multicellular-like compartmentalization of cytoplast in fossil larger era

Multicellular-like compartmentalization of cytoplast in fossillarger foraminifera

CARLES FERRANDEZ-CANÄ ADELL

Ferrandez-CanÄ adell, C. 2002 06 14: Multicellular-like compartmentalization of cytoplastin fossil larger foraminifera. Lethaia, Vol. 35, pp. 121–130. Oslo. ISSN 0024-1164.

Foraminifera are usually between 0.1 and 1 mm in size, thus falling within the range ofthe largest eukaryotic cells. However, some fossil and extant foraminiferal species reachdiameters of more than 100 mm. One hypothesis of how these gigantic sizes could havebeen attained by these unicellular organisms is the temporary compartmentalization ofcytoplasm into smaller volumes of effective metabolism, as reported for several recentspecies. Evidence of this phenomenon is shown in fossil genera of larger foraminiferabelonging to � ve families of Cretaceous to Oligocene age. Alternative interpretationsare discussed. & Cell size, Eocene, Foraminifera, lepidocyclinids, Oligocene, orbitoids,organic lining, orthophragminids, Upper Cretaceous.

C. Ferrandez-CanÄ adell [[email protected]], Departament d’Estratigra� a i Paleontologia,Facultat de Geologia, Universitat de Barcelona, Martõ´ Franques s/n, E-08028-Barcelona,Spain; 16th July 2001, revised 5th March 2002.

Foraminifera are unicellular marine organisms with anorganic, agglutinated (‘arenaceus’) or biomineralizedtest. They are usually between 0.1 and 1 mm in size(Lee & Hallock 1987), which falls within the range ofthe largest eukaryotic cells. Foraminifera include theso-called ‘larger foraminifera’, de� ned from theirstructural complexity rather than from their size.These comprise gigantic forms that usually attaincentimeter size and, on occasion, can exceed diametersof 10 cm.

More than 40 lineages – families in the currentsystematics (Loeblich & Tappan 1987) – of largerforaminifera have developed recurrently from severalforaminiferal stocks through the Phanerozoic, includ-ing groups of agglutinated, microgranular, porcella-neous and lamellar test (Hottinger 1982; Lee &Hallock 1987; Tappan & Loeblich 1988). This recur-rent origin of larger foraminiferal stocks is currentlyinterpreted as the result of a symbiotic relationshipwith unicellular algae (Lee et al. 1979; Hallock 1985;Lee & Hallock 1987; Tappan & Loeblich 1988; Lee &Anderson 1991), i.e. rhodophytes, dinophytes orchlorophytes, of about 4–10 mm in diameter (Lee etal. 1980; Leutenegger 1984). In other cases, such asElphidium and Nonion, the foraminifera feed on algaebut retain and use their chloroplasts (Lopez 1979; Lee& Anderson 1991).

Exceptionally large foraminifera are also found indeep-sea (Brasier 1984) and high-latitude (De Laca etal. 1980; Bowser et al. 1995) forms without algal

symbionts. In these cases, increased size is probablyrelated to ‘polar gigantism’, which is caused by lowtemperatures and metabolism, and by low oxygenavailability, thereby producing a reduction in growthrate but a larger � nal adult size (e.g. French et al. 1998;Chapelle & Peck 1999).

Among fossil larger foraminifera there are someexamples of extremely large tests: Permian micro-granular fusulinids with fusiform tests that reach100 mm in length and 10 mm in diameter (Dunbar1963); Upper Cretaceous agglutinated Loftusia, withfusiform tests of 80 mm in length (Loeblich & Tappan1964); Tertiary nummulitids and lepidocyclinids withdiscoidal tests of 120–160 mm in diameter (Douville1906; Blondeau 1972; Buxton 1988; Ungaro 1994) andporcellaneous alveolinids with fusiform tests of up to85 mm (Hottinger 1960). The largest reported for-aminiferal test is an Eocene Nummulites of at least19 cm in diameter (Pavlovec 1987). Recent largerforaminifera, with tests of 5–30 mm in diameter,include species from several groups (nummulitids,soritids, alveolinids, amphisteginids, calcarinids), allwith algal symbionts. Recent nummulitids include oneof the largest known foraminifera, Cycloclypeus car-penteri, whose discoidal tests can reach 13 cm (Koba1982; Hohenegger 1999), about 10 times the size of thesmallest vertebrates, the dwarf gobie Pandaka pyg-maea, about 1 cm in length, or the even smallerTrimmatom nanus.

Large size in foraminifera is facilitated by the

# 2002 Taylor & Francis

mineral test, which renders an economic control of cellshape, a certain degree of division of cytoplasmfunctions and stabilization of the positions of thenucleus, organelles and symbionts (Vogel & Gutmann1988; Anderson & Lee 1991). In foraminifera, the testgrows by the addition of new chambers, which areusually subdivided in larger foraminifera into furthercompartments called chamberlets. There are tens ofthousands of compartments in the largest forms, theirvolume falling within the usual range of sizes ofeukaryotic cells (from 10 to 200 mm). Nevertheless, thecompartments in a larger foraminifer test are con-nected by passages, foramina or stolons, so that thecytoplasm circulates throughout the whole test; stabledifferentiation is dif� cult and intergradations arecommon (Anderson & Lee 1991).

In 1938, Le Calvez reported the periodic, temporalcompartmentalization of the test of recent Planorbu-linella mediterranensis through round organic plugs inthe connections between chamberlets. Similar obtura-tions were described 39 years later (Leutenegger 1977)in Heterostegina depressa, Heterocyclina tuberculata,Amphistegina lobifera and were also observed inElphidium (Leutenegger 1993: pers. comm.). Hottin-ger (1984, 1986, 2000) interpreted this compartmen-talization as a way to reach the optimal volume forbiochemical reactions.

This study presents evidence of similar compart-mentalization in fossil larger foraminifera. Thisfeature, observed in eight genera from Upper Cretac-eous to Oligocene in age, differs from that observed inrecent species in that it is produced from a disc-likeextension of the organic lining in the connectionsbetween chamberlets.

Material and methods

The organic lining, a muccopolysaccharide sheathwhich lines the inner surface of the mineral test inforaminifera, is considered the vestige of the ancestralorganic test, before the appearance of mineral skeleton(Le Calvez 1947). It is not generally preserved infossils; however, the material studied here wasobtained from sites characterized by an exceptionalstate of fossil preservation (Table 1):

. Ency Quarry, Maastricht (The Netherlands), fromthe collection of the Geologisch-PalaontologischesInstitut of the University of Basel (Switzerland),provided by L. Hottinger. This sample yieldedUpper Cretaceous (Maastrichtian) Orbitoididae(Orbitoides) and Lepidorbitoididae (Lepidorbi-toides).

. Tuilerie of Gan and Bosdarros (southern France),two sites of Lower Eocene (early Cuisian) age. Amore detailed description can be found in Ferran-dez-CanÄ adell (1997). These sites yielded specimensof orthophragminids: Discocyclinidae (Discocyclinaand Nemkovella) and Orbitoclypeidae (Asterocy-clina and Orbitoclypeus).

. La Jerra beach (San Vicente de la Barquera, north-ern Spain). A Lower Oligocene (Chatian) site (Heck& Drooger 1984; Ferrandez et al. 1999) that yieldedwell-preserved specimens of lepidocyclinids(Nephrolepidina and Eulepidina).

In specimens of nine species of these genera (Table1), some remains of the organic lining were found tobe preserved locally. Specimens were studied using aHitachi 2300 scanning electron microscope located at

Table 1. Species of orbitoidiform larger foraminifera in which compartmentalization of the test by the organic lining was observed.

122 Carles Ferrandez-CanÄ adell LETHAIA 35 (2002)

the Serveis Cienti� co-Tecnics of the University ofBarcelona.

Results

The organic lining was studied in eight genera of fossillarger foraminifera belonging to � ve families fromUpper Cretaceous to Lower Oligocene age (Table 1).Although phylogenetically unrelated, all these generawere bilamellar-perforate foraminifera that shared aparticular structural model of the test, called orbitoidi-form, which is found only in fossil genera. Theorbitoidiform test (Fig. 1) consists of a central layer(equatorial plane) of chamberlets arranged in con-centric rings (annuli), with lateral chamberlets at bothsides. These chamberlets are interconnected by cylind-rical passages (stolons), which were apertures inprevious growth stages. In most genera, the equatorialchamberlets are rounded or arcuate, thereby makingthe test periphery lobate (Fig. 1). In Eocene ‘ortho-phragminids’, a term which has no taxonomic valueand that includes two phylogenetically unrelated

families, Discocyclinidae and Orbitoclypeidae, therings are � at, with a circular outline, and aresubdivided into rectangular chamberlets (Fig. 1).

The general features of the organic lining in theseeight genera, described in a previous paper (Ferran-dez-CanÄ adell 2001), are similar to those reported inother bilamellar foraminifera (e.g. Banner & Williams1973; Banner et al. 1973; Leutenegger 1977; Spindler1978). The lining has a laminate structure and coversall of the inner surface of the test, being continuousfrom one chamberlet to the next through the stolons,and sealing the inner mouth of pores. It is thicker inolder chambers and becomes progressively thinnertowards the periphery. The observation of a progres-sive increase in thickness towards older chambers,together with its laminate structure, and the observa-tion that it traps some strange bodies, such ascoccoliths, support the postulate that the organiclining is formed by periodic accretion (in each growthstep, when a new chamber is added to the test), andincludes waste material (Banner et al. 1973; Angell1980; Be et al. 1980; Oelschlager 1988; Bender 1992).In addition, the presence of coccoliths between thelayers of the organic lining provides information on

Fig. 1. Diagrammatic structure of the orbitoidiform foraminiferal test, showing a middle layer of equatorial chamberlets arranged inconcentric annuli and lateral chamberlets at both sides. The equatorial chamberlets can be arcuate, as in Orbitoididae, Lepidorbitoididae andLepidocyclinidae (A), or rectangular, as in Discocyclinidae and Orbitoclypeidae (B). Chamberlets are connected by stolons, cylindricalpassages of about 5 mm, which are radially aligned in orthophragminids and form crosswise circuits in opposite directions in genera withorbitoidal, arcuate chamberlets. Apertures are located in the peripheral margin and on the lateral surfaces of the test.

LETHAIA 35 (2002) Cytoplast in fossil larger foraminifera 123

the food source of these groups of foraminifera, whichdo not have extant equivalents (Ferrandez-CanÄ adell2001).

This study also revealed a particular arrangement ofthe organic lining, namely the closing of stolons. Theorganic lining extends toward the centre of the stolon,forming a rounded diaphragm perpendicular to thestolon axis and completely closing it (Figs 2–5). Thesestolon plugs were observed only in the proximal partof the test and mainly in equatorial chamberlets. Thisis probably due to differential preservation, becausethe organic lining is thicker in central chambers and isoften the only site where it is preserved. On the otherhand, the sections studied were mainly equatorial andthis could account for the relatively few observationsof the organic lining in lateral chamberlets. Stolonplugs of organic lining were observed in the generaOrbitoides (Fig. 2A–C), Lepidorbitoides (Fig. 2D),Discocyclina (Fig. 3A, C), Nemkovella (Fig. 3B, D–F),Orbitoclypeus (Fig. 3H, I), Asterocyclina, Eulepidina(Fig. 4A) and Nephrolepidina (Fig. 4B–D). This featureis therefore present in the � ve families studied.

Because the organic lining was only partiallypreserved, and the specimens were studied in section,it was not possible to observe the complete arrange-ment of stolon plugs throughout one specimen. Insome cases the organic lining was observed to plug allthe stolons in one chamberlet, thereby completelysealing it (Figs 4C, 5).

The thickness of the organic lining that plugs thestolons is usually similar to that of the organic lining inadjacent chamberlet walls. Thus, the plugs are thickerin older chambers. In Orbitoides, however, some plugsin equatorial chamberlets close to the embryo werenotably thickened to up to 14 mm (Fig. 2B, C).

Discussion

The observations in these fossil genera show compart-mentalization of the test by plugging the connectionsbetween chamberlets, thus avoiding cytoplasmic � ux

Fig. 2. Organic lining that closes off the connections between chamberlets (stolons) in Upper Cretaceous (Maastrichtian) Orbitoididae andLepidorbitoididae. &A. Equatorial section of Orbitoides gruenbachensis showing several stolons closed off by the organic lining (arrows). &B,C. Thickened plugs of organic lining in central chambers of O. gruenbachensis. &D. Closed stolons in Lepidorbitoides minor.


through the test and completely sealing some cham-berlets (Figs 4C, 5).

To date, compartmentalization by organic sheathshas not yet been reported in recent foraminifera,

although similar plugging of apertures and foraminahas been observed in recent Nummulites venosus(Bartholdy 2001: pers. comm.) and in bleaching-stressed Amphistegina (Hallock 2001, pers. comm.).

Fig. 3. Organic lining that closes off the connections between chamberlets (stolons) in Lower Eocene (lower Cuisian) orthophragminids,Discocyclinidae and Orbitoclypeidae. &A, C. Closed radial (A) and annular (C) stolons in Discocyclina dispansa. &B, D, E, F. Closed radialstolons in Nemkovella rota. &G, H, I. Closed radial stolons in Orbitoclypeus douvillei.


The only similar phenomenon which can be found inthe literature was reported by Wheeler (1982) infragmentary ‘foraminiferal linings’ from palynologicalpreparations, which are currently interpreted as theorganic lining of microforaminifera. Wheeler

described disc-shaped plugs, which he named ‘obtur-acula’ in the apertures and foramina of trochoid andbiserial Late Cretaceous foraminiferal linings fromIran. According to this author, the obturacula weremade of the same material as the foraminiferal lining.

Fig. 4. The organic lining in Lower Oligocene (lower Chatian) Lepidocyclinidae. &A. Equatorial section showing several plugged stolons(circles) in Eulepidina formosoides. &B. The organic lining partially preserved in an equatorial chamberlet, covering the lateral wall (andsealing the pore mouths), and the surface of stolon in Nephrolepidina praemarginata. &C. Equatorial section showing an equatorialchamberlet with all the connections closed off in N. praemarginata. &D. Stolon plugs of organic lining in a tilted equatorial section of N.praemarginata .

Fig. 5. Schematic drawing of thearrangement, in equatorial section,of the organic lining in equatorialchamberlets and closing stolons inorbitoidiform foraminifers. Outerlamella and inner lamella are themineral laminae from which thetest is constructed. The plugs oforganic lining are drawn only inthe chamberlets on the right.


Similar obturacula in uniserial microforaminiferallinings from Oxfordian sediments in Britain werereported by Stancliffe (1989). Because of their smallsize, usually less than 150 mm, these examples are notreadily comparable to orbitoidiform larger foramini-fera.

The temporal compartmentalization of the test byorganic plugs (‘bouchons’ of Le Calvez (1938),‘residual bodies’ of Leutenegger (1977); Fig. 6) at thestolons has been observed in a few recent foraminifera,and has been interpreted as a way in which to dividethe large bulk of cytoplasm into optimal volumes forbiochemical reactions (Hottinger 1984, 1986, 2000).Our observations of compartmentalization in the testsof orbitoidiform genera agrees with such an hypoth-esis. By plugging the stolons, the organic liningproduces several small compartments, which aresimilar in size to those of cells (about 50 £ 50 mm).The shape of the chamberlets is highly variable withinthese groups, but the usual size remains within thisrange. Chamberlets are rounded in orbitoidids,lepidorbitoidids and lepidocyclinids, and rectangularin discocyclinids and orbitoclypeids. Some species ofDiscocyclina have very narrow and elongated cham-berlets of 20 £ 180 mm. This change in shape does not,however, modify the volume of the compartment.

Of the extremely diverse morphologies and sizesthat have evolved in the organic world, cell size is theonly feature that has remained constant, and hasremarkably strict upper and lower limits (McMahon &Bonner 1983). Cell size is restricted to 0.02–400 mm inprokaryotes (Koch 1996), whereas cells in mosteukaryotic uni- or multicellular organisms are10–100 mm in diameter, with some ‘giant’ unicellularorganisms reaching 1 mm. Most alleged exceptions tothis general rule are actually not so: the largestprokaryotic cells reach sizes of up to 750 mm, butbecause of the presence of large vacuoles (e.g. Schulz etal. 1999). Within eukaryotes, a nerve cell (neuron)may have an extraordinarily long extension called anaxon. However, the cell body of the neuron, whichcontains the nucleus, falls into the normal size rangefor cells.

The constant size of cells is currently interpreted ascorresponding to the optimal volume to develop

metabolic biochemical reactions. In this view, cellsare a unit of effective metabolism, or catalytic unit,limited by physical factors, especially diffusion andtransportation distances (Sernetz et al. 1985; Bonner1988; Koch 1996; see also Thompson (1917) for areview of the � rst observations and interpretations oncell size). Prokaryotic and eukaryotic cells differ in sizemainly because of the presence of endoplasmicreticulum in the latter, which allows an economiccontrol of cell-shape and better transportation ofnutrients and waste products. Because of theserestricting factors, large sizes in organisms are attainedby multicellularity, that is, by the addition of metab-olic units, with a subsequent division of labour amongthe parts. The larger the organism, the higher thenumber of catalytic units (cells) (Sernetz et al. 1985;Bonner 1988), although an increase in cell size mightpartly account for increased body size (e.g. Stevensonet al. 1995; French et al. 1998). The main exception tothis rule is larger foraminifers, which, despite beingunicellular, can reach gigant sizes.

Although the cytoplasm does not � ll the testcompletely, the volume of the larger foraminifer cellis gigantic by protist standards. Severin & Lipps (1989)calculated the weight–volume relationship of the testin the recent alveolinid Alveolinella quoyi, which is upto 2 cm in length. Their results showed that the locularcavities of the test account for the 43% (23–54.4) ofthe test volume, and that only 39% of this is occupiedby the protoplasm. If these results were applied to aNummulites � at discoidal test of 140 cm in diameterand a maximum thickness of 7 mm, this giant mighthave surpassed 12 cm3 in cytoplasmic volume and 12 gin weight (that is, about threefold the mass of thesmallest mammal, the pigmy shrew Suncus etruscus).

In recent amphisteginids, nummulitids and elphii-dids, the cytoplasm is temporarily compartmentalizedinto small, cell-sized volumes, probably to attainoperative dimensions for metabolic reactions. Thecompartmentalization observed in fossil orbitoids,lepidorbitoids, discocyclinids, orbitoclypeids and lepi-docyclinids might be related to the same function.Because the organic lining is only permeable to gases,compartmentalization in order to facilitate metab-olical reactions can only be temporary, and its startand end has to be somehow regulated by the vegetativenuclei. Further research on compartmentalization inrecent species is called for to test this functionalhypothesis and understand the metabolic processesand their regulation.

Alternative interpretations

A number of alternative hypotheses can be proposedto account for compartmentalization in orbitoidiform

Fig. 6. Temporal compartmentalization of the test of recentPlanorbulinella mediterranensis by rounded plugs of organicmaterial that are temporarily placed at the stolons (redrawn fromLe Calvez 1938, � g. 6).


larger foraminifers: (a) protection, (b) differentiationbetween endo- and ectoplasm, and (c) buoyancycontrol.

Protection

When disturbed or when subjected to unfavourableenvironmental conditions, foraminifera retract theircytoplasm to the inner part of the test. In some recentspecies it has been observed that the organic lining isused to close off the aperture in unfavourableenvironments (e.g. Calcituba polymorpha Arnold1967). However, such a protective function for stolonplugging in the specimens studied here seems improb-able, because plugs were found in the internal part ofthe test, including the innermost chambers (theembryo).

Differentiation between endo- and ectoplasm

In larger foraminifers, and also in planktic foramini-fers, there is a partial separation between the endo-plasm (which contains the organelles and thesymbionts) and the ectoplasm (or pseudopodialcytoplasm). In the recent simple orbitoidiform (i.e.without lateral chamberlets) species Planorbulinellamediterranensis , there is some degree of separation: theendoplasm occupies the central part of the test and theectoplasm the periphery (Le Calvez 1938). Such aseparation can be improved by test structures, such ascanal systems of nummulitids or rotalids, but also byorganic sheats, as has been reported in the plankticforaminifer Globigerinoides sacculifer (Anderson & Be1976). Nevertheless, in the species studied here theplugging of stolons was observed in the innermostparts of the test; it does not divide the test into twozones, but forms many isolated compartments.

Buoyancy

Wheeler (1982) suggested that the obturacula heobserved in microforaminiferal linings could berelated to buoyancy during sexual reproduction.Following this hypothesis, the � otation compartmentallows gamonts to rise to the water surface, facilitatinggamete exchange. Such a reproductive strategy isfound in some benthic species of Rosalina, Neoconor-bina and Cymbaloporetta , which have independentlydeveloped a � nal ‘tretomphaloid’, imperforate, gas-� lled � oat chamber to release the gametes at the seasurface (Banner et al. 1985). However, the organiclining is permeable to gases (e.g. Leutenegger &Hansen 1979) and therefore a ‘� otation compartment’constructed by organic lining is not feasible.

Stolon plugs and orbitoidiform test structure

Some recent hyaline larger foraminiferal species havebeen cultured and their structure and cytology hasbeen studied, especially nummulitids (Heterostegina,Operculina) and amphisteginids (Amphistegina), butalso other groups, such as calcarinids (Calcarina,Baculogypsina). Compartmentalization by the organiclining has not been reported in any of these species,nor has it been reported in other recent foraminiferalgroups such as porcellaneous alveolinids (Alveoli-nella), soritids (Sorites, Marginopora), or agglutinatedforaminifera (e.g. Textularia). However, compartmen-talization by the organic lining occurred in all theorbitoidiform species studied here, which belong toeight genera of � ve, phylogenetically unrelatedfamilies. Upper Cretaceous orbitoids and lepidorbi-toids differ in their microspheric initial growth, whichis biserial in the former and spiral in the latter (e.g.Gorsel 1978). Also Paleocene–Eocene orthophragmi-nids, Discocyclinidae and Orbitoclypeidae have adifferent microspheric nepionic growth (Bronnimann1946; Ferrandez-CanÄ adell 1998). The microsphericjuvenarium of Tertiary Lepidocyclinids is similar tothat of Upper Cretaceous Lepidorbitoids, but the twogroups are separated by about 20 million years and areclearly phylogenetically unrelated.

Despite their distinct origin, these � ve families sharea common orbitoidiform test structure, and similargeneral features of the organic lining (Ferrandez-CanÄ adell 2001), and all show compartmentalization ofthe test by the organic lining. Compartmentalizationby the organic lining thus seems to be related to someparticularity of the orbitoidiform test. The distinctways in which compartmentalization occurs in num-mulitids, amphisteginids, calcarinids and elphiididscould be explained by differences in test structure, orby differences in the characteristics of their organiclining. However, it is dif� cult to � nd similaritiesbetween these groups, which mostly include spiralforms, but also some annular genera (Heterocyclina),and forms with different types of canal systems(nummulitids, calcarinids, Elphidium) and formswithout (amphisteginids). The organic lining alsoshows differences among these groups. For example,it is very thin in Elphidium (Sheehan & Banner 1972)and ‘extremely thick’ in calcarinids (Hottinger &Leutenegger 1980).

The absence of orbitoidiform equivalents in extantspecies hinders the interpretation of their palaeobiol-ogy. The most alike extant forms, such as Planorbu-linella, with a maximum size of 2.5 mm (Freudenthal1969), have a simpler test structure, with only onelayer of chamberlets arranged in concentric annuli,and do not have lateral chamberlets. Planorbulinella


also shows compartmentalization of the cytoplasm,but produced, as in nummulitids, amphisteginids,calcarinids and elphiidids, by rounded plugs oforganic material that are temporarily placed at thestolons (Le Calvez 1938, Fig. 6).

Although compartmentalization by the organiclining has not been reported in recent foraminifera,it cannot be completely excluded. The two kinds ofcompartmentalization (rounded plugs and organiclining) may occur in all groups, both fossil and extantlarge foraminifers, possibly related to different func-tions, the rounded plugs being used for short obtura-tion of stolons, and the organic lining for longercompartmentalization.

Conclusions

The study of fossil foraminiferal genera of � vedifferent families sharing a similar orbitoidiform teststructure shows that the organic lining may cover theconnections between chamberlets, thereby dividingthe test into several sealed compartments. Temporarycompartmentalization by placing organic plugs in theforamina mouths has been reported in recent largerforaminifera, and interpreted from a metabolical pointof view as a way to reach optimal volumes forbiochemical reactions. Unicellular larger foraminiferaare atypical cells which have reached gigantic cell sizes.Compartmentalization could produce small indepen-dent cell-sized volumes that facilitate metabolic reac-tions which would otherwise be hindered in the giantcytoplasm of larger foraminifera. The compartmenta-lization by the inner organic lining in the orbitoidi-form foraminifers could have the same function.

Acknowledgements. – This study was supported by the DGICYTproject PB 98-1263 and an F.P.U. grant from the Ministerio deEducacion y Cultura of the Spanish Goverment, and was partlycarried out in the Geologisch-Palaontologisches Institut of theUniversity of Basel (Switzerland). I thank L. Hottinger for pro-viding material from Maastrich and Bosdarros and for useful dis-cussions, and S. Leutenegger for providing unpublished informa-tion on stolon plugging in Elphidium. I also thank P. Hallockand J. Hohenegger for their critical review and useful commentson the manuscript.

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multicellular-like compartmentalization of cytoplast in fossil larger era

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