Abstract
Recent micro-analytical studies of coral skeletons have led to the discovery that the effects of biology on the skeletal chemical and isotopic composition are not uniform over the skeleton. The aim of the present work was to provide histological observations of the coral tissue at the interface with the skeleton, using Stylophora pistillata as a model, and to discuss these observations in the context of skeletal ultra-structural organization and composition. Several important observations are reported: (1) At all scales of observation, there was a precise morphological correspondence between the tissues and the skeleton. The morphological features of the calicoblastic ectoderm correspond exactly to the shape of individual crystal fiber bundles in the underlying skeleton, indicating that the calicoblastic cell layer is in direct physical contact with the skeletal surface. This is consistent with the previously observed chemical and isotopic composition of the ultra-structural components in the skeleton. (2) The distribution and density of desmocyte cells, which anchor the calicoblastic ectoderm to the skeletal surface, vary spatially and temporally during skeletal growth. (3) The tissue above the coenosteal spines lack endoderm and consists only of ectodermal cell-layers separated by mesoglea. These findings have important implications for models of vital effects in coral skeletal chemistry and isotope composition.
References
Adkins JF, Boyle EA, Curry WB, Lutringer A (2003) Stable isotopes in deep-sea corals and a new mechanism for ‘vital effects’. Geochim Cosmochim Acta 67:1129–1143
Aijaz S, Balda M, Matter K (2006) Tight junctions: molecular architecture and function. Int Rev Cytol 248:261–298
Allemand D, Tambutté É, Girard JP, 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
Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté É, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467
Allison N (1996) Comparative determination of trace and minor elements in coral aragonite by ion microprobe analysis, with implications from Phuket, southern Thailand. Geochim Cosmochim Acta 60:3457–3470
Allison N, Finch A, Newville M, Sutton SR (2005) Strontium in coral aragonite: 3. Sr coordination and geochemistry in relation to skeletal structure. Geochim Cosmochim Acta 69:3801–3811
Anderson J, Van Itallie C, Fanning A (2004) Setting up a selective barrier at the apical junction complex. Curr Opin Cell Biol 16:140–145
Barnes DJ (1970) Coral skeletons: an explanation of their growth and structure. Science 170:1305–1308
Barnes DJ (1972) The structure and formation of growth-ridges in scleractinian coral skeletons. Proc R Soc Lond B 182:331–350
Barnes DJ, Crossland CJ (1978) Diurnal productivity and apparent 14C calcification in the staghorn coral Acropora acuminata. Comp Biochem Physiol 59A:133–138
Barnes DJ, Devereux MJ (1984) Productivity and calcification on a coral reef: a survey using pH and oxygen electrode techniques. J Exp Mar Biol Ecol 9:213–231
Brown BE, Hewit R, Le Tissier MAA (1983) The nature and construction of skeletal spines in Pocillopora damicornis (Linnaeus). Coral Reefs 2:81–89
Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc Roy Soc Lond B 190:323–331
Clode PL, Marshall AT (2002) Low temperature FESEM of the calcifying interface of a scleractinian coral. Tissue Cell 34:187–198
Clode PL, Marshall AT (2003) Skeletal microstructure of Galaxea fascicularis exsert septa: a high-resolution SEM study. Biol Bull 204:146–154
Cohen AL, McConnaughey TA (2003) Geochemical Perspectives on Coral Mineralization. Rev Mineral Geochem 54:151–187
Cohen AL, Layne GD, Hart SR, Lobel SR (2001) Kinetic control of skeletal Sr/Ca in a symbiotic coral: implications for the paleotemperature proxy. Paleoceanogr 16:20–26
Cuif JP, Dauphin Y (1998) Microstructural and physico-chemical characterization of ‘centers of calcification’ in septa of some recent scleractinian corals. Paläontol Z 72:257–270
Cuif JP, Dauphin Y (2005) The Environment Recording Unit in corals skeletons - a synthesis of structural and chemical evidences for a biochemically driven, stepping-growth process in fibres. Biogeosci 2:61–73
Cuif JP, Dauphin Y, Freiwald A, Gautret P, Zibrowius H (1999) Biochemical markers of zooxanthellae symbiosis in soluble matrices of skeleton of 24 Scleractinia species. Comp Biochem Physiol 123A:269–278
Cuif JP, Dauphin Y, Doucet J, Salome M, Susini J (2003) XANES mapping of organic sulfate in three scleractinian coral skeletons. Geochim Cosmochim Acta 67:75–83
Cuif JP, Dauphin Y, Berthet P, Jegoudez J (2004) Associated water and organic compounds in coral skeletons: Quantitative thermogravimetry coupled to infrared absorption spectrometry. Geochem Geophys Geosyst 5:1–9
Duerden JE (1902) West Indian Madreporian polyps. Memoir Natl Acad Sci 8:482–484
Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, Bhat MA (2004) Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131:4931–4942
Fautin DG, Mariscal RN (1991) Cnidaria: anthozoa. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates. Cnidaria: Anthozoa, vol 2. Wiley, New York, pp 267–358
Flower NE (1986) Sealing junctions in a number of arachnid tissues. Tissue Cell 18:899–913
Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457
Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, Mc Laughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG, Peters EC, Reynolds TL, Rotstein DS, Sileo L, Woodley CM (2006) A report of the CDHC Coral Histopathology Workshop II. National Oceanic and Atmospheric Administration, Silver Spring, p 88
Gattuso JP (1987) Ecomorphologie, métabolisme, croissance et calcification du scléractiniaire à zooxanthelles Stylophora pistillata (Golfe d’Aqaba, Mer rouge). Influence de l’éclairement. Ph.D. thesis, Centre d’océanologie de Marseille, Université d’Aix-Marseille II, p 289
Gattuso JP, Allemand D, 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
Gladfelter EH (1983) Skeletal development in Acropora cervicornis: II. Diel patterns of calcium carbonate accretion. Coral Reefs 2:91–100
Goldberg WM (2001a) Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi. Tissue Cell 33:376–387
Goldberg WM (2001b) Desmocytes in the calicoblastic epithelium of the stony coral Mycetophyllia reesi and their attachment to the skeleton. Tissue Cell 33:388–394
Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull (Woods Hole) 116:59–75
Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under different conditions. Biol Bull (Woods Hole) 117:239–250
Green CR, Flower NE (1980) Two new septate junctions in the phylum coelenterata. J Cell Sci 42:43–59
Green C, Bergquist PR (1982) Phylogenetic relationships within the invertebrata in relation to the structure of septate junctions and the development of ‘occluding’ junctional types. J Cell Sci 53:279–305
Hand AR, Gobel S (1972) The structural organization of the septate and gap junctions of Hydra. J Cell Biol 52:397–408
Holley MC (1985) Changes in the distribution of filament-containing septate junctions as coelenterate myoepithelial cells change shape. Tissue Cell 17:1–11
Isa Y (1986) An electron microscope study on the mineralization of the skeleton of the staghorn coral Acropora hebes. Mar Biol 93:91–101
Johnston IS (1980) The ultrastructure of skeletogenesis in zooxanthellate corals. Int Rev Cytol 67:171–214
Kawaguti S (1937) On the physiology of reef corals II. The effect of light on colour and form of reef corals. Palao Trop Biol Stat Stud 2:177–186
Le Tissier MAA (1987) The nature and construction of skeletal spines in Pocillopora damicornis (Linnaeus), Ph.D. thesis, University of Newcastle upon Tyne, p 140
Le Tissier MAA (1990) The ultrastructure of the skeleton and skeletogenic tissues of the temperate coral Caryophyllia smithii. J Mar Biol Assoc UK 70:295–310
Le Tissier MAA (1991) The nature of the skeleton and skeletogenic tissues in the Cnidaria. Hydrobiologia 216/217:397–402
Lowenstam HA, Weiner S (1989) On Biomineralization. Oxford University Press, Oxford
Marshall AT, Wright A (1998) Coral calcification: autoradiography of a scleractinian coral Galaxea fascicularis after incubation in 45 Ca and 14°C. Coral Reefs 17:37–47
McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117
Meibom A, Stage M, Wooden JL, Constantz BR, Owen A, Dunbar RB, Grumet N, Bacon CR, Chamberlain CP (2003) Monthly strontium/calcium oscillations in symbiotic coral aragonite: biological effects limiting the precision of the paleotemperature proxy. Geophys Res Lett 307:1418. doi:10.1029/2002GL016864
Meibom A, Cuif JP, Hillion F, Constantz BR, Juillet-Leclerc A, Dauphin Y, Watanabe T, Dunbar RB (2004) Distribution of magnesium in coral skeleton. Geophys Res Lett 31. doi:10.1029/2004GL021313
Meibom A, Yurimoto H, Cuif J, Domart-Coulon I, Houlbrèque F, Constantz B, Dauphin Y, Tambutté É, Tambutté S, Allemand D, Wooden J, Dunbar R (2006) Vital effects in coral skeletal composition display strict three-dimensional control. Geophys Res Lett 33:L11608. doi:10.1029/2006GL025968
Meibom A, Mostefaoui S, Cuif JP, Dauphin Y, Houlbrèque F, Dunbar R, Constantz B (2007) Biological forcing controls the chemistry of reef-building coral skeleton. Geophys Res Lett 34: L02601. doi:10.1029/2006GL028657
Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523
Muscatine L, Tambutté É, Allemand D (1997) Morphology of coral desmocytes, cells that anchor the calicoblastic epithelium to the skeleton. Coral Reefs 16:205–213
Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D (2005) Stable isotopes (d13C and d15N) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102:1525–1530
Nelson W, Yeaman C, Grindstaff K (2000) Spatial cues for cellular asymmetry in polarized epithelia. In: Drubin D (ed) Cell polarity. Oxford University Press, Oxford, pp 106–140
Pearse VB, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull 141:350–363
Puverel S, Tambutté É, Zoccola D, Domart-Coulon I, Bouchot A, Lotto S, Allemand D, Tambutté S (2004) Antibodies against the organic matrix in scleractinians: a new tool to study coral biomineralization. Coral Reefs 24:149–156
Puverel S, Tambutté É, Pereira-Mouries L, Zoccola D, Allemand D, Tambutté S (2005) Soluble organic matrix of two Scleractinian corals: partial and comparative analysis. Comp Biochem Physiol B 141:480–487
Raz-Bahat M, Erez J, Rinkevich B (2006) In vivo light-microscopic documentation for primary calcification processes in the hermatypic coral Stylophora pistillata. Cell Tissue Res 325:361–368
Rinkevich B, Loya Y (1984) Does light enhance calcification in hermatypic corals? Mar Biol 80:1–6
Rollion-Bard C, Blamart D, Cuif J, Juillet-Leclerc A (2003a) Microanalysis of C and O isotopes of azooxanthellate and zooxanthellate corals by ion microprobe. Coral Reefs 22:405–415
Rollion-Bard C, Chaussidon M, France-Lanord C (2003b) pH control on oxygen isotopic composition of symbiotic corals. Earth Planet Sci Lett 215:275–288
Shaposhnikova T, Matveev I, Napara T, Podgornaya O (2005) Mesogleal cells of the jellyfish Aurelia aurita are involved in the formation of mesogleal fibres. Cell Biol Int 29:952–958
Simkiss K (1964) Phosphates as crystal poisons of calcification. Biol Rev 39:487–505
Sinclair D, Williams B, Risk MJ (2006) A biological origin for climate signals in corals - Trace element ‘vital effects’ are ubiquitous in Scleractinian coral skeletons. Geophys Res Lett 33. doi:10.029/2006GL02718£02713
Tambutté É (1996) Processus de calcification d’un scléractiniaire hermatypique, Stylophora pistillata (Esper, 1797). Ph.D. thesis, University of Nice Sophia-Antipolis, p 295
Tambutté É, Allemand D, Bourge I, Gattuso JP, Jaubert J (1995a) An improved 45 Ca protocol for investigating physiological mechanisms in coral calcification. Mar Biol 122:453–459
Tambutté É, Allemand D, Jaubert J (1995b) The Stylophora pistillata microcolony: a model for studying calcium transport process during coral biomineralization. In: Proceedings of the 7th International Symposium on Biomineralization, “Biomineralization 93”. Bull Inst Oceanogr (Monaco) No. 14.2, pp 79–87
Tambutté É, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041
Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747–784
Veron JEN (2000) Corals of the world. Australian Institute of Marine Sciences, Townsville
Wainwright SA (1964) Studies of the mineral phase of coral skeleton. Exp Cell Res 34:213–230
Wood RL (1959) Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J Biophys Biochem Cytol 6:343–351
Wright OP, Marshall AT (1991) Calcium transport across the isolated oral epithelium of scleractinian corals. Coral Reefs 10:37–40
Yamashiro H (1995) The effects of HEBP, an inhibitor of mineral deposition, upon photosynthesis and calcification in the scleractinian coral, Stylophora pistillata. J Exp Mar Biol Ecol 191:57–63
Yonge CM (1931) The significance of the relationship between corals and zooxanthellae. Nature 128:309–311
Zoccola D, Tambutté É, Sénegas-Balas F, Michiels J-F, Failla JP, Jaubert J, Allemand D (1999) Cloning of a calcium channel α1 subunit from the reef-building coral, Stylophora pistillata. Gene 227:157–167
Acknowledgments
This paper is dedicated to the memory of our dear friend and colleague Len Muscatine. Thanks are due to Dominique Desgré for coral maintenance. Thanks are also due to Jean-Pierre Laugier, Sophie Pagnotta and Pierre Gounon from the Centre Commun de Microscopie Appliquée at the University of Nice-Sophia Antipolis. This study was conducted as part of the Centre Scientifique de Monaco research program, supported by the Government of the Principality of Monaco, by the Agence Nationale de la Recherche and by IFREMER. This paper has greatly benefited from the highly constructive comments by Dr. Lasker and two anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor H.R. Lasker.
Rights and permissions
About this article
Cite this article
Tambutté, E., Allemand, D., Zoccola, D. et al. Observations of the tissue-skeleton interface in the scleractinian coral Stylophora pistillata . Coral Reefs 26, 517–529 (2007). https://doi.org/10.1007/s00338-007-0263-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-007-0263-5