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The Ultrastructure and Taxonomic Identity of the Symbiotic Algae of Heterostegina Depressa (Foraminifera: Nummulitidae)*

Published online by Cambridge University Press:  11 May 2009

R. Schmaljohann
Affiliation:
Institut für Allgemeine Mikrobiologie and Geologisch-Paläontologisches Institut der Universität Kiel (Germany)
R. Röttger
Affiliation:
Institut für Allgemeine Mikrobiologie and Geologisch-Paläontologisches Institut der Universität Kiel (Germany)

Extract

There are numerous examples of symbiotic associations between Foraminifera and unicellular algae. Most of these Foraminifera are larger Foraminifera which occur in the shallow, oligotrophic waters of tropical seas (Table 1). Some of the symbiotic algae have been studied by light microscopy (Table 1, nos. 1–6). Dietz-Elbrächter (1971) suggested that the symbionts of Heterostegina depressa might be diatoms. She was, however, unable to prove this statement satisfactorily. Hottinger & Dreher (1974) published electron micrographs of the symbionts of H. depressa and Operculina ammonoides. From these micrographs identification of the symbionts was not possible. To date, only the symbionts of the following Foraminifera have been classified by electron microscopy:Archaias angulatus, Sorites marginalis, Globigerinoides ruber, Hastigerina pelagica and Globigerinoides sacculifer (Table 1, nos. 7,10,12,13,14).

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1978

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References

REFERENCES

Alldredge, A. L. & Jones, B. M., 1973. Hastigerina pelagica: foraminiferal habitat for planktonic dinoflagellates. Marine Biology, 22, 131135.CrossRefGoogle Scholar
Anderson, O. R. & Be, A. W. H., 1976. The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates. Journal of Foraminiferal Research, 6, 121.CrossRefGoogle Scholar
Apelt, G., 1969. Die Symbiose zwischen dem acoelen Turbellar Convoluta convoluta und Diatomeen der Gattung Licmophora. Marine Biology, 3, 165187.CrossRefGoogle Scholar
Belcher, J. H., 1969 a. A morphological study of the phytoflagellate Chrysococcus rufescens Klebs in culture. British Phycological Journal, 4, 105117.CrossRefGoogle Scholar
Belcher, J. H., 1969 b. Some remarks on Mallomonas papillosa Harris and Bradley and M. calceolus Bradley. Nova Hedwigia, 18, 257270.Google Scholar
Belcher, J. H., 1974. Chrysosphaera magna sp. nov., a new coccoid member of the Chrysophyceae. British Phycological Journal, 9, 139144.CrossRefGoogle Scholar
Belcher, J. H. & Swale, E. M. F., 1967. Chromulina placentula sp. nov. (Chrysophyceae), a freshwater nannoplankton flagellate. British Phycological Bulletin, 3, 257267.CrossRefGoogle Scholar
Belcher, J. H. & Swale, E. M. F., 1971. The microanatomy of Phaeaster pascheri Scherffel (Chrysophyceae). British Phycological Journal, 6, 157169.CrossRefGoogle Scholar
Belcher, J. H. & Swale, E. M. F., 1972. Some features on the microanatomy of Chrysococcus cordiformis, Naumann. British Phycological Journal, 7, 5359.CrossRefGoogle Scholar
Berkaloff, C., 1961. Etude au microscope électronique des plastes de Laminaria saccharina L. Compte rendu hebdomadaire des séances de l'Académie des sciences, 252, 27472749.Google Scholar
Berkaloff, C., 1963. Les cellules méristématiques d'Himanthalia lorea (L.) S. F. Gray. Etude au microscope électronique. Journal de Microscopie, 2, 213228.Google Scholar
Bisalputra, T. & Bisalputra, A. A., 1967. Chloroplast and mitochondrial DNA in a brown alga Egregia menziesü. Journal of Cell Biology, 33, 511520.CrossRefGoogle Scholar
Bisalputra, T. & Bisalputra, A. A., 1969. The ultrastructure of chloroplast of a brown alga Sphacelaria sp. I. Plastid DNA configuration - the chloroplast genophore. Journal of Ultrastructure Research, 29, 151170.CrossRefGoogle Scholar
Bouck, G. B., 1965. Fine structure and organelle associations in brown algae. Journal of Cell Biology, 26, 523537.CrossRefGoogle ScholarPubMed
Casper, S. J., 1972. Zum Feinbau der GeiBeln der Chrysomonaden. I. Uroglena americana. Archiv für Protistenkunde, 114, 6582.Google Scholar
Casper, S. J., 1974. Grundzüge eines natürlichen Systems der Mikroorganismen. Jena: Fischer.Google Scholar
Christensen, T., 1962. Alger. In Botanik, vol. 2 (Systematisk Botanik), No. 2, Part 2 (ed. Böcher, T. W., Lange, M. and Sørensen, T.), 178 pp. Copenhagen: Munksgaard.Google Scholar
Clarke, K. J. & Pennick, N. C., 1975. Syncrypta glomerifera sp. nov., a marine member of the Chrysophyceae bearing a new form of scale. British Phycological Journal, 10, 363370.CrossRefGoogle Scholar
Cole, K., Bourne, V. & Lin, S. C., 1968. Electron microscope observations on chloroplasts of Leathesia difformis (L.) Aresch. Canadian Journal of Genetics and Cytology, 10, 63 ff.CrossRefGoogle Scholar
Coombs, J., Lauritis, J. A., Darley, W. M. & Volcani, B. E., 1968. Studies on the biochemistry and fine structure of silica shell formation in diatoms. V. Effects of colchicine on wall formation in Navicula pelliculosa (Bréb.) Hilse. Zeitschrift für Pflanzenphysiologie, 59, 124152.Google Scholar
Crawford, R. M., 1973. The cytoplasmatic ultrastructure of the vegetative cells of Melosira varians Ag. Journal of Phycology, 9, 5061.CrossRefGoogle Scholar
Cushman, J. A., 1922. Shallow-water foraminifera of the Tortugas region. Papers from the Department of Marine Biology of the Carnegie Institution of Washington, 17, 85 pp.Google Scholar
Dawson, P. A., 1973. Observations on the structure of some forms of Gomphonema parvulum Kütz. II. The internal organization. Journal of Phycology, 9, 165175.Google Scholar
Descomps, S., 1963 a. Contribution à l'étude infrastructurale des Vaucheries (Xanthophycées, Chromophytes). Compte rendu hebdomadaire des séances de l'Académie des sciences, 256, 13331335.Google Scholar
Descomps, S., 1963 b. Observations sur l'infrastructure de l'enveloppe des chloroplastes de Vaucheria (Xanthophycées). Compte rendu hebdomadaire des seances de l'Académie des sciences, 257, 727729.Google Scholar
Dietz-Elbrächter, G., 1971. Untersuchungen über die Zooxanthellen der Foraminifere Heterostegina depressa Orbigny 1826. ‘Meteor’ Forschungsergebnisse, Reihe C, No. 6, 4147.Google Scholar
Dodge, J. D., 1973. The Fine Structure of Algal Cells, xii, 261 pp. New York: Academic Press.Google Scholar
Dodge, J. D. & Crawford, R. M., 1971. A fine structural survey of dinoflagellate pyrenoids and food-reserves. Botanical Journal of the Linnean Society, 64, 105115.CrossRefGoogle Scholar
Drum, R. W., 1963. The cytoplasmic fine structure of the diatom Nitzschia palea. Journal of Cell Biology, 18, 429440.CrossRefGoogle ScholarPubMed
Drum, R. W., 1969. Light and electron microscope observations on the tube-dwelling diatom Amphipleura rutilans (Trentepohl) Cleve. Journal of Phycology, 5, 2126.CrossRefGoogle ScholarPubMed
Drum, R. W. & Pankratz, H. S., 1964. Pyrenoids, raphes, and other fine structure in diatoms. American Journal of Botany, 51, 405418.CrossRefGoogle Scholar
Drum, R. W., Pankratz, H. S. & Stoermer, E. F., 1966. Electron microscopy of diatom cells. In Diatomeenschalen im elektronenmikroskopischen Bild, vol. IV, (ed. Helmcke, J. C. and Krieger, W.). Lehre: Cramer.Google Scholar
Esser, K., 1967. Elektronemikroskopischer Nachweis von DNS in den Pyrenoiden von Streptotheca thamensis. Zeitschrift für Naturforschung, 22B, 993.CrossRefGoogle Scholar
Evans, L. V., 1966. Distribution of pyrenoids among some brown algae. Journal of Cell Science, 1, 449454.CrossRefGoogle ScholarPubMed
Evans, L. V., 1968. Chloroplast morphology and fine structure in British fucoids. New Phytologist, 67, 173178.CrossRefGoogle Scholar
Falk, H., 1967. Zum Feinbau von Botrydium granulatum Grev. (Xanthophyceae). Archiv für Mikrobiologie, 58, 212227.CrossRefGoogle Scholar
Falk, H. & Kleinig, H., 1968. Feinbau und Carotinoide von Tribonema (Xanthophyceae). Archiv für Mikrobiologie, 61, 347362.CrossRefGoogle ScholarPubMed
Franke, W. W. & Herth, W., 1973. Cell and lorica fine structure of the chrysomonad alga, Dinobryon sertularia Ehr. (Chrysophyceae). Archiv für Mikrobiologie, 91, 323344.CrossRefGoogle Scholar
Gibbs, S. P., 1962. Nuclear envelope – chloroplast relationships in algae. Journal of Cell Biology, 14, 433444.CrossRefGoogle ScholarPubMed
Gibbs, S. P., 1970. The comparative ultrastructure of the algal chloroplast. Annals of the New York Academy of Sciences, 175, 454473.Google Scholar
Gibbs, S. P., Cheng, D. & Slancis, T., 1974. The chloroplast nucleoid in Ochromonas danica. I. Three-dimensional morphology in light- and dark-grown cells. Journal of Cell Science, 16, 557577.CrossRefGoogle ScholarPubMed
Heitz, E., 1961. Das lamelläre Dünn-Dick-Muster der Chloroplasten von Chlamydomonas, Euglena, Fucus, Vaucheria. Zeitschrift für Zellforschung und mikroskopische Anatomie, 53, 444448.CrossRefGoogle Scholar
Hibberd, D. J., 1970. Observations on the cytology and ultrastructure of Ochromonas tuberculatus sp. nov. (Chrysophyceae), with special reference to the discobolocysts. British Phycological Journal, 5, 119143.CrossRefGoogle Scholar
Hibberd, D. J., 1971. Observations on the cytology and ultrastructure of Chrysamoeba radians Klebs (Chrysophyta). British Phycological Journal, 6, 207223.CrossRefGoogle Scholar
Hibberd, D. J., 1976. On the ultrastructure and taxonomy of the Chrysophyceae and Prymnesiophyceae: a survey with some new observations on the ultrastructure of the Chrysophyceae. Botanical Journal of the Linnean Society, 72, 5580.CrossRefGoogle Scholar
Holdsworth, R. H., (1968). The presence of a crystalline matrix in pyrenoids of the diatom Achnanthes brevipes. Journal of Cell Biology, 37, 831837.CrossRefGoogle ScholarPubMed
Hottinger, L. & Dreher, D., 1974. Differentiation of protoplasm in Nummulitidae (Foraminifera) from Elat, Red Sea. Marine Biology, 25, 4161.CrossRefGoogle Scholar
Hovasse, R. & Joyon, L., 1960. Contribution à l'étude de la Chrysomonadine Hydrurus foetidus. Revue algologique, 5, 6683.Google Scholar
Kowallik, K. V., 1974. Die Algen. In Ultrastruktur der pflanzlichen Zelle (ed. Robards, A. W.), pp. 181224. Stuttgart: Thieme.Google Scholar
Leadbeater, B. S. C., 1969. A fine structural study of Olisthodiscus luteus Carter. British Phycological Journal, 4, 317.CrossRefGoogle Scholar
Lee, J. J., Crockett, L., Hagen, J. & Stone, R., 1974. The taxonomic identity and physiological ecology of Chlamydomonas hedleyi sp. nov., algal flagellate symbiont from the foraminifer Archaias angulatus. British Phycological Journal, 9, 407422.CrossRefGoogle Scholar
Lefort, M., 1962. Contribution à l'étude inframicroscopique du Tribonema aequale (Pasch.). Compte rendu hebdomadaire des séances de l'Academie des sciences, 254, 30223024.Google Scholar
Manton, I. & Von Stosch, H. A., 1966. Observations on the fine structure of the male gamete of the marine centric diatom Lithodesmium undulatum. Journal of the Royal Microscopical Society, 85, 119134.CrossRefGoogle Scholar
Manton, I. & Harris, K., 1966. Observations on the microanatomy of the brown flagellate Sphaleromantis tetragona Skuja with special reference to the flagellar apparatus and scales. Journal of the Linnean Society (Botany), 59, 397403.CrossRefGoogle Scholar
Massalski, A. & Leedale, G. F., 1969. Cytology and ultrastructure of the Xanthophyceae. I. Comparative morphology of the zoospores of Bumilleria simla Borzi and Tribonema vulgare Pascher. British Phycological Journal, 4, 159180.Google Scholar
Müller-Merz, E. & Lee, J. J., 1976. Symbiosis in the larger foraminiferan Sorites marginalis (with notes on Archaias spp.). Journal of Protozoology, 23, 390396.CrossRefGoogle Scholar
Parke, M., Green, J. C. & Manton, I., 1971. Observations on the fine structure of zoids of the genus Phaeocystis (Haptophyceae). Journal of the Marine Biological Association of the United Kingdom, 51, 927941.CrossRefGoogle Scholar
Peterfi, L. S., 1969. The fine structure of Poteriochromonas malhamensis (Pringsheim) comb. nov. with special reference to the lorica. Nova Nedwigia, 17, 93103.Google Scholar
Röttger, R., 1972. Die Kultur von Heterostegina depressa (Foraminifera, Nummulitidae). Marine Biology, 15, 150159.CrossRefGoogle Scholar
Ross, C. A., 1972. Biology and ecology of Marginopora vertebralis (Foraminferida), Great Barrier Reef. Journal of Protozoology, 19, 181192.CrossRefGoogle Scholar
Rouiller, C. & Fauré-Fremiet, E., 1958. Structure fine d'un flagellé Chrysomonadien: Chrontulina psammobia. Experimental Cell Research, 14, 4767.CrossRefGoogle ScholarPubMed
Schnepf, E. & Deichgräber, G., 1969. Über die Feinstruktur von Synura petersenü unter besonderer Berücksichtigung der Morphogenese ihrer Kieselschuppen. Protoplasma, 68, 85106.CrossRefGoogle Scholar
Schnepf, E., Koch, W. & Deichgräber, G., 1966. Zur Cytologie und taxonomischen Einordnung von Glaucocystis. Archiv fur Mikrobiologie, 55, 149174.CrossRefGoogle Scholar
Stoermer, E. F., Pankratz, H. S. & Drum, R. W., 1964. The fine structure of Mastogloia grevillei. Protoplasma, 59, 113.CrossRefGoogle Scholar
Stoermer, E. F., Pankratz, H. S. & Bowen, C. C., 1965. Fine structure of the diatom Amphipleura pellucida. II. Cytoplasmic fine structure and frustule formation. American Journal of Botany, 52, 10671078.CrossRefGoogle Scholar
Swale, E. M. F., 1969. A study of the nannoplankton flagellate Pedinella hexacostata Vysotskü by light and electron microscopy. British Phycological Journal, 4, 6586.CrossRefGoogle Scholar
Taylor, D. L., 1972. Ultrastructure of Cocconeis diminuta Pantocsek. Archiv für Mikrobiologie, 81, 136145.CrossRefGoogle Scholar
Taylor, D. L., 1974. Symbiotic marine algae: taxonomy and biological fitness. In Symbiosis in the Sea (ed. Vernberg, W. B.), pp. 245262. Columbia: University of South Carolina Press.Google Scholar
Throndsen, J., 1971. Apedinella gen. nov. and the fine structure of Apedinella spinifera (Throndsen) comb. nov. Norwegian Journal of Botany, 18, 4764.Google Scholar
Van Der Veer, J., 1970. Ancylonoton luteum (Chrysophyta), a new species from the Tamar Estuary, Cornwall. Acta botanica neerlandica, 19, 616636.CrossRefGoogle Scholar
Van Valkenberg, S. D., 1971. Observations on the fine structure of Dictyocha fibula Ehrenberg. II. The protoplast. Journal of Phycology, 7, 118132.CrossRefGoogle Scholar
Winter, F. W., 1907. Zur Kenntnis der Thalamophoren. Archiv für Protistenkunde, 10,1113.Google Scholar
Zucker, W. H., 1973. Fine Structure of Planktonic Foraminifera and their Endosymbiotic Algae. Ph.D. Thesis, City University of New York.Google Scholar