from surface waters of the Pacific Ocean ca. 2 km off Santa. Catalina Island, California, USA. The formation of a spher- ical chamber by this planktonic foraminifer ...
Marine Biology 99, 9-20 (1988)
Marine ................. o- B i o l o g y 9 Springer-Verlag 1988
Ultrastructural examination of chamber morphogenesis and biomineralization in the planktonic foraminifer Orbulina universa H . J . Spero Department of Geological Sciences, University of South Carolina, Columbia, South Carolina 29208, USA
Abstract Pre-sphere, trochospiral Orbulina 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/~m 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 the O. universa spherical chamber is discussed with respect to other foraminiferal species.
Introduction Orbulina universa is a widely distributed species of symbiontbearing foraminifera that is found in the surface plankton between 45 ~ and 45 ~ latitude (B~ et al. 1973). A unique feature of this species is the single, large spherical chamber which surrounds a multi-chambered trochospiral form. This sphere is the final chamber secreted prior to gametogenesis and once formed, the protozoan can only increase in size through thickening of the test wall (Spero 1986, Spero and DeNiro 1987).
Despite an extensive fossil history dating back into the Miocene (Kennett and Srinivasan 1983), Orbulina universa is not commonly used in paleoenvironmental studies for two reasons. First, there is a lack of understanding of the significance of the spherical chamber from a biological, ecological and ultimately, taxonomic perspective (Parker 1962, 1967, Bandy, 1966), and second, the large variability in size, porosity and stable isotopic composition of the shell (B6 et al. 1973, 1976, B6 and Duplessy 1976, Hecht et al. 1976, Malmgren and Healy-Williams 1978, Colombo and Cita 1980, Killingley et al. 1981). In order to interpret the environmental information contained within the shells of fossil Orbulina universa, it is necessary to understand the biological processes that are responsible for the formation of the test in living individuals. Early studies examined plankton and surface sediment samples of O. universa in order to describe the surface morphology and spine structure of the spherical chamber (Le Calvez 1936, B~ et al. 1973, Vilks and Walker 1974, Very and Le Campion 1976). More recently, laboratory experiments with living O. universa have addressed questions regarding the effects of light and temperature on the morphology and stable isotopic composition of the O. universa shell (BouvierSoumagnac and Duplessy 1985, Bouvier-Soumagnac et al. 1986, Spero 1986, Caron et al. 1987, Spero and DeNiro 1987). To date, a detailed study of spherical chamber morphogenesis at the ultrastructural level has not been published. In this study, light, scanning and transmission electron micrography were used to document the development of the spherical chamber of O. universa and to elucidate the taxonomic and functional significance of this morphological feature.
Materials and methods Pre-sphere, trochospiral Orbulina universa were handcollected by scuba divers from the surface waters of the Pacific Ocean, approximately 2 km NNE off the Catalina
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H.J. Spero: Shell morphogenesis in Orbulina universa
Fig. 1. Orbulina universa. (a) Juvenile whorl of trochospiral stage, with proloculus (P) surrounded by six chambers. Secondary apertures (A) are evident. Bar = 25 pro; (b) trochospiral stage, full spiral side. Secondary whorl pattern of 4 chambers replace juvenile whorl pattern. Bar = 50/~m; (c) umbilical side. New chambers (N) are devoid of cytoplasm. The outline of the 1~ aperture is evident (arrow). Bar = 100 #m; (d) initial cytoplasmic bulge at start of sphere formation, Stage I. Bar=200 #m; (e) edge (arrow) of the expanding cytoplasmic layer in Fig. 1 d. Bar = 60 #m; (f) specimen after 10 min of cytoplasm expansion. Bar = 200 #m; (g) SEM of secreted cytoplasmic layer surrounding the trochospiral shell during Stage I of sphere formation. Bar = 100 #m; (h) high magnification view of Fig. 1 g. Bar = 5 #m
M a r i n e Science Center (CMSC), Santa Catalina Island, California (33~ 118~ Individuals were captured between June and September, 1982 to 1984 in 120-ml glass jars and t r a n s p o r t e d to C M S C where all experiments were carried out. The surface water temperature during the study was 19.2 ~ to 23.5~ Procedures for planktonic foraminifera1 maintenance have been described (B6 et al. 1977, 1981). Single Orbulina universa were transferred to 120-ml glass jars containing
filtered seawater (pore s i z e = 1.2 #m), and were fed one l - d - o l d Artemia sp. nauplius every other day. Individuals were maintained at 20~ ~ throughout the study. Illumination was provided on a t2 h light: 12 h d a r k cycle at an intensity o f 60 #E m - z s - t using G E F20T12CW fluorescent bulbs. A p p r o x i m a t e I y 100 Orbutina universa were observed daily. The size and the addition of trochospiral chambers o f each individual were recorded using a U n i t r o n Inverted
H.J. Spero : Shell morphogenesis in Orbulina universa compound microscope. Since the spherical chamber is secreted predominantly at night, individuals were observed hourly between dusk and dawn (18:00 hrs to 06:00 hrs local time) using only low level illumination. All statistical calculations are _+1 SD. Light micrographs were taken with a Nikon Microflex EFM compound microscope. Living individuals were fixed at 4 ~ for 1 h with 3% glutaraldehyde and post-fixed for 3 h with 2% osmium tetroxide (O.R. Anderson personal communication). Both fixative solutions were prepared in 0.005 M sodium cacodylate-buffered seawater (pH 8.0). For
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