Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata

Journal of Experimental Biology

Volumn 207, Issue 9, 2004, Pages 1461-1469

  Houlbrèque, Fanny ^a   Tambutté, Eric ^a   Allemand, Denis ^a   Ferrier Pagès, Christine ^a  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

Author keywords

14C aspartate; 45Ca; Calcification; Coral; Feeding; Organic matrix; Photosynthesis

Indexed keywords

ASPARTIC ACID; CALCIUM; CARBON; CHLOROPHYLL;

ALGA; ANIMAL; ANTHOZOA; ARTICLE; COMPARATIVE STUDY; EATING; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; SYMBIOSIS; ZOOPLANKTON;

ALGAE; ANIMALS; ANTHOZOA; ASPARTIC ACID; CALCIUM; CALCIUM RADIOISOTOPES; CARBON RADIOISOTOPES; CHLOROPHYLL; EATING; PHOTOSYNTHESIS; SYMBIOSIS; ZOOPLANKTON;

ALGAE; ANIMALIA; ANTHOZOA; ARTEMIA SALINA; SALINA; SCLERACTINIA; STYLOPHORA PISTILLATA;

EID: 2342511078     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00911     Document Type: Article

References (62)

1. 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.
2. Anthony, K. R. N. (1999). Coral suspension feeding on fine particulate matter. J. Exp. Mar. Biol. Ecol. 232, 85-106.
3. 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.
4. 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.
5. Barnes, D. J. (1973). Growth in colonial scleractinians. Bull. Mar. Sci. 23, 280-298.
6. 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.
7. Barnes, D. J. and Chalker, B. E. (1990). Calcification and photosynthesis in reef-building corals and algae. In Ecosystems of the World, vol 25, Coral Reefs (ed. Z. Dubinsky), pp. 109-131. Amsterdam: Elsevier.
8. 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.
9. Buddemeier, R. W. and Kinzie, R. A. (1976). Coral growth. Oceanogr. Mar. Biol. Annu. Rev. 14, 183-225.
10. Constantz, B. R. (1986). Coral skeleton construction: A physiochemically dominated process. The Society of Economic Paleontologists and Mineralogists. Palaios 1, 152-157.
11. Constantz, B. and Weiner, S. (1988). Acidic macromolecules associated with the mineral phase of scleractinian coral skeletons. J. Exp. Zool. 248, 253-258.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Falini, G., Albeck, S., Weiner, S. and Addadi, L. (1996). Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271, 67-69.
20. Falkowski, P. G., Dubinsky, Z., Muscatine, L. and Porter, J. W. (1984). Light and bioenergetics of a symbiotic coral. Bioscience 11, 705-709.
21. 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.
22. 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.
23. 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.
24. Fitt, W. K. (2000). Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. 198, 110-120.
25. +-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am. J. Physiol. 278, 870-881.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 2 in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pflanz. 17, 191-194.
32. 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.
33. Kim, K. and Lasker, H. R. (1998). Allometry of resource capture in colonial cnidarians and constraints on modular growth. Funct. Ecol. 12, 646-654.
34. 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.
35. Lewis, J. B. (1992). Heterotrophy in corals: zooplankton predation by the hydrocoral Millepora complanata. Mar. Ecol. Prog. Ser. 90, 251-256.
36. Marsh, J. A., Jr. (1970). Primary productivity of reef building calcareous red algae. Ecology 51, 255-263.
37. McConnaughey, T. A. and Whelan, J. F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth-Science Rev. 967, 95-117.
38. Muscatine, L. and Cernichiari, E. (1969). Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 137, 506-523.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. Rosenfeld, M., Bresler, V. and Abelson, A. (1999). Sediment as a possible source of food for corals. Ecol. Lett.. 2, 345-348.
45. Sebens, K. P., Johnson, A. S. (1991). Effects of water movement on prey capture and distribution of reef corals. Hydrobiol. 216/217, 247-248.
46. 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.
47. 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.
48. 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.
49. Sorokin, Y. U. (1991). Biomass, metabolic rates and feeding of some common reef Zoantharians and Octocorals. Aust. J. Mar. Freshwater Res. 42, 729-741.
50. Swanson, R. and Hoegh-Guldberg, O. (1998). Amino acid synthesis on the symbiotic sea anemone Aiptasia pallida. Mar. Biol. 131, 83-93.
51. 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.
52. 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar. Biol. 122, 453-459.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. Wainwright, S. A. (1963). Skeletal organization in the coral, Pocillopora damicornis. Quart. J. Microsc. Sci. 104, 169-183.
59. 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.
60. Weiner, S. and Addadi, L. (1991). Acidic macromolecules of mineralized tissues. The controllers of crystal formation. Trends Biochem. Sci. 16, 252-256.
61. 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.
62. Young, S. D. (1971). Organic material from scleractinian skeletons. I Variation in composition between several species. Comp. Biochem. Physiol. 40B, 113-120.