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Multicellular-like compartmentalization of cytoplast in fossillarger foraminifera
CARLES FERRA`NDEZ-CAN
  Ä
ADELL
Ferra`ndez-Can
  Ä
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 of the 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 of cytoplasm 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. Ferra`ndez-Can
 Ä
adell [cferran@geo.ub.es], Departament d’Estratigraa i Paleontologia,Facultat de Geologia, Universitat de Barcelona, Mart 
õ
´Franque`s 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 of the 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 currently interpreted 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
m
m in diameter (Lee
et al.
1980; Leutenegger 1984). In other cases, such as
Elphidium
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
et al.
1980; Bowser
et al.
1995) forms without algalsymbionts. In these cases, increased size is probably related 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 (Douville´1906; 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 smaller
Trimmatom nanus.
Large size in foraminifera is facilitated by the
#
2002 Taylor & Francis
 
mineral test, which renders an economic controlofcellshape, 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 of thousands of compartments in the largest forms, theirvolume falling within the usual range of sizes of eukaryotic cells (from 10 to 200
m
m). 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 in
Elphidium
(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-Pala¨ontologischesInstitut 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 Ferra`n-dez-Can
  Ä
adell (1997). These sites yielded specimensof orthophragminids: Discocyclinidae (
Discocyclina
and
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; Ferra`ndez
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 Ferra`ndez-Can
 Ä
adell 
LETHAIA 35 (2002)
 
the Serveis Cientico-Te`cnics of the University of Barcelona.
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 ofthe 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 unrelatedfamilies, 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 (Ferra`n-dez-Can
  Ä
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; Oelschla¨ger 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
m
m, 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
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