Interactions between the carbon and carbonate cycles at organism and community levels in coral reefs; a review on processes, rates and environmental control
Gattuso, Jean-Pierre; Allemand, Denis; Frankignoulle, Michel
[en] Photosynthesis and calcification in zooxanthellate scleractinian corals
and coral reefs are reviewed at several scales: cellular (pathways and transport
mechanisms of inorganic carbon and calcium), organismal (interaction between
photosynthesis and calcification, effect of light) and ecosystemic (community primary
production and calcification, and air-sea CO2 exchanges).
The coral host plays a major role in supplying carbon for the photosynthesis by
the algal symbionts through a system similar to the carbon-concentrating mechanism
described in free living algal cells. The details of carbon supply to the calcification
process are almost unknown, but metabolic CO2 seems to be a significant
source. Calcium supply for calcification is diffusional through oral layers, and
active membrane transport only occurs between the calicoblastic cells and the site
of calcification. Photosynthesis and calcification are tightly coupled in zooxanthellate
scleractinian corals and coral reef communities. Calcification is, on average,
three times higher in light than in darkness. The recent suggestion that calcification
is dark-repressed rather than light-enhanced is not supported by the literature.
There is a very strong correlation between photosynthesis and calcification at both
the organism and community levels, but the ratios of calcification to gross photosynthesis
(0.6 in corals and 0.2 in reef communities) differ from unity, and from
each other as a function of level.
The potential effect of global climatic changes (pCO2 and temperature) on the
rate of calcification is also reviewed. In various calcifying photosynthetic organisms
and communities, the rate of calcification decreases as a function of increasing
pCO2 and decreasing calcium carbonate saturation state. The calculated decrease
in CaCO, production, estimated using the scenarios considered by the International
Panel on Climate Change (IPCC), is 10% between 1880 and 1990, and 9-30%
(mid estimate: 22%) from 1990 to 2100. Inadequate understanding of the mechanism
of calcification and its interaction with photosynthesis severely limits the ability
to provide an accurate prediction of future changes in the rate of calcification.
Frankignoulle, Michel; Université de Liège - ULiège
Language :
English
Title :
Interactions between the carbon and carbonate cycles at organism and community levels in coral reefs; a review on processes, rates and environmental control
Publication date :
1999
Journal title :
American Zoologist
ISSN :
0003-1569
Publisher :
Society for Integrative and Comparative Biology, United States - Virginia
Adey, W.H., The microcosm: A new tool for reef research (1983) Coral Reefs, , 1:193-201
Agegian, C.R., The biogeochemical ecology of Porolithon gardineri (Foslie) (1985) Ph.D. Diss., University of Hawaii.
Al-Moghrabi, S., Goiran, C., Allemand, D., Speziale, N., Jaubert, J., Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinofiagellate association. 2 (1996) Mechanisms for Bicarbonate Uptake. J. Exp. Mar. Biol. Ecol., , 199:227-248
Allemand, D., Furla, P., Bénazet-Tambutté, S., Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa (1998) Can. J. Bot., , 76:925-941
Allemand, D., Grillo, M.-C., Biocalcification mechanism in Gorgonians. 45Ca uptake and deposition by the mediterranean red coral Corallium nibmm (1992) J. Exp. Zool., , 262:237-246
Allemand, D., Tambutté, É., Girard, J.-P., Jaubert, J., Organic matrix synthesis in the Scleracti-nian coral, Stytophora pistillata: Role in biomineralization and potential target of the organotin TBT (1998) J. Exp. Biol., 201, pp. 2001-2009
Barnes, D.J., Chalker, B.E., Calcification and photosynthesis in reef-building corals and algae (1990) In Z. Dubinsky (Ed.). Coral Reefs, Pp., , 109131. Eisevier, Amsterdam
Barnes, D.J., Lough, J.M., Coral skeletons: Storage and recovery of environmental information (1996) Glob. Change Biol., , 2:569-582
Batham, E.J., Pantin, C.F.A., Muscular and hydrostatic action in the sea-anemone Metridium senile (L.) (1950) J. Exp. Biol., , 27:264-289
Beardall, J., Beer, S., Raven, J.A., Biodiversity of marine plants in an era of climate change: Some predictions based on physiological performance (1998) Bot. Mar., , 41:113-123
Bénazet-Tambutté, S., Allemand, D., Water permeability of the oral epithelial layers of the sea anemone, Aneinonia viridis (1997) J. Exp. Zool., , 279:1-8
Bénazet-Tambutté, S., Allemand, D., Jaubert, J., Inorganic carbon supply to symbiont photosynthesis of the sea anemone, Aneinonia viridis: Role of the oral epithelial layers (1996) Symbiosis, , 20: 199-217
Bénazet-Tambutté, S., Allemand, D., Jaubert, J., Permeability of the oral epithelial layers in cnidarians (1996) Mar. Biol., , 126:43-53
Benzie, J.A.H., Genetic structure of coral reef organisms: Ghosts of dispersal past (1999) Amer. Zool., , 39:131-145
Boiseau, M., Cornu, H., Turpin, L., Juillet-Leclerc, A., Sr/Ca and J'O ratios measured from Acropora nobilis and Parités Ititea: Is Sr/Ca paleothermometry always reliable? C (1997) R. Acad. Sei. Paris, Earth Planet. Sei., , 325:747-752
Boron, W.E., Intracellular pH regulating mechanism of squid axon (1985) Relation between the External Na+ and HCO{ Dependences. J. Gen. Physiol., , 85:325-345
Borowitzka, M.A., Photosynthesis and calcification in the articulated coralline red algae Ainphiroa anceps and A. foliacea (1981) Mar. Biol., , 62:1723
Borowitzka, M.A., Larkum, A.W.D., Calcification in the green alga Halimeda (1976) III. the Sources of Inorganic Carbon for Photosynthesis and Calcification and A Model of the Mechanisms of Calcification. J. Exp. Bot., , 27:879-893
Bown, A.W., CO2 and intracellular pH (1985) Plant Cell Environ., , 8:459-465
Broecker, W.S., Peng, T.-H., Tracers in the sea (1982) Lamont-Doherty Geological Observatory, Columbia University, Palisades, New York.
Bronner, F., Transcellular calcium transport (1990) In F. Bronner (Ed.), Intracellular Calcium Regulation, Pp., , 415-437. Wiley-Liss, New York
Brown, B.E., Adaptations of reef corals to physical environmental stress (1997) Adv. Mar. Biol., , 31: 221-299
Brown, B.E., Disturbances to reefs in recent times (1997) In C. Birkeland (Ed.), Life and Death of Coral Reefs, Pp., , 354-379. Chapman & Hall, New York
Brownlee, C., Nirner, N., Dong, L.E., Merrett, M.J., Cellular regulation during calcification in Emiliana hiixleyi (1994) In J. C. Green and B. S. C. Leadbeater (Eds.). the Hapwphyte Algae, Pp., , 133148. Clarendon Press, Oxford
Buddemeier, R.W., Symbiosis, calcification, and environmental interactions (1994) Bull. Inst. Oceanogr., Monaco N Spec., , 13:119-131
Buddemeier, R.W., Smith, S.V., Coral adaptation and acclimatization: A most ingenious paradox (1999) Amer. Zool., , 39:1-9
Burris, J.E., Porter, J.W., Laing, W.A., Effects of carbon dioxide concentration on coral photosynthesis (1983) Mar. Biol., , 75:113-116
Busa, W., Nucitelli, R., Metabolic regulation via intracellular pH (1984) Amer. J. Physiol., , 246:R409R438
Carafoli, E., Penniston, J.T., Sei. Am., , I985. The calcium signal. 253:50-58
Carlon, D.B., Calcification rates in corals (1996) Science, , 274:117
Chalker, B.E., Calcium transport during skeletogenesis in hermatypic corals (1976) Comp. Biochem. Physiol., , 54A:455-459
Chalker, B.E., Skeletogenesis in scleractinian corals: The transport and deposition of strontium and calcium (1981) In S. C. Skoryna (Ed.). Handbook of Stable Strontium, Pp., , 47-63. Plenum Publishing Corporation, New York
Chalker, B.E., Taylor, D.L., Light-enhanced calcification and the role of oxidative phosphorylation in calcification of the coral Acropora cervicomis (1975) Proc. R. Soc. London B, , 190:323-331
Chapman, D.M., Cnidarian histology (1974) In L. Muscatine and H. M. Lenhoff (Eds.), Coelenterate Biology. Reviews and New Perspectives, Pp., , 1-92. Academic Press, New York
Grassland, C.J., Barnes, D.J., The role of metabolic nitrogen in coral calcification (1974) Mar. Biol., , 28:325-332
Dickson, A.G., Millero, F.J., A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media (1987) Deep-Sea Res., , 34:1733-1743
Done, T.J., Coral community adaptability to environmental change at the scales of regions, reefs, and reef zones (1999) Amer. Zool., , 39:66-79
Dunbar, R.E., Cole, J.E., Coral records of ocean-atmosphere variability (1993) NOAA Climate and Global Change Program, Special Report No., , 10, University Corporation for Atmospheric Research, Boulder
Dunlap, W.C., Shick, J.M., Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: A biochemical and environmental perspective (1998) J. Phycol., , 34:418-430
Erez, J., Vital effect on stable-isotope composi-tion seen in Foraminifera and coral skeletons (1978) Nature, , 273:199-202
Frankignoulle, M., Canon, C., Gattuso, J.-P., Marine calcification as a source of carbon dioxide-positive feedback of increasing atmospheric CO2 Limnol (1994) Oceanogr., , 39:458-462
Frankignoulle, M., Gattuso, J.-P., Biondo, R., Bourge, I., Copin-Montégut, G., Pichon, M., Carbon fluxes in coral reefs. 2 (1996) Eulerian Study of Inorganic Carbon Dynamics and Measurement of Air-sea CO, , 2 exchanges. Mar. Ecol. Prog. Ser. 145:123-132
Frankignoulle, M., Pichon, M., Gattuso, J.-P., Aquatic calcification as a source of carbon dioxide (1995) In M. A. Beran (Ed.), Carbon Séquestration in the Biosphere, Pp., , 266-271. Springer-Verlag, Berlin
Furla, P., Bénazet-Tambutté, S., Jaubcrt, J., Allemand, D., Diffusional permeability of dissolved inorganic carbon through the isolated oral epithelial layers of the sea anemone Anemonia viridis..J (1998) Exp. Mar. Biol. Ecol., , 221:71-88
Furla, P., Bénazet-Tambutté, S., Jaubert, J., Allemand, D., Functional polarity of the tentacle of the sea anemone Anemonia viridis: Role in inorganic carbon acquisition (1998) Amer. J. Physiol., , 274: R303-R310
Gao, K., Aruga, Y., Asada, K., Ishihara, T., Akano, T., Kiyohara, M., Calcification in the articulated coralline alga Corallina pilidifera, with special reference to the effect of elevated CO2 concentration (1993) Mar. Biol., , 117:129-132
Gao, K., Aruga, Y., Asada, K., Kiyohara, M., Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis (1993) J. Appl. Phycol., , 5:563-571
Gates, R.D., Edmunds, P.J., The physiological mechanisms of acclimatization in tropical reef corals (1999) Amer. Zool., , 39:30-43
Gattuso, J.-P., Frankignoulle, M., Bourge, I., Romaine, S., Buddemeier, R.W., Effect of calcium carbonate saturation of seawater on coral calcification (1998) Global Planet. Change, , 18:37-46
Gattuso, J.-P., Frankignoulle, M., Smith, S.V., Ware, J.R., Wollast, R., Coral reefs and carbon dioxide (1996) Science, , 271:1298
Gattuso, J.-P., Frankignoulle, M., Wollast, R., Carbon and carbonate metabolism in coastal aquatic ecosystems (1998) Annu. Rev. Ecol. Syst., , 29:405-433
Gattuso, J.-P., Payri, C.E., Pichon, M., Delesalle, B., Frankignoulle, M., Primary production, calcification, and air-sea CO2 fluxes of a macroalgaldominated coral reef community (Moorea, French Polynesia) (1997) J. Phycol., , 33:729-738
Gattuso, J.-P., Pichon, M., Delesalle, B., Canon, C., Frankignoulle, M., Carbon fluxes in coral reefs. 1 (1996) Lagrangian Measurement of Community Metabolism and Resulting Air-sea CO, , 2 disequilibrium. Mar. Ecol. Prog. Ser. 145:109-121
Gattuso, J.-P., Pichon, M., Delesalle, B., Frankignoulle, M., Community metabolism and airsea CO2 fluxes in a coral reef ecosystem (Moorea, French Polynesia) (1993) Mar. Ecol. Prog. Ser., , 96:259267
Gattuso, J.-R., Pichon, M., Frankignoulle, M., Biological control of air-sea CO, fluxes: Effect of photosynthetic and calcifying marine organisms and ecosystems (1995) Mar. Ecol. Prog. Ser., , 129:307312
Goiran, C., Al-Moghrabi, S., Allemand, D., Jaubert, J., Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association. 1 (1996) Photosynthetic Performances of Symbionts and Dependence on Sea Water Bicarbonate. J. Exp. Mar. Biol. Ecol., , 199:207-225
Goreau, T.F., The physiology of skeleton formation in corals (1959) I. A Method for Measuring the Rate of Calcium Deposition by Corals under Different Conditions. Biol. Bull., , 116:59-75
Goreau, T.F., Problems of growth and calcium deposition in reef corals (1961) Endeavour, , 20:32-39
Goreau, T.F., Calcium carbonate deposition by coralline algae and corals in relation to their roles as reef builders (1963) Ann. N. Y. Acad. Sei., , 109:127167
Goreau, T.F., Bowen, V.T., Calcium uptake by a coral (1955) Science, , 122:1188-1189
Goreau, T.F., Goreau, N.I., The physiology of skeleton formation in corals (1959) II. Calcium Deposition by Hermatypic Corals under Various Conditions in the Reef. Biol. Bull., , 117:239-250
Goreau, T.J., Coral skeletal chemistry: Physiological and environmental regulation of stable isotopes and trace metals in Montastrea annnlaris (1977) Proc. R. Soc. London B, , 196:291-315
Hendrey, G.R., FACE: Free-air CO2 enrichment for plant research in the field (1993) CRC Press, USA.
Holley, M.C., Adaptation of a ciliary basal apparatus to cell shape changes in a contractile epithelium (1985) Tissue & Cell, , 17:321-334
Houghton, J.T., Meira Filho, L.G., Callander, B.A., Harris, N., Kattenberg, A., Maskell, K., Climate change 1995 (1996) The Science of Climate Change. Cambridge University Press, Cambridge., , 572 pp
Ip, Y.K., Krishnaveni, P., Incorporation of strontium ('"Sr2) into the skeleton of the hermatypic coral Galaxea fascicnlaris (1991) J. Exp. Zool., , 258:273-276
Ip, Y.K., Lim, A.L.L., Lim, R.W.L., Some properties of calcium-activated adenosine triphos-ahatase from the hermalypic coral Galaxea fascicularis (1991) Mar. Biol., , 111:191-197
Isa, Y., An electron microscope study on the mineralization of the skeleton of the staghorn coral Acropora liebes (1986) Mar. Biol., , 93:91-101
Isa, Y., Ikehara, N., Yamazato, K., Evidence for the occurence of Ca2f-dependent adenosine triphosphatase in a hermatypic coral Acropora liebes (Dana) (1980) Sesoko Mar. Sei. Lab. Tech. Rep., , 7:1925
Isa, Y., Okazaki, M., Some observations on the Ca2t-binding phospholipids from scleractinian coral skeletons (1987) Comp. Biochem. Physiol., , 87B: 507-512
Isa, Y., Yamazato, K., The distribution of carbonic anhydrase in a staghorn coral, Acropora hebes (Dana) (1984) Galaxea, , 3:25-36
Jacques, T.G., Marshall, N., Pilson, M.E.Q., Experimental ecology of the temperate scleractinian coral Astrangia danae (1983) II. Effect of Temperature, Light Intensity and Symbiosis with Zooxanthellae on Metabolic Rate and Calcification. Mar. Biol., , 76:135-148
Jacques, T.G., Pilson, M.E.Q., Experimental ecology of the temperate scleractinian coral Astrangia danae (1980) I. Partition of Respiration, Photosynthesis and Calcification between Host and Symbionts. Mar. Biol., , 60:167-178
Jacques, T.G., Pilson, M.E.Q., Cummings, C., Marshall, N., Laboratory observations on respiration, photosynthesis and factors affecting calcification in the temperate coral Astrangia danae (1977) Proc., , 3rd Int. Coral Reef Symp. 2:455-461
Jaubert, J., An integrated nitrifying-denitrifying biological system capable of purifying sea water in a closed circuit aquarium (1989) Bull. Inst. Océanogr., Monaco N Spec., , 5:101-106
Johnston, I.S., The ultrastructure of skeletogenesis in hermatypic corals (1980) Int. Rev. Cytol., , 67: 171-214
Kajiwara, K., Nagai, A., Ueno, S., Yokochi, H., Examination of the effect of temperature, light intensity and zooxanthellae concentration on calcification and photosynthesis of scleractinian coral Acropora piilchra (1995) J. Sch. Mar. Sei. Technol. Tokai Univ. Tokaidai Kiyo Kaiyogakubu, , 40:95103
Kawaguti, S., Sakumoto, D., The effects of light on the calcium deposition of corals (1948) Bull. Oceanogr. Inst. Taiwan, , 4:65-70
Kawaguti, S., Sato, K., Electron microscopy on the polyp of staghorn corals with special reference to its skeleton formation (1968) Biol. J. Okayama Univ., , 14:87-98
Kayanne, H., Suzuki, A., Saito, H., Diurnal changes in the partial pressure of carbon dioxide in coral reef water (1995) Science, , 269:214-216
Keith, M.L., Weber, J.N., Systematic relationships between carbon and oxygen isotopes in carbonates deposited by modern corals and algae (1965) Science, , 150:498-501
Kinchington, D., Calcification processes in cool temperate scleractinian corals (1980) Ph.D. Thesis, University of London, King's College, London.
Kinsey, D.W., Metabolism, calcification and carbon production (1985) I. System Level Studies. Proc., , 5th Int. Coral Reef Cong. 6:505-526
Kleypas, J.A., McManus, J.W., Menez, L.A.B., Environmental limits to coral reef development: Where do we draw the line? Amer (1999) Zool., , 39:146-159
Krishnaveni, P., Chou, L.M., Ip, Y.K., Deposition of calcium (45Ca:!) in the coral Galaxea fascicularis (1989) Comp. Biochem. Physiol., , 94A:509513
Kühl, M., Cohen, Y., Dalsgaard, T., Jorgensen, B.B., Revsbech, N.P., Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light (1995) Mar. Ecol. Prog. Ser., , 117:159-172
Kuileer, B.H., Erez, J., Padan, E., Competition for inorganic carbon between photosynthesis and calcification in the symbiont-bearing omm
ier Amphistegina lobifera (1989) Mar. Biol., , 103: 253-259
Kuileter, B.H., Erez, J., Padan, E., Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera (1989) Mar. Biol., , 103:241-251
Land, L.S., Lang, J.C., Smith, B.N., Preliminary observations on the carbon isotopic composition of some reef coral tissues and symbiotic zooxanthellae (1975) Limnol. Oceanogr., , 20:283-287
Lough, J.M., Barnes, D.J., Several centuries of variation in skeletal extension, density and calcification in massive Porites colonies from the Great Barrier Reef: A proxy for seawater temperature and a background of variability against which to identify unnatural change (1997) J. Exp. Mar. Biol. Ecol., , 211:29-67
Lucas, J.M., Knapp, L.W., A physiological evaluation of carbon sources for calcification in the octocoral Leptogorgia virgulala (Lamarck) (1997) J. Exp. Biol., , 200:2653-2662
Mackenzie, F.T., Agegian, C.R., Biomineralization and tentative links to plate tectonics (1989) In R. E. Crick (Ed.), Origin, Evolution, and Modem Aspects of Biomineralization in Plants and Animals, Pp., , 11-27. Plenum Press, New York
Madshus, I.H., Regulation of intracellular pH in eukaryotic cells (1988) Biochem. J., , 250:1-8
Marshall, A.T., Calcification in hermatypic and ahermatypic corals (1996) Science, , 271:637-639
Marshall, A.T., Calcification rates in coralsresponse (1996) Science, , 274:117-118
Marshall, A.T., Wright, A., Coral calcification: Autoradiography of a scleratinian coral Galaxea fascicularis after incubation in 45Ca and I4C (1998) Coral Reefs, , 17:37-47
McConnaughey, T., Calcification in Chara corallina: CO2 hydroxylation generates protons for bicarbonate assimilation (1991) Limnol. Oceanogr., , 36: 619-628
McConnaughey, T.A., Ion transport and the generation of biomineral supersaturation (1995) Bull. Inst. Oceanogr., Monaco N Spec., , 14:1-18
McConnaughey, T.A., Calcification, photosynthesis, and global carbon cycles (1994) Bull. Inst. Océanogr., Monaco N Spec., , 13:137-161
Mucci, A., The solubility of calcite and aragonite in seawater at various salinities, temperature, and one atmosphere total pressure (1983) Am. J. Sei., , 283: 780-799
Munoz, J., Merrett, M.J., Inorganic-carbon transport in some marine eukaryotic microalgae (1989) Planta, , 178:450-455
Muscatine, L., Tambutté, É., Allemand, D., Morphology of coral desmocytes, cells that anchor the calicoblastic epithelium to the skeleton (1997) Coral Reefs, , 16:205-213
Neglescu, P., Machen, T., Lowering extracellular sodium or pH raised intracellular calcium in gastric cells (1990) J. Memb. Biol., , 116:239-248
Nijs, I., Kockelbergh, F., Teughels, H., Blum, H., Hendrey, G., Impens, I., Free air temperature increase (FATI): A new tool to study global warming effects on plants in the field (1996) Plant Cell Environ., , 19:495-502
Nimer, N.A., Merrett, M.J., Calcification rate in Emiliania huxleyi Lohmann in response to light, nitrate and availability of inorganic carbon (1993) New Phytol., , 123:673-677
Opdyke, B.N., Walker, J.C.G., Return of the coral reef hypothesis: Basin to shelf partitioning of CaCO, and its effect on atmospheric CO2 (1992) Geology, , 20:733-736
Pandolfi, J.M., Responses of Pleistocene coral reefs to environmental change over long temporal scales (1999) Amer. Zool., , 39:113-130
Pearse, V.B., Incorporation of metabolic CO2 into coral skeleton (1970) Nature, , 228:383
Pearse, V.B., Sources of carbon in the skeleton of the coral Fungia scitlaria In II, M. Lenhoff, L. Muscatine, and L. V. Davis (Eds.), Experimental Coelenterate Biology, Pp., , I971. 239-245. Univ. of Hawaii Press, Honolulu
Pccheux, M., Is present coral reef mass-bleaching due to CO2 rise? 7th Int (1993) Symp. Biomin., , 174. (Abstr.)
Peterson, B.J., Aquatic primary productivity and the I4C-CO2 method: A history of the productivity problem (1980) Annu. Rev. Ecol. Syst., , 11:359-385
Pichon, M., Coral reef metabolism in the IndoPacific: The broader picture (1997) Proc., , 8th Int. Coral Reef Symp. 1:977-980
Pittock, A.B., Coral reefs and environmental change: Adaptation to what? Amer (1999) Zool., , 39:1029
Rands, M.L., Douglas, A.E., Loughman, B.C., Ratcliffe, R.G., Avoidance of hypoxia in a cnidarian symbiosis by algal photosynthetic oxygen (1992) Biol. Bull., , 182:159-162
Raven, J.A., Energy and nutrient acquisition by autotrophic symbioses and their asymbiotic ancestors (1992) Symbiosis, , 14:33-60
Raven, A., Inorganic carbon acquisition by marine autotrophs (1997) Adv. Bot. Res., , 27:85-209
Rinkevich, B., Loya, Y., Does light enhance calcification in hermatypic corals? Mar (1984) Biol., , 80: 1-6
Rowan, R., Whitney, S.M., Fowler, A., Yellowlees, D., Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family (1996) Plant Cell, , 8:539-553
Roy, R.N., Roy, L.N., Vogel, K.M., Porter-Moore, C., Pearson, T., Good, Ç.E., Millero, F.J., Campbell, D.M., The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45C (1993) Mar. Chem., , 44:249-267
Simkiss, K., Phosphates as crystals poisons of calcification (1964) Biol. Rev., , 39:487-505
Simkiss, K., Wilbur, K.M., Biomineralizalion: Cell biology and mineral deposition (1989) Academic Press, New York.
Smith, A.D., Roth, A.A., Effect of carbon dioxide concentration on calcification in the red coralline alga Bossiella orbigniana (1979) Mar. Biol., , 52: 217-225
Smith, R.G., Inorganic carbon transport in biological systems, Comp (1988) Biochem. Physiol., , 90B: 639-654
Smith, S.V., Carbon dioxide dynamics: A record of organic carbon production, respiration and calcification in the Eniwetok reef flat community (1973) Limnol. Oceanogr., , 18:106-120
Smith, S.V., Physical, chemical and biological characteristics of CO2 gas flux across the air-water interface (1985) Plant. Cell~Environ., , 8:387-398
Smith, S.V., Reflections on the measurement and significance of carbon metabolism on coral reefs (1995) Kansas Geological Survey Open-File Report, , 9596a, Kansas Geological Survey, Lawrence, Kansas
Smith, S.V., Buddemeier, R.W., Global change and coral reef ecosystems (1992) Annu. Rev. Ecol. Syst., , 23:89-118
Smith, S.V., Veeh, H.H., Mass balance of biogeochemically active materials (C, N, P) in a hypersaline gulf (1989) Est. Coast. Shelf Sei., , 29:195215
Tambutté, É., Allemand, D., Bourge, I., Gattuso, J.-P., Jaubert, J., An improved 45Ca protocol for investigating physiological mechanisms in coral calcification (1995) Mar. Biol., , 122:453-459
Tambutté, É., Allemand, D., Mueller, E., Jaubert, J., A companmental approach to the mechanism of calcification in hermatypic corals (1996) J. Exp. Biol., , 199:1029-1041
Taylor, D.L., Mineralization in symbiotic sys-terns (1983) In H. E. A. Schenk and W. Schwemmler (Eds.), Endocytobiology II. Intracellular Space As Oligogenetic Ecosystem, Pp., , 689-697. Walter de Gruyter, Berlin
Trivedi, B., Danforth, W.H., Effect of pH on the kinetics of frog muscle phosphofructokinase (1966) J. Biol. Chem., , 241:4110-4112
Vandermeulen, J.H., Studies on reef corals (1975) III. Fine Structural Changes of Calcicoblast Cells in Pocillopora Damicomis during Settling and Calcification. Mar. Biol., , 31:69-77
Vandermeulen, J.H., Muscatine, L., Influence of symbiotic algae on calcification in reef corals: Critique and progress report (1974) In W. B. Vernberg (Ed.). Symbiosis in the Sea, Pp., , 1-19. University of South Carolina Press, Columbia, South Carolina
Wainwright, S.A., Skeletal organization in the coral Pocillopora damicornis (1963) Quart. J. Micros. Sei., , 104:164-183
Ware, J.R., Smith, S.V., Reaka-Kudla, M.L., (1992) Coral'reefs: Sources or Sinks of Atmospheric CO, , 2? Coral Reefs 11:127-130
Whitney, S.M., Shaw, D.C., Yellowlees, D., Evidence that some dinoflagellates contain a ribulose-l,5-bisphosphate carboxylase oxygenase related to that of the alphà-proteobacteria (1995) Proc. R. Soc. London, , 259:271-275
Wilbur, K.M., Simkiss, K., Carbonate turnover and deposition by metazoa (1979) In P. A. Trudinger and D. J. Swaine (Eds.), Studies in Environmental Sciences., , 3. Biochemical cycling of min-eral-fonning elements, pp. 69-106. Elsevier, Amsterdam
Wollast, R., Garrels, R.M., Mackenzie, F.T., Calcite-seawater reactions in ocean surface waters (1980) Am. J. Sei., , 280:831-848
Wright, O.P., Marshall, A.T., Calcium transport across the isolated oral epithelium of scleractinian corals (1991) Coral Reefs, , 10:37-40
Yamaji, Y., Moe, O.W., Miller, R.T., Alpern, R.J., Acid activation of immediate early genes in renal epithelial cells (1994) J. Clin. Invest., , 94:12971303
Yamashiro, H., The effects of HEBP, an inhibitor of mineral deposition, upon photosynthesis and calcification in the scleractinian coral, Stylophora pistillata (1995) J. Exp. Mar. Biol. Ecol., , 191:57-63
Yonge, C.M., Living corals (1968) Proc. R. Soc. London B, , 169:329-344
Zimmerman, R.C., Kohrs, D.G., Steller, D.L., Alberte, R.S., Impacts of CO2 enrichment on productivity and light requirements of eelgrass (1997) Plant Physiol., , 115:599-607
Zoccola, D., Allemand, D., (1996) Cloning of An Ltype Calcium Channel Involved in Coral Calcification., , 8th International Coral Reef Symposium Abstract Volume:216
Zaccola, D., Tambutté, E., Sénégas-Balas, F., Michiels, J.F., Failla, J.P., Jaubert, J., Allenmand, D., Cloning of A Calcium Channel Ctl Subunit from the Reef-building Coral Stylophora Pistillata Gene.
