O. Roger Anderson'. Michael ... Rosalina floridana (Cushman) (Angell, 1967); Bolivina doniezi Cushman and .... According to Angell (1967) the anlage is an.
Allan W. H. Bel Christoph HemlebenO. Roger Anderson' Michael Spindler?
Chamber formation in planktonic foraminifera
+Lemont-Dohertv Geological Observatory Columbia University Palisades. New York 10964 21nstitut für Geologie und Paläontologie Universität Tübingen Sigwartstrasse 10 Tübingen, West Germany
ABSTRACT
INTRODUCTlor~
Chamber formation in Globorotalia hirsuta and G. truncatulinoides begins at ST (start time) with the retraction of the normal, long rhizopodia and the emergence of a growing cytoplasmic bulge from the aperture. Short. thick rhizopodia fan out from the bulge about 30 min. after ST. When the distal tips of the RR (radiating rhizopodia) are maximally extended, they stretch about 20 to 30 p.m beyond the periphery of the chamber-to-be (1 hr. after ST). The translucent bulge expands gradually to form the shape of the new chamber (1 hr. 10min. after ST). Retraction of the R Rand the simultaneous transformation of the coarsely undulating periphery of the translucent bulge to a smooth border signals the development of the "anlaqe." an organic structure which is the nucleation site for calcification of the chamber wall (1 hr. 20 min. after ST). An OPE (outer. organic protective envelope) shields the anlage, where calcification starts with the secretion of minute calcareous plaques on both sides of the POM (primary organic membrane) (2 to 3 hrs. after ST). As the jigsaw-puzzle-shaped calcareous plaques increase in size and number. they eventually coalesce to form abilamellar wall several micrometers in thickness. Formation of such a new thin-walled chamber takes about 5 to 6 hours. The wall can be further thickened by lamellar accretion, mainly when the foraminifer adds successive chambers to its shell.
Shell growth and events leading to the formation and calcification of new chambers in foraminifera have been studied by a number of investigators. Schultze (1854) was the first to observe chamber formation in foraminifera. Since then in vivo shell growth has been investigated in the following benthic species: Peneroplis pertusus (Forskäl) (Winter, 1907); Quinqueloculina sp. (Hofker, 1930); Patellina corrugata Williamson (Myers, 1935; Berthold, 1976); Glabratella (= "Discorbis") patelliformis (Myers, 1940); Tretomphalus bulloides (d'Orbigny) (Mvers. 1943); Elphidium crispum (Linne) (= Polystomella crispa) (Lister. 1903; Schaudinn, 1911; Jepps, 1942); Discorbinella bertheloti (d'Orbiqnv) (Le Calvez. 1938); Rosalina floridana (Cushman) (Angell, 1967); Bolivina doniezi Cushman and Wickenden (Sliter, 1970); and Heterostegina depressa d'Orbigny (Spindler, 1976; Spindler and Röttger, 1973), These observations have been restricted until now to benthic foraminifera and. except for Anqell's (1967) and Spindler's (1976) electron-microscopic studies. the earlier ones were limited to light-microscopic investigations. Recent progress in collecting techniques and maintaining planktonic foraminifera in the laboratory (Be et al.. 1977) heraids the start of biological experimentation on various topics of geological interest including chamber formation and mode of biomineralization in these free-floating marine organisms. We have observed the addition of new chambers and spine growth in spinose Globigerinoides ruber (d'Orbigny), but observations of the complete chamber formation process were impeded in this species by the density of its spines and rhizopodial network and the frequent rotation and floating habit of the globular shell. These difficulties are minimized in the non-spinose group of planktonic foraminifera, because they remain on the bottom of the culture vessel and do not possess spines that tend to obscure the shell. Moreover, in those species with a relatively flat shell. such as Globorotalia hirsuta (d'Orbiqnv). the spiral or apertural side is usually oriented parallel to the culture vessel bottom and hence allows plan-viewing of the construction of a new chamber. METHODS
AND
MATERIALS
Numerous specimens of Globorotalia truncatulinoides (d'Orbigny) and G. hirsuta were collected during the winter months (December to March) of 1976, 1977 and 1978 by slowly towing plankton nets (202-J.Lm mesh aperture) in the surface water about 4 miles south off Bermuda. The collecting procedure and maintenance methods in the laboratory were described by Be et al. (1977). Most light microscopic observations were carried out at the Bermuda Biological Station. Live micropaleontology,
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specimens of G. hirsuta were also sent by airplane to Lamont-Doherty Geological Observatory, where they were kept in natural sea-water from the collecting site, treated with an antibiotic/antimycotic mixture 100x from Grand Island Biological Co .. Grand lsland. N.Y. (1 ml/100 ml seawater). The present study is based on detailed light-microscope observations of chamber formation in 29 specimens of G. truncatulinoides and 14 of G. hirsuta. Of these, 5 specimens of the former species and 7 of the latter were also studied with the transmission electron microscope. The light-microscopic observations were carried out with Leitz "Diavert" and Zeiss inverted polarizing microscopes. Low light intensity during microscopic viewing is necessary to prevent the specimens fram aborting or halting chamber formation. For critical point drying and scanning electron microscopy, the specimens were fixed in 0.2-4% glutaraldehyde buffered with 0.2 M cacodylate, pH-8.0, at 25°C, dehydrated in a graded ethanol series. critical-point-dried using liquid CO2 as the transitional fluid, coated with carbon and Au :Pd alloy (3 :2) in a vacuum evaporator, and examined in a Cambridge Mark Ila scanning electron micrascope. Specimens for transmission electron microscopy were fixed for 1 hour at 25°C in 3% glutaraldehyde prepared in 0.2 M cacodylate-buffered seawater, pH = 8.0. The specimens were washed in cacodylate-buffered seawater and suspended in agar, which after solidification was dissected into small cubes surreunding each specimen, and post-fixed for 2 hours at 3°C in 2% osmium tetroxide in the same cacodylate buffer as prepared for glutaraldehyde fixation. The osmiumfixed specimens were dehydrated in a graded ethanol series, cleared ir) propylene oxide and embedded in Epon 812. Ultrathin sections were obtained with a diamond knife in a Porter-Blum MT-2 ultramicrotome, collected on uncoated copper grids, and examined with a Philips EM 200 electron microscope operated at 60 kV. LIGHT
AND
ELECTRON
MICROSCOPIC
OBSERVATIONS
Specimens of Globorotalia hirsuta and G. truncatulibrought into the laboratory remain on the bottom of the culture vessels, where by means of their widely dispersed rhizopodia they may move over short distances (several centimeters/day) and generally in circular paths. The long rhizopodia (pI. 1, figs. 1, 2) are also used to capture food organisms and to eject waste material. Rhizopodia are normally several millimeters in length, although individual strands can be as long as 15 mm ; their distal ends are often so thickened as to resemble miniature wheat stalks. These thickened segments are not fixed in position, but can be seen to
no/des
move along the rhizopodia in both directions. The nature and configuration of the rhizopodial network on the outer shell surface of G. truncatulinoides are shown in plate 1, figures 3 and 4. In the following general discussion of chamber formation in Globorotalia hirsuta and G. truncatulinoides, we shall describe our observations involving various specimens in terms of the number of minutes lapsed since onset of chamber formation. Most of our observations of chamber formation were made during the day, although chambers also form at night. Because of their close similarity in temporal and ultrastructural development of a new chamber wall, we deem it valid to make light- and transmission electron microscopic cornparisons between these two species. Extrusion of a growing protoplasmic
bulge
The first indication of the impending formation of a new chamber (ST. or Start Time) is the withdrawal and reduced activity of the long, thin rhizopodia in the apertural region and an increase of cvtoplasrnic streaming inside the shell. This is followed by the extrusion of an apparently unorganized cytoplasmic bulge from the aperture (pI. 1, figs. 5, 6). Soon short. thick rhizopodia radiate from the bulge in a fanlike arrangement (30 min. after ST; pi. 2, fig. 1 ; pI. 4, fig. 1). These RR (radiating rhizopodia) differ from the longer, thinner and more widely-spaced rhizopodia that normally surround the rest of the shell (pI. 2, fig. 2). During chamber formation prior to calcification the specimens lie still on the bottom of the culture vessel. In about 50% of the chamber-forming specimens, the bulge is differentiated into an inner section of opaque, densely granular cvtoplasrn (probably cytoplasm protruding from the last chamber) and an outer section that is translucent and less dense and consists of a closely interwoven network of radiating rhizopodia (pI. 2, fig. 1 ; pI. 4, figs. 1-8). In the remaining specirnens. the bulge is homogeneously translucent. indicating that the presence of "opaque" cytoplasm is not essential to new chamber formation. About 1 hour after ST. the distal ti ps of the RR reach their maximum extent and form the outline of the OPE (outer protective envelope), thuscreating a transparent region between the OPE and the translucent bulge (pI. 2, figs. 1, 2). The translucent bulge expands gradually toward and up to the OPE. The opaque section (if present) expands only slightly and occupies at maximum the inner third or inner half of the bulge. Formation of the Anlage
When the translucent bulge has attained its maximum expansion about 1 hr. after ST (pI. 2, fig. 2; pI. 4, fig. 3),
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a rapid transformation of its periphery takes place that changes it from a roughly undulating surface (pI. 4, fig. 3) to a smooth one (pI. 4, fig. 5). The process takes only about 10min., starting with the formation of a distinct border between the translucent and transparent regions and ending with the disappearance of the RR. Concurrently, the smoothen ing of the periphery starts at or near the aperture and spreads to other peripheral parts of the bulge. When completed at 1 hr. 20 min. after ST, the smooth peripheral surface of the translucent bulge forms the true position and outline of the new chamber that is now ready for calcification (pI. 2, fig. 5; pI. 4, fig. 5). We conclude that the peripheral region of the translucent section is the actual site of calcification of the chamber vva!l. based on the observation that 2 ultrastructural elements at the bulge periphery are consistently and closely associated with the first appearance of calcareous plaques. These structures are the CE (cytoplasmic envelope) and the POM (primary organic membrane), which we shall term collectively the "anlaqe". According to Angell (1967) the anlage is an aggregation of vesicles held together by a filamentous groundmass upon which calcification takes place. Although our and Angell's ultrastructural observations of the anlage differ sornevvhat. due to differences in cytoplasmic organization between planktonic and benthic foraminifera, we use the term anlage to broadly mean the organic structures that are directly responsible for the initial calcification of the chamber wall.
in p/anktonic
foraminifera
The CE (cytoplasmic envelope) is a densely stained, membranous cytoplasmic layer which is formed by differentiation and lateral extension of the distal RR (pI. 5, figs. 1,2). In transmission electron micrographs the units that make up the CE measure up to 3 f.Lm in Ie-ngth. Their connection to the RR and the presence of a plasma membrane indicate that the CE is a living structure (pi. 5, fig. 2). Based on many ultrathin sections. it appears that the approximately equidimensional units are either organized as an open-Iattice grille or as a patchwork of plaques interconnected by narrow bridges. The POM (primary organic membrane) is situated almost directly against the proximal side of the CE (pI. 5, figs. 1,4). The extremely thin (500-600 A) but continuous POM is the initial template for calcification, as we shall demonstrate later. Since the POM and CE are intimately associated, we speculate that the POM may originate by secretory activity of the CE. High magnification TEM images of CE sections reveal a fine calyx of organic fibrils on the outer surface of the membrane which could have such a secretory function. However, we cannot dismiss the possibility thatthe RR could also contribute toward the stabilization and possible synthesis of the POM. The fact that the CE is always present on the distal and not on the proximal side of the POM, and that calcification occurs on both sides of the POM, indicates that the CE itself is not exclusively involved in calcite secretion if at all. Moreover, wherever calcification is at a
PLATE 1 Specimens of Globorotalia truncatulinoides (d'Orbigny) collected in plankton tows off Bermuda in January, 1976. The specimens in figures 2, 3 and 4 were prepared by critical point drying and viewed with a scanning electron microscope. Specimen with long, thin rhizopodia (arrow), x 195. 2 3-4
capturing
spherical dinoflagellate
Rhizopodial network forms a diameter of 8 mm around shell.
x
cells of Crypthecodinium
cohnii
20.
Rhizopodial network on shell surface. 3, x 125; 4, x 1260.
5
Impending chamber formation is signaled by emergence of cytoplasmic bulge, x 160. Note general absence of rhizopodia in bulge region.
6
The cytoplasmic bulge produces many rhizopodia. Same specimen as figure 5, 11 minutes later.
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relatively advanced stage, the CE is either absent or some distance off and not in direct contact with the calcareous units (pI. 6, fig. 2), suggesting the possibility that the CE is about to disperse and hence that it may not be directly involved in calcification. Formation of the OPE (outer protective envelope)
When the RR have reached their fuillength, their distal tips form a thin, peripheral border-the OPE (pI. 2, figs. 1-3). The long rhizopodia emanating from adjacent chambers mayaiso take part in forming the OPE by bending lengthwise and shaping its peripheral outline. The extent of any interaction between these neighboring rhizopodia and the RR in forming the OPE is not clearly understood. The time of OPE formation seems to vary between different species and between individual specimens. In Globorotalia truncatulinoides, the OPE can be detected at a relatively early stage when the RR still protrude quite far from the translucent bulge and thus leave a wide transparent zone between the OPE and translucent bulge (pi. 2. figs. 1. 2). However, in some specimens of G. truncatulinoides and in most G. hirsuta specimens we have observed at the stage in which their RR are extended, the OPE is either so thin as to be invisible under the light microscope or not yet formed. In these specimens, the OPE comes into being at the same time or after the peripheral smoothening and the formation of the anlage (1 hr. 20 min. after ST; pI.4,fig, 5).
in p/anktonic
foraminifera
We envisage the OPE as a complex structure that may consist of rhizopodia as weil as a thin, organically secreted, non-living amorphous layer. This amorphous laver. visible with the TEM in ultrathin sections (pi. 5, fig. 1), va ries in thickness from about 0.2 to 1.0 tut: and is only from 3 to 5 fLm from the anlage at relatively advanced stages of chamber formation. We believe that the OPE shields the nearby, delicate rhizopodia and other organelles which produce the anlage. There is a structural resemblance between the OPE and the "pellicle" of the benthic species, Discorbinella bertheloti, described by Le Calvez (1938, p. 267). However, whereas Le Calvez considered the pellicle to be the first element of the shell upon which calcite particles are secreted and gradually coalesce, we believe that the OPE does not take part in calcification except in a protective role. Considering the fact that the OPE and the anlage are only separated by about 5 fLm from each other, at least in the 2 planktonic species we have studied, and that Le Calvez's observations were obtained by light microscopy with limited resolution, it is understandable why he would not have been able to distinguish these 2 structural features if they were present in the benthic species he investigated. In some specimens of G. hirsuta a granular mass of material is sometimes extruded directly outside the OPE. It resembles a protective growth cyst that is commonly constructed prior to chamber formation in benthic foraminifera (Le Calvez, 1938; Sliter, 1970;
PLATE 2 Chamber formation in a single individual of Globorotalia truncatulinoides (d'Orbigny) collected January 5, 1976. OPE, outer protective envelope; RR, radiating rhizopods; TB, translucent bulge; OB, opaque bulge. The sequence of events is: 1
09:35:TranslucentbulgewithRR.DistaltipsofRRincontactwithOPE,
2
09:45: Translucent bulge expands, thereby filling "transparent"
3
10 :35: Retraction of RR in transparent region indicates anlage has been formed, close to bulge (arrow).
4
10 :37 : Calcification
5
10 :55: Anlage has been formed and small calcareous particles begin to appear (arrow). OPE is clearly separated from peripherv of new chamber, x 135.
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not yet evident under polarized light
x
270.
region between it and OPE, x
x
135.
135. Note tha,t OPE is now
x 135.
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Spindler and Röttger, 1973). In planktonic foraminifera, however. this granular material does not form a continuous, well-defined structure and its occurrence is so sporadic that it probably is not essential in the chamber formation process.
in p/anktonic
foraminifera
an organic layer similar in appearance to the POM (pI. 5, fig. 4). The calcite on the proximal side of the POM is normally thinner than that on the distal side. The fact that calcite is formed on both sides of the POM is evidence that the POM is the nucleating site for calcification.
Calcification
Two to three hours from the start of our observations a few small dark specks appear on the cytoplasm exterior (pI. 3, fig. 3; pI. 4, figs. 7, 8) and their optical interference figures under the polarizing microscope indicate that they are initial secretions of calcareous particles (pI. 3, figs. 1-2). Specimens fixed at this stage for transmission electron microscopic studies confirmed that calcareous plaques had indeed formed (pI. 5, figs. 3,4). Plate 5, figure 3 shows the ultrastructural elements just prior to or at the point of calcification of a new chamber wall. The anlage is indicated by a relatively dense concentration of rhizopodia and other ultrastructural elements. The space between the incipient wall and the cytoplasm is filled by rhizopodia of varying density that makes up the translucent bulge. The smallest calcareous plaques (pI. 5, figs. 3, 4) measure about 5 J..Lm in diameter and about 3 J..Lm in thickness. Each plaque is bisected by the POM and is completely surrounded by
We conjecture that plate 6, figures 1 and 2 are 2 successive stages in the lateral enlargement of a calcareous plaque and that those parts of the POM and the plaque upon wh ich the densely granular rhizopodia impinge are sites of active calcification. Plate 6, figure 1 exhibits two calcite layers-a thin proximal and a thicker distal calcite layer-which are separated by the POM and are enveloped by organic layers. The appearance of calcareous plaques as tiny dark specks (2 hrs. 30 min. after ST), their lateral growth to irregularly shaped plaques (4 hrs. 5 min. after ST), and the coalescence of the jigsaw-puzzle-shaped pieces (5 hrs. 5 min. after ST) are shown in a sequence of light micrographs (pI. 3, figs 3-6). In wall cross-sections. the junctions of these calcareous plaques are marked by the vertically oriented organic envelopes of the plaques (pI. 6, fig. 2). As more and more plaques coalesce. they eventually form two continuous layers of the so-called "bilarnellar" wall (Reiss, 1957).
PLATE 3 Continuation
1-2 3
of chamber formation in the same individual of Globorotalia truncatulinoides (d'Orbigny)
as in plate 2.
11 :20: Under polarized light calcareous plaques grow rapidly, showing up as white discontinuous patches on surface of anlage, x 185. 11 :27: Calcareous plaques become more visible, but still isolated from each other. x 185.
4 12 :00: Several plaques coalesce and become part of continuous calcite laver.
x
185.
5 13:10: Calcareous plaques grow larger and are shaped as jig-saw puzzles. Some plaques start to coalesce. Pore areas are visible as small dark depressions, x 285. 6
300
14:10: Calcareous plaques show further growth and coalesce to form larger continuous x 285.
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Inner organic lining
It should be noted that when a thin. bilamellar wall is formed (pi. 6, fig. 2) there is as yet no evidence of an IOl (inner organic lining). The IOl is usually a prominent structure on the proximal shell surface of earlier, more mature chambers (Hemleben et al.. 1977, pI. 6, fig. 3). The question arises: when and how is the IOl formed in a new chamber? Since in the benthic foraminifer Heterostegina depressa the IOl develops several days after the new chamber is completed (Spi ndler, 1978), it is conceivable that the 10l in planktonic foraminifera mav also require considerable time to form after the construction of a new chamber wall. Pore formation
and further wall-thickening
In the present study we have not concerned ourselves with pore formation and wall-thickening, since Hemleben et al. (1977) have investigated these aspects in a related species, Globorotalia menardii. The wall microstructure in G. truncatulinoides and other planktonic foraminifera have been described by Be and lott (1964), Takayanagi, Niitsuma and Sakai (1968), Pessagno and Miyano (1968), Towe and Cifelli (1967), and Towe (1971).
To elucidate the relationship between pores and wall development, the appearance of pores in a 2-f1.m thick wall of G. hirsuta is shown in plate 6, figure 2. It is noteworthy that the pore plate is already developed when the chamber wall is still relatively thin and that the pore plate is basically a direct extension of the POM. At an early stage of wall formation, the keel area is covered by pores. These pores disappear in time, as successive accretions of calcite are built over this peripheral region of the shell (Hemleben et al.. 1977). When the original bi lamellar wall has reached its maximum development, there can be additional thickening by the superposition of one or more calcite lavers on the distal side. Plate 6, figure 3 shows one such layer that is deposited on a 5-f1.m thick bilamellarwall. The process of wall thickening in G. menardii was described in detail by Hemleben et al. (1977). SUMMARY
The following events in the formation of a new chamber have been followed with the light microscope in a number of specimens of Globorotalia hirsuta and G. truncatulinoides collected off Bermuda. The actual time
PlATE 4 All figures are of a single specimen of Globorotalia hirsuta (d'Orbigny) that built a new chamber on March 26, 1977. All figures are magnified x 166. 1
13 :51 : Emergence of cytoplasmic bulge that consists of inner opaque and outer. translucent sections. Note RR.
2
14:10: Translucent bulge gradually expands.
3
14 :20: RR are maximally extended and protrude about 20 to 30 f1.m from the coarsely undulating bulge peripherv.
4
14 :25: Retraction of RR starts and translucent bulge begins to form smooth peripherv, Anlage is believed to develop when rough, irregular periphery is transformed into smooth rim.
5
14 :29: Periphery is smooth and RR are completely retracted indicating that anlage has been completed.
6
15 :16 : Further retraction of RR toward opaque cytoplasm creates light band that is concentric to the peripherv.
7
16 :25 : First calcareous plaques appear.
8
16:43: There is an increase in size and number of calcareous plaques.
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for each event may differ somewhat from individual to individual. but the relative time spans are believed to be representative for the 2 species. Fine-structural developments inferred from transmission electron micrographs are listed in a time-sequence corresponding to the light-microscopic observations. 1.
ST (start time)-Retraction of the thin, long rhizopodia in the apertural region is followed by the emergence of a cytoplasmic
transformed into a smooth border. The anlage consists of the CE and the POM. Concurrently with or prior to the formation of the anlage, an OPE is formed to shield the delicate anlage. The RR exhibits cytoplasmic streaming. 7.
2 to 3 hrs. after ST-Start of calcification is evident in appearance of smalI, opaque calcareous plaques over the surface of the translucent bulge. Calcite is deposited on both sides of the POM. The CE is discarded soon after calcification.
8.
4 hrs after ST-Increase in number and lateral growth platelike calcareous plaques.
9.
5 to 6 hrs. after ST-The jig-saw puzzle-shaped units coalesce to to form 2 continuous calcite layers between which the POM is located. Thus. a newly calcified chamber has a bilamellar wall. Further wall thickening occurs by secretion of successive calcite layers mainly on the distal side of the shell.
mass.
2.
30 min. after ST-Impending formation of new chamber becomes evident with rapid growth of the cytoplasmic bulge, from which short. thick rhizopodia (RR) radiate outward in a fanlike network.
3.
45 min. after ST-Gradual expansion and flowing of the translucent bulge among the R R. The opaque inner part of the bulqe. if present. expands only sliqhtlv,
4.
1 hr after ST-Maximum expansion of cvtoplasrnic bulge with the distal tips of the R R extending from 20 to 30 p.m beyond the peripheral outline of the chamber-to-be. The duration required to complete the outline of the new chamber is relatively short. i.e. about an hour after the first detection of an expanding cytoplasmic bulge.
5.
1 hr 30 min. after ST-Retraction opment of anlage.
of RR signals start of devel-
6.
1 hr 40 min. after ST-Completion the rough, undulating periphery
of anlage is inferred when of the translucent bulge is
of the
ACKNOWLEDGMENTS
We gratefully acknowledge the assistance of Dr. Ch. Sautter and Saijai Tuntivate-Choy in the laboratory. This study was supported by National Science Foundation Grants OCE 78-25450 and OCE 76-0220 and from the Sonderforschungsbereich 53, "Palökolcqie" (D30) of the Deutsche Forschungsgemeinschaft. This paper is Lamont-Doherty Geological Observatory Contribution no. 2820 and Sonderforschungsbereich 53 Konstruktionsmorphologie no. 110.
PLATE 5 Transmission electron micrographs of early stages of chamber formation in Globorotalia truncatulinoides (d'Orbigny) and Globorotalia hirsuta (d'Orbigny). 1
Globorotalia truncatulinoides (insert) has just smoothened the periphery of its translucent cytoplasmic bulge, and it is inferred that the formation of the anlage complex is completed. The electron micrograph taken at the bulge periphery shows anlage complex, which consists of amorphous OPE, a highly convoluted, densely stained, segmented CE, and a thin. continuous POM. OPE is distal rim of translucent bulge. Specimen fixed forTEM about 90 min. after start of chamber forrnation. x 16,820.
2
Detail of a segment of CE of G. truncatulinoides, showing it is a flattened cytoplasmic ferentiation and lateral extension of the rhizopodia, x 17,000.
3
SmalI, calcareous plaque (arrow) is secreted on both sides of POM of Globorotalia hirsuta. Note that more calcareous matter is formed on distal side than _onproximal side of POM. CE is almost directly up against distal side of POM. Between opaque cytoplasm (below) and POM is translucent region of cytoplasmic bulge. Specimen fixed for TEM about 3 hrs. 20 min. after start of chamber formation, x 2,500.
4
Evidence that POM is nucleation site for calcification lies in the fact that calcite is secreted on both sides of POM and that POM continues uninterruptedly on either side of plaque in close association with CE. Note that calcareous plaque is surrounded by organic layer. Same specimen as figure 3, x 6180.
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REFERENCES ANGELL, R. W., 1967. The process of chamber formation in the foraminifer Rosa/ina f/oridana (Cushman). Jour. Protozool.. 14: 566-574. BE, A. w. H., HEMLEBEN, CH., ANDERSON, O. R., SPINDLER, M., HACUNDA. J., and TUNTIVATE-CHOY, S., 1977. Laboratory and field observations of living planktonic foraminifera. Micropaleontology, 23 (2): 155-179. BE, A. W. H., and LOTT, L., 1964. Shell growth and structure planktonic foraminifera. Science, 145 (3634) : 823-824.
of
BERTHOLD, w.-U .. 1976. Test morphology and morphogenesis in Patellina corrugata Williamson, Foraminiferida. Jour. Foram. Res., 6: 167-185. HEMLEBEN, cu.. BE, A. W. H., ANDERSON, O. R., and TUNTIVATE-CHOY, S., 1977. Test morphology, organic layers and chamber formation of the planktonic foraminifer Globorotalia menardii (d'Orbigny). Jour. Foram. Res., 7 (1): 1-25. HOFKER, J., 1930. Notizen über die Foraminiferen von Neapel. Publ. Staz. Napoli, 10: 365-405. JEPPS, M. W., 1942. Studies on Po/ystomel/a Mar. Biol. Ass. U. K., 25: 607-666.
des Golfes
Lamarck.
Jour.
LE CALVEZ, J., 1938. Recherches sur les forarninlferes. I. Developpement et reproduction. Arch. Zool. Exp. Gen.. 80 (3) : 163-333. LISTER, J. J., 1903. The foraminifera. In: Lenkester. A Treatise on Zoology., Part 1, 2: 47-149. London.
E. R., Ed.,
MYERS, E. H., 1935. The life history of Patellina corrugata Williamson, a foraminifer. Bull. Scripps Inst. Oceanogr., Univ. Calif.. Tech. Ser., 3 (16) : 355-375. --,
--,
1940. Observations on the origin and fate of flagellated gametes in multiple tests of Discorbis (Foraminifera). Jour. Mar. Biol. Ass. U. K., 24: 201-236. 1943. Biology, ecology and morphogenesis foraminifer. Stanford Stud.. Biol. Sci., 9 : 5-30.
in p/anktonic
foraminifera
PESSAGNO, E. A., Jr.. and MIYANO, K., 1968. Notes on the wall structure of the Globigerinacea. Micropaleontology, 14 (1): 38-50. REISS, Z.,.1957. The Bilamellidea, nov. superfam., on Cretaceous globorotaliids. Cushman Found. Contr.i B (4): 127-145. SCHAUDINN. and Leipzig:
F., 1911. Fritz Schaudinn's Leopold Voss.
and remarks Foram. Res.,
Arbeiten.
SCH U LTZE, M. S., 1854. Über den Organismus mien. 68 pp, Leipzig: Verlag Wilhelm Engelmann.
Hamburg
der Polythala-
SLiTER, W. V., 1970. Bo/ivina doniezi Cushman and Wieken den in clone culture. Cushman Found. Foram. Res., Contr., 21 (3): 87-99. SPINDLER, M., MS. Gehäuseanatomie und Ablauf des Kammerbauvorgangs bei Heterostegina depressa (Nummulitidae: Foraminifera). Untersuchungen im Licht und Elektronenmikroskop. Unpubl. Ph. D. Thesis, 1976, Univ. Kiel, Germany, 181 pp. --,
1978. The development of the organic lining in Heterostegina depressa (Nummulitidae: Foraminifera). Jour. Foram. Res., 8 (3) : 258-261.
SPINDLER, M., and RÖTTGER, R., 1973. Der Kammerbauvorgang der Grossforaminifere Heterostegina depressa (Nummulitidae). Mar. Biol., 18: 146-159. TAKAYANAGI, Y., NIITSUMA, N., and SAKAI, 1.. 1968. Wall microstructures of G/oborotalia truncatu/inoides (d'Orbiqnv). Sei. Rep. Tohoku Univ., 2 (geol.) (40): 141-170. TOWE, K. M., 1971. Lamellar wall construction in planktonic foraminifera. Proc. Sec. Plankt. Conf. Roma: 1213-1224. TOWE, K. M., and CIFELLI, R., 1967. Wall ultrastructure in the calcareous foraminifera: erystallographic aspects and a model for calcifieation. Jour. Pal.. 41 (3): 742-762. WINTER, F. W., 1907. Zur Kenntnis Protistenk., 10: 1-113.
der Thalamophoren.
Areh.
of a pelagic
Manuscript received July 27, 1978.
PlATE 6 Three successive stages of wall formation and thickening Calcareous plaque enlarged laterally and bisected by POM. Distal (upper) part of plaque is thicker than proximal (Iower) part. Same specimen of Globorotalia hirsuta (d'Orbiqnv) as in plate 5, figure 3, x 9000. 2
Two continuous calcite layers form new bi lamellar wall that is only about 2 to 3 tut. thick. Junctions between calcareous plaques are indicated by vertically oriented organic layers (small arrows). A pore penetrates thin wall. Note that pore plate (Iarge arrow) is continuous with POM. Specimen of Globorotalia truncatulinoides (d'Orbiqnv) fixed for TEM about 6 hours after start of chamber forrnation. x 5040.
3
Wall of this specimen of G. truncatulinoides has grown thicker by lamellar accretion. Top calcite layer is deposited on bilamellar wall. which is bisected by POM. Note continuity of POM and pore plate (PP). IOl forms dense layer against inner wall. x 8685.
306
l
A. W. H. Be, C. Heraleben. O. R. Anderson & M. Spind/er
micropeteontoloqv,
vo/ume 25, number 3
PLATE
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