Download Diurnal patterns of chlorophyll a fluorescence and stomatal

 Springer-Verlag 1997
Trees (1997) 11: 363 – 369
O R I G I N A L A RT I C L E
Eduardo A. de Mattos ? Thorsten E. E. Grams
Erika Ball ? Augusto C. Franco ? Angela Haag-Kerwer
Britta Herzog ? Fabio R. Scarano ? Ulrich Lüttge
Diurnal patterns of chlorophyll a fluorescence and stomatal conductance
in species of two types of coastal tree vegetation in southeastern Brazil
Received: 29 April 1996 / Accepted: 14 November 1996
AbstractmDiurnal measurements of chlorophyll fluorescence parameters and stomatal conductance to water vapour
were carried out in five woody species and a bromeliad
from two coastal vegetation types in Brazil, the rock outcrop of Pão de Açúcar and the sand dunes of Macaé. The
environmental conditions of both study sites are characterized by high temperatures and light levels. The studied
species comprised C3 plants with different degrees of
stomatal closure during the day, overall daily stomatal
conductance and a plant with a typical CAM pattern. Plants
on Pão de Açúcar exhibited only a small decline in
potential quantum yield throughout the day. The nonphotochemical quenching and the approximate photosynthetic electron transport rates were maximal during the peak
of irradiance. In Macaé, light response curves of fluorescence parameters in the CAM-tree Clusia hilariana showed
a clear differentiation between phases III and IV of CAM.
In phase III, decarboxylation of organic acids probably
maintained high internal CO2 levels and there was only a
small decrease in photochemical quenching with saturating
light levels. In phase IV, the depletion of the organic acid
E.A. de Mattos
Departamento de Botânica, Universidade Federal de São Carlos,
caixa postal 676, São Carlos, SP, 13565-090, Brazil
T.E.E. Grams1 ? E. Ball ? A. Haag-Kerwer2 ? B. Herzog
U. Lüttge ( )
Institut für Botanik, Technische Hochschule Darmstadt,
Schnittspahnstrasse 3 – 5, D-64287 Darmstadt, Germany
A.C. Franco
Departamento de Botânica, Universidade de Brası́lia,
caixa postal 04631, Brası́lia, DF 70919-970, Brazil
F.R. Scarano
Departamento de Ecologia, Universidade Federal do Rio de Janeiro,
Rio de Janeiro, RJ 21941-970, Brazil
Present address:
GSF-Forschungszentrum für Umwelt und Gesundheit,
Expositionskammern, Ingolstaedter Landstrasse 1,
D-85764 Oberschleissheim, Germany
2 Botanisches Institut, Ruprecht-Karls-Universität,
Im Neuenheimer Feld 360, D-69120 Heidelberg, Germany
1
pool and low stomatal conductances resulted in much lower
levels of effective quantum yield and a substantial increase
in both 1-qP and non-photochemical quenching with increasing light levels. This behaviour during phase IV in the
CAM-tree C. hilariana was comparable to the performance
of the C3-Clusia C. aff parviflora at Pão de Açúcar. It is
seen that both the C3 species and the CAM tree occurring in
the two coastal communities effectively adjust their photochemical efficiency to environmental conditions and especially to diurnal variations of stress.
Key wordsmChlorophyll fluorescence ? Stomatal
conductance ? Rock outcrops ? Sand dune formations
Photosynthesis diurnal changes
?
Introduction
Evaluations of chlorophyll a fluorescence have been used
to describe and detect the effects of multiple environmental
stresses in plants of diverse habitats (Demmig-Adams et al.
1989, Lovelock et al. 1994; Larcher 1995), and as pointed
out by Ball et al. (1995) the functioning of photosystem II
(PS II) is one of the most sensitive indicators of environmental stress in plants. Plants occurring in environments of
high irradiance are more prone to photoinhibition, i.e., a
sustained decrease in the efficiency of photosynthetic energy conversion, when high quantum fluxes are concomitant with other kinds of stress, such as water deficit, nutrient
depletion or extremes of temperature (Demmig-Adams and
Adams 1992; Osmond 1994). Photoinhibition develops
when the capacity of the photosynthetic apparatus to utilize
the excitation energy reaching the photosynthetic reaction
centres or to avoid excess excitation is limited or reduced.
Over the course of a day, a reversible decline in PS II
efficiency is generally accompanied by an increase in nonradiative energy dissipation. This protects the photosystems
against irreversible damage. The larger fraction of energy
dissipated before it reaches the PS II centres is thought to be
mediated by an increase in the xanthophyll cycle-dependent
364
energy dissipation in the light-harvesting antennae (Demmig-Adams 1990).
In terms of comparative ecophysiology of tropical plants
it is important to investigate how species are able to cope
with the high light levels that are common in these habitats.
For most of the atlantic coast of southeastern Brazil the
presence of rock outcrops and sand dune formations is
characteristic. The plants occurring in these areas are often
subjected to high light levels and water shortage. In this
report, with focus on the trees of these vegetation types we
aim to address the following questions: (1) Are different
modes of photosynthesis (C3 or CAM) expressed among
trees ? (2) How are the species equipped to adjust their
stomatal conductance and photochemical efficiency to environmental conditions and especially potential diurnal
variations of stress ?
Materials and methods
Study site and plant material
Field studies were conducted on the rock outcrop of Pão de Açúcar
(22° 579S, 43° 599W) in the municipality of Rio de Janeiro and in the
Cabiúnas sand dune formation (22° 149S, 41° 349W) in the municipality of Macaé, approximately 200 km NE of the city of Rio de
Janeiro. The distribution of plants in both types of vegetation is
characterized by the presence of hemispherical clumps of different
sizes. In the case of Pão de Açúcar the size of the clumps is more or
less related to the inclination of the rock and some species (as
atmospheric bromeliads “sensu” Pittendrigh 1948) have the capacity
of establishment directly on bare rock. Clusia aff parviflora Saldanha
& Engl. (Clusiaceae) and Stilingia dichotoma Muell. Arg. (Euphorbiaceae) are the most abundant trees. Vriesia geniculata (Wawra) Wawra
(Bromeliaceae) is one of the most common tank bromeliads in this type
of habitat. It is found on bare rock of low inclination, on the border or
underneath the hemispherical clumps of trees like C. aff parviflora
(Meirelles et al. 1996a). Annual rainfall is about 1500 mm and mean
air temperature is 24 °C (Niemer 1979). Clusia hilariana Planchon &
Triana (Clusiaceae) is the dominant woody species in the sand dune
formation of Cabiúnas. This species forms hemispherical clumps with
other trees like Protium icicariba (DC) March and Andira legalis (Vell.
Conc.) Toledo (Henriques et al. 1986). In contrast to Pão de Açúcar the
climate is characterized by a dry period from June to August and a
mean annual rainfall of 1164 mm, whereas mean air temperature is
22.6 °C (Henriques et al. 1986).
obtained with a NiCr-Ni thermocouple pressed against the lower leaf
surface.
The chlorophyll a fluorescence measurements were performed with
a pulse-amplitude modulation fluorometer (PAM 2000, Walz, Effeltrich, Germany). The leaf was kept at a constant distance (ca. 1 cm) and
angle (60 °) to the fiber optics by the leaf clip that comes with the
instrument. Measurements of light intensity close to the leaf surface
were taken by a micro-quantum sensor calibrated against a LI-COR
quantum sensor (Neb., USA). For measurements of fluorescence
parameters in the light adapted state care was taken not to shade the
leaves by the fibre optics and the leaf clip. Readings of potential
quantum yield of photosystem II (Fv/Fm) were taken on a different set
of leaves following a 10 min dark period. This time interval was
checked to be sufficient to relax all fast components of total nonphotochemical quenching (qN) prior to the measurements. qN, photochemical quenching (qP) and the term 1-qP, which was used as a
measure of the reduction state of QA, the primary electron acceptor of
photosystem II (PSII), were calculated according to van Kooten and
Snel (1990). The pre-dawn measurements of maximum fluorescence
(Fm) and ground-level fluorescence (Fo) were used to calculate these
quenching parameters. The effective quantum yield of PSII (∆F/F9m)
was calculated as (F9m-F)/F9m, where F is fluorescence of the lightadapted sample and F9m is the maximum light-adapted fluorescence
when a saturating light pulse of 600 ms duration is superimposed to the
prevailing environmental light levels (Schreiber and Bilger 1993).
Approximate rates of photosynthetic electron transport (ETR) were
obtained as ∆F/F9m × PPFD and Stern-Volmer non-photochemical
quenching (NPQ) was calculated as NPQ = (Fm-F9m)/F9m. A correction
for changes in the temperature of the PAM-2000 that affected the
output of the measuring beam over the course of the day was applied to
the fluorescence data (Bilger et al. 1995). In addition to diurnal
measurements, light response curves were performed with readings
on individual leaves during different times of the day to examine the
potential effects of reduced gH2O in the middle of the day or different
phases of CAM on ∆F/F9m, qN and 1-qP.
Leaves adjacent to the ones that were used in the transpiration and
fluorescence measurements were collected for biochemical analyses at
dawn and dusk. The leaves were enclosed in plastic bags and
immediately stored on ice for 1 – 2 h, until it was possible to transport
the samples to the field station where the fresh weight of the leaves was
determined and the material was dried in a microwave oven for
subsequent measurements of dry weight, titratable protons, malate,
citrate and carbon isotope composition. Prior to organic acid determinations, the material was boiled in distilled water. Malate and citrate
were determined enzymatically according to Hohorst (1965) and
Möllering (1985), respectively. Composite samples of the dry leaf
material of exposed and shade plants were ground for carbon isotope
analysis and combusted in an oxygen bomb. Carbon isotope ratios were
determined as described by Osmond et al. (1975).
Results
Gas exchange, chlorophyll a fluorescence and biochemical analyses
Transpirational loss of water vapour from the leaves was determined
with a portable gas exchange system (CID, Vancouver, USA). Measurements were carried out with six mature leaves of three individuals
of each species studied. The CID system uses dew point sensors to
monitor changes in relative humidity (RH), an infra-red thermometer
to measure leaf temperature (Tleaf) and a thermistor to measure air
temperature (Tair). These parameters were used to calculate leaf
conductance to water vapour (gH2O). The high humidity levels prevented a reasonable estimate of gH2O during most of the night period.
At each sampling time the leaf remained clamped in the porometer
chamber for 1 – 2 min. Air temperature and relative humidity were
measured with a portable Cole-Parmer thermohygrometer (Niles,
USA) and photosynthetic photon flux density (PPFD) with a silicium
photodiode calibrated against a LI-COR (Neb., USA) quantum sensor.
In addition to the measurements of leaf temperature by the infra-red
thermometer of the porometer chamber, leaf temperatures were also
Diurnal patterns of environmental variables and stomatal
conductance
Figure 1 depicts environmental variables measured on the
rock outcrop of the Pão de Açúcar and in the sand dunes of
Macaé. There were differences in the pattern of PPFD
between the two localities. Because the plants studied are
located at the bottom of the Pão de Açúcar, the inselberg
itself affected the radiation level reaching the plants. Thus,
light intensity changed very abruptly in the early morning
and in the early afternoon on Pão de Açúcar (Fig. 1A), but
not in the sand dune site (Fig. 1B). Relative humidity
reached lower values in the sand dunes of Macaé. Although
air temperature was somewhat variable at Pão de Açúcar
365
Fig. 1mDaily courses of environmental conditions, photosynthetic
photon flux density (PPFD) at a
plane surface, relative air humidity (RH) and air temperature (Tair)
on 8 August 1994 at Pão de
Açúcar (A) and on 16 August
1994 at Macaé (B)
maximum values were comparable to those from Macaé,
where maximal values of about 32 °C occurred between
1000 to 1200 hours (Fig. 1).
The daily pattern of gH2O of all species studied at the two
sites was typical for the C3 photosynthetic pathway
(Fig. 1A – C and E – F), except in C. hilariana in the sand
dunes of Macaé which showed a clear CAM pattern with
the four typical CAM phases (Fig. 1D).
Maximum leaf temperatures (Tleaf) and leaf to air vapour
pressures (VPD) reached during the days of measurements
together with other leaf characteristics of the C3 species are
given in Table 1. At Pão de Açúcar gH2O of the plants
increased in the morning and declined again during the
middle of the day with some recovery later in the afternoon.
By contrast to the Pão de Açúcar site gH2O of the C3 plants
at Macaé was already high in the early morning, but again
there was a tendency of a decline of gH2O during the hotter
and drier times of the day. The differences in early morning
gH2O between the two sites may be due to the differences in
PPFD at this time of the day (Fig. 1). At Pão de Açúcar
maximum Tleaf and VPD varied to some extent among the
three plants studied, and this was correlated with the
minimum gH2O reached at the middle of the day, i.e.
between shortly before 1200 and 1300 hours. At Macaé
maximum VPD was more similar for the two plants and
minimum gH2O was identical (Table 1). The three day-time
phases of the CAM-type pattern of gH2O, i. e. some stomatal
opening in the morning and in the afternoon and stomatal
Table 1mSome characteristics of leaves with C3-photosynthesis-type
pattern of gH2O studied at the two sites. Tleaf-max (°C) and VPD-max
(kPa ? MPa–1) are the maximal leaf temperatures and leaf to air vapour
pressure differences, respectively, reached during the day; gH2O-min
(mmol ? m–2 ? s–1) is the minimal leaf conductance to water vapour
attained during times of maximal Tleaf and VPD; gH2O-int (mol-
closure in the middle of the day (Osmond 1978), in C.
hilariana can be better demonstrated when additional data
from 15 August are plotted together with the measurements
carried out on 16 August, even though the leaf to air VPD
of the previous day was clearly lower (Fig. 2D). During the
phase III stomatal closure in the middle of the day leaf
temperatures reached 38 °C (not shown).
Leaf characteristics and organic acid levels
None of the five species with a C3-photosynthesis type
pattern of gH2O (Fig. 2A – C, E – F; Table 1) showed any
significant day-night oscillations of organic acids (malate
and citrate), nor any substantial changes in the amount of
titratable protons (data not shown). It is interesting to note,
however, that for C. aff parviflora the citrate levels were
relatively high, i.e. about 90 mmol m – 2, but without
significant variation in dawn/dusk levels, and malate levels
were below 10 mmol m – 2 as in the other four species (data
not shown). The carbon isotope signatures of all the five
species were typical of the C3 photosynthetic pathway.
Conversely, C. hilariana showed the pronounced day/
night oscillations of organic acid levels, which are characteristic of CAM (Table 2). Both levels of malate and
citrate participated in these oscillations as commonly observed in CAM species of the genus Clusia (Franco et al.
1992; Haag-Kerwer et al. 1992; Lüttge 1988). The carbon
isotope ratio of the dried leaf material was – 14.36 , i.e.
%
m–2 ? day) is the integrated stomatal conductance for the daily courses
given in Fig. 1; δ13C (‰) is carbon isotope ratio of dried leaf material;
FW/A (g ? m–2) is the fresh weight to area ratio. Numbers in brackets
for VPD-max, gH2O-min and FW/A are the standard deviations for n = 6
leaves
Sites and species
Tleaf-max
VPD-max
gH2O-min
gH2O-int
δ13C
FW/A
Pao de Acucar
C. parviflora
S. dichotoma
V. geniculata
30.7
36.3
39.1
24 (4)
39 (4)
49 (6)
138 (38)
82 (59)
31 (20)
3371
2942
2049
–30.12
–26.89
–25.72
535 (15)
490 (15)
590 (70)
Macaé
P. icicariba
A. legalis
40.7
42.5
49 (3)
56 (9)
160 (28)
161 (14)
7046
6040
–29.76
–26.27
238 ( 7)
278 (20)
366
Fig. 2mDiurnal changes in leaf
conductance to water vapour
(gH2O) and leaf to air vapour
pressure difference (VPD) for the
studied species in both localities
and on the 2 days presented in
Fig. 1. For C. hilariana (D)
closed symbols give additional
data obtained on 15 August 1994.
Vertical bars indicate standard
deviations
much less negative than for the other five species (Table 1)
and also typical of CAM. These data confirm the conclusion drawn from the daily pattern of gH2O that C. hilariana
is a CAM performing plant in the sand dunes of Macaé. Its
degree of succulence, i.e. FW/A ratio was also much higher
than for the other five species; with 1390
85 g m– 2 (SD,
n = 6) FW/A in C. hilariana was about 2.5 fold the value
obtained for the other Clusia species studied, the C3 species
C. aff parviflora at Pão de Açúcar, showing the increased
succulence typical of CAM leaves.
+
Diurnal course of chlorophyll a fluorescence in the plants
on Pão de Açúcar
Plants on the Pão de Açúcar exhibited only a small decline
of the Fv/Fm ratio throughout the day (Fig. 3). The ratio of
variable to maximal fluorescence (Fv/Fm) remained fairly
constant, around 0.80, all day long in C. aff parviflora
whilst S. dichotoma showed slightly lower mean values, i.e.
Table 2mDawn and dusk analyses of malate and citrate (mmol ? m–2)
for C. hilariana at Macaé. The values are presented as average of six
leaves with standard deviations in brackets
Dawn
Dusk
Dawn minus dusk
Malate
Citrate
286 (40)
45 (12)
241 (30)
164 (10)
68 (20)
96 (16)
0.78, and in V. geniculata there was a decrease from 0.80 to
about 0.73 at midday. Although Clusia aff parviflora was
exposed to slightly lower mean irradiance levels during the
middle of the day, it presented a similar reduction in ∆F/F9m
as observed in V. geniculata (lowest values around 0.20). In
contrast, leaves of S. dichotoma did not show values of
∆F/F9m below 0.26. These differences were enough to cause
large differences in the photosynthetic electron transport
rates (ETR) between the three species. Thus, S. dichotoma
showed the highest rates of photosynthetic activity as given
by ETR (around 660
42 µmol m – 2 s – 1). In contrast,
maximum ETR were around 350 127 and 400 68 µmol
m – 2 s – 1 for C. aff parviflora and V. geniculata, respectively.
With regard to the capacity for energy dissipation, the
highest values of both total non-photochemical quenching
(qN) and Stern-Volmer equation (NPQ) were found in
Clusia aff parviflora (Fig. 3). The lowest capacity for
energy dissipation in the pigment bed of PSII was measured
on V. geniculata, (NPQ = 3.1
1.4), but only slightly
lower than for S. dichotoma (NPQ = 3.4
1.0). It is
interesting to note that the differences were slightly higher
if they were based on NPQ instead of qN. In both Clusia aff
parviflora and S. dichotoma qN started to increase faster
than NPQ during the morning. However, this was not the
case for V. geniculata. Maximum average levels of the
reduction state of the primary electron acceptor, QA, estimated as 1-qP, were 0.52
0.22 in C. aff parviflora,
0.40
0.01 in S. dichotoma and 0.56
0.23 in V.
geniculata.
+
+
+
+
+
+
+
+
367
Light response curves of fluorescence parameters of the C3Clusia and the CAM-Clusia
Figure 4 depicts the light response curves for some of the
chlorophyll a fluorescence parameters in the C3-Clusia C.
aff parviflora at Pão de Açúcar and the CAM-Clusia C.
hilariana at Macaé. Light response curves for chlorophyll a
fluorescence parameters of C. hilariana during phases III
and IV of CAM were substantially different (Fig. 4B). A
more pronounced drop of ∆F/F9m with increasing PPFD
was observed in phase IV in comparison to phase III. At a
PPFD of around 1600 µmol m – 2 s – 1 the value observed
during phase IV was approximately 4-fold lower than the
lowest value measured in phase III. In contrast, qN values
were substantially higher in phase IV. In response to
increasing light levels qN in phase IV rapidly approached
saturation values of about 0.90 at PPFD levels around
750 µmol m – 2 s – 1. The maximum value of qN in phase
III was about 0.50 at the highest PPFD level (about
1600 µmol m – 2 s – 1). High light intensities resulted in
only a small increase in 1-qP in phase III (maximal average
values around 0.30). However, 1-qP began to increase
clearly at PPFD above 250 µmol m–2 s – 1 and reached the
highest value (0.80) at about 2100 µmol m – 2 s – 1 in phase
IV. As known from studies with other CAM plants (Winter
and Demmig 1987; Guralnick et al. 1992) including other
CAM species of Clusia (Winter et al. 1992; Franco et al.
1996) these differences between CAM phases are due to the
fact that in phase III photosynthesis occurs at high internal
CO2 concentrations built up behind closed stomata due to
decarboxylation of organic acids while in phase IV CO2 is
obtained from the atmosphere via open stomata as in C3photosynthesis. Indeed, the light response curves of fluorescence parameters obtained from the C3-Clusia C. parviflora between 1000 – 1300 hours (Fig. 4A) when gH2O was
Fig. 3mDiurnal time courses of photosynthetic photon flux density at
the leaf level (PPFD), potential quantum yield (Fv/Fm), effective
quantum yield (∆F/F9m), apparent electron transport rate (ETR), the
reduction state of the primary electron acceptor of photosystem II
(1-qp), total non-photochemical quenching (qN) and Stern-Volmer nonphotochemical quenching (NPQ) from sun leaves of C. parviflora,
S. dichotoma and V. geniculata at Pão de Açúcar on 8 August 1994.
Vertical bars indicate standard deviations
high and almost constant (Fig. 2A) are much more closely
comparable to those of phase IV than to those of phase III
in C. hilariana.
Discussion
There were clear differences in the diurnal patterns of gH2O
among the species in the two coastal habitats. Their
performance comprised C3 patterns with different values
of integrated stomatal conductance, gH2O-int, over the day
and with gH2O declining by various degrees towards midday
and a typical CAM pattern (Fig. 2; Tables 1, 2). In the C3
species both at Pão de Açúcar and at Macaé the carbon
isotope ratio was in tendency correlated with the degree of
stomatal aperture, i.e., those species showing lower values
of daily integrated gH2O also showed lower 13C discrimination (less negative δ13C values; Table 1). Less negative
values for the carbon isotope ratios would be indicative of
higher water use efficiency (WUE) of carbon assimilation
or at least may indicate a lower operational range for the
ratio between CO2 concentration at sites of evaporation
within substomatal cavities to the CO2 concentration in
bulk air (Farquhar et al. 1989).
368
Fig. 4mLight response curves of effective quantum yield (∆F/F9m),
total non-photochemical quenching (qN) and the reduction state of the
primary electron acceptor of photosystem II (1-qP) for C. parviflora (A)
at Pão de Açúcar and C. hilariana (B) at Macaé. For C. parviflora open
and closed symbols represent two separate measurements on two
different leaves taken between 1000 and 1300 hours and the line
drawn indicates the average; for C. hilariana open symbols are
measurements during phase III of CAM (1400 – 1500 hours) and closed
symbols are measurements during phase IV of CAM
(1700 – 1800 hours) performed on one leaf. Squares are ∆F/F9m, circles
qN and triangles 1-qP
Differences in the degree of control of gH2O between the
studied species were observed after some rainy days.
Hence, regardless of the differences in substrate between
the granitic outcrop and the sand dune vegetations, we
cannot explain the different patterns of gH2O by the establishment of a pronounced soil water deficit. However, leaf
temperatures and leaf to air VPD reached fairly high values
during the middle of the day. Several investigations have
shown depression of leaf gas exchange in plants growing in
hot and arid environments, during periods when leaf temperatures and leaf to air VPD are greatest (Mooney et al.
1975; Tenhunen et al. 1981; Roessler and Monson 1985).
In this study, in C3 plants growing on the granitic
outcrop of Pão de Açúcar, we observed a close relationship
between ETR and NPQ, which could keep the reduction
state of QA on the safe side even during some midday
depression of gH2O, as evidenced by high Fv/Fm values
during the day. Demmig-Adams et al. (1989) in water
stressed plants of Arbutus unedo, observed marked reductions in Fv/Fm concomitantly with increased levels of non
radiative energy dissipation during midday depression of
gH2O and net CO2 uptake. However, this decline was
reversible and at the end of the day Fv/Fm showed a
pronounced recovery reaching the values prior to the midday depression. These results suggests that the controlled
utilization or dissipation of a high excitation pressure
within PS II, which can lead to a high degree of reduction
state of QA, the primary electron acceptor of PS II, may
prevent irreversible damage to the photosynthetic apparatus
by high irradiance.
In CAM plants, as observed by Adams et al. (1989) in
three species of cacti in northern Venezuela and Franco et al.
(1996) in exposed leaves of seedlings of C. hilariana in
natural conditions, the phase IV of CAM seems more prone
to sustained decreases in Fv/Fm. Some authors have postulated that nocturnal accumulation of organic acids in CAM
plants may alleviate photoinhibition (Franco et al. 1992;
Haag-Kerver et al. 1992 Maxwell et al. 1992). The light
response curves presented here showed a clear differentiation between phase III and phase IV of CAM in C.
hilariana, when higher 1-qP and qN were observed in this
latter phase. It is believed that as the organic acid decarboxylation during phase III raises the internal CO2 concentration, a higher photosynthetic electron use should help
to maintain a low reduction state of QA even at high PPFD
levels. During phase IV, lower values for ∆F/F9m and the
increase in qN and 1-qP at high PPFD levels in C. hilariana
may be explained by the depletion of the organic acid pool.
The capacity to ordered use and/or safe dissipation of
excitation energy may be limited at high PPFD approaching
full sunlight when 1-qP values greater than 0.50 were
measured for some of the studied species. It is interesting
to note that the small declines observed in photochemical
efficiency occurred without soil water deficit. Both vegetation types are probably more subjected to some limitation
of water availability mainly during the hot summers that are
characteristic of this part of Brazil. Over the summer, even
1 or 2 weeks without rain are enough to elicit leaf rolling
and dehydration of small clumps of desiccation tolerant
species on rock outcrops of southeastern Brazil (Meirelles
et al. 1996b).
In conclusion, it seems clear from this study that both
the C3 species and the CAM plants occurring in these two
coastal communities are able to effectively adjust their
photochemical efficiency to environmental conditions. In
wet soils these plants are apparently not prone to an
irreversible damage of their photosynthetic apparatus induced by an intense photoinhibitory situation. However,
these habitats are frequently subjected to high irradiance
levels concomitantly with other environmental stress such
as water deficits, high temperature and salinity. Further
studies are necessary to address these questions.
AcknowledgementsmWe thanks Escola de Comando e Estado Maior
do Exército for providing us with logistic support in the Pão de Açúcar
rock outcrop. We would also like to thank Prof. Francisco de Assis
Esteves for providing us with accommodation and scientific facilities
in the city of Macaé, Rio de Janeiro, Brazil, Prof. Hubert Ziegler for
the carbon isotope determinations and Walz GmbH for lending us the
PAM 2000. This investigation was supported by the program PROBAL
from Fundacão Coordenção de Aperfeiçoamento de Pessoal de Nı́vel
Superior, Brazil and Deutscher Akademischer Austauschdienst, Germany, and by the Deutsche Forschungsgemeinschaft, Germany.
369
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