Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef
Centre for Marine Studies, The University of Queensland, St Lucia, Queensland 4072, Australia
* Author for correspondence (e-mail: m.fine{at}marine.uq.edu.au)
Accepted 9 November 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: bleaching, endolithic algae, thermal stress, photoacclimation, photoinhibition, coral, Montipora monasteriata, Symbiodinium
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Coral bleaching involves the disruption of the association between coral
hosts and their endosymbiotic photosynthetic algae. It is a stress response
that results in abrupt decreases in the population density of symbiotic
dinoflagellates after changes to the physical and chemical environment
surrounding corals. These changes may include low salinity
(Goreau, 1964;
Egana and DiSalvo, 1982
); low
or high photosynthetic radiation (Vaughan,
1914
; Yonge and Nichols,
1931
; Hoegh-Guldberg and
Smith, 1989
; Jones et al.,
1998
); elevated ultraviolet radiation
(Gleason and Wellington, 1993
;
Lesser et al., 1990
); toxins,
e.g. cyanide (Jones and Hoegh-Guldberg,
1999
), copper ions (Jones,
1997
), diuron and atrazine
(Jones et al., 2003
);
microbial infection, e.g. Vibrio
(Kushmaro et al., 1996
) and
temperature (high: Jokiel and Coles,
1977
,
1990
;
Coles and Jokiel, 1978
;
Hoegh-Guldberg and Smith,
1989
; Glynn and D'Croz,
1990
; low: Saxby et al.,
2003
). More recently, global episodes of mass coral bleaching have
occurred that are linked to elevated seawater temperature
(Goreau and Hayes, 1994
;
Glynn, 1991
,
1993
;
Brown, 1997
;
Hoegh-Guldberg, 1999
). These
responses are exacerbated by high irradiance due to the effect of elevated sea
temperatures on the ability of symbiotic dinoflagellates in affected corals to
process light excitations.
While the response of corals and symbiotic dinoflagellates to
thermal/irradiance stress have been the focus of a wide range of studies,
microendolithes have been largely overlooked. Several lines of information
suggest, however, that endolithic algae may be important for the survival of
bleached corals (Fine and Loya,
2002). Furthermore, it is most likely that the phototrophic
endolithic community has influenced measurements and interpretations of
aspects such as symbiont pigment concentrations
(Kleppel et al., 1989
) and
photosynthetic efficiency (Fine et al.,
2004
). Understanding endoliths response to temperature and light
stress is of great importance if we wish to better understand holobiont
(corals and their many associates) during and following stressful events.
We hypothesised that endoliths will survive increased temperature as long as the loss of symbiotic dinoflagellates lags behind the temperature stress, hence the deterimental combination of light and temperature stress is avoided. We have also hypothesised that exposure to the combined effect of temperature and light stress, will affect the rate of recovery from photoinhibition.
We extend previous studies that have largely concentrated on the ability of
Ostreobium sp. to harvest light and photosynthesise in dim
environments (Halldal, 1968;
Schlichter et al., 1997
;
Fork and Larkum, 1989
;
Koehne et al., 1999
) by
examining the response of an endolith phototrophic community (consisting
mainly of the green algae Ostreobium sp.) within the coral
Montipora monasteriata Forskal exposed to extreme solar and thermal
stress. We also examine the protective effect of the dinoflagellates during
stressful events and the following recovery of the endoliths. Our results
confirm a complex interaction between endolithic algae, symbiotic
dinoflagellates and their coral hosts.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The response of phototrophic endoliths to temperature and light stress
The portable underwater Pulse Amplitude Modulated (PAM) fluorometer
(Diving-PAM, Walz Gmbh, Effeltrich, Germany) was used to examine the
photosynthetic efficiency of endolithic algae inhabiting the skeletons of the
coral Montipora monasteriata Förskal under elevated light and
temperature. To examine possible synergistic effect of temperature and light
on the photosynthetic performance of phototrophic endoliths in M.
monasteriata we exposed corals to two levels of temperature and
irradiance in aquaria with sea water flow-through at Heron Island Research
Station. Pieces from five colonies of M. monasteriata were collected
at Wistari Reef, from an environment with PAR of 200-300 µmol
m-2 s-1 (at midday low tide), and cut into fragments
(3x3 cm-5x5 cm) using a band saw (fragments from different
colonies were mixed).
Fragments were acclimated in a tank with water flow-through and natural irradiance of 250 µmol m-2 s-1 (at midday) for 48 h prior to the experiment (Fig. 1). Coral tissue was removed from half of the surface area of 72 fragments (randomly picked from our pool of fragments) using an air gun, to expose the endoliths to increased irradiance. Twelve fragments were put in each aquarium: six that had their tissue removed from half their surface area and six that were left intact. Photosynthetic efficiency (Fv/Fm, where Fv is the variable fluorescence, Fm is the maximal fluorescence) was measured after adapting the corals to the dark for 30 min on the intact and exposed sections at the beginning of the experiment The fragments were then subjected to one of four treatments (three aquarium tank were included within each treatments); in treatment 1, fragments were exposed to sunlight (similar to habitat light levels, 300-350 µmol m-2 s-1 at midday) and heated to 31°C over 24 h to inflict both thermal and light stress; in treatment 2, fragments were exposed to sunlight and a temperature of 25°C; in treatment 3, fragments were shaded (50-100 µmol m-2 s-1 at midday) and heated to 31°C and in treatment 4, they were shaded and exposed to temperature of 25°C. 24 h after the beginning of the experiment the tissue from the intact half of each fragment and from three out of six of the intact fragments was removed using an air gun. At this point, measurement of dark-adapted Fv/Fm was repeated for the intact and exposed sections. The temperature in all treatments was stabilized at 25°C from 24 h onwards, and a daily measurement of Fv/Fm (dark-adapted) was performed on each of the fragments to examine their recovery from the heat/light stress. This was carried out for 6 days from the end of the heat stress (7 days from the beginning of the experiment, Fig. 1).
|
Since no significant difference was found between the Fv/Fm of fragments from different aquaria within a treatment, we analysed the results after pooling them together.
Two-way ANOVA was performed after transformation of log(x+1) to examine whether light level (sunlight/shaded) and temperature (25°C/31°C) affect the photosynthetic efficiency.
ANCOVA analysis was performed after transformation of log(x+1) to test the hypothesis that recovery of dinoflagellates and endolites varied following the different treatments.
Photosynthetic efficiency in exposed versus shaded endoliths
We measured the diurnal changes in photosynthetic efficiency of the
endolithic phototrophs under high and low irradiance. Three fragments of
M. monasteriata (10 cmx10 cm,) were ground using an industrial
grinder (in seawater) on their underside until the green band of the
endolithic phototrophes was exposed. Coral tissue was removed from half of the
surface of the fragment (Fig.
2A,B) using an air gun. Two fibre optic cables from two PAM
fluorometers were mounted under the coral fragment using `coral clips' (Walz
Gmbh), one facing the intact tissue section and one under the exposed bare
skeleton where tissue had been removed. The underside and sides of the coral
fragment were covered with black plasticine to allow light penetration through
the upper part only (i.e. through the dinoflagellates, coral tissue and
skeleton, or the coral skeleton only where tissue was removed). Measurements
were undertaken in aquaria under natural irradiance similar to that
experienced by the colonies within their habitat on the reef (200-300 µmol
m-2 s-1 at midday). PAR was monitored using the external
light meter of the PAM fluorometer. Two horizontal grooves were drilled into
the endoliths green band (one under intact and one under the exposed section)
and the coral sections carefully washed to remove any remaining skeletal dust.
The light sensor of the PAM fluorometers was inserted into each of the grooves
(Fig. 2B) so that it faced
upwards and then the groove was sealed using black plasticine. The light
sensor was pre-calibrated against a Li-Cor quantum sensor (LI-189; Li-Cor,
Lincoln, NE, USA). Measurements of both PAR and dynamic photosynthetic
efficiency were taken over a 24 h period.
|
Mass bleaching occurred in the reef flat and crest of Heron island in March
2004, after unusually high sea temperatures were experienced in the Coral Sea
and Great Barrier Reef in February and March 2004. We collected five partially
bleached colonies of M. monasteriata during this event as well as
performing measurements on the photosynthetic capacity of the phototrophic
endoliths under healthy and bleached sections of each colony. Rapid light
curves (RLC) were measured on dark-adapted corals to investigate the
photosynthetic performance of the endoliths and the endosymbiotic
dinoflagellates in bleached and healthy sections. To do this, optic fibre
sensors were positioned on the coral surface so that the tips were 3 mm from
the coral tissue surface. RLC consisted of dynamic yield measurements being
performed after each of a series of eight irradiances (lasting 10 s each). The
effective photosynthetic yield Y of photosystem II (PSII) was derived
from the Genty equation
Y=(Fm'-F)/Fm'
(Genty et al., 1989), where
F is the fluorescence under a given irradiance and
Fm' is the maximal fluorescence in light-adapted
dinoflagellate symbionts after the application of a short flash (0.8 s) of PAR
that was saturating for photosynthesis (approx. 6000 µmol photons
m-2 s-1).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
The photosynthetic performance of the endoliths (Fig. 3B,C) revealed a similar pattern to that seen in dinoflagellates. That is, there was a significant difference between Fv/Fm measured at time 0 and that measured 24 h after, fragments were exposed to 31°C (two-way RM-ANOVA, LSD, P<0.001) but no significant difference between time 0 and 24 h after, of fragments at 25°C (two-way RM-ANOVA, P>0.05). The lowest dark Fv/Fm was seen in heated and sun-exposed endoliths (Fig. 3B), which was significantly lower than the Fv/Fm of endoliths from the other three treatments (two-way RM-ANOVA, LSD, P<0.001). Endoliths from fragments that were heated in the shade and those kept at normal temperatures but exposed to sunlight had significantly higher dark-adapted Fv/Fm values than endoliths that were exposed to sun and heated (two-way ANOVA with repeated measures, LSD, P<0.001). Endoliths under the dinoflagellates (at 24 h) demonstrated significantly higher maximum dark-adapted Fv/Fm than endoliths that were exposed after tissue removal (two-way RM-ANOVA, LSD; P<0.001; Fig. 3C). These changes persisted even after longer periods of darkness, implying that the exposed endoliths had experienced chronic photoinhibition. Endoliths under dinoflagellates from fragments that were kept at 25°C (ambient temperatures) and exposed to sunlight showed the highest maximum dark-adapted Fv/Fm, followed by endoliths in shade at control temperatures (25°C) and heated (31°C) in the shade. The lowest values were always found under the combination of elevated temperature (31°C) and normal sunlight. The recovery of dinoflagellates following heating revealed that elevated temperature and sunlight can adversely affect the capability of dinoflagellates to recover from photodamage (r2=0.98; P<0.001; Fig. 4A). Even after a week, fragments that were exposed to 31°C and normal sunlight had not recovered fully whereas dinoflagellates from other treatments (including those exposed to 31°C in shade) recovered (ANCOVA, GLM analysis P<0.001; Fig. 4A).
|
Endoliths exposed to 31°C and normal sunlight exhibited a similar pattern of photosynthetic efficiency to the dinoflagellate symbionts and had not recovered after a week (ANCOVA; GLM analysis P<0.001; Fig. 4B). Endoliths from other treatments, however, recovered to their initial level, even reaching a higher dark-adapted values of Fv/Fm, possibly because of their photoacclimation to the increased irradiances after removal of the tissue and dinoflagellates. Endoliths that were shaded by the coral tissue and dinoflagellates recovered very rapidly under all treatments (ANCOVA, GLM analysis P<0.001; Fig. 4C).
Diurnal cycle
Comparison between the diurnal cycle of endoliths exposed to sun for 24 h
(after tissue removal) with those under healthy coral tissue revealed that the
dark-adapted Fv/Fm of the exposed
endoliths was constantly lower (Fig.
5). This corresponded with the irradiance measured within the
skeleton habitat of these endoliths after tissue removal. Irradiance in the
skeletons under dinoflagellates and coral tissue reached 25 µmol
m-2 s-1 at midday while irradiance within the skeletons
after tissue removal reached 200 µmol m-2 s-1 at
midday (Fig. 5 inset).
|
The dynamic (i.e. not dark-adapted) Fv/Fm of phototrophic endoliths from both healthy and exposed sections of the colony showed distinct changes over the course of the day, dropping from 0.5 to less than 0.3 by noon for endoliths under dinoflagellates and coral tissue. Dynamic Fv/Fm in endoliths in exposed skeletons decreased from 0.35 to less than 0.2 by noon. The lowest values of dynamic Fv/Fm always coincided with the highest irradiance. Fv/Fm began to increase again as light levels began to decrease in the early afternoon and had returned to their pre-dawn values 2 h after the initial drop in efficiency. Recovery of Fv/Fm after midday high irradiance was at a lower rate in exposed endoliths than endoliths under healthy tissue.
Endolithic algae of bleached corals on the reef crest
Exposed endoliths had significantly higher photosynthetic efficiencies than
those under more pigmented parts of partially bleached colonies found on the
Heron Island reef crest during the 2004 bleaching event (maximum dark-adapted
Fv/Fm was 0.44 and 0.53 respectively;
Fig. 6). Photosynthetic
efficiencies of dinoflagellates in more pigmented parts of the colony were
significantly higher than those in the bleached parts of the same colony (max
Fv/Fm of 0.69). Endoliths under
bleached areas had a max Fv/Fm of 0.58
whereas endoliths under more pigmented areas (under dinoflagellates)
demonstrated significantly lower quantum efficiency under all irradiances
during RLCs than endoliths under bleached parts of the colony, implying
photoacclimation of the latter (Regression analysis
r2=0.99, P<0.001,
Fig. 6).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In the present study we demonstrate that the response of phototrophic
microendoliths to thermal and irradiance stress is similar to that of the
symbiotic dinoflagellates. As in symbiotic dinoflagellates, the combined
affect of temperature and light on the microendoliths is detrimental to the
ability of the organisms to process captured light excitations (Warner et al.,
1996,
1999
) and recovery from the
combined damage may take several days to weeks, depending on intensity and
period of exposure. The combined effects of elevated temperature and
irradiance were much higher in both dinoflagellates and endoliths, causing a
decrease of 25% and 80% in dark-adapted
Fv/Fm, respectively. Increased
temperature or irradiance alone causes the
Fv/Fm of exposed endoliths to decrease
by 53% or 14%, respectively. Elevated temperature in this case caused a more
severe photoinhibition than increased irradiance following exposure. This
finding was reinforced by the higher performance of endoliths in areas of the
skeleton covered by tissue and symbionts, as compared to exposed areas. The
former demonstrated a decrease in
Fv/Fm when incubated in 31°C as
compared with their equivalent fragments that were incubated in the ambient
temperature of 25°C (Fig.
3C).
Our findings suggest that if a coral is shaded or does not lose all of its
endosymbiotic dinoflagellates during bleaching, conditions are less stressful
and promote a more rapid recovery of the skeletal endoliths. These results
match those of Fine et al.
(2004), who demonstrated that
the endolithic algae of shade adapted Mediterranean coral, Oculina
patagonica, rapidly photoacclimate to increased irradiance during
repetitive bleaching events. In the Mediterranean, temperature stress on the
holobiont may prevail for 3 month and coral colonies may remain bleached for
almost 8 months of the year.
The recovery of phototrophic endoliths was also found to be delayed by the
combined effect of thermo/solar stress
(Fig. 4). Intact endoliths that
were under the protection of dinoflagellates during the extreme thermal
stress, showed a rapid increase in
Fv/Fm when tissue was removed at the
end of the thermal stress, suggesting photoacclimation to increased
irradiance. This may explain the observations from previous studies in which
endolithic algae bloom after bleaching
(Diaz-Pulido and McCook, 2002;
Fine and Loya, 2002
;
Fine et al., 2004
) or coral
death (Le Campion-Alsumard, 1995).
Our observations suggest that outcome for endoliths after stressful conditions depends to a large extent on two major parameters. These are (1) the microhabitat the coral lives in (reef-flat, reef-crest, overhang) and (2) the response time of the coral host and endosymbiont to the stress and recovery. In coral species that respond quickly to the thermal/solar stress and consequently bleach or die rapidly, the endoliths will be exposed to the combined effect and photo-damage may significantly prolong recovery time. In short events or in the case of more tolerant coral species, this may allow rapid recovery and photoacclimation of the endoliths, even if the coral eventually bleach after the thermal stress is over. This is supported by our observations in a natural bleaching event where endoliths under the bleached section of the coral showed higher Fv/Fm, and hence photoacclimation, than endoliths under more normally pigmented parts of the same colony (Fig. 6).
Mass coral bleaching events are triggered by periods in which sea
temperatures rise above the long-term averages for a particular region.
Plant-animal endosymbioses appear sensitive to changes in temperature, which
result in an increased sensitivity of the dinoflagellate symbiont to
photoinhibition (Iglesias-Prieto et al.,
1992; Fitt and Warner,
1995
; Iglesias-Prieto,
1995
; Warner et al.,
1996
; Jones et al.,
1998
), cellular damage and eventually disintegration (but see
Takahashi et al., 2004
). Our
findings suggest that increased sea water temperature leads to increased
sensitivity to photoinhibition of the phototrophic microendoliths and that
heat stress is amplified by the presence of PAR.
The endolithic-reef-building coral relationship is considered to be an
ectosymbiosis (Schlichter et al.,
1995) yet the symbiosis does not break down following thermal
stress as does coral-dinoflagellate symbioses. Healthy photoacclimated
endolithic communities may be beneficial to bleached coral as pointed out by
Fine and Loya (2002
), showing
that endolithic algae in bleached areas of a coral colony can be a significant
source of photoassimilates. Photoassimilates released from the phototrophic
endolithic algae reach the coral tissue and, the dissolved organic substances
can be taken up by the coral utilised
(Schlichter et al., 1995
).
We suggest that the response of the holobiont to stress is a result of the combined responses of each of its components (host zooxanthellae and endoliths) to the stress factor.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Brown, B. E. (1997). Coral bleaching, causes and consequences. Proc. 8th Int. Coral Reef Symp.65 -74.
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.[CrossRef]
Diaz-Pulido, G. and McCook L. J. (2002). The fate of bleached corals: Patterns and dynamics of algal recruitment. Mar. Ecol. Prog. Ser. 232,115 -128.
Egana, A. C. and DiSalvo, L. H. (1982). Mass expulsion of zooxanthellae by Easter Island corals. Pacific Sci. 36,61 -63.
Fine, M. and Loya, Y. (2002). Endolithic algae - an alternative source of energy during coral bleaching. Proc. R. Soc. Lond. B. 269,1205 -1210.[CrossRef][Medline]
Fine, M. Steindler, L. and Loya, Y. (2004). Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar. Freshwater Res. 55,115 -121.[CrossRef]
Fitt, W. K. and Warner, M. E. (1995). Bleaching patterns of four species of Caribbean reef corals. Biol. Bull. 187,298 -307.
Fork, D. C. and Larkum, A. W. D. (1989). Light harvesting in the green-alga Ostreobium sp, a coral symbiont adapted to extreme shade. Mar. Biol. 103,381 -385.[CrossRef]
Genty, B., Briantais, J. M. and Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990,97 -102.
Gleason, D. F. and Wellington, G. M. (1993). Ultraviolet-radiation and coral bleaching. Nature 365,836 -838.[CrossRef]
Glynn, P. W. and D'Croz, L. (1990). Experimental evidence for high temperature stress as the cause of El Niño coincident coral mortality. Coral Reefs 8, 181-191.[CrossRef]
Glynn, P. W. (1991). Coral-reef bleaching in the 1980s and possible connections with global warming. Trends Ecol. Evol. 6,175 -179.[CrossRef]
Glynn, P. W. (1993). Coral-reef bleaching-ecological perspectives. Coral Reefs 12, 1-17.
Goreau, T. F. (1964). Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science 145,383 -386.
Goreau, T. J. and Hayes, R. L. (1994). Coral bleaching and ocean `hot spots'. Ambio 23,176 -180.
Halldal, P. (1968). Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol. Bull. Mar. Biol. Lab, Woods Hole 134,411 -424.
Highsmith, R. C. (1981). Lime-boring algae in coral skeletons. J. Exp. Mar. Biol. Ecol. 55,267 -281.[CrossRef]
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 zooxanthallae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J. Exp. Mar. Biol. Ecol. 129,279 -303.[CrossRef]
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50,839 -866.
Iglesias-Prieto, R. Matta, J. L., Robins, W. A. and Trench, R. K. (1992). Photosynthetic response to elevated temperature in the symbiotic dinoflagellates Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. USA 89,10302 -10305.[Abstract]
Iglesias-Prieto, R. (1995). The effects of elevated temperature on the photosynthetic responses of symbiotic dinoflagellates. In Light to Biosphere (ed. P. Mathis), pp. 793-796. Netherlands: Kluwer.
Jeffrey, S. W. (1968). Pigment composition of siphonale algae in the brain coral Favia. Biol. Bull. 135,141 -148.
Jokiel, P. L. and Coles, S. L. (1977). Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol. 43,201 -208.[CrossRef]
Jokiel, P. L. and Coles, S. L. (1990). Response of Hawaiian and other Indo-Pacific reef corals to elevated temperatures. Coral Reefs 8,155 -161.[CrossRef]
Jones, R. J. (1997). Zooxanthella loss as a bioassay for assessing stress in corals. Mar. Ecol. Prog. Ser. 149,163 -171.
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.[CrossRef]
Jones, R. J. and Hoegh-Guldberg, O. (1999). Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing. Mar. Ecol. Prog. Ser. 177, 83-91.
Jones, R. J., Muller, J., Haynes, D. and Schreiber, U. (2003). Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia. Mar. Ecol. Prog. Ser. 251,153 -167.
Kanwisher, J. W. and Wainwright, S. A. (1967). Oxygen balance in some reef corals. Biol. Bull. 133,378 -390.
Kleppel, G. S., Dodge, R. E. and Reese, C. J. (1989). Changes in pigmentation associated with the bleaching of stony corals. Limnol. Oceanogr. 34,1331 -1335.
Koehne, B., Elli, G., Jennings, R. C., Wilhelm, C. and Trissl, H. W. (1999). Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim. Biophys. Acta Bioenerget. 1412,94 -107.[CrossRef]
Kushmaro, A., Loya, Y., Fine, M. and Rosenberg, M. (1996). Bacterial infection and coral bleaching. Nature 380,396 .
Le Campion-Alsumard, T., Golubic, S. and Hutchings, P. (1995). Microbial endoliths in skeletons of live and dead corals, Porites lobata (Moorea, French Polynesia). Mar. Ecol. Prog. Ser. 117,149 -157.
Lesser, M. P., Stochaj, W. R., Tapley, D. W. and Shick, J. M. (1990). Bleaching in coral-reef anthozoans - effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8, 225-232.
Lukas, K. J. (1974). Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J. Phycol. 10,331 -335.
Saxby, T., Dennison, W. C. and Hoegh-Guldberg, O. (2003). Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Mar. Ecol. Prog. Ser. 248,85 -97.
Schlichter, D., Zscharnack, B. and Kerisch, H. (1995). Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82,561 -564.[CrossRef]
Schlichter, D., Kampmann, H. and Conrady, S. (1997). Trophic potential and photoecology of endolithic algae living within coral skeletons. PSZN. Mar. Ecol. 18,299 -317.
Shashar, N., Banaszak, A. T., Lesser, M. P. and Amrami, D. (1997). Coral endolithic algae: life in a protected environment. Pacific Sci. 51,167 -173.
Shibata, K. and Haxo, F. T. (1969). Light transmition and spectral distribution through epi- and endozoic algal layers in the brain coral Favia. Biol. Bull. 136,461 -468.
Takahashi, S., Nakamura, T., Sakamizu, M., van Woesik, R. and
Yamasaki, H. (2004). Repair machinery of symbiotic
photosynthesis as the primary target of heat stress for reef-building corals.
Plant Cell Physiol. 45,251
-255.
Vaughan, T. W. (1914). Reef corals of the Bahamas and of southern Florida. Carnegie Institution of Washington, Year Book for 1914:222 -226.
Warner, M. E., Fitt, W. K. and Schmidt, G. W. (1996). The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 19,291 -299.
Warner, M. E., Fitt, W. K. and Schmidt, G. W.
(1999). Damage to photosystem II in symbiotic dinoflagellates: A
determinant of coral bleaching. Proc. Natl. Acad. Sci.
USA 96,8007
-8012.
Yonge, C. M and Nichols, A. G. (1931). Studies on the physiology of corals: The effect of starvation in light and in darkness on the relationship between corals and zooxanthellae. Sci. Rep. Great Barrier Reef Exp. 1,177 -211.