Skip to main content
SpringerLink
Log in

Ultrastructural examination of chamber morphogenesis and biomineralization in the planktonic foraminiferOrbulina universa

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Pre-sphere, trochospiralOrbulina universa (d'Orbigny) were hand-collected between June and September, 1982 to 1984, from surface waters of the Pacific Ocean ca. 2 km off Santa Catalina Island, California, USA. The formation of a spherical chamber by this planktonic foraminifer was studied with light and electron microscopy. Chamber morphogenesis is preceded by the secretion of a cytoplasmic layer rich in mitochondria. The layer expands away from the pre-existing foraminiferal shell surface in a spherical pattern. Full cytoplasm expansion is followed by the secretion of an organic matrix (OM) approximately 200 μm above the original shell surface. Cytoplasm, mitochondria and/or vesicles may play a role in OM secretion. Calcification and chamber thickening, new spine growth and pore development are documented and continue for a period of 1–7 d. Approximately 24 h prior to gamete release, the foraminiferal spines are resorbed and a veneer of calcite is deposited on the shell surface. An extensive intracellular organelle unique to foraminifera, the fibrillar system, is examined and is hypothesized to play a role in the biomineralization process. The taxonomic and functional significance of theO. universa spherical chamber is discussed with respect to other foraminiferal species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Adshead, P. C. (1967). Collection and laboratory maintenance of living planktonic foraminifera. Micropaleontology. 13: 32–40

    Google Scholar 

  • Anderson, O. R., Bé, A. W. H. (1976). The ultrastructure of a planktonic foraminifer,Globigerinoides sacculifer (Brady) and its symbiotic dinoflagellates. J. foraminiferal Res. 6: 1–21

    Google Scholar 

  • Anderson, O. R., Faber, W. W. Jr. (1984). An estimation of calcium carbonate deposition rate in a planktonic foraminiferGlobigerinoides sacculifer using45Ca as a tracer: a recommended procedure for improved accuracy. J. foraminiferal. Res. 14: 303–308

    Google Scholar 

  • Angell, R. W. (1967). The process of chamber formation in the foraminiferRosalina floridana (Cushman). J. Protozool. 14: 566–574

    Google Scholar 

  • Bandy, O. L. (1966). Restrictions of the “Orbulina” datum. Micropaleontology 12: 79–86

    Google Scholar 

  • Bandy, O. L., Vincent, E., Wright, R. C. (1969). Chronologic relationships of Orbulines to theGloborotalia fohsi lineage. Rev. Esp. Micropaleontol. 1: 131–145

    Google Scholar 

  • Bé, A. W. H. (1980). Gametogenic calcification in a spinose planktonic foraminifer,Globigerinoides sacculifer (Brady). Mar. Micropaleontol. 5: 283–310

    Google Scholar 

  • Bé, A. W. H., Anderson, O. R. (1976). Gametogenesis in planktonic foraminifera. Science, N. Y. 192: 890–892

    Google Scholar 

  • Bé, A. W. H., Caron, D. A., Anderson, O. R. (1981). Effects of feeding frequency on life processes of the planktonic foraminiferGlobigerinoides sacculifer (Brady) in laboratory culture. J. mar. biol. Ass. U.K. 61: 257–277

    Google Scholar 

  • Bé, A. W. H., Duplessy, J.-C. (1976). Subtropical convergence fluctuations and quaternary climates in the middle latitudes of the Indian Ocean. Science N.Y. 194: 419–422

    Google Scholar 

  • Bé, A. W. H., Harrison, S. M., Frerichs, W. E., Heiman, M. E. (1976). Variability in test porosity ofOrbulina universa d'Orbigny at two Indian Ocean localities. In: Takayanagi, Y., Saito, T. (eds.) Progress in Micropaleontology. Amer. Mus. nat. Hist., New York, p. 1–9

    Google Scholar 

  • Bé, A. W. H., Harrison, S. M., Lott, L. (1973).Orbulina universa d'Orbigny in the Indian Ocean. Micropaleontology, 19: 150–192

    Google Scholar 

  • Bé, A. W. H., Hemleben, C. (1970). Calcification in a living planktonic foraminifera,Globigerinoides sacculifer (Brady). Neues Jahrb. Geol. Paleontol. Abh. 134: 221–234

    Google Scholar 

  • Bé, A. W. H., Hemleben, C., Anderson, O. R., Spindler, M. (1979). Chamber formation in planktonic foraminifera. Micropaleontology 25: 294–307

    Google Scholar 

  • Bé, A. W. H., Hemleben, C., Anderson, O. R., Spindler, M. (1980). Pore structures in planktonic foraminifera. J. foraminiferal Res. 10: 117–128

    Google Scholar 

  • Bé, A. W. H., Hemleben, C., Anderson, O. R., Spindler, M., Hacunda, J., Tuntivate-Choy, S. (1977). Laboratory and field observations of living planktonic foraminifera. Micropaleontology 23: 155–179

    Google Scholar 

  • Bé, A. W. H., Spero, H. J. (1981). Shell regeneration and biological recovery of planktonic foraminifera after physical injury induced in laboratory culture. Micropaleontology, 27: 305–316

    Google Scholar 

  • Blow, W. H. (1956). Origin and evolution of the foraminiferal genus “Orbulina” d'Orbigny. Micropaleontology 2: 57–70

    Google Scholar 

  • Bouvier-Soumagnac, Y., Duplessy, J.-C. (1985). Carbon and oxygen isotopic composition of planktonic foraminifera from laboratory culture, plankton tows and Recent sediment: implications for the reconstruction of paleoclimatic conditions and of the global carbon cycle. J. foraminiferal Res. 15: 302–320

    Google Scholar 

  • Bouvier-Soumagnac, Y., Duplessy, J.-C., Bé, A. W. H. (1986). Isotopic composition of a laboratory cultured planktonic foraminifer,O. universa implications for paleoclimatic reconstructions. Oceanol. Acta 9: 519–522

    Google Scholar 

  • Brighton, C. T., Hunt, R. M. (1976). Histochemical localization of calcium in growth plate mitochondria and matrix vesicles. Fed. Proc. Fed. Am. Soc. exp. Biol. 35: 143–147

    Google Scholar 

  • Carafoli, E., Crompton, M. (1978). The regulation of intracellular calcium. Curr. Top. Membr. Transp. 10: 151–216

    Google Scholar 

  • Caron, D. A., Faber, W. W., Jr., Bé, A. W. H. (1987). Growth of the spinose planktonic foraminiferOrbulina universa in laboratory culture and the effect of temperature on life processes. J. mar. Biol. Ass. U.K. 67: 343–358

    Google Scholar 

  • Colombo, M. R., Cita, M. B. (1980). Changes in size and test porosity ofOrbulina universa d'Orbigny in the Pleistocene record of Cape Bojador (DSDP site 397, eastern North Atlantic). Mar. Micropaleontol. 5: 13–29

    Google Scholar 

  • Febvre-Chevalier, C. (1971). Constitution ultrastructurale deGlobigerina bulloides d'Orbigny, 1826 (Rhizopoda-Foraminifera). Protistologica 7: 311–324

    Google Scholar 

  • Hecht, A. D., Bé, A. W. H., Lott, L. (1976). Ecologic and paleoclimatic implications of morphologic variation ofOrbulina universa in the Indian Ocean. Science, N.Y. 194: 422–424

    Google Scholar 

  • Hemleben, C., Bé, A. W. H., Anderson, O. R., Tuntivate, S. (1977). Test morphology, organic layers and chamber formation of the planktonic foraminiferGloborotalia menardii (d'Orbigny). J. foraminiferal Res. 7: 1–25

    Google Scholar 

  • Hofker, J. (1954).Candorbulina universa Jedllitschka andOrbulina universa d'Orbigny. Micropaleontologist 8: 38–39

    Google Scholar 

  • Hofker, J. (1969). Have the generaPorticulasphaera, Orbulina (Candorbulina) andBiorbulian a biologic meaning. In: Brönniman, P., Renz, H. H. (eds.) Proceedings of the First International Conference on Planktonic Microfossils. Vol. 2. E. J. Brill, Leiden, p. 279–286

    Google Scholar 

  • Isa, Y. (1986). An electron microscope study on the mineralization of the skeleton of the staghorn coralAcropora hebes. Mar. Biol. 93: 91–101

    Google Scholar 

  • Kennett, J. P., Srinivasan, M. S. (1983). Neogene planktonic foraminifera, a phylogenetic atlas. Hutchinson Ross, Stroudsburg, Pennsylvania, p. 81

    Google Scholar 

  • Killingley, J. S., Johnson, R. F., Berger, W. H. (1981). Oxygen and carbon isotopes of individual shells of planktonic foraminifera from Ontong-Java Plateau. Palaeogeogr. Palaeoclimatol. Palaeoceol 33: 193–204

    Google Scholar 

  • Le Calvez, J. (1936). Modifications du test des Foraminifères pélagiques en rapport avec la reproduction:Orbulina universa d'Orb. etTretomphalus bulloides d'Orb. Ann. Protistol. 5: 125–133

    Google Scholar 

  • Lee, J. J., Freudenthal, H. D., Kossoy, V., Bé, A. W. H. (1965). Cytological observations on two planktonic foraminifera,Globigerina bulloides d'Orbigny, 1826 andGlobigerinoides ruber (d'Orbigny, 1839) Cushman 1927. J. Protozool. 12: 531–542

    Google Scholar 

  • Malmgren, B., Healy-Williams, N. (1978). Variation in test diameter ofOrbulina universa in the paleoclimatology of the late quaternary of the Gulf of Mexico. Palaeogeogr. Palaeoclimatol. Palaeoecol. 25: 235–240

    Google Scholar 

  • Mann, S. (1983). Mineralization in biological systems. Struct. Bonding (Berlin) 54: 125–174

    Google Scholar 

  • Mann, S., Skarnulis, J., Williams, R. J. P. (1981). Inorganic and bioinorganic chemistry in vesicles. Israel J. Chem. 21: 3–7

    Google Scholar 

  • Mann, S., Hannington, J. P., Williams, R. J. P. (1986). Phospholipid vesicles as a model system for biomineralization. Nature, Lond. 324: 565–567

    Google Scholar 

  • Parker, F. L. (1962). Planktonic foraminiferal species in Pacific sediments. Micropaleontology. 8: 219–254

    Google Scholar 

  • Parker, F. L. (1967). Later tertiary biostratigraphy (planktonic foraminifera) of tropical Indo-Pacific deep-sea cores. Bull. Am. Paleontol. 52: 111–208

    Google Scholar 

  • Rhumbler, L. (1911). Die Foraminiferen (Thalamophoren) der Plankton-Expedition; Teil 1. Die allgemeinen Organisationsverhältnisse der Foraminiferen. Plankton-Exped. Humboldt-Stiftung, Ergebn. 3, L, C, 1: 1–331

    Google Scholar 

  • Spero, H. J. (1986). Symbiosis, chamber formation and stable isotope incorporation in the planktonic foraminifer,Orbulina universa. Ph. D. dissertation, University of California Santa Barbara, Santa Barbara, California, USA

    Google Scholar 

  • Spero, H. J. (1987). Symbiosis in the planktonic foraminifer,Orbulina universa, and the isolation of its symbiotic dinoflagellate,Gymnodinium béii sp. nov. J. Phycol 23: 307–317

    Google Scholar 

  • Spero, H. J., DeNiro, M. J. (1987). The influence of symbiont photosynthesis on the Σ18O and Σ13C values of planktonic foraminiferal shell calcite. Symbiosis 4: 213–228

    Google Scholar 

  • Spero, H., Hagan, D., Vastano, A. (1979). An SEM examination ofSagitta tenuis Conant (Chaetognatha), utilizing a special sedation and handling procedure. Trans. Am. micros. Soc. 98: 139–141

    Google Scholar 

  • Spero, H. J., Parker, S. L. (1985). Photosynthesis in the symbiotic planktonic foraminiferOrbulina universa, and its potential contribution to oceanic primary productivity. J. foraminiferal Res. 15: 273–281

    Google Scholar 

  • Spindler, M., Hemleben, C. (1980). Symbionts in planktonic foraminifera (protozoa). In: Schwemmler, W., Schenk, H. E. A.: (eds.) Endocytobiology, Endosymbiosis and Cell Biology. 1. Walter de Gruyter & Co., Berlin-New York, p. 133–140

    Google Scholar 

  • Sverdlove, M. S., Bé, A. W. H. (1985). Taxonomic and ecological significance of embryonic and juvenile planktonic foraminifera. J. feraminiferal Res. 15: 235–241

    Google Scholar 

  • Towe, K. M. (1971). Lamellar wall construction in planktonic foraminifera. In: Farinacci, A. (ed.) Proc. Second int. Conf. Plank. Microfossils, Roma 1970, Vol. II. p. 1213–1224

    Google Scholar 

  • Very, J.-M., Le Campion, J. (1976). Texture et structure de épines rigides d'Orbulina universa D'Orbigny (Foraminifère planctonique). C. R. Sóances, SPHN Genève, NS 11: 14–17

    Google Scholar 

  • Vilks, G., Walker, D. A. (1974). Morphology ofOrbulina universa d'Orbigny in relation to other spinose planktonic foraminifera. J. foraminiferal Res. 4: 1–8

    Google Scholar 

  • Zucker, W. H. (1973). Fine structure of planktonic foraminifera and their endosymbiotic algae. Ph. D. dissertation, City University of New York, New York, USA

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Geological Sciences, University of South Carolina, 29208, Columbia, South Carolina, USA

    H. J. Spero

Authors
  1. H. J. Spero
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. P. Grassle, Woods Hole

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spero, H.J. Ultrastructural examination of chamber morphogenesis and biomineralization in the planktonic foraminiferOrbulina universa . Mar. Biol. 99, 9–20 (1988). https://doi.org/10.1007/BF00644972

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00644972

Keywords

Search

Navigation