2 m)2), tree height and stem diameter at
1Æ3 m were 13Æ4 ± 0Æ1 m and 15Æ8 ± 0Æ2 cm, respectively (means ±
standard deviation).
To analyse effects of diffuse and direct radiation on CO2 assimilation processes, two successive periods during the growing season
(July) were used for the present analysis. The first period (16th–18th
July) – cloudy was characterized by a high diffuse index (DI > 0Æ7;
DI is defined here as the ratio between the diffuse and total intensity
of photosynthetically active radiation), whereas the second period
(29th–31st July) – sunny was characterized by a DI < 0Æ3 (clear sky)
at maximum solar elevation angles.
MEASUREMENTS OF MICROCLIMATIC FACTORS
Interpretation of the carbon assimilation data was based on the incident photosynthetic photon flux density (I, waveband 400–700 nm).
Two quantum sensors (LI-190; Li-Cor, Lincoln, NE, USA) were
located above the stand canopy at the top of a 15-m high meteorological mast. To measure daily courses of diffuse I, one quantum sensor
was shielded from direct light by shadow ring (CM 121B ⁄ C; Kipp &
Zonen, Delft, the Netherlands). A laboratory-made optical device,
the canopy Fibre Optic System (CANFIB, Institute of Systems Biology and Ecology, Czech Republic), was used for the measurement of
I within the tree canopy (see Urban et al. 2007 for detailed description). CANFIB sensors, calibrated according to LI-190 (Li-Cor),
were located at four levels (i.e. on 5th, 8th, 10th and 15th whorl)
within the vertical structure of the canopy (i.e. 2Æ9, 5Æ4, 6Æ9 and 9Æ1 m
from the apex of the tree). Each sensor was fixed perpendicular to the
main shoot axis. Instantaneous readings were taken every 30 s and
stored on a data logger (Delta-T, Burwell, Cambridgeshire, UK).
The spectral composition of incident (above canopy) and transmitted (below canopy) solar radiation was obtained using a portable
spectroradiometer, LI-1800 (Li-Cor) equipped with a cosine
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
48 O. Urban et al.
corrector. Simultaneously, I was recorded using an LAI-2000
(Li-Cor) with a quantum sensor (LI-190) in the same place. Data were
collected at 8:30, 13:30 and 18:30 local solar time (i.e. at one-half,
maximum and one-quarter of expected maximum I, respectively),
during both clear and cloudy sky conditions. A single spectral scan
between 300 and 1100 nm with 1-nm spectral resolution took about
40 s and was measured only when irradiance fluctuated by <20%
during the scan. Spectral scans were normalized to actual irradiances.
Measurements of air temperature and humidity profiles (model
RHA1; Delta-T) were made during the eddy flux measuring campaigns. Subsequently, the values of vapour pressure deficit (D) were
calculated according to formula published by Buck (1981). Soil temperature (thermistor model Pt100) was measured at five depths of
0Æ05–0Æ50 m. The signals from all sensors were recorded as halfhourly averages using a data logger (Delta-T). In addition, soil moisture at a depth of 0Æ2 m was measured close to the trees investigated
at 2-h intervals during the measuring periods by time domain
reflectometry (TDR; TRIME-FN, IMKO, Ettingen, Germany).
EDDY COVARIANCE MEASUREMENTS
An eddy covariance system was used to measure the CO2 and water
vapour fluxes between the forest and the atmosphere. The system
comprised: (i) a three-axis ultrasonic anemometer Solent 1012R2 (Gill
Instruments, Lymington, Hampshire, UK) mounted on the top of a
15-m tall triangular steel tower, (ii) an infrared gas analyser Li-6262
(Li-Cor) measuring the instantaneous concentration of CO2 and
water vapour in the air with a frequency of 10 Hz and (iii) the software for real-time (Edisol) and post-processing analysis (EdiRe).
The half-hourly averaged H2O and CO2 flux values were evaluated
for data quality. The spike removal and quality check of the raw
signals were performed using the Quality Control (QC) Software
(Vickers & Mahrt 1997) and according to the most recent CarboEurope-IP recommendations (Gockede et al. 2008). Raw data were used
for the evaluated variables of vertical and the horizontal wind components w and u, air temperature T, and H2O and CO2 concentrations
(see details in Urban et al. 2007).
COMPLEMENTARY PHYSIOLOGICAL MEASUREMENTS
Shoot-level physiological measurements were carried out on three
representative trees situated within the flux footprint. Two shoots per
tree and whorl with SSW orientation were investigated in the upper
canopy (5th whorl; 1-year-old shoots), the middle canopy (8th and
10th whorl; 2-year-old shoots) and lower canopy (15th whorl; >2year-old shoots). Shoots for the estimation of water potential, nitrogen and chlorophyll content were cut from the same branches. The
same shoots ⁄ branches were measured on cloudy and sunny days.
Chlorophyll fluorescence measurements
Measurements of chlorophyll a fluorescence emission (PAM 2000
fluorometer; H. Walz, Effeltrich, Germany) were simultaneous with,
and used the same shoots within the canopy profile as, the gas
exchange measurements. Apparent photosynthetic electron transport
rate (J) was estimated as (Valentini et al. 1995):
J¼
F0M FS
I 0:5 a;
F0M
where FS is the fluorescence emission induced by the actual photosynthetic photon flux density (I), F¢M is the maximal fluorescence
emission observed during a 1-s saturating pulse, the factor 0Æ5
assumes that the incident quanta, used to excite both photosystems
(PSII and PSI), are equal, and a is the absorptance (0Æ82) estimated
for Norway spruce needles by spectroradiometric measurements.
See Spunda et al. (2005) for a detailed description.
Water potential and nitrogen analyses
The leaf water potential (W) was determined using a pressure chamber
(Model 610; PMS Instrument Co., Albany, Oregon USA). Shoots
from the same crown levels were sampled at 4:00 (pre-dawn), 8:00,
13:00, 18:00 and 20:00.
Subsequently, nitrogen concentration in the dry mass of needles
was measured by an automatic analyser (CNS-2000; LECO Corporation, St. Joseph, MI, USA) in 100 mg of mixed samples. Before analysis, each sample was dried to a constant mass in an oven (80 C) over
2 days. The specific leaf area of the needles (SLA) was defined as the
ratio between projected leaf area (one side of the needles) and leaf dry
mass.
MODELLING OF PHYSIOLOGICAL PROCESSES
Instantaneous rates of CO2 assimilation at both canopy (NEP) and
shoot (A) levels were modelled as a general nonrectangular hyperbolic
function of incident I:
/A2 ðaI þ Amax ÞA þ aIAmax ¼ 0 ð2Þ
where a is the AQY, / is a number between 0 and 1 determining
the shape of light response curve and Amax is the light-saturated value
of A.
The rate of photorespiration (RL) during the day was calculated
from gas exchange measurements (A, Rd) and fluorescence measurements (J), according to Valentini et al. (1995):
RL ¼
Gas exchange measurements
Daily courses of CO2 assimilation rate (A) and stomatal conductance
(GS) were measured on intact shoots at their natural orientation using
two identical gas exchange systems Li-6400 (Li-Cor) under conditions
of ambient CO2 concentration (385 lmol CO2 mol)1), natural irradiance, leaf temperature and D. Shoots at four levels were measured at
2 h intervals from 3:30 (pre-dawn) till 21:30 h (after sunset) and again
at 23:00 h (fully dark adapted). Night-time data were used for estimation of the dark mitochondrial respiration rate (RD). The vertical distribution of mitochondrial respiration determined during the day
after 5 min of dark adaptation (Rd) was also determined.
ð1Þ
J 4ðA þ Rd Þ
;
12
ð3Þ
where Rd is the mitochondrial respiration determined during the
day after 5 min of dark adaptation. This equation assumes that
other electron-consuming processes are negligible.
STATISTICAL DATA ANALYSIS
Two-way analysis of variance (ANOVA) was performed to evaluate the
physiological effects of different sky conditions and position of shoots
within canopy. To compare the differences between means, Tukey’s
post hoc test (P = 0Æ05) was used. All statistical tests were performed
using STATISTICA software (StatSoft, Tulsa, OK, USA).
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
Vertical distribution of photosynthesis 49
Results
MICROCLIMATIC CONDITIONS
The measuring campaigns included days that primarily differed in the proportion of diffuse radiation. There were transient changes in photosynthetic photon flux density (I;
Fig. 1a), but the diffuse index (DI) mostly remained <0Æ3
and more than 0Æ7 during the sunny and cloudy days, respectively (Fig. 1b). Diffuse radiation penetrated to lower depths
I (µmol photons m–2 s–1)
2000
(a)
of the canopy more efficiently than direct radiation (Fig. 2b).
Extinction coefficients for the whole tree canopy were c. 0Æ33
for cloudy days and 0Æ48 for sunny days. Microclimatic characteristics, such as temperature and vapour pressure deficit,
measured above (Table 1) and within canopy (Fig. 2c,d), as
well as diurnal changes in leaf water potential (Table 2), followed highly distinctive patterns for these selected days. The
average microclimatic conditions over the three preceding
days were similar to those during the measuring campaigns
(data not shown).
CANOPY NEP ANALYSES AND LEAF-LEVEL VERTICAL
1750
DISTRIBUTION OF PHOTOSYNTHETIC ACTIVITY
1500
Based on the NEP light response curves (NEP–I; Fig. 3a), we
found significantly higher NEP during the cloudy day compared with the sunny day at corresponding irradiances.
Cloudy sky conditions resulted in a lower compensation irradiance (by 38–51%), lower saturating irradiance (by 24–34%)
and higher AQY (by 77–121%), as compared with sunny
days, while night-time respiration remained almost
unchanged (Table 3). As the soil temperature of the dense
spruce stand was stable during the study period (9Æ5–10Æ5 C),
soil respiration amounted to 4Æ6 lmol m)2 s)1 irrespective of
sky conditions (data not shown). Canopy light use efficiency
(LUEcanopy), defined as the ratio between half-hourly averaged NEP and incident I, was up to 3-fold higher during
cloudy days as compared with sunny days (Fig. 3b).
1250
1000
750
500
250
0
DI (dimensionless)
1·0
(b)
0·8
0·6
0·4
0·2
Sunny
Cloudy
0·0
03:00
06:00
09:00
12:00
15:00
18:00
21:00
Table 1. Minimal (min) and maximal (max) values of air
temperature above the canopy (Tair), leaf temperature (Tleaf), vapour
pressure deficit (D) and soil moisture at a depth of 0Æ2 m. Mean
values (±standard deviations) of soil moisture are presented
(N = 20)
Time (h)
Tair (C)
Fig. 1. Diurnal courses of incident photosynthetic photon flux density (I; a) and diffuse index (DI; b) during sunny (open circles and
dashed lines) and cloudy (closed circles and solid lines) days when
physiological measurements were carried out. The mean (points) and
standard deviations (error bars) of 30-min intervals are presented.
(a)
(b)
Tleaf (C)
D (kPa)
Min Max Min Max Min Max Soil moisture (%)
Cloudy 11Æ7
Sunny 18Æ8
18Æ7
25Æ1
(c)
13Æ4
19Æ2
22Æ7
28Æ7
0Æ3
0Æ9
1Æ0
2Æ5
30 (±5Æ2)
20 (±5Æ7)
(d)
Whorl
5
8
10
15
Sunny
Cloudy
0
5
10
15
Projected leaf area (m2 )
20
0
20
40
60
80
Transmitted I (%)
100 12 14 16 18 20 22 24 26 28 0·0
Air temperature (°C)
0·5
1·0
1·5
D (kPa)
Fig. 2. Vertical distribution of projected leaf area (a), transmitted photosynthetic photon flux density (I; b), air temperature (c) and vapour pressure deficit (D; d) at near-noon (11:00–13:00) during sunny (open circles) and cloudy days (black circles). The mean values (symbols) and standard
deviations (error bars) corresponding to the whorls investigated are presented. N = 18.
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
50 O. Urban et al.
Table 2. Mean values ± standard deviations of physiological parameters estimated within the spruce canopy profile during cloudy and sunny
days: pre-dawn (Wpre-dawn) and noon (Wnoon) leaf water potentials, Chl (a + b) – total chlorophyll content per unit area, Chl a ⁄ b – ratio between
chlorophyll a and b, N – total nitrogen concentration per unit leaf dry mass and SLA – specific leaf area
Whorl
5th
Cloudy
Sunny
8th
Cloudy
Sunny
10th
Cloudy
Sunny
15th
Cloudy
Sunny
Wpre-dawn (MPa)
Wnoon (MPa)
Chl (a + b) (g m)2)
Chl a ⁄ b (r.u.)
N (mg g)1)
SLA (m2 kg)1)
)0Æ6 ± 0Æ10bcd
)0Æ9 ± 0Æ14abc
)1Æ3 ± 0Æ03ab
)2Æ2 ± 0Æ12c
0Æ36 ± 0Æ02ab
0Æ40 ± 0Æ03abc
3Æ28 ± 0Æ03a
3Æ22 ± 0Æ04a
12Æ3 ± 0Æ2a
12Æ5 ± 0Æ4a
4Æ6 ± 0Æ1ab
4Æ3 ± 0Æ1a
)0Æ8 ± 0Æ12abcd
)1Æ1 ± 0Æ05a
)1Æ2 ± 0Æ04a
)2Æ3 ± 0Æ10c
0Æ36 ± 0Æ05a
0Æ40 ± 0Æ03abc
3Æ14 ± 0Æ06a
3Æ14 ± 0Æ06a
11Æ9 ± 0Æ5a
11Æ7 ± 0Æ2a
5Æ3 ± 0Æ1b
5Æ1 ± 0Æ4ab
)0Æ4 ± 0Æ11d
)1Æ1 ± 0Æ24ab
)1Æ0 ± 0Æ03a
)1Æ9 ± 0Æ22bc
0Æ39 ± 0Æ03abc
0Æ38 ± 0Æ02ab
2Æ90 ± 0Æ02b
2Æ89 ± 0Æ06b
11Æ3 ± 0Æ4a
11Æ5 ± 0Æ3a
6Æ6 ± 0Æ4c
6Æ7 ± 0Æ2c
)0Æ6 ± 0Æ10cd
)1Æ1 ± 0Æ16a
)1Æ1 ± 0Æ08a
)1Æ5 ± 0Æ17ab
0Æ44 ± 0Æ02c
0Æ41 ± 0Æ03bc
2Æ50 ± 0Æ14c
2Æ63 ± 0Æ06d
9Æ7 ± 0Æ4b
9Æ2 ± 0Æ6b
7Æ9 ± 0Æ3d
7Æ8 ± 0Æ4d
Identical letters indicate homogeneous groups with statistically nonsignificant differences (P > 0Æ05). N = 6–12.
30
(a)
NEP (µmol CO2 m–2 s–1)
25
20
15
10
5
Cloudy AM
Cloudy PM
Sunny AM
Sunny PM
Fit
0
–5
–10
0
250
500
750
1000 1250 1500 1750
2000
LUE Canopy (mol CO2 mol–1 photons)
I (µmol photons m–2 s–1)
0·05
(b)
Cloudy
Sunny
0·04
0·03
mediate and shade needles (Table 3). Likewise, lower chlorophyll a ⁄ b ratio and nitrogen concentration per unit dry mass
in older shade needles compared with younger sun needles,
and higher SLA in shade compared with sun needles, demonstrate distinct acclimation to the light environment within the
canopy profile (Table 2).
During the sunny days, an afternoon depression of NEP in
response to I was evident at canopy level (Fig. 3a). Similarly,
there was an afternoon depression of A in response to I in
shoots located in the upper parts of the crown (Fig. 4a,b).
This depression in the afternoon is associated with decreases
in the AQY of shoots from the 5th and 8th whorls, corresponding with a large increase in the light compensation point
(LCP). Accordingly, the eddy covariance data show a lower
AQY (by 20%) and a higher LCP (by 27%) during the afternoon on sunny days (see Table 3). In contrast, afternoon
depression was not present in the shade shoots of the 10th
and 15th whorl, neither during the cloudy day at the level of
whole forest stand (Fig. 3a) nor at shoot-level throughout the
canopy profile (Fig. 4a–d).
0·02
ANALYSIS OF STOMATAL RESPONSES
0·01
0·00
03:00
06:00
09:00
12:00
15:00
18:00
21:00
Time (h)
Fig. 3. Relationship between photosynthetic photon flux density (I)
and canopy net ecosystem production (NEP) (a) and the diurnal
course of canopy light use efficiency (LUEcanopy) during sunny (open
symbols) and cloudy (closed symbols) days (b). The nonrectangular
hyperbolic function (eqn 2) was fitted to the NEP data (R2 = 0Æ84–
0Æ89; P < 0Æ01). Morning (circles) and afternoon (triangles) NEP
data for sunny and cloudy days were analysed separately. Parameters
of fitted NEP–I response curves are summarized in Table 3.
Parameters of the A–I response curves at shoot-level (A;
Fig. 4), derived from daily courses of A at different vertical
positions, reflected the typical differences between sun, inter-
Subsequently, we tested whether the changes in shoot-level
stomatal conductance (GS) represent the primary reason for
the afternoon depression in carbon assimilation. At the
corresponding I, cloudy sky conditions led to higher GS
(Fig. 5) as anticipated and consequently to higher A values
compared with clear sky conditions. In addition, GS of the
upper shoots (5th and 8th whorls) was higher in the morning
than afternoon (up to 120%). On the contrary, no significant
differences between morning and afternoon GS at corresponding I were evident during the cloudy days (Fig. 5a).
We made a detailed analysis to identify the reasons behind
the marked GS increase under cloudy sky conditions at low I
(£200 lmol photons m)2 s)1). Figure 5c shows that GS
tightly correlates with the intensity of the diffuse fraction of
the incident light, in particular at low irradiances, irrespective of sky conditions. Although GS increases with increasing
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
Vertical distribution of photosynthesis 51
Table 3. Mean values ± standard deviations of selected parameters of CO2 assimilation light response curves at the canopy level (see fits in
Fig. 3a) and shoot level (see fits in Fig. 4a–d). Amax – light-saturated rate of CO2 assimilation, AQY – apparent quantum yield, RD – dark (nighttime) respiration rate, LCP – light compensation point and LSE – light saturation estimate
Canopy
Sunny AM
Sunny PM
Cloudy AM
Cloudy PM
5th whorl
Sunny AM
Sunny PM
Cloudy AM
Cloudy PM
8th whorl
Sunny AM
Sunny PM
Cloudy AM
Cloudy PM
10th whorl
Sunny
Cloudy
15th whorl
Sunny
Cloudy
Amax
(lmol CO2 m)2 s)1)
AQY
(mol CO2 mol)1 photon)
RD
(lmol CO2 m)2 s)1)
LCP
(lmol photon m)2 s)1)
LSE
(lmol photon m)2 s)1)
26Æ8
25Æ6
33Æ1
34Æ4
±
±
±
±
0Æ9
2Æ6
1Æ4
3Æ8
0Æ035
0Æ028
0Æ053
0Æ061
±
±
±
±
0Æ003
0Æ004
0Æ004
0Æ009
7Æ9
7Æ8
7Æ9
7Æ3
±
±
±
±
0Æ4
0Æ6
0Æ4
0Æ7
225
285
148
152
±
±
±
±
23
33
22
28
995
1144
769
717
8Æ3
14Æ0
9Æ6
9Æ9
±
±
±
±
0Æ7
1Æ8
0Æ5
0Æ6
0Æ049
0Æ016
0Æ042
0Æ037
±
±
±
±
0Æ009
0Æ002
0Æ009
0Æ003
1Æ3
1Æ1
1Æ1
1Æ7
±
±
±
±
0Æ4
0Æ2
0Æ2
0Æ3
27
64
26
48
±
±
±
±
8
11
8
15
195
922
255
325
8Æ3
10Æ3
10Æ2
11Æ7
±
±
±
±
0Æ7
1Æ0
1Æ8
1Æ1
0Æ031
0Æ020
0Æ038
0Æ032
±
±
±
±
0Æ004
0Æ003
0Æ005
0Æ005
0Æ9
0Æ9
1Æ1
1Æ7
±
±
±
±
0Æ1
0Æ1
0Æ5
0Æ2
28
44
29
52
±
±
±
±
6
11
8
14
263
567
298
417
6Æ0 ± 0Æ2
4Æ7 ± 0Æ4
0Æ024 ± 0Æ002
0Æ032 ± 0Æ005
0Æ6 ± 0Æ1
0Æ4 ± 0Æ1
26 ± 5
23 ± 5
277
171
1Æ1 ± 2Æ7
1Æ8 ± 0Æ2
0Æ035 ± 0Æ016
0Æ060 ± 0Æ008
0Æ3 ± 0Æ03
0Æ3 ± 0Æ1
9±2
5±2
42
35
Photosynthetic parameters are expressed per unit ground area (canopy level) or per unit leaf area (shoot-level). N = 6.
(c)
(d)
A (µmol CO2 m–2 s–1)
A (µmol CO2 m–2 s–1)
A (µmol CO2 m–2 s–1)
(b)
A (µmol CO2 m–2 s–1)
Fig. 4. Relationship between photosynthetic photon flux density (I) and CO2 assimilation rate (A) at the shoot level in the vertical
canopy profile, i.e. at the 5th (a), 8th (b), 10th
(c) and 15th (d) whorl during sunny (open
symbols) and cloudy (closed symbols) days.
The A–I relationships of shoots located at the
5th and 8th whorls were divided into morning
(00:00–11:30; solid line) and afternoon
(12:00–23:30; dashed line) parts. The nonrectangular hyperbolic function (eqn 2) was fitted to the data (R2 = 0Æ80–0Æ91; P < 0Æ01).
Parameters of fitted light response curves are
summarized in Table 3.
(a)
l (µmol photons m–2 s–1)
intensity of blue light (400–500 nm), this stimulation was
significantly less under clear as compared with cloudy skies
(Fig. 5b). In addition to these effects, we found reduction in
GS with increasing DLeaf (Fig. 5d), which was closely related
to the reduction in WLeaf on the sunny day (Table 2). High
DLeaf values, typical for clear sky conditions, lead to the stomatal closure even at low I (0–100 lmol photons m)2 s)1).
Thus, an increase in I during the morning is not followed by
the corresponding increase in A, which would otherwise be
expected and results, particularly at the top of the canopy,
l (µmol photons m–2 s–1)
in A saturation at relatively low irradiances (see light saturation estimate in Table 3).
LEAF-LEVEL PHOTOCHEMICAL AND RESPIRATORY
PROCESSES
The photochemical efficiency of PSII [(FM¢)FS) ⁄ FM¢ in
eqn 1] did not decrease below 0Æ3 and 0Æ4 during the
sunny and cloudy day, respectively. Accordingly, photoinhibition was not observed on these days. Contrary to
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
52 O. Urban et al.
0·25
(b)
200
0·20
150
0·15
100
0·10
Cloudy
Sunny
Fit
IBlue vs I
Cloudy AM
Cloudy PM
Sunny AM
Sunny PM
Fit
0·05
0·00
0
200
400
600
800
1000
1200 0
10
I (µmol photons m–2 s–1)
20
40
50
0
60
I Blue (µmol photons m–2 s–1)
0·30
0·30
G S (mol H2O m–2 s–1)
30
50
0·20
I = 0–10 µmol m–2 s–1
I = 10–100 µmol m–2 s–1
0·25
I = 100–1000 µmol m–2 s–1
Fit
0·20
0·15
0·15
0·10
0·10
(c)
0·25
(d)
0·05
0·05
Cloudy
Sunny
Fit
0·00
0
G S (mol H2O m–2 s–1)
G S (mol H2O m–2 s–1)
(a)
I (µmol photons m–2 s–1)
250
0·30
0·00
20 40 60 80 100 120 140 160 180 0·0
0·5
1·0
1·5
2·0
2·5
D Leaf (kPa)
I Diffusive (µmol photons m–2 s–1)
Fig. 5. Relationships between stomatal conductance (GS) and actual total photosynthetic photon flux density (I; a), blue light (400–500 nm)
intensity (IBlue; b), diffuse fraction of photosynthetic photon flux density (IDiffusive; c) and leaf vapour pressure deficit (DLeaf; d) estimated during
cloudy (closed symbols) and sunny days (open symbols). The shoot-level data derived from daily course measurements of the 5th and 8th whorls
are presented. In figures (b and c), the GS values estimated only at I below 200 lmol photons m)2 s)1 are used. Dashed lines in figure (b) represent
the relationships between IBlue and I during cloudy (I = 3Æ54IBlue; thick dashed line) and sunny days (I = 3Æ65IBlue; thin dashed line),
respectively. The relationships between GS and light intensities (a–c) were fitted using the model (Fit) proposed by Keen & Spain (1992);
R2 = 0Æ73–0Æ89 (P < 0Æ01). The exponential functions were fitted to the relationships between GS and D. The data were separated to three categories: I < 10 (circles; y = 0Æ10e)1Æ20x; R2 = 0Æ57; P < 0Æ01), 10 £ I < 100 (triangles; y = 0Æ25e)1Æ24x; R2 = 0Æ50; P < 0Æ01) and I ‡ 100
(squares; y = 0Æ29e)0Æ75x; R2 = 0Æ75; P < 0Æ01).
(a) Sunny
160
(b) Cloudy
120
120
80
80
5th whorl
8th whorl
10th whorl
15th whorl
Fit
40
5th whorl
8th whorl
10th whorl
15th whorl
Fit
0
40
J (µmol e–1 m–2 s–1)
J (µmol e–1 m–2 s–1)
160
0
0
200
400
600
I (µmol photons
800
m–2
1000 1200 0
s–1)
200
400
600
I (µmol photons
800
m–2
1000 1200
s–1)
Fig. 6. Relationship between electron transport rate (J) and photosynthetic photon flux density (I) estimated on the basis of daily course measurements in the vertical profile, i.e. at the 5th, 8th, 10th and 15th whorl, of Norway spruce canopy during sunny (a) and cloudy (b) days. The nonrectangular hyperbolic function was fitted (Fit) to the J data of shoots from the 5th (thick line), 8th (thin solid line) and 10th (thin dashed line)
whorl (R2 = 0Æ85–0Æ98; P < 0Æ01).
A, there were almost identical relationships between I and
apparent photosynthetic electron transport rate (J), irrespective of shoot position within the vertical canopy profile and sky conditions, in particular at irradiances up to
400 lmol photons m)2 s)1 (Fig. 6). Moreover, there were
no deviations from the J–I relationships neither in the
morning nor in the afternoon. Thermal energy dissipation,
estimated on the basis of chlorophyll fluorescence emission, reached 0Æ6 during the sunny day, while it was only
0Æ35 during the cloudy day (data not shown). Similarly,
to J, the relationships between thermal energy dissipation
and I were identical, irrespective of shoot position and
sky conditions.
The calculated rate of photorespiration during day-light
periods (RL; Fig. 7) typically reached up to 9 lmol CO2 m)2 s)1 during the sunny day, while RL exceeded
4 lmol CO2 m)2 s)1 only occasionally during the cloudy
day. However, similar RL values were observed at low I
(£400 lmol photons m)2 s)1) irrespective of sky conditions.
Specifically in shoots from the 5th whorl, RL at corresponding irradiances was higher by 15–20% during the afternoon
of sunny days as compared with the morning. This differ-
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
Vertical distribution of photosynthesis 53
(a) Sunny
10
(b) Cloudy
8
8
6
6
4
4
5th whorl AM
5th whorl PM
8th whorl
10th whorl
Fit
2
5th whorl
8th whorl
10th whorl
2
0
R L (µmol CO2 m–2 s–1)
R L (µmol CO2 m–2 s–1)
10
0
0
200
400
600
800
1000
1200
0
200
I (µmol photons m–2 s–1)
400
600
800
1000
1200
I (µmol photons m–2 s–1)
LEAF- TO CANOPY-LEVEL PROCESSES
For the cloudy and sunny days, the total fixed CO2 over 24-h
periods (Fig. 8a) and day-time LUE (Fig. 8b) in four investigated whorls were calculated on the basis of measurements of
I, light response curves of A (Fig. 4), measurement of nighttime respiration rates (Table 3) and with respect to the vertical distribution of leaf area (Fig. 2a). Although the total sum
of assimilated CO2 within the investigated whorls ranged
between 154–170 g during cloudy days, it was only 89–108 g
during sunny days. Figure 8a shows increased assimilation
activity in the middle (8th) and shaded (10th and 15th) sections of the canopy on cloudy days. Whereas shoots located
even in the lowest part of the canopy attained markedly positive carbon balance during cloudy days, only marginal or
even negative carbon balance was achieved by the middle and
shaded parts of the canopy during sunny days. The LUE values, estimated for the individual whorls (Fig. 8b), were generally higher on cloudy compared with sunny days (by 91%,
61%, 131% and 165% at 5th, 8th, 10th and 15th whorl,
respectively).
Discussion
Many researchers have now observed an enhancement in canopy photosynthesis under cloudy as opposed to sunny conditions (Hollinger et al. 1994; Law et al. 2002; Gu et al. 2003;
Niyogi et al. 2004; Schwalm et al. 2006; Urban et al. 2007;
Knohl & Baldocchi 2008; Mercado et al. 2009; Barr et al.
2010; Dengel & Grace 2010; Pingintha et al. 2010; Zhang
et al. 2010). This difference was further confirmed in our
study with the coniferous species (Fig. 3). However, it is less
clear what causes the observed difference. The present work
(a)
80
a
a
Cloudy
Sunny
b
60
40
c
c
c
20
d
d
0
LUEWhorl (mol CO2 mol–1 photons)
ence was probably associated with higher needle temperatures (by 1Æ2–2Æ8 C at comparable irradiances) in the
afternoon than the morning. This difference was not evident in the lower parts of the crown nor during the cloudy
days.
Sum of CO2 assimilated (g)
Fig. 7. Relationships between photorespiration rate (RL) and photosynthetic photon flux density (I) in the canopy vertical profile observed during sunny (a) and cloudy (b) days. The RL rates at the 15th whorl were negligible during both days studied with maximum rates up to 0Æ75 lmol CO2 m)2 s)1, and they are not shown in the figure. The nonrectangular hyperbolic function was fitted (Fit) to the RL data estimated on sunny
days (a) on shoots from the 5th (thick line), 8th (thin solid line) and 10th (thin dashed line) whorl (R2 = 0Æ86–0Æ96; P < 0Æ01). The RL data for
the uppermost shoots were analysed for the morning (black thick line) and afternoon (grey thick line) separately. Because of the low values of RL
at high irradiances, the hyperbolic function was not fitted to RL data on the cloudy days.
c
(b)
0·03
0·02
b
b
b
a
a
a
a
0·01
0·00
5th
8th
10th
15th
Whorl
Fig. 8. The total amount of assimilated CO2 over a 24-h period per
whorl (a) and day-time (light intensity > 0 lmol photon m)2 s)1)
light use efficiency (LUEWhorl; b) during the cloudy and sunny days.
LUEWhorl has been calculated as the ratio between the total amount
of assimilated CO2 and sum of photosynthetically active radiation
incident on the surface of whorls studied. Means (columns) and standard deviations (bars), calculated on the basis of three consecutive
days, are presented. Identical letters indicate homogeneous groups
with statistically nonsignificant differences (P > 0Æ05).
has explored various possible hypotheses to explain the
enhancement in NEP and found evidence supporting two of
these hypotheses.
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
54 O. Urban et al.
1. Effective penetration of anisotropic diffuse radiation into
the canopy (Fig. 2b) causes lower whorls to receive more
radiation, and therefore become a major contributor to
canopy photosynthesis during cloudy days (Fig. 8). Modelling the net CO2 exchange in a broad-leaved deciduous
forest stand, Still et al. (2009) found shade-leaf cumulative photosynthetic fluxes to be less than half of sun-leaf
fluxes on sunny days, whereas they equalled or even
exceeded sun-leaf fluxes on partly cloudy and cloudy
days. However, directly measured leaf-level CO2 assimilation rates corroborating these presumptions were missing, as well as the contributions of individual canopy
layers to the integrated net carbon exchange remained
unknown.
2. In days of predominantly direct radiation, the sunlit leaves
show an afternoon depression in photosynthetic rate
(Fig. 4), which is caused by substantial afternoon stomatal
closure (Fig. 5) associated and presumably caused by
higher vapour pressure deficits on those days and lower
leaf water potentials (Table 2). A similar afternoon
depression of photosynthesis was reported at the canopy
level of a peanut field (Pingintha et al. 2010). Recently, the
crucial contribution of GS to the midday depression of
photosynthesis under high D was confirmed in a study of
mist-spray effect in citrus (Hu et al. 2009). In addition,
sunlit leaves are often brightly illuminated during sunny
days, and they photosynthesize at saturating rates, leading, thus, to a dramatically lower LUE than that of shaded
leaves (Fig. 8b).
Based on our data, we rejected the following alternative
hypotheses.
1. Although there are reports of a stimulating effect of blue
light on the hydraulic conductance of leaf blades (Sellin
et al. 2011) and on the activation of photosynthetic processes (Kosvancova-Zitova et al. 2009), blue light enrichment in diffuse conditions did not cause a substantial
stimulation of photosynthesis through its effect on stomatal conductance (Fig. 5b). On the contrary, GS tightly correlated with the flux of diffuse fraction of the incident light
irrespective of sky conditions (Fig. 5c). As the stomata are
usually located on the abaxial leaf side, anisotropic diffuse
light, thus, forms an important environmental driver of GS
and A, particularly in spruce species (Leverenz & Jarvis
1979).
2. As revealed by fluorescence, there were no differences in
photo-inhibition and electron transport rates between
sunny and cloudy conditions (Fig. 6) nor in the afternoon
compared with the morning. Rapid degradation of D1
protein, decreased rate of plastoquinone reduction and
increased inactivation of PSII reaction centres have
already been identified as possible reasons for the decline
in electron transport on sunny days as the afternoon progresses (Guo et al. 2009). It is likely that efficient heat dissipation of absorbed light energy was sufficient under the
given environmental conditions to protect spruce needles
against photo-inhibitory damage (Spunda et al. 2005;
Stroch et al. 2010).
3. Although a high rate of photorespiration was identified as
an important mechanism contributing to photosynthetic
depression with a potentially photoprotective role against
excessive light energy (Kitao et al. 2006; Zhang, Meng &
Cao 2009), photorespiration rates were similar functions
of incident radiation in sunny and cloudy conditions
(Fig. 7). Specifically, in shoots from the 5th whorl, RL was
up to 40% higher during the afternoon of sunny days as
compared with the morning at equivalent irradiances
(Fig. 7a). Increases in RL rates are usually associated with
low CO2 concentration in the chloroplasts and increased
leaf temperature leading to decreases in the ratios between
Michaelis–Menten constants for carboxylation and oxygenation and between CO2 and HCO3) concentrations
and the inhibition of Rubisco activase activity (Muraoka
et al. 2000; Xu et al. 2009).
In accordance with findings in broadleaf (Still et al. 2009)
as well as coniferous forest (Chasmer et al. 2008), we found
that LUE is inversely proportional to incident irradiance at
both canopy (Fig. 3b) and leaf ⁄ whorl level (Fig. 8b) and that
it significantly increases as the diffuse radiation fraction
increases. It has been shown that increases in LUE with an
increasing fraction of diffuse radiation depend on canopy
structure and its openness (Alton et al. 2005), and on changes
in LUE in individual canopy layers. In our study, all canopy
layers displayed stimulation of LUE by diffuse light; however, the LUE stimulation in shade leaves seemed to be higher
compared with sun leaves (Fig. 8b).
Diffuse radiation, thus, has important direct effects on the
productivity and structure of vegetation (Roderick et al.
2001). On sunny days, most of the leaves in canopies with
high densities (LAI > 7 m2 m)2) are in deep shade, performing at marginal or negative carbon balances (Fig. 8).
Increased penetration and LUE under diffuse light conditions
may explain how forests with a high LAI can maintain a positive carbon balance, despite having an apparently high degree
of self-shading by individual shoots (Roderick et al. 2001).
Forest canopies are, thus, probably adapted to the most common light conditions that they receive. We can expect that if a
forest is growing at a site where conditions are predominantly
cloudy, they will have a high LAI. This view is supported
by the results of measurements over dense forest canopies
(Hollinger et al. 1994; Law et al. 2002; Urban et al. 2007).
Acknowledgements
This work is part of the research supported by grants 2B06068
(INTERVIRON), SP ⁄ 2d1 ⁄ 93 ⁄ 07 (CzechTerra) and IAA600870701
(GA AV). This article is a product of the CzechGlobe Centre that is
being developed within the OP RDI and co-financed from EU funds
and the State Budget of the Czech Republic (CZ.1Æ05 ⁄ 1Æ1Æ00 ⁄
02Æ0073). The experimental site Bı́lý Křı́ž is within the National infrastructure for carbon observations – CzeCOS ⁄ ICOS supported by
Ministry of Education CR (LM2010007).
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55
Vertical distribution of photosynthesis 55
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Received 6 June 2011; accepted 10 October 2011
Handling Editor: David Whitehead
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 26, 46–55