Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata
Centre Scientifique de Monaco, Avenue Saint-Martin, MC-98000 Monaco (Principality)
* Author for correspondence (e-mail: fhoulbreque{at}centrescientifique.mc)
Accepted 2 February 2004
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Summary |
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Key words: coral, feeding, photosynthesis, calcification, organic matrix, 14C-aspartate, 45Ca
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Introduction |
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The major role of feeding is to provide the symbiosis with essential
nutrients such as nitrogen and phosphorus
(Rahav et al., 1989;
Cook et al., 1994
). Both host
and algal symbionts respond quickly to food availability
(Fitt, 2000
). At the algal
level, Dubinsky et al. (1990
)
as well as Titlyanov et al.,
(2000a
,b
,
2001
) showed an enhancement of
the areal pigmentation and zooxanthellae density in fed corals, leading to an
increase in the areal photosynthesis. At the animal level, heterotrophy tends
to increase the amount of tissue synthesis
(Jacques and Pilson, 1980
;
Sebens and Johnson, 1991
;
Kim and Lasker, 1998
). An
enhancement in skeletal growth has also been observed, suggesting that corals
allocate a high proportion of the energy brought by food to calcification
processes (Jacques and Pilson,
1980
; Witting,
1999
; Ferrier-Pagès et
al., 2003
; Houlbrèque
et al., 2003
). Although it is well known that nutrients are
continuously exchanged between the two partners
(Muscatine, 1990
), few studies
have focused on the simultaneous effect of feeding on the algal and animal
components (Witting, 1999
;
Ferrier-Pagès et al.,
2003
; Houlbrèque et
al., 2003
). Here, we build on this knowledge base by providing an
experimental analysis of the interactions between heterotrophy, photosynthesis
and calcification in corals.
Feeding has also been shown to enhance skeletal growth, suggesting that
corals allocate a high proportion of the energy brought by food to
calcification processes (Jacques and
Pilson, 1980; Witting,
1999
; Ferrier-Pagès et
al., 2003
; Houlbrèque
et al., 2003
). It is important to note that calcification is also
a dual process, involving the secretion of an organic matrix and the
deposition of a CaCO3 fraction. The presence of an organic matrix
in coral skeletons is widely documented
(Goreau and Goreau, 1959
;
Wainwright, 1963
;
Young, 1971
;
Constantz and Weiner, 1988
;
Cuif and Gautret, 1995
:
Dauphin and Cuif, 1997
) and is
considered an essential prerequisite in the formation of a biomineral strucure
(Goreau and Goreau, 1959
;
Cuif et al., 1997
;
Allemand et al., 1998
). This
matrix potentially plays key roles in various processes such as crystal
nucleation and growth, crystal size and orientation and regulation of skeletal
formation (Weiner and Addadi,
1991
; Falini et al.,
1996
; Belcher et al.,
1996
). Cuif et al.
(1999
) demonstrated that the
composition of the matrix was different between symbiotic and asymbiotic
corals, and Allemand et al.
(1998
) suggested that
heterotrophy is a source of aspartic acid, one of the major components of the
coral matrix (Young, 1971
;
Cuif and Gautret, 1995
;
Dauphin and Cuif, 1997
). We
therefore investigated the effect of feeding on both organic matrix synthesis
and calcification.
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Materials and methods |
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Tanks were supplied with oligotrophic Mediterranean seawater, pumped from
50 m depth at a rate of 2 l h1 and mixed using a submersible
pump (Aquarium system, mini-jet MN 606, Mentor, OH, USA). The velocity of flow
across the corals was approximately 0.61 cm s1, as
measured by timing the passage of neutrally buoyant beads. Filtered seawater,
maintained at 26°C, had low amounts of organic and inorganic nutrients
(Ferrier-Pagès et al.,
1998). Corals received a constant irradiance of 350 µmol
photons m2 s1 (photoperiod was 12 h:12 h
light:dark) using metal halide lamps (Philips, HPIT, 400 W, Eindhoven, The
Netherlands). Tanks and nylon nets were cleaned several times per week in
order to avoid algal growth on the nylon nets.
Experimental design
Microcolonies were then divided into two groups (two tanks per group)
corresponding to two feeding levels: (1) starved corals (SC) were not fed
during the whole experiment; (2) fed corals (FC) were fed 4 days per week
(Monday, Wednesday, Thursday and Friday). On Monday and Friday corals were fed
Artemia salina nauplii (2022±115 shrimps l1)
and on Wednesday and Thursday they were fed freshly collected Mediterranean
zooplankton (1005±164 organisms l1). Copepods
represented 94% of the plankton, followed by lesser numbers of siphonophores,
brachiopods, crustacean larvae and jellyfish. The ingestion of prey was
controlled under a dissecting microscope during feeding
(Ferrier-Pagès et al.,
2003). The number of prey items ingested was proportional to prey
density and capture rates varied from 0.06 to 1 prey items
polyp1 day1
(Ferrier-Pagès et al.,
2003
). These rates were in the same range as previous estimates
for other coelenterates (Lasker et al.,
1983
; Sebens et al.,
1996
).
Plankton were collected using a WP2 net and immediately brought back to the laboratory. They were concentrated with a reverse filtration apparatus on a 10 µm filter, to remove small algae and detritus. They were then added to heated seawater, and the actively swimming portion of the sample was fed to the corals during a 1 h period. A 100 ml sample was collected from the aquaria at each feeding time to determine the nature and abundance of the planktonic prey using a binocular microscope (Wild M3, 40x) and a Dolfuss tank. After feeding, the aquaria were emptied entirely and refilled with fresh filtered seawater to avoid contamination by dissolved and organic nutrients coming from the degrading prey.
Microcolonies were maintained under these conditions for 8 weeks. Changes in photosynthesis, tissue composition (protein and chlorophyll contents), cell-specific density (CSD), rates of aspartic acid incorporation and calcification were measured after 3 and/or 8 weeks, depending on the assay.
Photosynthesisirradiance (P/I) curves
Rates of photosynthesis and respiration were measured after 3 weeks on five
microcolonies (replicates) taken from each tank (total=20 colonies, 10 fed and
10 starved corals, respectively). Each microcolony was placed in a
respirometric glass chamber containing a `Strathkelvin 928®' electrode
(Glasgow, UK) and immersed in a water bath (26°C). The incubation medium
was continuously stirred with a magnetic stirring bar. Photosynthesis
vs. irradiance (P/I) curves were constructed by measuring production
rates across a range of irradiances. Samples were incubated for 10 min under
different light levels (0, 50, 80, 120, 200, 300, 400, 500, 600, 800 µmol
m2 s1). Light was provided by a 400 W
metal halide lamp (Philips, HPIT) attenuated to the desired intensity with
screens placed between the light source and the aquaria. Before each
experiment, the oxygen sensor was calibrated against air-saturated seawater
(100% oxygen) and a saturated solution of sodium dithionite (zero oxygen).
Oxygen was monitored every 10 s on an acquisition station. Rates of
photosynthesis and respiration were estimated by regressing oxygen data
against time.
The following function was fitted to the photosynthesisirradiance
data (Barnes and Chalker,
1990).
![]() | (1) |
From the same corals, chlorophylls a and c2
were extracted twice in 100% acetone (24 h at 4°C). The extracts were
centrifuged at 6000 g for 20 min and the absorbencies read at
630, 663 and 750 nm. Chlorophyll concentrations were computed according to the
spectrometric equations of Jeffrey and Humphrey
(1975) and were expressed per
surface area (cm2). Surface area was measured using the aluminium
foil technique (Marsh,
1970
).
Estimation of the cell-specific density (CSD)
After 3 weeks, CSD was determined for five colonies (replicates) taken from
each tank (N=10 fed and 10 starved corals, respectively). Cells were
extracted mechanically by shaking (using a wrist-action) crushed coral in a
flask (Muscatine and Cernichiari,
1969). Host cells containing symbionts were observed under a Leica
microscope (50x; Wetzlar, Germany), and the number of algae contained in
each cell was counted for 300 host cells per sample. Data were expressed in
terms of the frequency or percentage distribution of host cells
(fi) with a given number of algae per cell
(ri).
The average cell-specific density (CSD) was calculated as:
![]() | (2) |
Measurements of skeletal calcium and aspartic acid incorporation
Measurements were performed both in the light and in the dark after 3 and 8
weeks of treatment. Corals were incubated in the morning to avoid variations
due to endogenous circadian rhythms
(Buddemeier and Kinzie, 1976;
Tambutté et al., 1995
).
For each sampling period (3 and 8 weeks), three replicates microcolonies,
randomly taken in each tank, were used for each measurement (a total of 48
colonies, N=6 for starved and fed corals and each measurement,
respectively). Calcification rates were measured using 45Ca
according to the method of Tambutté et al.
(1995
). Organic matrix
synthesis was measured as skeletal incorporation of 14C-aspartic
acid and protocols were adapted from Allemand et al.
(1998
) and Tambutté et
al. (1995
,
1996
). 45Ca- and
14C-aspartic acid incorporations were studied in separate
colonies.
Each microcolony was placed in a plastic holder and incubated for 2 h in an
8 ml beaker containing either 16 kBq ml1 of
45CaCl2 (NEN, LifeScience Products, France) or 833 Bq
ml1 of 14C-aspartic acid (NEN) dissolved in
seawater. Corals for dark incubations were sampled at the end of the night (1
h before the lights were switched on) and were maintained in the dark during
the whole incubation. The results are expressed either as nmol Ca2+
g1 dry skeletal mass or as a fraction of the total
radioactivity initially present in the external medium (%RAV;
14C-aspartic acid g1 dry skeletal mass)
(Allemand et al., 1998).
Protein content of the radioactive tissue was measured using the BC Assay Kit
(Interchim, Montluçon, France), based on the colorimetric determination
of the amount of protein (Smith et al.,
1985
). The standard curve was established with bovine serum
albumin.
In the Results, the amounts of protein and chlorophyll are normalized per
unit surface area and the rates of photosynthesis per unit surface area or per
amount of chlorophyll. The rates of calcification and aspartic acid
incorporation are normalized per g skeletal dry mass in order to facilitate
comparisons with the previous results of Allemand et al.
(1998).
Statistical analyses
The effects of feeding on the physiological parameters were tested using a
t-test (software Stat-View 4.01, Abacus concept, Inc, Berkeley, CA,
USA). The effect of feeding on the CSD was analysed using a Pearson
2 test.
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Results |
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|
|
Photosynthesisirradiance (P/I) curves
Mean P/I curves obtained for each treatment are shown in
Fig. 2. Table 2 represents the
calculated mean values for
, Ik,
Ic and
. When normalized per surface area, feeding
significantly increased the rates of maximum net photosynthesis
(
) (570±60
vs. 200±20 nmol O2 cm2
h1 for FC and SC, respectively) and the Talling index
(Ik) (403±27 and 203±11 µmol photons
m2 s1, respectively, for FC and SC).
Conversely, when data were normalised per chlorophyll a
concentrations, feeding did not have any significant effect on
(t-test, d.f.=4,
P=0.13) (Table 2). For
both normalizations, there was no significant difference in the respiration
rates between FC and SC (t-test, d.f.=0.6, P=0.50)
(Table 2).
|
|
Cell-specific density
Fig. 3 shows the percentage
distribution of the number of algae per host cell. Host cells containing a
single dinoflagellate (singlet) predominate (62.3% and 70.4% of the total
cells for FC and SC, respectively) followed in decreasing frequency by those
containing two (doublet) (34.3% in FC and 28.3% in SC), three (triplet; 3.0%
in FC and 0.7% in SC), and up to four cells (quadruplet; 0.4% in FC and 0.7%
in SC). In FC, the number of doublets and triplets significantly increased
during the incubation compared to the SC. Therefore, CSD was significantly
higher in FC (1.416±0.028) than in SC (1.316±0.015) (Pearson
2 test, d.f.=1, P=0.04).
|
Calcification rates
After 3 weeks, there was no significant difference in the calcification
rates measured in the light between FC and SC
(Fig. 4A,
Table 1). However, after 8
weeks, FC showed significantly higher light calcification rates than SC
(Fig. 4B,
Table 1). For the two sampling
periods, feeding enhanced the dark calcification rates, which were twice as
high in FC compared to starved corals (Fig.
4A,B, Table 1). For
the two sampling periods, rates of dark calcification were 610 times
lower than those of light calcification
(Fig. 4A,B).
|
Effects of feeding on organic matrix synthesis
After 3 weeks, we found no significant effect of feeding on the light and
dark incorporations (Fig. 5A,
Table 1). After 8 weeks,
however, feeding significantly changed the rate of incorporation in both the
light and the dark (Fig. 5B,
Table 1). Incorporation rates
in the light were increased by two thirds in FC compared to SC. The uptake
rates in the dark were three times higher in FC than in SC. In both cases,
darkness markedly reduced the incorporation of 14C aspartic acid
into the skeleton (Fig. 5A,B).
After 8 weeks, the rates of incorporation in the dark were, respectively, 14
and 8 times lower than the uptake rates in the light for starved and fed
corals (Fig. 5B). Feeding did
not affect the ratios of calcification rate/aspartic acid incorporation,
measured in the light (Fig. 6).
However this ratio is 1.822.64 higher in the dark for both fed and
starved corals, respectively.
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Discussion |
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One of the aims in this work was to understand by which mechanism feeding
enhances calcification. Both light and dark calcification rates were greatly
enhanced by feeding; after 8 weeks of incubation, these rates were twice as
high in fed than in starved corals. This stimulation had already been noticed
in a previous experiment performed with the same species
(Houlbrèque et al.,
2003) and validates recent results showing a positive effect of
heterotrophy on coral growth (Kim and
Lasker, 1998
; Anthony and
Fabricius, 2000
; Witting,
1999
; Ferrier-Pagès et
al., 2003
). A light-enhanced (or dark-repressed) calcification
(Goreau and Goreau, 1959
;
Barnes and Chalker, 1990
;
Gattuso et al., 1999
;
Houlbrèque et al.,
2003
) was also noticed with rates of dark calcification 610
times lower than rates of light calcification.
Calcification is carried out in two processes, i.e. the secretion of an
organic matrix and the deposition of calcium carbonate. The presence of an
organic matrix in corals has been a matter of much controversy
(Constantz, 1986), but its
existence is now well-demonstrated, both from studies performed on
scleractinian corals (Goreau and Goreau,
1959
; Cuif et al.,
1997
; Allemand et al.,
1998
) and on other calcifying organisms
(Belcher et al., 1996
;
Falini et al., 1996
). Cuif and
Gautret (1999
) showed that the
amino acid composition of the organic matrix differs between zooxanthellate
and azooxanthellate corals, suggesting that their nutritive source may affect
the organic matrix synthesis. Aspartic acid, for example, is one of the major
and most abundant amino acids in the coral matrix
(Young, 1971
;
Cuif and Gautret, 1995
;
Dauphin and Cuif, 1997
).
Allemand et al. (1998
) also
showed that no aspartic acid pool was present inside the coral tissue,
suggesting the need for a constant supply from an exogenous source. By using
14C-aspartic acid as a precursor for organic matrix synthesis
(Allemand et al., 1998
), we
measured a higher incorporation of this amino acid into the organic matrix of
fed corals. Since feeding has increased the unlabelled amino acid pool present
within the tissue, the rates of incorporation in fed animals are likely to be
underestimated, suggesting that the enhancement of the organic matrix
synthesis by feeding is even higher.
Feeding might therefore have enhanced the construction of the organic
matrix by (i) supplying additional input of energy, especially for the dark
processes. Under high plankton concentrations, such as those provided for the
fed corals in this study, uptake of organic carbon (and hence energy) may be
significant and could provide some energy for calcium/proton exchange at
night. Alternatively, the larger biomass of fed corals may have provided
larger energy stores for dark processes
(McConnaughey and Whelan,
1997; Anthony et al.,
2002
). Thus, feeding might have (ii) directly provided the
necessary `external' amino acids and/or (iii) indirectly increased
photosynthesis and therefore the supply of `autotrophic' amino acids. When
normalized per amount of chlorophyll, the rates of photosynthesis were
unchanged between fed and starved corals, suggesting that feeding does not
increase the efficiency with which symbionts (or reaction centers) use light
for photosynthesis. However, when normalized per surface area, the rates of
photosynthesis were higher in fed corals, with a change in photosynthetic
parameters, such as
and
Ik. The increase in
, already observed by
Titlyanov et al. (2001
),
generally corresponds to an increase in the number of photosynthetic units
(Prezelin, 1987
). Davy and
Cook (2001
) obtained similar
results in fed and starved sea anemones and showed that the percentage
translocation of photosynthates remained unchanged between the two treatments.
This is presumably because the surplus carbon was stored by the algae rather
than being translocated. However, several authors have demonstrated that even
if the amount of translocated photosynthates is unchanged between starved and
fed animals, their quality is completely different
(Swanson and Hoegh-Guldberg,
1998
; Wang and Douglas,
1999
). Since the supply of nitrogen directly influences the
zooxanthellar C:N ratio (Snidvongs and
Kinzie III, 1994
; Grover et
al., 2002
), feeding might have increased the amino acid synthesis
compared to the production of non-nitrogenous compounds such as glycerol and
glucose (Swanson and Hoegh-Guldberg,
1998
; Wang and Douglas,
1999
). This higher amount of translocated amino acids might have
enhanced the synthesis of the organic matrix. However, this question can only
be answered by investigating the quality of the photosynthates produced by fed
and starved corals.
The second main conclusion that can be derived from this study is that the
effect of feeding on aspartic acid incorporation is comparable to its effect
on calcium incorporation. Feeding enhanced both light and dark processes, with
a higher enhancement in the dark (threefold increase) than in the light
(1.6-fold increase). To determine the link between the deposition of organic
and mineral fractions, we compared the ratio of CaCO3/aspartate
incorporation. The dark ratio was 1.82.6 higher than the light ratio
(for fed and starved corals, respectively), which suggests that the
interactions between the organic and mineral fractions were affected by
light/dark conditions. In the dark, there may have been a decrease in the
organic matrix synthesis, an increase in the mineral fraction deposition or a
combination of both events. From Figs
4B and
5B, it appears that the more
important process should be a decrease of dark organic-matrix synthesis. This
decreased fourteen-fold (Fig.
5B), while dark calcification decreased only sevenfold
(Fig. 4B). This phenomenon,
observed here for the first time, could be responsible for the diurnal bands
observed in coral skeletons (Barnes,
1973). A higher dark inhibition of organic matrix synthesis
vs. CaCO3 deposition may be explained by the lack of
photosynthates as organic matrix precursors
(Cuif et al., 1999
) or by some
other unknown process. In either case, this suggests a close relationship
between calcification, organic matrix synthesis and photosynthesis. These
results are in agreement with the hypothesis of Barnes et al.
(1989
, 1990) and Taylor et al.
(1993
), who suggested a cyclic
deposition of skeleton leading to the formation of skeletal banding in
scleractinian corals.
Feeding did not affect the CaCO3/aspartate deposition in the
light. This result suggests a close coupling between organic matrix synthesis
and CaCO3 deposition in the light. This coupling appears less
strict in the dark where feeding induces a slight decrease of the ratio. Since
it has been previously shown that the organic matrix synthesis is a
prerequisite step for calcification
(Allemand et al., 1998), the
increase in the rates of calcification in fed corals might therefore be
induced by an increase in the rates of feeding-induced organic matrix
synthesis. Corals may derive some important source of amino acid and/or energy
for their growth from external food supplies. Another conclusion can be drawn
from the comparison of the ratio between starved/fed and light/dark
treatments. Since these ratios were different from each other, we suggest that
autotrophy and heterotrophy do not affect calcification in the same way.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Allemand, D., Tambutté, E., Girard, J. P. and Jaubert,
J. (1998). Organic matrix synthesis in the scleractinian
coral Stylophora pistillata: role in biomineralization and potential
target of the organotin tributyltin. J. Exp. Biol.
201,2001
-2009.
Anthony, K. R. N. (1999). Coral suspension feeding on fine particulate matter. J. Exp. Mar. Biol. Ecol. 232,85 -106.[CrossRef]
Anthony, K. R. N. and Fabricius, K. E. (2000). Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252,221 -253.[CrossRef][Medline]
Anthony, K. R. N., Connolly, S. R. and Willis, B. L. (2002). Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol. Oceanogr. 47,1417 -1429.
Barnes, D. J. (1973). Growth in colonial scleractinians. Bull. Mar. Sci. 23,280 -298.
Barnes, D. J., Lough, J. M. and Tobin, B. J. (1989). Density measurements and the interpretation of X-radiographic images of slices of skeleton from the colonial hard coral Porites. J. Exp. Mar. Biol. Ecol. 131, 45-60.[CrossRef]
Barnes, D. J. and Chalker, B. E. (1990). Calcification and photosynthesis in reef-building corals and algae. In Ecosystems of the World, vol25 , Coral Reefs (ed. Z. Dubinsky), pp.109 -131. Amsterdam: Elsevier.
Belcher, A. M., Wux, X. H., Christensen, R. J., Hansma, P. K., Stucky, G. D. and Morse, D. E. (1996). Control of crystal phase switching and orientation by soluble mollusc shell proteins. Nature 381,56 -58.[CrossRef]
Buddemeier, R. W. and Kinzie, R. A. (1976). Coral growth. Oceanogr. Mar. Biol. Annu. Rev. 14,183 -225.
Constantz, B. R. (1986). Coral skeleton construction: A physiochemically dominated process. The Society of Economic Paleontologists and Mineralogists. Palaios 1, 152-157.
Constantz, B. and Weiner, S. (1988). Acidic macromolecules associated with the mineral phase of scleractinian coral skeletons. J. Exp. Zool. 248,253 -258.
Cook, C. B., Muller-Parker, G., Orlandini, C. D. (1994). Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanthellae symbiotic with the reef corals Madracis mirabilis and Montastrea annularis. Mar. Biol. 118,157 -165.
Cuif, J. P. and Gautret, P. (1995). Glucides et protéines de la matrice soluble des biocristaux de Scléractiniaires Acroporidés. C. R. Acad. Sci. Paris II 320,273 -278.
Cuif, J. P., Dauphin, Y. and Gautret, P. (1997). Biomineralization features in scleractinian coral skeletons source of new taxonomic criteria. Bol. Real. Soc. Esp. Hist. Nat. Section Geolog. 92,129 -41.
Cuif, J. P., Dauphin, Y., Freiwald, A., Gautret, P. and Zibrowius, H. (1999). Biochemical markers of zooxanthellae symbiosis in soluble matrices of skeleton of 24 Scleractinia species. Comp. Biochem. Physiol. 123A,269 -278.
Dauphin, Y. and Cuif, J. P. (1997). Isoelectric properties of the soluble matrices in relation to the chemical composition of some skeractinian skeletons. Electrophoresis 18,1180 -1183.[Medline]
Davy, S. K. and Cook, C. B. (2001). The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Mar. Biol. 139,999 -1005.[CrossRef]
Dubinsky, Z., Stambler, N., Ben-Zion, M., McCloskey, L. R., Muscatine, L. and Falkowski, P. G. (1990). The effect of external nutrient resources on the optical properties and photosynthic efficiency of Stylophora pistillata. Proc. R. Soc. Lond. B 239,231 -246.
Falini, G., Albeck, S., Weiner, S. and Addadi, L. (1996). Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271, 67-69.[Abstract]
Falkowski, P. G., Dubinsky, Z., Muscatine, L. and Porter, J. W. (1984). Light and bioenergetics of a symbiotic coral. Bioscience 11,705 -709.
Farrant, P. A., Borowitzka, M. A., Hinde, R. and King, R. J. (1987). Nutrition of the temperate Australian soft coral Capnella gaboensis. Mar. Biol. 95,575 -581.
Ferrier-Pagès, C., Allemand, A., Gattuso, J. P. and Jaubert, J. (1998). Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol. Oceanogr. 43,1639 -1648.
Ferrier-Pagès, C., Witting, J., Tambutté, E. and Sebens, K. (2003). Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22,229 -240.[CrossRef]
Fitt, W. K. (2000). Cellular growth of host and symbiont in a cnidarianzooxanthellar symbiosis. 198,110 -120.
Furla, P., Allemand, D. and Orsenigo, M. N. (2000). Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am. J. Physiol. 278,870 -881.
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.
Goreau, T. F. and Goreau, N. I. (1959). The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under different conditions. Biol. Bull. 117,239 -250.
Grover, R., Maguer, J. F., Reynaud-Vaganay, S. and Ferrier-Pagès, C. (2002). Uptake of ammonium by the scleractininan coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations. Limno. Oceanol. 47,782 -790.
Houlbrèque, F., Tambutté, E. and Ferrier-Pagès, C. (2003). Effect of zooplankton availability on the rates of photosynthesis, tissue and skeletal growth of the scleractinian coral Stylophora pistillata J. Exp. Mar. Biol. Ecol. 296,145 -166.[CrossRef]
Jacques, T. G. and Pilson, M. E. Q. (1980). Experimental ecology of the temperate scleractinian coral Astrangia danae. I Partition of respiration, photosynthesis and calcification between host and symbionts. Mar. Biol. 60,167 -178.
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. 17,191 -194.
Jokiel, P. L, Maragos, J. E., Franzisket, L. (1978). Coral growth: buoyant weight technique. In Coral Reefs: Research Methods. Monographs on Oceanographic Methodology, vol. 5 (ed. D. R. Stoddart and R. E. Johannes), pp. 379-396. Paris: UNESCO.
Kim, K. and Lasker, H. R. (1998). Allometry of resource capture in colonial cnidarians and constraints on modular growth. Funct. Ecol. 12,646 -654.[CrossRef]
Lasker, H. R., Gottfried, M. D. and Coffroth, M. A. (1983). Effects of depth on the feeding capabilities of two octocorals. Mar. Biol. 73, 73-78.
Lewis, J. B. (1992). Heterotrophy in corals: zooplankton predation by the hydrocoral Millepora complanata. Mar. Ecol. Prog. Ser. 90,251 -256.
Marsh, J. A., Jr. (1970). Primary productivity of reef building calcareous red algae. Ecology 51,255 -263.
McConnaughey, T. A. and Whelan, J. F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth-Science Rev. 967,95 -117.
Muscatine, L. and Cernichiari, E. (1969). Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 137,506 -523.
Muscatine, L. (1980). Productivity of Zooxanthellae. In Primary Productivity in the Sea (ed. P. G. Falkowski, P. G.), pp. 381-402. New York: Plenum Publishing Corp.
Muscatine, L. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. In Ecosystems of the World, vol 25, Coral Reefs (ed. Z. Dubinsky), pp. 75-87. Amsterdam: Elsevier.
Muscatine, L., Ferrier-Pagès, C., Blackburn, A., Gates, R. D., Baghdasarian, G. and Allemand, D. (1998). Cell-specific density of symbiotic dinoflagellates in tropical anthozoans.Coral Reefs. 17,329 -337.[CrossRef]
Prezelin, B. B. (1987). Photosynthetic physiology of Dinoflagellates. In The Biology of Dinoflagellates Botanical Monographs, no. 21 (ed. F. J. R. Taylor), pp.174 -223. Oxford: Blackwell Scientific Publications.
Rahav, O., Dubinsky, Z., Achituv, Y. and Falkowski, P. G. (1989). Ammonium metabolism in the zooxanthellate coral, Stylophora pistillata. Proc. R. Soc. Lond. B 236,325 -337.
Rosenfeld, M., Bresler, V. and Abelson, A. (1999). Sediment as a possible source of food for corals. Ecol.Lett.. 2,345 -348.
Sebens, K. P., Johnson, A. S. (1991). Effects of water movement on prey capture and distribution of reef corals. Hydrobiol. 216/217,247 -248.
Sebens, K. P., Vandersall, K. S., Savina, L. A and Graham, K. R. (1996). Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar. Biol. 127,303 -317.
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.[Medline]
Snidvongs, A. and Kinzie III, R. A. (1994). Effects of nitrogen and phosphorus enrichment on in vivo symbiotic zooxanthellae Pocillopora damicornis. Mar. Biol. 118,705 -711.
Sorokin, Y. U. (1991). Biomass, metabolic rates and feeding of some common reef Zoantharians and Octocorals. Aust. J. Mar. Freshwater Res. 42,729 -741.
Swanson, R. and Hoegh-Guldberg, O. (1998). Amino acid synthesis on the symbiotic sea anemone Aiptasia pallida.Mar. Biol. 131,83 -93.[CrossRef]
Szmant-Froelich, A. and Pilson, M. E. (1984). Effect of feeding frequency and symbiosis with zooxanthellae on nitrogen metabolism and respiration of the coral Astrangia danae. Mar. Biol. 81,153 -162.
Tambutté, E., Allemand, D., Bourge, I., Gattuso, J. P. and Jaubert, J. (1995). An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar. Biol. 122,453 -459.
Tambutté, E., Allemand, D., Mueller, E. and Jaubert,
J. (1996). A compartmental approach to the mechanism of
calcification in hermatypic corals. J. Exp. Biol.
199,1029
-1041.
Taylor, R. B., Barnes, D. J. and Lough, J. M. (1993). Simple models of density band formation in massive corals. J. Exp. Mar. Biol. Ecol. 167,109 -125.[CrossRef]
Titlyanov, E. A., Tsukahara, J., Titlyanova, T. V., Leletkin, V. A., Van Woesik, R. and Yamazato, K. (2000a). Zooxanthellae population density and physiological state of the coral Stylophora pistillata during starvation and osmotic shock. Symbiosis 28,303 -322.
Titlyanov, E. A., Bil, K., Fomina, L., Titlyanova, T., Leletkin, V., Eden, N., Malkin, A. and Dubinsky, Z. (2000b). Effects of dissolved ammonium addition and host feeding with Artemia salina on photoacclimation of the hermatypic coral Stylophora pistillata. Mar. Biol. 137,463 -472.[CrossRef]
Titlyanov, E. A., Titlyanova, T. V., Yamazato, K. and Van Woesik, R. (2001). Photoacclimatation of the hermatypic coral Stylophora pistillata while subjected to either starvation or food provisioning. J. Exp. Mar. Biol. Ecol. 257,163 -181.[CrossRef][Medline]
Wainwright, S. A. (1963). Skeletal organization in the coral, Pocillopora damicornis. Quart. J. Microsc. Sci. 104,169 -183.
Wang, J. T. and Douglas, A. E. (1999). Essential amino acid synthesis and nitrogen recycling in an alga-invertebrate symbiosis. Mar. Biol. 135,219 -222.[CrossRef]
Weiner, S. and Addadi, L. (1991). Acidic macromolecules of mineralized tissues. The controllers of crystal formation. Trends Biochem. Sci. 16,252 -256.[CrossRef][Medline]
Witting, J. H. (1999). Zooplankton capture and coral growth: the role of heterotrophy in Carribean reef corals. PhD dissertation, Northeasten University, Boston, MA, USA.285 pp.
Young, S. D. (1971). Organic material from scleractinian skeletons. I Variation in composition between several species. Comp. Biochem. Physiol. 40B,113 -120.[CrossRef]
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