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First published online May 2, 2008
Journal of Experimental Biology 211, 1579-1586 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016345
Photosynthetic response of the Mediterranean zooxanthellate coral Cladocora caespitosa to the natural range of light and temperature
1 Centre Scientifique de Monaco, MC-98000, Principality of Monaco
2 Observatoire Océanologique de Villefranche, BP 28, 06230
Villefranche-sur-Mer, France
* Author for correspondence at present address: Marine Biology and Ecology Research Centre, PL4 8AA Plymouth, UK (e-mail: riccardo.rodolfo-metalpa{at}plymouth.ac.uk)
Accepted 20 March 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Key words: photoacclimation, photosynthesis, light, temperature, Cladocora caespitosa, temperate coral
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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; Muller-Parker and Davy,
2001). In addition, temperate corals are exposed to marked
seasonal variability in the main environmental parameters
(Muller-Parker and Davy,
2001), including daily integrated irradiance fluxes that can be
4–7 times higher in summer than in winter. Coral photoacclimation has
mainly been studied in tropical species, which adapt to the light level by
changing zooxanthellae density and/or pigment concentration, in order to
maintain optimal rates of photosynthesis
(Falkowski and Dubinsky, 1981;
Iglesias-Prieto and Trench,
1997). They also develop some protection against damages of excess
light (Hoegh-Guldberg and Jones,
1999; Furla et al.,
2005).
In contrast to tropical species, the response to a change in light
intensity of temperate corals has received little attention. Such corals are
different from their tropical counterparts, however, because they display
greater plasticity in their association with symbionts
(Szmant-Froelich and Pilson,
1984; Muller-Parker and Davy,
2001). Kevin and Hudson (Kevin
and Hudson, 1979) were among the first to assess the effect of
light (12 µmol m–2 s–1) or dark
conditions on the zooxanthellae density and photosynthesis of the temperate
coral Plesiastrea urvillei (i.e. P. versipora). This coral
retained zooxanthellae in the dark for more than 48 days and oxygen production
was well adapted to the low light levels received by this species. The
photosynthetic response of the ahermatypic temperate coral, Astrangia
danae, to a change in temperature and light was then studied
(Jacques and Pilson, 1980;
Jacques et al., 1983). Corals
were acclimated to 16 µmol m–2 s–1 and
photosynthesis was measured at different light levels and seawater
temperatures. It was shown that oxygen production increased with temperature,
as well as with light up to 120 µmol m–2
s–1. The dependency of photosynthesis on temperature was
later confirmed in P. versipora
(Howe and Marshall, 2001;
Davy et al., 2006); however, in
this species an impairment of photosynthesis could occur during heat-stress,
temperatures of 28°C inducing a rapid decrease in the photosynthetic
efficiency (Jones et al.,
2000).
Among the few symbiotic corals inhabiting the Mediterranean, Cladocora
caespitosa (Linnaeus 1767) is the most important constructional species,
and can form structures comparable to tropical reefs
(Schuhmacher and Zibrowius,
1985; Kru
ic and
Poar-Domac, 2003). Large fossil formations dating from the
late Pleistocene/early Holocene have been found all over the Mediterranean
(Zibrowius, 1980;
Aguirre and Jiménez,
1997; Peirano et al.,
2004), and some large banks are still found in the Ligurian
(Morri et al., 1994), Adriatic
(Kruic and Poar-Domac,
2003) and Aegean seas
(Kühlmann, 1996). This
coral harbours symbiotic dinoflagellates in its tissue and lives at depths
from 3 to 40 m, on hard or soft bottoms, and often in turbid environments
(Peirano et al., 2005). Growth
irradiance levels and temperatures measured in the Adriatic Sea ranged from
ca. 20–250 µmol m–2 s–1 and from 12
to 24°C, respectively (Schiller,
1993). Despite its importance as one of the rare reef builders in
the Mediterranean Sea, only two studies have measured the photosynthetic
response of this coral to a change in light and/or temperature
(Schiller, 1993;
Rodolfo-Metalpa et al., 2008),
or its response to abnormally high seawater temperatures
(Rodolfo-Metalpa et al.,
2006a; Rodolfo-Metalpa et al.,
2006b). Schiller measured rates of photosynthesis at temperatures
ranging from 9 to 21°C (Schiller,
1993), and at low temperatures high feeding levels increased
zooxanthellae density and chlorophyll (chl) content
(Rodolfo-Metalpa et al.,
2008).
The first aim of this paper was to investigate the photoacclimation
capacity of C. caespitosa to different light levels at the
non-stressing temperature of 18°C. For this purpose, corals were cultured
at three light levels (30, 80 and 250 µmol m–2
s–1), corresponding to the range of irradiance previously
described for this species (Schiller
1993; Peirano et al.,
1999). We then examined the acclimation capacity of this
Mediterranean symbiosis (both in hospite and on freshly isolated
zooxanthellae) to an eightfold change in its growth irradiance. We also tested
the photosynthetic response of C. caespitosa to two extreme
situations of light and temperature, corresponding to `winter' (14°C and
30 µmol m–2 s–1) and `summer' (23°C
and 250 µmol m–2 s–1) conditions
(Schiller, 1993), to assess
its acclimation to a changing environment. The second aim of this work was to
evaluate the relationship between oxygen respirometry, which measures the net
photosynthetic gas exchange over the whole coral, and fluorometry, which
assesses gross photosynthetic electron transport from a small coral area.
While respirometry has been extensively used and investigated, pulse amplitude
modulated (PAM) fluorometry is a relatively new method of non-intrusive in
situ measurement of photosynthetic parameters of the algal symbionts
(Beer et al., 1998a;
Beer et al., 1998b;
Ralph et al., 1999). The
comparison between the results of these two techniques on temperate corals is
critical in order to validate the use of fluorescence as an accurate
measurement of photosynthesis on symbiotic corals. However, to our knowledge,
only one study has so far investigated this topic for a tropical species
(Hoogenboom et al., 2006).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Temperature and light conditions in the tanks were then gradually changed
(by 1°C and 20–30 µmol m–2 s–1
per day, respectively) giving a total of five different treatments (two tanks
per treatment). In the first three treatments (respectively called
18°C/30; 18°C/80; 18°C/250), samples were maintained at 18°C
and at 30, 80 or 250 µmol m–2 s–1
(photoperiod: 12 h:12 h dark:light), in order to study the photoacclimation of
this coral maintained at a constant temperature. Irradiance levels were chosen
from the literature (Schiller
1993; Peirano et al.,
1999) and our in situ observations (10–300 µmol
m–2 s–1 throughout the year). In the other
two treatments, samples were maintained either at 14°C and 30 µmol
m–2 s–1 (called 14°C/30) or at 23°C
and 250 µmol m–2 s–1 (called
23°C/250), in order to study the concurrent effect of light and
temperature on the photosynthetic response of the corals, mimicking winter
(14°C/30) and summer (23°C/250) conditions in the Ligurian Sea
(Schiller, 1993;
Peirano et al., 1999). In
these treatments, photoperiods were 14 h:10 h dark:light and 8 h:14 h
dark:light for winter and summer conditions, respectively. Corals were
cultured under these five conditions for 4 weeks (the acclimation period)
before measurements (described below) were performed. Preliminary experiments
showed that this incubation length is sufficient for acclimation of
photosynthesis and growth rates to new light and temperature conditions
(Rodolfo-Metalpa et al.,
2006b). During the whole incubation, corals were fed once a week
with Artemia salina nauplii; feeding took place 3 days before
recording any measurements of photosynthesis.
Chlorophyll and zooxanthellae measurements
Chlorophyll and zooxanthellae measurements were performed on five single
polyps collected in each tank (N=10 for each treatment). Samples were
frozen at –80°C and processed as described
(Rodolfo-Metalpa et al.,
2006a). Chl a and c2 were determined
according to the equations of Jeffrey and Humphrey
(Jeffrey and Humphrey, 1975)
using a spectrophotometer, and zooxanthellae were counted (number of
fields=10, total counted >300 cells) using an inverse microscope (Leica,
Wetzlar, Germany) and an improved version of the Histolab 5.2.3 image analysis
software (Microvision, Every, France). Results were normalized to polyp
surface area (Rodolfo-Metalpa et al.,
2006a).
Fluorescence measurements and oxygen production in polyps
Pulse amplitude modulated (PAM) fluorometry assesses gross photosynthetic
electron transport from a small area of the coral surface whereas oxygen
respirometry measures gas exchange over the entire coral surface. With both
techniques, the same light intensities were applied to the same three polyps
randomly sampled in each tank (N=6 for each treatment) in order to
establish the relationship between the gross photosynthesis (Pg) normalized to
chl a and the relative electron transport rate (rETR)
(Hoogenboom et al., 2006).
This relationship was then fitted using a linear and a double exponential
saturating function (Platt et al.,
1980).
For measurements of rates of net photosynthesis (Pn) versus
irradiance (E) and dark respiration (R), a random draw of
sampling between tanks was used. Each polyp was placed in a closed
thermostated Perspex chamber filled with 0.45 µm-filtered seawater
continuously stirred with a stirring bar, and oxygen was measured using
Clark-type electrodes connected to a Strathkelvin 928 oxygen meter and a
computer. Electrodes were calibrated against O2-free (using sodium
dithionite) and air-saturated (100% O2) seawater. The 100%
O2 concentration was calculated according to the experimental
temperature and salinity values (table on:
http://www.unisense.com/Default.aspx?ID=117).
Polyps were allowed to acclimate for at least 15 min, and then subjected to
the following light intensities: 0, 14, 44, 86, 158, 363, 493 and 739 µmol
m–2 s–1, as measured using a LiCor LI-192
underwater quantum sensor. Since light exposure enhanced dark respiration in
corals (Edmunds and Davies,
1988), this effect was measured in a preliminary experiment.
Respiration rate increased when corals were exposed to increased light
intensity from 14 to 170 µmol m–2 s–1,
and then remained stable at higher PAR (photosynthetically active radiation).
Therefore, dark respiration in this experiment was measured at the end of the
158 µmol m–2 s–1 light intensity. Gross
photosynthesis (Pg) was then calculated by summing the rates of R and
Pn and plotted versus irradiance [P/E curves, formerly P/I
(Falkowski and Raven, 1997)].
All measurements were normalized to chl a content [µg
O2 (µg chl a)–1 h–1]
or to surface area (µg O2 cm–2
h–1). P/E curves were fitted with Pro Fit, Quantum Soft
(Vetikon am See, Switzerland) software using the function of Harrison and
Platt (Harrison and Platt,
1986) as described by Ralph and Gademann
(Ralph and Gademann, 2005),
for the determination of the maximum Pg rate (Pgmax), the
saturation irradiance (Ek), and the initial slope of the
curve (
).
The relative electron transport rate (rETR) was assessed using a Diving PAM
(Walz GmbH, Effeltrich, Germany), on the same corals as those used for the
photosynthetic rate measurements, by two different methods. The first method
applied a saturation pulse to the corals incubated in the same chambers as
those used for the oxygen photosynthetic measurements after 15 min of
acclimation to each light level, by which time the photosystem was considered
to be in steady state. The rETR was then calculated according to Ralph and
Gademann (Ralph and Gademann,
2005) and the ETR/irradiance curves hereafter obtained will be
called steady-state light curves (SLC). The second method assessed rETR using
the rapid light curve (RLC) function of the PAM fluorometer, followed by 5 min
relaxation in the dark (RLC+Rec), for corals sampled in the different
conditions. 5–10 s after the coral was placed in the dark
(Ralph and Gademann, 2005) the
effective quantum yield (
F/F'm) and
rETR were measured after exposure for 10 s to the same eight light intensities
as those used for oxygen measurements (0, 14, 44, 86, 158, 363, 493 and 739
µmol m–2 s–1). At the end of the last
light level of the RLC, polyps remained in complete darkness and
F/F'm was determined after 30 s, 1,
2 and 5 min. Non-photochemical quenching (NPQ), which is a measure of the
thermal dissipation of the excess absorbed excitation energy, was also
calculated during the RLC and relaxation periods. The kinetics of relaxation
of NPQ allows the discrimination of the processes that led to the dissipation
of excess absorbed light. Two main components of NPQ can be distinguished: (i)
energy-dependent quenching (qE), which is a protective mechanism related to
the build-up of the transthylakoid pH gradient, and which quickly relaxes
after light exposure, and (ii) photoinhibitory quenching (qI), which results
from damage to photosystems and relaxes much slowly [>10 min to several
hours (Krause, 1988;
Ralph and Gademann, 2005)]
because it corresponds to a long-term photodamage. In non-stressful culture
conditions, qE is expected to be the main source of NPQ and thus NPQ would
dissipate quickly following exposure to a saturating light pulse, such as
during the RLC. In contrast, if the coral experiences photodamage (e.g. excess
light and temperature), NPQ relaxes much more slowly, even under dark
conditions, indicating the temporary limited ability of the coral to
recover.
Extraction of zooxanthellae and fluorescence measurements
rETR was also measured for the three light treatments (18°C/30;
18°C/80; 18°C/250) on freshly isolated zooxanthellae (FIZ) from three
nubbins randomly sampled from each tank (N=6 for each treatment).
This experiment was performed in order to compare the response of FIZ with
in hospite zooxanthellae and assess if the animal pigments offer some
protection to light. Zooxanthellae were detached from the skeleton by a gentle
flow of air and re-suspended into 50 ml of 0.45 µm-filtered seawater. They
were allowed to rest (under the treatment conditions) for 30 min before taking
measurements. RLCs were performed by placing the 8 mm optic fibre in direct
contact with a 10 ml glass chamber containing FIZ in suspension. 10 s later,
FIZ were placed in the dark, F/F'm
and rETR were measured by exposure for 10 s periods, to eight light
intensities between 0 and 1064 µmol m–2
s–1. RLCs were fitted as described for the P/E curves (see
above). Such protocol gave very good initial
F/F'm values (0.58±0.05,
0.57±0.009 and 0.65±0.09 for the three light levels), suggesting
that the zooxanthellae had not suffered from the extraction procedure.
Statistical analysis
All data were tested for assumptions of normality and homoscedasticity by
the Cochran test and were log-transformed when required. Data corresponding to
each treatment were pooled since there was no significant difference between
replicated tanks (P>0.05). One-way ANOVAs were used to test the
effect of light (18°C/30; 18°C/80; 18°C/250) or to compare the two
light and temperature treatments (14°C/30; 23°C/250). When ANOVAs
showed significant differences, Tukey's honest significant difference test
(HSD) attributed differences to specific factors and their interaction only.
Statistical analyses were performed using STATISTICA® software (StatSoft,
Tulsa, USA). Significant differences were assessed at P<0.05. All
data were expressed as mean ± standard error (s.e.m.).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Photosynthesis measured using fluorometry
A plateau was not reached in any of the RLCs obtained with the whole polyp
(Fig. 2B), therefore only
values measured at the end of the RLC (rETRmax) were compared. At
the constant temperature of 18°C, significant differences were obtained
between light levels (ANOVA, P<0.05). rETRmax was
indeed significantly higher for corals maintained at 250 µmol
m–2 s–1
(Fig. 2B; HSD test:
30=80<250). These corals also showed the smallest increase in fluorescence
(F) (Fig. 3B),
corresponding to the largest decrease in maximum fluorescence yield
(F'm) and increase in NPQ
(Fig. 3C,D). After relaxation,
NPQ rapidly decreased by up to 65% of its maximal value, showing that most of
quenching was energy-dependent (qE). Conversely, corals maintained at 30
µmol m–2 s–1 showed the highest increase
in fluorescence yield (F), reflecting the closure of photosystems
(photochemical quenching) but a reduced decline in
F'm, resulting in a limited development of NPQ
(Fig. 3C,D). NPQ did not
decrease during the whole relaxation period, suggesting that a significant
fraction of the quenching was due to photoinhibitory quenching (qI) and not to
energy dependent NPQ (qE). Results of RLCs measured at 14°C/30 and
23°C/250 are comparable to those obtained for the effect of light alone
(30 and 250 µmol m–2 s–1).
|
RLCs performed on zooxanthellae freshly isolated from corals and maintained at the three light levels (Fig. 4) showed that the plateau (ETRmax=95.9±4.3) was reached at an irradiance above 1000 µmol m–2 s–1, with corresponding Ek values equal to 346±13 µmol m–2 s–1 for the three light treatments. Relaxation curves were in good agreement with those obtained for the RLCs performed on the entire association (results not shown).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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), but the range of light investigated was smaller
(50–120 µmol m–2 s–1; 7-week
acclimation). In the two experiments cited above zooxanthellae densities were
similar to previous findings reported for the same species collected in
situ [2.36±0.4x106 zoox cm–2 and
4.9 µg cm–2, recalculated using a mean polyp surface of
0.7 cm2 (Schiller,
1993)]. Other temperate species such as Plesiastrea
versipora [0–10x106 zoox cm–2
(see Kevin and Hudson, 1979;
Howe and Marshall, 2001)] and
Astrangia danae [0–7x106 zoox
cm–2 (see Szmant-Froelich
and Pilson, 1980)] have a larger range of zooxanthellae density
per surface area, perhaps due to the facultative symbiosis. Temperate sea
anemones also have a stable symbiosis, since their zooxanthellae persist at
high densities when exposed to a pronounced light gradient or to the dark for
several weeks (Muller-Parker and Davy,
2001; Verde and McCloskey,
2002). The lack of change in symbiont density and chl content
might have been for several reasons. (1) Lack of any photoacclimation with
respect to pigment and cell densities when light is the only parameter
changing. (2) A lower range of light intensities compared to that experienced
by the corals in situ. In this experiment we used the upper light
values reported for this coral (Schiller,
1993; Peirano et al.,
1999), but since C. caespitosa can be distributed both in
turbid as well as in sun washed habitats, it might experience higher light
levels. (3) The acclimation period (4 weeks), which might be too short to
allow a change in algal density since temperate symbioses seem to be
particularly resilient to changes in their environment. This hypothesis seems
unlikely, however, since a change in temperature induces rapid changes in
zooxanthellae density and pigment concentration
(Rodolfo-Metalpa et al., 2008)
(and this study). In contrast to this temperate coral, most tropical corals
quickly photoacclimate (within 1–2 weeks), presenting lower contents of
chl and/or zooxanthellae in organisms adapted to high light (e.g.
Chalker, 1981;
Falkowski and Dubinsky, 1981;
Iglesias-Prieto and Trench,
1994). Our results, however, confirm that symbiosis is affected by
a change in temperature, since a significant increase in symbiont and total
pigment concentration was observed in the low light/low temperature condition
of this study, as well as in the low temperature treatments (both low and high
light) in Rodolfo-Metalpa et al.
(Rodolfo-Metalpa et al.,
2008). In both studies, the corals were fed. This
temperature-dependency of algal growth needs to be further investigated, since
this trend was not observed in other tropical and temperate symbioses, in
which algal concentrations either remained stable between 13 and 20°C [in
Anthopleura elegantissima
(Muller-Parker et al., 2007)]
or increased with temperature increase [in P. versipora
(Howe and Marshall,
2001)].
This study, however, demonstrates that the coral symbiosis of C.
caespitosa photoacclimates rapidly to a wide range of irradiances by
changing the rate of respiration and photosynthesis, and that the combination
with both low and high temperatures did not change the pattern of
photoacclimation (at least in the range of temperature investigated). Light
did indeed affect the rates of photosynthesis, since Pgmax and
Ek (normalized either to surface area or to mg chl
a) were always higher in corals maintained at 250 than at 30 µmol
m–2 s–1. This is considered an
`optimization' process, since Ek (subsaturation irradiance) is one
of the most reliable indicators of photoacclimation and reflects changes in
the effective absorption cross section of the photosystems and in the minimal
turnover time for carbon reduction (Kolber
and Falkowski, 1993). Pgmax also reflects the number of
PSUs, i.e. photosystem units, an increase in Pgmax corresponding to
an increase in PSUs. C. caespitosa therefore rapidly acclimates to
high photon flux, and this mechanism is further highlighted by the results
obtained with RLCs of corals maintained at 250 µmol m–2
s–1, which presented different evolutions of the F,
F'm and NPQ than the corals maintained at the lowest
light levels. The relative constant fluorescence yield in the 250 µmol
m–2 s–1 corals showed that there were almost
no, or few, sink limitations to the photochemical pathway, even under very
high irradiances, and that the sink could cope with the full range of light
intensities (Ralph and Gademann,
2005). The decrease in F'm (by
30–40%) was linked to the development of NPQ, which dissipates the
incoming energy and prevents damage to the photochemical pathway. The
light–dark relaxation kinetics showed that the photosystem recovered
well from the light exposure since most of the NPQ
(Fig. 3C), corresponding to the
removal of the energy dependent NPQ (qE), relaxed in less than 5 min, leaving
only ca. 20% or less associated to the inhibition quenching (qI). This ability
of NPQ to return to low values is an additional indicator of the tolerance of
the zooxanthellae of C. caespitosa to high light, and explains the
increase in Ek observed in the photosynthetic curves.
However, the quantum yield in these corals remained low relative to first
values. Conversely, corals maintained at 30 µmol m–2
s–1 light intensity did not show a great ability to dissipate
energy as heat, and most NPQ was due to photoinhibition (qI) and was not
dissipated during the relaxation in the dark.
At high irradiance, acclimation processes in these temperate zooxanthellae
therefore appear to be partly driven by a change in the NPQ capacity of the
algal cells, and to a maximal rate of photon utilization, which results in a
higher rate of light saturated photosynthesis. Following exposure to high
light, these corals also largely increased their rates of respiration,
suggesting a high capacity for metabolic activity once irradiance increases.
Conversely, polyps maintained in the low light treatment had to maximize the
capture of the low photon flux and minimize their energy costs
(Anthony and Hoegh-Guldberg,
2003), and therefore presented a lower Ek but
also lower respiration rates than corals maintained under high light.
Respiration rates were also very low when both light and temperature were
decreased. This is a common response of cnidarians maintained under low
temperature (Jacques and Pilson,
1980; Verde and McCloskey,
2001) or low light (Falkowski
and Dubinsky, 1981; Falkowski,
1990) conditions and corresponds to a decrease in the energy
expenditure.
Whereas tropical symbioses often photoacclimate to different light levels
by changing all autotrophic components, both increasing the algal density
(Titlyanov et al., 2001), or
the pigmentation per cell (Falkowski and
Dubinsky, 1981) and the photosynthetic parameters of light
saturation curves (Falkowski and Dubinsky,
1981; Mass et al.,
2007), photoacclimation in C. caespitosa mostly involves
a change in Pgmax and R, without any change in pigment
concentration or zooxanthellae density. This acclimation can be achieved by
changes in Rubisco levels, pigment ratios (diatoxanthin increasing from 26 to
34% of chlorophyll a for corals maintained at 30 and 250 µmol
m–2 s–1 light intensity, respectively; P. J.
Lopez, unpublished results), and also quantum yield of photosynthesis (i.e.
the efficiency of the use of absorbed energy), as observed here and elsewhere
(Stambler and Dubinsky, 2004).
When both temperature and light are modified, however, photoacclimation goes
through a change in all photosynthetic components.
Although photoacclimative responses observed in this study could be
regarded as not being directly relevant to in situ conditions, they
do provide information on the photo-physiological capacities of this
Mediterranean coral. Rates of photosynthesis measured for C.
caespitosa, both under low and high light conditions (36.7–78.4
µg O2 cm–2 h–1 or
1.5–5.1 µg O2 chl a–1
h–1), are in the range of those measured for temperate
(Kevin and Hudson, 1979;
Schiller, 1993;
Howe and Marshall, 2001) and
also tropical corals (Lasker,
1981; Porter et al.,
1984; Hoegh-Guldberg and
Smith, 1989; Muscatine,
1990). Increased photosynthesis under high light/high temperature
conditions might therefore allow in situ corals to increase their
autotrophic acquisition of energy during the summer season, as already
observed for other temperate corals (Howe
and Marshall, 2001) and sea anemones
(Verde and McCloskey, 2007).
This season is commonly characterized by food shortage
(Coma and Ribes, 2003;
Rossi et al., 2006) and
increased autotrophy might help the corals in such conditions. Conversely, in
winter, when PAR is low in the Mediterranean, the corals' capacity to
acclimate to low light levels might allow them to maintain a non-negligible
level of autotrophy.
Relationship between respirometry and fluorometry
The second aim of this study was to evaluate the functional relationship
between measurements obtained with fluorometry and respirometry. Whereas P/E
curves rapidly saturated (Fig.
2A) RLCs showed that saturation was not reached at ca. 800 µmol
m–2 s–1
(Fig. 2B) as already observed
in some high-light-adapted corals (Beer et
al., 1998a; Ralph et al.,
1999). This lack of saturation was not due to a limited exposure
time to the actinic light during RLCs since steady-state light curves (SLC)
did not saturate either (results not shown). Self-shading of the symbionts
(Ralph et al., 1999), or
shading by animal pigments (Klueter et
al., 2006), also seem to be excluded, because RLCs performed on
(optically thin) freshly isolated zooxanthellae
(Fig. 4) showed that the
plateau was reached at a high irradiance up to 1000 µmol
m–2 s–1. Additionally, RLCs on FIZ or on the
entire symbiosis did not show photoinhibition, and did not present the typical
pattern observed for temperate photosynthetic organisms such as macroalgae
(Beer et al., 1998b;
Figueroa et al., 2003). This
could be due to the fact that C. caespitosa is in symbiosis with a
Symbiodinium species belonging to the temperate clade A as almost all
Mediterranean symbioses (Visram et al.,
2006). This clade is widespread in the whole Mediterranean Sea,
and it might be responsible for C. caespitosa high light resistance.
Indeed, this species also shows exceptional plasticity in its habitat
conditions, since it can also be found along the Lebanon and Israeli coasts
where light levels can be much higher than those experienced in the Ligurian
Sea.
The relationships between respirometry and fluorometry measurements were
therefore non-linear, except at moderate light, from 0 to ca. 160 µmol
m–2 s–1
(Fig. 5A). This result
indicates that some oxygen evolved during the RLC was used before leaving the
symbiosis or that less oxygen was produced per charge separation under high
light. In a tightly coupled system, the photosynthesis products are expected
to be rapidly respired by the host, and respiration rates are expected to
increase with light intensity, leading to a more or less constant P/E curve.
Therefore, the non-linearity could be due to an under-estimation of the
light-enhanced respiration rates of the animal
(Edmunds and Davies, 1988). If
the saturation of Pg originates mainly from an increased utilisation of oxygen
by the algae (and not the animal), two mechanisms leading to
non-photosynthetic electron transport
(Figueroa et al., 2003) are
likely: the development of the Mehler cycle or photorespiration processes [due
to an increased O2 concentration in the cell
(Kühl et al., 1995)].
Another explanation is cyclic flow of electrons around PSII
(Falkowski et al., 1986;
Prasil et al., 1996). This
process does not require increase oxygen utilisation, but a reduced production
of O2 per charge separation at photosystem II (PSII). Such a
mechanism has indeed been observed in diatoms at high light and proposed as a
mechanism for photoprotection (Lavaud et
al., 2002a; Lavaud et al.,
2002b). We cannot, with the present data, evaluate which
process(es) is/are responsible for this observation. Clearly, more focused
studies on the photosynthetic and symbiosis physiology will be required to
understand the differences between the fluorometric and the oxygen evolution
measurements. Both measurements have their limitation and neither is
infallible when it comes to estimating primary production. However, from our
study it is evident that caution must be exercised when comparing ETR obtained
by fluorometry to photosynthetic performances obtained by oxygen evolution of
the temperate coral–algal complex as they clearly provide different
information.
|
CONCLUSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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When both temperature and light conditions are modified, however, photoacclimation goes through a change in all photosynthetic components, including symbiont density and pigment concentration. Since rates of photosynthesis measured using respirometry saturated at lower light values compared to the electron transport rates, the relationship between respirometry and fluorometry was only linear at low light intensities; while different hypotheses were suggested to account for this difference, there is a clear need for further studies in this area. Until then the fluorometric tool remains an excellent probe of the physiology of the symbiosis and should be used to complement but not replace oxygen evolution measurements.
LIST OF ABBREVIATIONS
F/
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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