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First published online November 1, 2006
Journal of Experimental Biology 209, 4546-4556 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02550
Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures
1 Centre Scientifique de Monaco, Av. Saint Martin, MC-98000, Principality of
Monaco
2 UMR 1112 INRA-UNSA, Faculté des Sciences, Université de Nice
Sophia-Antipolis, bp 71, F-06108, Nice Cedex 02, France
* Author for correspondence (e-mail: rrmetalpa{at}centrescientifique.mc)
Accepted 13 September 2006
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Key words: corals, Mediterranean Sea, temperature, growth, photosynthesis, PAM, Cladocora caespitosa, Oculina patagonica
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). Recent
evidence has also shown a large-scale warming of the Mediterranean Sea
(Bethoux et al., 1990;
Walther et al., 2002),
corresponding to a 0.3-0.7°C increase in the mean water temperature from
1961 to 1990 (Walther et al.,
2002). In the Ligurian Sea (NW Mediterranean), at 10-20 m depth,
summer water temperatures recorded usually reach a maximum of 24°C during
2-3 weeks (from 1992 to 1997 and 2000;
Table 1). In contrast, during
the summers of 1998, 1999 and 2003-2005, positive thermal anomalies occurred
(Table 1)
(Romano et al., 2000;
André et al., 2004;
Harmelin, 2004). In the summer
of 1999, for instance, the long-term increase was characterized by a lowering
of the thermocline (down to 40 m depth) and by mean temperatures of up to
24°C over at least 4 weeks between August and September
(Fig. 1). In the summer of
2003, large temperature shifts, up to 7.5°C, were recorded within a few
hours, reaching 27.2°C at 12 m depth
(Harmelin, 2004). Long periods
of elevated temperatures have also been observed more recently, in the summer
of 2005, with mean temperatures at 11 m depth exceeding 24°C for 6 weeks
(Fig. 1).
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During these warm summer periods, several mass-mortality events, on both
large and small spatial scales, have been reported in the Ligurian Sea,
affecting scleractinian corals such as Cladocora caespitosa and
Balanophyllia europaea
(Rodolfo-Metalpa et al., 2000;
Rodolfo-Metalpa et al., 2005),
sponges, gorgonians (Cerrano et al.,
2000; Cerrano et al.,
2001; Garrabou et al.,
2001), and other sessile benthic species
(Perez et al., 2000). Several
hypotheses have been proposed to explain these mortality events, such as high
temperatures, pathogen contaminations, and energetic constraints
(Cerrano et al., 2000;
Garrabou et al., 2001;
Coma and Ribes, 2003).
Necrosis was observed in gorgonians and sponges when temperatures remained
above or equal to 24°C over several weeks and coincided with the
occurrence of opportunistic organisms
(Cerrano et al., 2000;
Cerrano et al., 2001). Energy
shortage was also observed in taxa exhibiting summer dormancy such as
anthozoans and sponges (Coma et al.,
2000). Therefore, the elevated temperature, together with the
stability of the water column, were suggested to be the most likely cause of
benthic mortality because they affected a wide variety of taxa down to a depth
of 40 m (above the lowered thermocline), over a large geographical area
(Coma et al., 2002;
Coma and Ribes, 2003;
Linares et al., 2005).
The response of temperate corals to temperature stress has been poorly
studied (Jacques et al., 1983;
Jones et al., 2000;
Nakamura et al., 2003),
particularly in the Mediterranean corals
(Rodolfo-Metalpa et al.,
2006). The only extended studies performed were to understand the
bleaching of the coral Oculina patagonica along the Israeli coasts
(e.g. Kushmaro et al., 1996).
In this location, O. patagonica bleach during summer due to infection
by Vibrio shiloi, which becomes virulent when the temperature rises
above 26°C (Rosenberg and Falkovitz,
2004).
The aim of the present study was to monitor the response, in terms of
photosynthesis and growth rate, of two symbiotic Mediterranean corals,
Cladocora caespitosa (Linnaeus 1767) and O. patagonica
(Angelis 1908), to different temperature conditions. C. caespitosa is
a symbiotic scleractinian coral (Faviidae), native to the Mediterranean Sea
(Zibrowius, 1980), which can
form large banks of several m2
(Peirano et al., 2001;
Kruzi
and Pozar-Domac,
2003). In the Ligurian Sea, it is mainly distributed between 7 m
and 15 m depth, and lives in turbid water at relatively low irradiance
(Schiller, 1993;
Peirano et al., 2005). O.
patagonica is also a symbiotic scleractinian coral that is found, between
3 m and 10 m depth, in several Mediterranean Sea locations
(Fine et al., 2001). The range
of temperatures investigated was from 20°C to 26°C, 20°C being the
temperature encountered in spring and autumn, and 24-26°C being recorded
during recent warm summers (1999 and 2005). The length of exposure (3-7 weeks)
was comparable to that experienced by the corals in situ
(Fig. 1). Temperature was also
increased up to 28°C, which is a normal summer temperature in the SE
Mediterranean, where both corals are also found
(Zibrowius, 1980).
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). Small replicate samples (nubbins) of O.
patagonica were cut with pliers from mother colonies, attached to nylon
threads and suspended in seawater. After ca. 3 weeks, tissue had re-covered
the skeleton. Branches of C. caespitosa containing 10-15 polyps (for
growth rates measurements) and single polyps (for the other measurements),
referred to as nubbins, were detached from mother colonies, carefully cleaned
of epiphytes, associated fauna and sediment using a brush, and placed on PVC
supports. Twice a week, corals were abundantly fed with Artemia
salina nauplii.
Experimental design
The experiment was designed to measure the growth and photosynthesis of
corals maintained under different conditions: (i) at 20°C, which is the
spring and autumn temperature; (ii) at 24°C, which is the mean summer
temperature during a 2-3 week period in normal summers and more than 4 weeks
in warm summers (Table 1;
Fig. 1); (iii) at 26°C and
28°C, temperatures that might occur over a 2-3 week period in warm
summers.
For this purpose, corals were randomly transferred into eight 15 l experimental tanks (2 tanks at each of 4 temperatures). Each tank contained 41 and 23 nubbins of C. caespitosa and O. patagonica, respectively. The experimental design was as described in Fig. 2. (a) Two tanks were maintained at 20°C throughout the whole experiment (48 days). (b) In two other tanks, temperature was slightly (by 1°C per day) increased from 20°C to 24°C and maintained during the 48 day period to mimic a long-term occurrence of high temperature as already observed in situ (Table 1, Fig. 1). (c) In the last four tanks, the temperature was first increased from 20°C to 24°C during a 14 day period (from T0 to T14), to mimic a normal summer temperature increase (Fig. 1); then, temperature was elevated at 26°C (in two tanks) and 28°C (in two other tanks) over an additional 3 week period, to mimic an abnormal warm summer (from T14 to T34). The temperature was then returned to 24°C over two further weeks (T48). Temperatures were kept constant using aquarium heaters connected to electronic controllers (±0.3°C accuracy). Small submersible pumps ensured seawater circulation in the tanks. Light intensity, seawater renewal and food level were maintained constant during the whole experiment, as described above.
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Nubbins were sampled 5 times during the experiment, at the beginning (T0), after 14 days (T14), 24 days (T24), 34 days (T34) and 48 days (T48), and several measurements (biomass parameters, rates of photosynthesis, respiration and growth, photosynthetic efficiency of the PSII and electron transport rate) were performed. During the entire experiment, corals were checked under a binocular for tissue degradation (necrosis or retraction into the polyps).
Biomass measurements
For each species, zooxanthellae density and chlorophyll contents (chl
a and c2) were measured for the 4 temperatures
and the 5 sampling times. Three samples were randomly taken in each tank
(N=6 samples per temperature). Samples were frozen at -80°C if
not immediately processed. Coral tissue was detached using a Water Pick
(Brown, Kronberg, Germany) in 0.45 µm filtered seawater. The slurry was
homogenised using a Potter tissue grinder and a 2 ml sub-sample was taken for
zooxanthellae density determination using an improved version of the
Histolab® 5.2.3 image analysis software (Microvision, Every, France)
(Rodolfo-Metalpa et al.,
2006). For chl measurement, 10 ml sub-samples were centrifuged at
5000 g for 10 min at 4°C and the pellet containing the
zooxanthellae was resuspended in 10 ml of pure acetone. Pigments were
extracted at 4°C during 24 h. The extract was recentrifuged at 10 000
g for 15 min and chl a and c2
were determined according to published methods
(Jeffrey and Humphrey,
1975).
Data were normalized per skeletal surface area on both corals. For O.
patagonica it was measured by the aluminum foil technique
(Marsh, 1970), which has been
found to be more accurate than the wax technique. For C. caespitosa,
the mean polyp surface (PS) was calculated according to the following
equation (Rodolfo-Metalpa et al.,
2006):
PS=(2
R)H+R2, where
R is the polyp radius, and H the exosarc extension.
Growth rates
Six nubbins of C. caespitosa and five nubbins of O.
patagonica were randomly chosen in each tank (N=12 and 10 for
each temperature, respectively) and their growth rates were measured
throughout the whole experiment on the same nubbins using the buoyant weight
method (Davies, 1989). Daily
growth rates (skeleton and tissue) of both corals were calculated as the
difference between two subsequent weights and normalized to the tissue surface
area for both corals and by the initial weight for O. patagonica. Wet
weight was converted into dry weight using an aragonite density of 2.93 g
cm-3.
Photosynthesis and respiration rates
These measurements were performed only for C. caespitosa, due to a
lower number of samples of O. patagonica. Photosynthesis was assessed
for the 4 temperatures and the 5 sampling times. Three nubbins were therefore
taken in each tank (N=6) and were incubated in a glass thermostated
chamber (from 20°C to 28°C, depending on the treatment) containing a
Strathkelvin 928® oxygen electrode. The chamber was filled with 0.45
µm-filtered seawater continuously stirred with a stirring bar. The
electrodes were calibrated before each experiment against air-saturated
seawater and a saturated solution of sodium dithionite (zero oxygen). Samples
were allowed to acclimate to chamber conditions and measurement started when
polyps were expanded. Changes in dissolved oxygen concentrations were
monitored on a computer during 15 min at the culture irradiance of 110 µmol
photons m-2 s-1 (P110) and in the
dark (R). Light was provided by a metal halide lamp (Philips, HPIT
400 W, Guildford, Surrey, UK). Rates of P110 and
R were estimated by regressing oxygen data against time, taking into
account the seawater volume in the chamber. At the end of measurements,
samples were frozen at -80°C for chl a measurements. Data were
normalised by chl a content (µg O2 µg chl
a-1 h-1) or by surface area (µg
O2 cm-2 h-1).
Chlorophyll a fluorescence of PSII
Chl a fluorescence of PSII was always measured at the same time in
the morning, during the whole experiment using a PAM fluorometer (DIVING-PAM,
Walz, Germany). Five nubbins of C. caespitosa and three nubbins of
O. patagonica were chosen in each tank (N=10 and 6 for each
temperature, respectively) and followed during the whole experiment. The
minimal (F0 or F) and maximal
(Fm or Fm) fluorescence yields were
measured by applying a weak pulsed red light (max. intensity <1 µmol
photon m-2 s-1, width 3 µs, frequency 0.6 kHz), and a
saturating pulse of actinic light (max. intensity >8000 µmol photon
m-2 s-1, width 800 ms), respectively. The maximum
photosynthetic efficiency in dark-adapted corals
(Fv/Fm=(Fm-F0)/Fm,
where Fv is the variable fluorescence) and the relative
electron transport rate
[ETR=
F/Fm'x0.5xPAR
(photosynthetic active radiation), with
F=Fm'-F] were used to
assess the efficiency of the PSII between treatments. Rapid light curves
(RLCs) were generated by illuminating corals for 10 s periods, eight times
from 0 to 768 µmol photon m-2 s-1. During
measurements, the 8 mm optical fibre was maintained perpendicular to the
coral's surface using a black-jacket at a fixed distance of 5 mm. Values of
light intensities (PAR list) received by the corals during RLCs were obtained
using the internal Light-Calibration program of the Diving-PAM. When
Fv/Fm was <0.2 due to thermal
stress, samples were considered dead and eliminated from the analysis.
Statistical analyses
Changes in growth rate, Fv/Fm and
ETRmax were tested using repeated-measures ANOVAs since
measurements were performed on the same corals. The following statistics were
performed: (1) one-way ANOVAs testing the effect of time-exposure
(T0, T14, T24,
T34, T48) on corals incubated at
20°C and at 24°C; (2) one-way ANOVAs testing the effect of
time-exposure (T14, T24 and
T34) on corals incubated at 26°C and at 28°C; (3)
one-way ANOVAs testing the effect of decreased temperature from 26°C and
28°C to 24°C (from T34 to
T48). When ANOVA revealed significant differences
(P<0.05), mean values were compared using Tukey HSD or Tukey HSD
for unequal numbers (Spjotvoll/Stoline test).
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In O. patagonica, 24°C had a rapid effect on most parameters, which had already changed during the first 14 days (Figs 6, 7, 8; Table 3). Therefore, Fv/Fm and ETRmax decreased by 29% and 33%, respectively, between T0 and T14 (Fig. 6A,B), and there was also a 59% and 75% reduction in zooxanthellae and chl c2 contents, respectively, (Fig. 7A,C; Tukey test, P<0.05). These parameters, however, did not show any further decrease from T14 to T48, in contrast to C. caespitosa (Tukey test, P<0.05). At T24 growth rate significantly decreased and was reduced by ca. 70% at the end of the incubation (Tukey test; P<0.05: T34=T48<T0=T14=T24; Fig. 8). No sign of necrosis was observed.
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Measurements at 26°C and 28°C
From T14 to T34 temperature was
elevated to 26°C and 28°C and most parameters significantly decreased
in both corals (Table 2). For
C. caespitosa, P110 was negative or null
(Fig. 3B) because rates of
respiration increased, despite a large variability
(Fig. 3C).
Fv/Fm and ETRmax decreased
by ca. 40-50% at both temperatures (Fig.
4A,B,C) although a significant difference in
Fv/Fm was only found at 26°C
(Tukey test, P<0.05; Table
2). Zooxanthellae density was significantly reduced at
T34 by 40% and 82%, for temperatures of 26°C and
28°C, respectively (Tukey test, P<0.05;
Fig. 5A). No significant
differences were found in chl a and c2 content,
however, due to the high variability (Fig.
5B,C; Table 2).
Growth rates increased during the first 10 days of incubation (from
T14 to T24) by 45% and 18%, at
26°C and 28°C, respectively (Fig.
3A), but then drastically decreased at T34 by
ca. 50% of their initial values (T0) (Tukey test,
P<0.05). Almost all samples presented signs of necrosis at
T34 in parallel with zooxanthellae density decrease
(Fig. 5A). Two and five nubbins
out of ten maintained at 26°C and 28°C, respectively, died at
T34. Fewer than 5% of the polyps did not show necrosis but
were pale (= bleached) at 28°C.
When the temperature was returned to 24°C, P110, R, Fv/Fm and ETRmax did not show any further decrease (Fig. 3B,C and Fig. 4A,B; Table 2). Growth rates kept on decreasing, to become null at the end of the experiment (Table 2; Fig. 3A). 100% nubbins maintained at 26°C and 28°C underwent necrosis. As a consequence, zooxanthellae and chl content were 65-70% lower than the values measured at the beginning of the experiment (Fig. 5A-C).
In O. patagonica, no significant further change in Fv/Fm and ETRmax values was induced by an increase in temperature from 24°C to 26°C or 28°C (Fig. 6A,B; Table 3). A significant decrease was found in zooxanthellae and chl a and c2 content from T14 to T24, however (Tukey test, P<0.05: T14>T24=T34; Fig. 7A-C). Growth rate was also significantly reduced at these temperatures (Tukey test, P<0.05; Fig. 8). Only two nubbins maintained at 28°C showed signs of tissue retraction. When temperature was returned to 24°C, there was a continuous decrease in growth rate, which was reduced by 80% at the end of the experiment for both 26°C and 28°C (Fig. 8; Table 3). Nubbins that showed signs of tissue retraction recovered from the stress by producing new tissue.
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Growth and photosynthesis at 20°C
At 20°C, all the parameters measured remained constant during the
incubation, suggesting that both corals were fully adapted to such conditions.
Rates of photosynthesis and growth of Mediterranean corals under normal
temperature and light conditions have been poorly investigated
(Peirano et al., 1999;
Peirano et al., 2005;
Schiller, 1993). Comparison of
the growth rate measurements with other studies performed on temperate corals
is difficult, because they all used various growth indices, including linear
extension rate (Schiller,
1993; Goffredo et al.,
2004; Peirano et al.,
2005), skeletal density pattern
(Peirano et al., 1999),
internal growth lines (Nagelkerken et al.,
1997), incorporation of 45Ca
(Howe and Marshall, 2002;
Marshall and Clode, 2004), or
% wet mass (Miller, 1995).
Growth rates at 20°C of O. patagonica and C.
caespitosa were equal to 0.2 and 0.8 mg cm-2 day-1,
respectively. If we assume that growth is sustained continuously throughout
the year, we get a maximal calcium deposition of 0.73 and 2.92 kg
CaCO3 m-2 year-1, respectively. An annual
maximal production of 1.7 kg CaCO3 m-2 year-1
was measured in C. caespitosa using sclerochronology
(Peirano et al., 2001), a
value slightly lower than our estimation. When compared to other temperate
corals, similar growth rates were obtained for Plesiastrea versipora
[0.15-0.18 mg cm-2 day-1
(Kevin and Hudson, 1979;
Howe and Marshall, 2002)] and
Astrangia danae [0.6 mg cm-2 day-1
(Jacques et al., 1983)].
Growth rates of the Mediterranean corals are therefore much lower (5 times)
than those experienced by tropical scleractinian species [ca. 4 mg
cm-2 day-1 (Lough
and Barnes, 2000;
Carricart-Garnivet, 2004)],
despite the fact that they are symbiotic. Low growth rates seem to be a
feature of temperate corals, and could be explained by several parameters such
as temperature (Lough and Barnes,
2000), light (Bak,
1974) and carbonate saturation state
(Kleypas et al., 1999), all of
which are decreased in temperate compared to tropical waters.
In terms of photosynthesis/photosynthetic efficiency, to our knowledge
there are few data available, either for Mediterranean
(Schiller, 1993;
Fine et al., 2004) or for
other temperate corals (Jones et al.,
2000; Howe and Marshall,
2001; Nakamura et al.,
2003). At 20°C, the dark-adapted
Fv/Fm of the symbiotic zooxanthellae
of both corals (0.6-0.65) were in the range of values observed in marine algae
(Büchel and Wilhelm, 1993)
and in zooxanthellae symbiotic with tropical corals (e.g.
Jones et al., 1998). The rate
of photosynthesis measured for C. caespitosa at the culture
irradiance of 110 mol photons m-2 s-1 [2 µg
O2 µg chl a-1 h-1 or ca. 20 µg
O2 cm-2 h-1] is also in the range of those
previously measured for other temperate corals under conditions of similar
irradiance (Schiller, 1993;
Howe and Marshall, 2001).
Finally, C. caespitosa and O. patagonica contained high
densities of zooxanthellae (3x106 and 16x106
zooxanthellae cm-2, respectively) compared to tropical reef corals
[usual range: 0.3-3.5x106 zooxanthellae cm-2 (e.g.
Hoegh-Guldberg and Smith,
1989; Muller-Parker et al.,
1994; Stimson et al.,
2002)]. This seems a typical feature of temperate corals
(Kevin and Hudson, 1979;
Jacques et al., 1983;
Schiller, 1993;
Howe and Marshall, 2001),
adapted to a shade environment during most of the year
(Muller-Parker and Davy,
2001). This symbiosis seems also to be stable, since the
zooxanthellae density does not change with the season or the depth
(Schiller, 1993). Despite the
fact that Mediterranean corals contain a high density of zooxanthellae with a
maximal photosynthetic efficiency, their growth rates are much lower than
tropical corals, suggesting that fewer photosynthates are allocated for
calcification in Mediterranean corals and may be used as energy to accommodate
lower temperature conditions, or released as mucus. Indeed, at least for
C. caespitosa, high rates of mucus release [44% of its respiration
(Herndl and Velimirov, 1986)]
seems to be an adaptation to the life in turbid waters
(Schiller, 1993).
Growth and photosynthesis at high temperatures
The growth of tropical (Lough and
Barnes, 2000;
Carricart-Garnivet, 2004;
Marshall and Clode, 2004;
Edmunds, 2005) or temperate
scleractinian corals (Jacques et al.,
1983; Miller,
1995; Howe and Marshall,
2002; Peirano et al.,
2005) has often been investigated under the normal range of
temperatures experienced by corals in their natural environments. Few studies,
however, have assessed the effect of a small but prolonged 1-2°C
temperature increase above the optimum, and these studies have been performed
only with tropical corals (Jokiel and
Coles, 1977;
Abramovitch-Gottlib et al.,
2003; Reynaud et al.,
2004). They demonstrated an impairment of skeletal growth at high
temperatures. In the same way, the effect of elevated temperatures on
photosynthesis of temperate scleractinian species has been poorly studied
(Jones et al., 2000;
Nakamura et al., 2003), in
contrast to tropical corals (e.g. Coles
and Jokiel, 1978; Baghooli and
Hidaka, 2003; Hill et al.,
2004).
In this study, O. patagonica showed a significant decrease in
growth rate, when the temperature of 24°C was maintained for more than 3
weeks, suggesting that this maximum summer temperature is already a breaking
point for the growth of this coral. A similar trend was observed in another
temperate coral Plesiastrea versipora
(Howe and Marshall, 2002),
whose calcification was maximum at 3°C below the maximum summer
temperature of 21°C. In parallel to the growth rate decline, there was
also a significant decrease in the photosynthetic parameters
(Fv/Fm, ETR) after 2 weeks at
24°C, suggesting a coupling between photosynthesis and calcification, as
it has been already shown for other tropical
(Gattuso et al., 1999) and
temperate corals (Kevin and Hudson,
1979). The decrease in F/Fm (from ca.
0.6 to 0.4) coincided with the loss of zooxanthellae (from
16x106 to 4x106 cells cm-2) and
chl, suggesting that corals were stressed. This loss of symbionts occurred
without any sign of necrosis and can be considered as a bleaching phenomenon.
The decrease in growth and photosynthetic efficiency observed at 24°C (and
above) is intriguing because this coral is also spread along the Israeli
coasts, where it experiences, in the summer months, long-term exposure (4-6
months) to elevated temperatures (from 24°C to 30°C)
(Shenkar et al., 2005). We may
therefore be dealing with a different genetic population (either the algal or
animal partner, or both), or there could have been some adaptive adjustments
in the capability of the colonies to withstand high temperatures
(Clausen and Roth, 1975). More
comparative studies between the Oculina species originating from the
Ligurian Sea and the coast of Israel are needed to understand their
differences.
The results also show different responses of C. caespitosa
compared to O. patagonica to the elevation in temperature. The first
difference was in the pattern of growth response. In contrast to O.
patagonica, the growth rate of C. caespitosa significantly
increased during the first 3 weeks of temperature increase, especially at
24°C and 26°C, suggesting a temperature enhancement of growth in this
coral. In general the temperature-growth response of corals is characterized
by a minimum growth rate at the lowest temperature, enhancement up to a
threshold temperature, and a decline thereafter
(Edmunds, 2005). Accordingly,
the positive effect of elevated temperature on growth rate of C.
caespitosa was limited for the first 3 weeks, after which a decrease was
observed. This may be due to a lack of energy to sustain these higher growth
rates, since the rates of photosynthesis, as well as the photosynthetic
efficiency significantly decreased during, respectively, the third (for
26°C and 28°C) and the fourth (for 24°C) week of incubation.
The second difference was in the mortality response. In contrast to O.
patagonica, which rapidly (after 2 weeks at 24°C) bleached but showed
no sign of necrosis, C. caespitosa underwent necrosis after 5 weeks
at elevated temperatures, leading to the loss of the coral tissue and its
associated zooxanthellae. The process started with a retraction of the tissue
inside the calyx of the polyp, leaving large zones of skeleton without tissue
(Fig. 9A); this has been
interpreted, when observed in situ and in summer, as a way of
protecting the photosynthetic apparatus during short periods of high
irradiance and temperature (Brown et al.,
1994; Brown et al.,
2002; Peirano et al.,
2005). However, in the present study, the retraction was followed
by tissue necrosis (Fig. 9B,C)
and 100% mortality of the nubbins of C. caespitosa at the end of the
incubation at 26°C and 28°C. During this experiment, O.
patagonica, by remaining alive and without necrosis, was more able than
C. caespitosa to resist to high temperature conditions. Its rapid
capacity to bleaching was maybe one of the keys to its success.
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). Less
attention has been given to temperate marine organisms, and especially to the
Mediterranean benthic fauna (Cerrano et
al., 2000). However, mass mortality events in the Mediterranean
Sea have increased during the last 10 years, presumably due to global warming.
Average temperatures have already increased by 0.3-0.7°C
(Walther et al., 2002) and
might be higher in the next few years. The results obtained show that the two
symbiotic scleractinian corals, especially C. caespitosa, which is
endemic to the Mediterranean, may already suffer during warm summers. Further
studies are required to provide a better knowledge of the ability of
Mediterranean species to recover from such stress and perhaps adapt to it.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Abramovitch-Gottlib, L., Katoshevski, D. and Vago, R. (2003). Responses of Stylophora pistillata and Millepora dichotoma to seawater temperature elevation. Bull. Mar. Sci. 73,745 -755.
André, J.-C., Déqué, M., Rogel, P. and Planton, S. (2004). La vague de chaleur de l'été 2003 et sa prévision saisonnière. C. R. Geoscience 336,491 -503.[CrossRef]
Baghooli, R. and Hidaka, M. (2003). Comparison of stress susceptibility of in hospite isolated zooxanthellae among five coral species. J. Exp. Mar. Biol. Ecol. 291,181 -197.
Bak, R. P. M. (1974). Available light and other factors influencing growth of stony corals through the year in Curacao. Proc. 2nd Int. Coral Reef Symp. 2, 229-233.
Bethoux, J. P., Gentili, B., Raunet, J. and Tailliez, D. (1990). Warming trend in the western Mediterranean deep water. Nature 347,660 -662.[CrossRef]
Brown, B. E., Le Tissier, M. D. A. and Dunne, R. P. (1994). Tissue retraction in the scleractinian coral Coeloseris mayeri, its effect upon coral pigmentation, and preliminary implications for heat balance. Mar. Ecol. Prog. Ser. 105,209 -218.
Brown, B. E., Downs, C. A., Dunne, R. P. and Gibb, S. W. (2002). Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. J. Exp. Mar. Biol. Ecol. 277,129 -144.
Büchel, C. and Wilhelm, C. (1993). In vivo analysis of slow chlorophyll fluorescence incubation kinetics in algae: progress, problems and perspectives. Photochem. Photobiol. 58,137 -148.
Carricart-Garnivet, J. P. (2004). Sea surface temperature and the growth of the West Atlantic reef building coral Montastrea annularis. J. Exp. Mar. Biol. Ecol. 302,249 -260.
Cerrano, C., Bavestrello, G., Bianchi, C. N., Cattaneo-Vietti, R., Bava, S., Morganti, C., Morri, C., Picco, P., Sara, G., Schiaparelli, S. et al. (2000). A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecol. Lett. 3,284 -293.[CrossRef]
Cerrano, C., Magnino, G., Sarà, A., Bavestrello, G. and Gaino, E. (2001). Necrosis in a population of Petrosia ficiformis (Porifera, Demospongiae) in relation with environmental stress. Ital. J. Zool. 68,131 -136.
Clausen, C. D. and Roth, A. A. (1975). Effect of temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar. Biol. 33, 93-100.
Coles, S. L. and Jokiel, P. L. (1978). Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar. Biol. 49,187 -195.
Coma, R. and Ribes, M. (2003). Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101,205 -215.[CrossRef]
Coma, R., Ribes, M., Gili, J. M. and Zabala, M. (2000). Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol. Oceanogr. 47,324 -331.
Coma, R., Ribes, M., Gili, J. M. and Zabala, M. (2002). Seasonality in coastal benthic ecosystems. Trends Ecol. Evol. 15,448 -453.
Davies, P. S. (1989). Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar. Biol. 101,389 -395.
Edmunds, P. J. (2005). The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef. Oecologia 146,350 -364.[CrossRef][Medline]
Fine, M., Zibrowius, H. and Loya, Y. (2001). Oculina patagonica: a nonlessepsian scleractinian coral invading the Mediterranean Sea. Mar. Biol. 138,1195 -1203.
Fine, M., Steindler, L. and Loya, Y. (2004). Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar. Freshw. Res. 55,115 -121.[CrossRef]
Garrabou, J., Perez, T., Sartoretto, S. and Harmelin, J. G. (2001). Mass mortality event in Red coral Corallium Rubrum populations in the Provence regions (France, NW Mediterranean). Mar. Ecol. Prog. Ser. 217,263 -272.
Gattuso, J.-P., Allemand, D. and Frankignoulle, M. (1999). Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am. Zool. 39,160 -183.
Goffredo, S., Mattioli, G. and Zaccanti, F. (2004). Growth and population dynamics model of the Mediterranean solitary coral Balanophyllia europeae (Scleractinia, Dendrophylliidae). Coral Reefs 23,433 -443.[CrossRef]
Harmelin, J.-G. (2004). Environnement thermique du benthos côtier de l'ile de Port-Cros (parc national, France, Méditerranée nord-occidentale) et implications biogéographiques. Sci. Rep. Port-Cros Natl. Park Fr. 20,173 -194.
Herndl, G. J. and Velimirov, B. (1986). Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora caespitosa. Mar. Biol. 90,363 -369.
Hill, R., Schreiber, U., Gademann, R., Larkum, A. W. D., Kühl, M. and Ralph, P. J. (2004). Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of corals. Mar. Biol. 144,633 -640.
Hoegh-Guldberg, O. and Smith, G. J. (1989). The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef coral Stylophora pistillata (Esper) and Seriatopora hystrix (Dana). J. Exp. Mar. Biol. Ecol. 129,279 -303.
Howe, S. A. and Marshall, A. T. (2001). Thermal compensation of metabolism in the temperate coral Plesiastrea versipora (Lamarck 1816). J. Exp. Mar. Biol. Ecol. 259,231 -248.[CrossRef][Medline]
Howe, S. A. and Marshall, A. T. (2002). Temperature effects on calcification rate and skeletal deposition in the temperate coral, Plesiastrea versipora (Lamarck). J. Exp. Mar. Biol. Ecol. 275,63 -81.
Jacques, T. G., Marshall, N. and Pilson, M. E. Q. (1983). Experimental ecology of the temperate scleractinian coral Astrangia danae: II. Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar. Biol. 76,135 -148.
Jeffrey, S. W. and Humphrey, G. F. (1975). New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167,191 -194.
Jokiel, P. L. and Coles, S. L. (1977). Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol. 43,201 -203.
Jones, R. J., Hoegh-Guldberg, O., Larkum, A. W. D. and Schreiber, U. (1998). Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21,1219 -1230.
Jones, R. J., Ward, S., Amri, A. Y. and Hoegh-Guldberg, O. (2000). Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar. Freshw. Res. 51,63 -71.
Kevin, K. M. and Hudson, R. C. L. (1979). The role of zooxanthellae in the hermatypic coral Plesiastrea urvillei (Milne Edwards and Haime) from cold waters. J. Exp. Mar. Biol. Ecol. 36,157 -170.
Kleypas, J. A., McManus, J. W. and Menez, L. A. B. (1999). Environmental limits to coral reef development: where do we draw the line? Am. Zool. 39,146 -159.
Kruzi, P. and Pozar-Domac, A. (2003).
Banks of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in
the Adriatic Sea. Coral Reefs
22, 536.[CrossRef]
Kushmaro, A., Rosenberg, E., Fine, M., Ben-Haim, Y. and Loya, L. (1996). Bacterial infection and coral bleaching. Nature 380,396 .
Linares, C., Coma, R., Diaz, D., Zabala, M., Hereu, B. and Dantart, L. (2005). Immediate and delayed effects of a mass mortality event on gorgonian dynamics and benthic community structure in the NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 305,127 -137.
Lough, J. M. and Barnes, D. J. (2000). Environmental controls on growth of the massive coral Porites. J. Exp. Mar. Biol. Ecol. 245,225 -243.[CrossRef][Medline]
Marsh, Y. A. (1970). Primary productivity of reef-building calcareous and red algae. Ecology 55,225 -263.
Marshall, A. T. and Clode, P. (2004). Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23,218 -224.
Miller, M. W. (1995). Growth of a temperate coral: effects of temperature, light, depth and heterotrophy. Mar. Ecol. Prog. Ser. 122,217 -225.
Muller-Parker, G. and Davy, S. K. (2001). Temperate and tropical algal-sea anemone symbioses. Invertebr. Biol. 120,104 -123.[CrossRef]
Muller-Parker, G., McCloskey, L. R., Hoegh-Guldberg, O. and McAuley, P. J. (1994). Effect of ammonium enrichment on animal and algal biomass of the coral Pocillopora damicornis. Pac. Sci. 48,273 -283.
Nagelkerken, I., Van Der Velde, G. and Avesaath, P. H. V. (1997). A description of the skeletal development pattern of the temperate coral Caryophyllia smithii based on internal growth lines. J. Mar. Biol. Assoc. U. K. 77,375 -387.
Nakamura, E., Yokohama, Y. and Tanaka, J. (2003). Photosynthetic activity of a temperate coral Acropora pruinosa (Scleractinia, Anthozoa) with symbiotic algae in Japan. Phycol. Res. 51,38 -44.
Peirano, A., Morri, C. and Bianchi, C. N. (1999). Skeleton growth and density pattern of the temperate, zooxanthellate scleractinian Cladocora caespitosa from the Ligurian Sea (NW Mediterranean). Mar. Ecol. Prog. Ser. 185,195 -201.
Peirano, A., Morri, C., Bianchi, C. N. and Rodolfo-Metalpa, R. (2001). Biomass, carbonate standing stock, and production of the Mediterranean coral Cladocora caespitosa.Facies 44,75 -80.
Peirano, A., Abbate, M., Cerrati, G., Difesca, V., Peroni, C. and Rodolfo-Metalpa, R. (2005). Monthly variations in calyx growth, polyp tissue, and density banding of the Mediterranean scleractinian Cladocora caespitosa (L.). Coral Reefs 24,404 -409.[CrossRef]
Perez, T., Garrabou, J., Sartoretto, S., Harmelin, J.-G., Francour, P. and Vacelet, J. (2000). Mortalité massive d'invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. C. R. Acad. Sci. Paris 323,853 -865.[Medline]
Reynaud, S., Hemming, N. G., Juillet-Leclerc, A. and Gattuso, J.-P. (2004). Effect of pCO2 and temperature on the boron isotopic composition of the zooxanthellate coral Acropora sp. Coral Reefs 23,539 -546.
Rodolfo-Metalpa, R., Bianchi, C. N., Peirano, A. and Morri, C. (2000). Coral mortality in NW Mediterranean. Coral Reefs 19,24 .[CrossRef]
Rodolfo-Metalpa, R., Bianchi, C. N., Peirano, A. and Morri, C. (2005). Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital. J. Zool. 72,271 -276.
Rodolfo-Metalpa, R., Richard, C., Allemand, D., Bianchi, C. N., Morri, C. and Ferrier-Pagès, C. (2006). Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar. Biol. 150,45 -55.
Romano, J. C., Bensoussan, N., Younes, W. and Arlhac, D. (2000). Anomalies thermiques dans les eaux du golfe de Marseille durant l'été 1999. Une explication partielle de la mortalité d'invertébrés fixés. C. R. Acad. Sci. Paris 323,415 -427.[Medline]
Rosenberg, E. and Falkovitz, L. (2004). The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 58,143 -159.[CrossRef][Medline]
Shenkar, N., Fine, M. and Loya, M. (2005). Size matters: bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294,181 -188.
Schiller, C. (1993). Ecology of the symbiotic coral Cladocora caespitosa (L) (Favidae, Scleractinia) in the Bay of Piran (Adriatic Sea): II. Energy budget. PSZN Mar. Ecol. 14,221 -238.
Stimson, J., Sakai, K. and Sembali, H. (2002). Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21,409 -421.
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, J. C., Fromentin, J.-M., Hoegh-Guldberg, O. and Bairlein, F. (2002). Ecological responses to recent climate change. Nature 416,389 -395.[CrossRef][Medline]
Wilkinson, C. R. (ed.) (2004). Status of the Coral Reefs of the World: 2004. Vol.1 . Townsville, Queensland, Australia: Global Reef Monitoring Network and Australian Institute of Marine Science.
Zibrowius, H. (1980). Les Scléractiniaires de la Méditerranée et de l'Atlantique nord-oriental. Mem. Inst. Oceanogr. Monaco 11, 1-284.
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