The “face” of benthic foraminiferapaleoitalia.org/media/u/archives/075_090_Hottinger.pdf · 2012. 4. 29. · (Hottinger 2005, fig. 5A). Possibly, the interiomarginal, extraumbilical-peripheral

75Bollettino della Società Paleontologica Italiana, 45 (1), 2006, 75-89. Modena, 30 settembre 2006

ISSN 0375-7633

INTRODUCTION

In the search for a biological understanding ofbenthic foraminiferal shell morphology, themorphological features observed on the “apertural face”(current term designating the surface of the frontal wallof the last chamber bearing a single or multiple primaryapertures of the shell) are of particular importance,because this part of the shell reflects the primarycommunication between the protoplast and its ambientenvironment through the apertures. But not only thenumber and the distribution pattern of the apertures onthe apertural face is significant for the functionalmeaning of the morphology but also its ornamentation.The latter, if specific, different from the rest of theshell surface, may extend over parts of earlier chambersexposed to the ambient environment and are forming afunctional unit. This is particularly obvious in smallerbenthic trochospiral rotaliids with a ventral (umbilical)differentiation of the shell turned towards the substrate,often underlined by the lack or scarcity of pores, and aregularly perforate spiral side. Therefore, the current

term “apertural face” is complemented in this note bya more general term “face” including all differentiatedparts of the shell’s surface delimited by modificationsof shell shape, wall texture and/or particularornamentation, where single or multiple apertures ororifices of a canal system are grouped to form afunctional unit (Pl. 1).

In permanently attached forms, the surface ofattachment does not include the main apertures of theshell cavities. It is therefore not a “face”: trochospiralbenthics use their spiral (dorsal; see also Tyszka, 2005)side for attachment in order to keep their aperturesfrom being obstructed by the firm substrate. Often,however, we observe small supplementary openings insutural position apparently responsible for the releaseof substances cementing the shell to its firm substrate(Hottinger 2005, fig. 5A). Possibly, the interiomarginal,extraumbilical-peripheral position of the main aperturein cibicidids (Figs. 1f-g) or Korobkovella predisposesthese groups to realize sessile genera.

“Faceless” shells may be observed in isotropicenvironments, either floating in the open water column,

The “face” of benthic foraminifera

Lukas HOTTINGER

L. Hottinger, Museum of Natural History, CH-4001 Basel, Switzerland; [email protected]

KEY WORDS - Functional morphology, Ornamentation, Microtubuli, Motility, Plastogamy, Teeth, Trematophore, Mask.

ABSTRACT - Surfaces on the foraminiferal shell delimited by usually angular modifications of shell shape, characterized by adifferentiation of wall texture and/or ornamentation and including the apertures and/or orifices of an interlocular space are conceivedas functional units and called “face”. The links between number and distribution of apertures on faces of non-lamellar shells andchamber cavity volume or the number of chamber compartments during ontogeny and phylogeny reflects relationships with the rates ofmetabolic activity of the animal. Neither for teeth and toothplates nor for peristomes there are convincing functional interpretations.Ornaments on the face are interpreted as reflecting mechanical functions such as motility or temporary fixation of paired shells duringplastogamy. Ornaments may participate in the masking of apertures. The concept of “face” as a functional unit in the externalmorphology of the foraminiferal shell complements the current concepts of internal morphology (architecture) and enhances thebiological understanding of foraminiferal shells.

RIASSUNTO - [Le “facce” dei foraminiferi bentonici] - Le superfici dei gusci dei foraminiferi bentonici possono essere distinte perla presenza di particolari tessiture del guscio stesso, disposizione delle perforazioni e/o ornamentazioni, nonché per essere delimitateda cambiamenti angolari netti della forma del guscio. Laddove tali superfici contengano l’apertura (o le aperture) principale e/o orifizio spazi interloculari, queste sono interpretate come unità funzionali e qui dette “facce”.

L’estensione progressiva del lato aperturale durante l’accrescimento determina il numero di aperture e potrebbe riflettere ilcrescente bisogno di cibo all’aumentare della velocità di crescita per ogni stadio successivo. Nelle forme filogeneticamente più avanzate,l’estensione del lato aperturale ed il numero di aperture su tale lato può aumentare in modo sproporzionato per ispessimento marginale,o anche per ripiegamento di un guscio planispirale/anulare evoluto. Ciò può avvenire tramite l’estensione dei prolungamenti alari, conforma di vortice o meandriforme nei gusci planispirali involuti, oppure per torsione polare nei gusci planispirali fusiformi. Attualmentenon esiste una spiegazione funzionale convincente per peristomi, denti e e piastre dentali (toothplates).

Nelle forme lamellari perforate, la “faccia” diventa progressivamente indipendente dalle aperture primarie e dalla loro disposizionesulla superficie del guscio: la funzione delle aperture primarie è limitata alla crescita, mentre gli orifizi dello spazio interloculareassumono ulteriori funzioni autoecologiche, di raccolta del cibo, motilità, rilascio dei gameti o degli embrioni, ecc. L’ornamentazionesulla “faccia” è interpretata come funzionale alla motilità, o alla fissazione temporanea di individui accoppiati durante la plastogamia.L’ornamentazione potrebbe inoltre contribuire ad occultare le aperture.

Quindi, il concetto di “faccia” come unità funzionale della morfologia esterna dei gusci dei foraminiferi completa gli attuali concettidi morfologia interna (o architettura) dei foraminiferi bentonici, migliorando la comprensione delle parti dure dei foraminiferi in unaprospettiva biologica.

76 Bollettino della Società Paleontologica Italiana, 45 (1), 2006

or dwelling in the sediment, when there is no activemovement. In unkeeled, spinose planktonic species, theglobular chamber walls serve as mechanical supportfor the radial spines. The latter, in their turn, supportthe clothes-lines produced by the pseudopods to exposethe symbionts during daytime to light and free gasexchange in the open water (Hemleben et al., 1989).Thus, all surfaces of the shell have the same uniformfunction. If accretion rates during growth are highenough, the shell will reach a perfect globular shape,as in Orbulina. Whether the umbilical side of keeledplanktonic species, as in Globorotalia, is an “umbilicalface” with a particular functional meaning is at presentunclear.

In the benthic realm, globular shells without anydifferentiation of their surface are rare but may beexemplified by Sphaerogypsina globula. This speciesseems to be a representative of a predominantlyencrusting, permanently attached group freely living inthe isotropic interstices between sand grains of similarsize as the shells themselves. Their movement mightbe restricted to passive transport within or on thesurface of the sediment.

The purpose of this note is to review selected typesof faces and to discuss their functional meaning. Thefunctional significance of faces in general is deducedfrom the numerous repetitions of trends in independentphyletic lineages interpreted as reflecting progressiveadaptation. The interpretation of the specific functionor functions of a particular face pattern must be basedas much as possible on all available knowledge on the

biology and ecology of the living organisms. The generalnature of this condensed review paper obliges to cite aconsiderable number of foraminiferal taxa as examplesand to use many specialized morphological terms. Onlya few of them can be illustrated here. The reader iskindly requested to use Loeblich and Tappan’s (1987)treatise and Hottinger et al. (1993) for complements ofillustration and their glossaries for the definition ofmorphological terms. Also available on the web:Hottinger, L. and Scheuring, V. 1997: Glossary of Termsused in Foraminiferal Research. Preliminary Version:h t tp : / /www.ucmp.berkeley.edu/people / j l ipps /glossary.html.

THE NUMBER OF PRIMARY APERTURES ANDTHE SIZE OF THE APERTURAL FACE IN NON-

LAMELLAR, IMPERFORATE FORMS (Pl. 1)

With size increase of the shell, the number ofapertures on the apertural face is multiplied. The sizeof the apertures, their shape and their spacingcharacterizes the respective group and remains moreor less constant during ontogeny and phylogeny. Thus,their increase in numbers is always linked to anenlargement of the apertural face.

The surface of the apertural face, and its growthduring ontogeny and phylogeny, depends on thegeometry of the chambers and its modification throughtime. The latter depends on volume accretion rates insuccessive growth steps under the constraints of a shell

EXPLANATION OF PLATE 1

Faces as a consequence of chamber shape and arrangement. Schematic drawings, not to scale, from various sources.

figs. 1-3 - Conical shells with a biserial to uniserial chamber arrangement. Note multiplication of primary apertures with theenlargement of the apertural face and the final formation of a cone margin with particular, radially oblique marginalapertures.

figs. 4-7 - Planispiral-evolute chamber arrangement with progressively elongated chambers becoming annular in the adult. Note thethickening and final folding of the disc’s periphery to accomodate more apertures on an enlarged apertural face.

fig. 8 - Planispiral involute chamber arrangement where the alar prolongations form a vortex enlarging the apertural face. Annularultimate growth stages loose their alar prolongations and produce for compensation a lateral, meandrine architecture (seeHottinger, 2005).

figs. 9-10 - Trochospiral, lamellar-perforate shells use the orifices of the interlocular spaces produced by their umbilical architectureto create an umbilical face. The function of the primary aperture is reduced to governing the growth of additional chambers.9 - Basic pattern of umbilical face in rotaliines: Rotorbinella.10 - Umbilical face in high-spired lockhartiines: Sakesaria.

figs. 11-14 - From streptospiral-involute, globular to planispiral-involute, fusiform shells as in alveolinids. Note the long apertural slitin pseudonummuloculinid shells (11, 12) replaced by regular rows of rounded apertures corresponding to the internalchamber compartmentation.14 - Fusiform shell as of Alveolina. A - axial section; E - equatorial section. Note columellar pathway (col) representing theshortest possible connection through the spiral shell and the polar torsion enlarging the apertural face for admission ofadditional apertures. White arrow: direction of movement; black arrow: direction of growth.

fig. 15 - Basic morphology of fusulinids with fluted septa. Note tunnel and septal pores, the latter multiplied by polar torsion ofthe apertural face.

figs. 16-19 - From miliolid to lacazinid (uniserial-concentric) chamber arrangement and from single, miliolid, circular apertures withmiliolid teeth to trematophores, ultimately getting annular. Note the difference between alveolinid spiral shell axes in 12-13 (horizontal) and miliolid apertural axes in 16-17 (vertical).

Abbreviations: a - aperture; af - apertural face; apax - apertural axis; fol - folium; ma - marginal aperture; n - notch; per - periphery; potort- polar torsion; pst - peristome; s - septum; sp - septal pores; spax - spiral axis; sut - chamber suture; t - tunnel; tr - trematophore; uch- ultimate chamber; uf - umbilical face; v - vortex.

77L. Hottinger - The “face” of benthic foraminifera Pl. 1


architecture by successive, more or less closedchambers producing a particular shape of the shell.Accretion rates depend on the intensity of metabolicsynthesis of additional chamber plasm per growth stepand may be linked to the rate of food uptake. Thus,there may be a link between increasing volume accretionrates and increasing surface of the apertural faceadmitting increasing numbers of apertures (Pl. 1, figs.1-6). However, this link is not simply governed by avolume-surface relationship: in many cases, the numberof apertures is linked directly to the number of chambercompartments subdividing the protoplast intovolumetrically uniform units of metabolic activity, asfor instance a single aperture per chamberlet in a simple,praealveolinid architecture, two apertures perchamberlet in a globular or oval Eocene alveolinid(Reichel, 1937) or in a discoidal planorbulinellid. Weobserve, however, an acceleration of the productionof apertures on the apertural face relative to chambervolume and/or to the number of chamber compartmentswith time in phyletically advanced forms (Hottinger,

1967). This is a general trend, realized in different groupswith different modifications of chamber shape: inuniserial-conical shells (Pl. 1, figs. 2-3) by an annularmodification of discoidal adult chambers (as in large,discoidal orbitolinas), in discoidal-evolute shells bythickening of the shell margin (Orbitopsella) and,eventually, by additional folding of the thickened margins(some microspheric soritines; Pl. 1, fig. 7), in spiral-involute, lenticular to discoidal shells by the formationof a vortex (Pl. 1, fig. 8) supplemented by meandrinesupplemental chambers in the case of final concentricgrowth (Meandropsina and archaiasines; Hottinger,2005), in spiral-involute, fusiform shells by polar torsion(elongate fusulinids, elongate alveolinids, Pl. 1, figs.14-15; Leppig, 1992), and in globular-concentricmiliolids by a modification of the discoidal trematophoreto an annulus (Lacazina; Pl. 1, figs. 18-19). To myknowledge, no quantitative data on this subject arecurrently available.

In the case of polar torsion in large, elongatealveolinids, we know from direct observation of living

Fig. 1 - Apertural face and surface of attachment. All specimens from the Gulf of Aqaba, recent. SEM graphs. a, f, g from Reiss &Hottinger (1984); b-e from Hottinger et al. (1993), modified. Scale bars = 0.2 mm.a - Sahulia barkeri (Hofker) attached to solid substrate. White arrows: direction of extruding pseudopods from the gap between thesubstrate and the penultimate chamber. Oblique lateral view; b-d - Textularia sp. C in Hottinger et al. (1993). b - apertural view showingshell face comprising the smoothened surfaces of both, ultimate and penultimate, frontal chamber walls; c - lateral view of shell showingrough surface of lateral chamber walls; d - broken specimen showing smooth septal faces and paraporous wall texture; e - Valvulinaovoidea d’Orbigny. There are three chambers in the last whorl, the ultimate chamber is missing. Note valvular tooth and smooth face;f - Paracibicides edomica Perelis and Reiss attached to solid surface by its spiral side in order to keep the aperture free fromobstructions. Note imperforate face extending into the umbilical depression; g - Caribbeanella elatensis Perelis and Reiss attached byits spiral side to a brachiopod shell fragment.Abbreviations: a - aperture; af - apertural face; f - foramen; pp - parapores; s - septum; sf - septal face; vt - valvular tooth.

79L. Hottinger - The “face” of benthic foraminifera

Alveolinella that the apertures on the polarenlargements of the apertural face are used for motility(in polar direction) whereas the primary row ofapertures running along the entire apertural face is activeduring the growth process (Pl. 1, fig. 14). This is afirst hint at the idea that the apertural features of largerforaminifera may respond to several separate functionsduring different periods in their life time. Their numberbeyond the number of chamber compartments mayrepresent an increasing independence from constraintsby the geometry of chamberwise growth. On the otherhand, we have to keep in mind, that large nodosariidsand in particular Frondicularia, remain with singleapertures in spite of their large size of 5 or some moremm. The nodosariids are interpreted as forms withparticularly low metabolic rates due to their slow gasexchange through minute, slitlike pores in their thickand compact chamber walls. Their sluggish metabolismmight tolerate a very low rate of exchange between theprotoplast and its ambient environment. The peripheralposition of the single apertures (with their enigmaticapertural chamberlets) in the planispiral shells ofLenticulina, representing the longest possible way ofintercameral communication, points in the samedirection.

Some smaller, perforate benthic foraminifera exhibitvery numerous, small-sized apertures on their more orless inflated apertural face (Scarificatina, Cincoriola,Paleocene; Fig. 7e, h). These apertures seem not to bealigned in subsequent septa, an indication that theirpseudopods may have been armed not by microtubuli

but by some other, shorter fibers of actin or intermediatefibrous proteins. The septal pores of the fusulines,although less densely disposed (Pl. 1, fig. 15), raisethe same questions.

There are non-lamellar, imperforate (fusulinids,pfenderinids) and lamellar-perforate groups(nummulitids) masking their aperture or apertures untilthey are incorporated into the interior of the shell bysubsequent growth of new chambers. The more orless calcified masks obstructing the apertures areremoved prior to the growth process of a new chamber.These openings are subsequently enlarged by preciselylocalized resorption to a so-called tunnel (Pl. 1, fig. 15;Fig. 8b) securing the communication between thechamber cavities of the shell by a comparatively largeforaminal opening. Whereas the tunnel in pfenderinidsproduce a deep incision in the columella of the shelland - by this geometrical position - represents theshortest possible way of communication between thespiral chambers (as the columellar pathway inalveolinids with an approximate relation 1:10 in respectto the equatorial path; Pl. 1, fig. 14), the tunnels offusulinids and nummulitids remain in the equator ofthe shell without contribution to shorten the ways ofcommunication. The presence of tunnels seems todepend on the presence of other means ofcommunication between the protoplast and the ambientenvironment: septal pores in fusulinids, unobstructedpassages in the latest parts of the columella inpfenderinids and canal systems (see below) innummulitids.

Fig. 2 - Teeth and trematophores. All specimens from the Gulf of Aqaba, recent. From Hottinger et al. (1993) modified. SEM graphs.Black scale bars = 0.1 mm.a-c - Spiroloculina sp. B in Hottinger et al. (1993): single bifid miliolid tooth as extension of the basal layer; d-f - Spiroloculina attenuataCushman & Todd: paired teeth demonstrating the potential participation of every part of the inner chamber wall in the formation ofteeth; g-h - Pyrgo striolata (Brady) with an enlarged aperture and a broad “bifid” tooth. Note in h the presence of such a tooth in theinner part of the shell demonstrating its nature, in spite of its unusual shape, as a true tooth, not as a mask; i- j - Sigmohauerina bradyi(Cushman) with three chambers in the last whorl bearing a trematophore. Note on detail in j more or less regular marginal “teeth”, eachsupported from the interior by a ridge on the inner part of the chamber wall. Abbreviations: mat - marginal miliolid tooth; mt - miliolidtooth; smt - supplementary miliolid tooth; tph - trematophore.


TEETH, TOOTHPLATES AND PERISTOMES(Figs. 2-4)

Many non-lamellar and lamellar foraminifera exhibita face which is reduced to the immediate surroundingsof a single aperture in terminal position. In many groups,the lumen of such a single aperture is restricted bytooth-like structural elements. Many of these groupspossess a neck, many also peristomes of various sizesand shapes. The teeth might be slightly modified inshape when incorporated into the interior of the shellafter addition of new chambers but they remain alwayspresent. The tooth-like structures characterizing thegenus Borelis (Alveolinidae; Hottinger et al., 1993, pl.75) obstruct exclusively the apertures and disappearwithout trace from septal faces. They are thereforeinterpreted, for the time being, as a particular kind ofmask. Whereas peristomes and all kinds of masks areobserved also in forms with multiple apertures, teethseem to occur only in taxa with single apertures.

There are at least three fundamental ways to generateteeth or teeth-shaped structures: Valvular teeth areproduced by cutting out parts of the frontal wall ofchambers (Fig. 1e). Miliolid teeth are localized extensionsof the inner part of the porcelaneous chamber wall,most frequently but not always of the basal layer,

producing a single or several pointed or bifidprotuberances in the aperture (Figs. 2a-h). Toothplatesoccur frequently in lamellar foraminifera (see below).

Many miliolids, but also other porcelaneousforaminifera, exhibit thickened rims around the aperturalopening of the shell, i.e. peristomes (Fig. 4). These areproduced by extension of the outer layer including theoutermost pavement of biocrystals covering theporcelaneous chamber wall (Debenay et al. 2000, fig.10). They often exhibit protruding rims or walls whichmay be folded in complicated ways. Large triangularapertures (as in Dendritina for instance) may berestricted and transformed to dendroid shapes or totallysubdivided by fusion of the peristomal folds. In lamellar-perforate groups, reussellids for instance (Figs. 4f-g)similar structures occur but their lamellar nature is notknown. Peristomal structures are not modified to asignificant extent when incorporated into the interiorof the shell after the addition of a new chamber duringontogeny, in contrast to masks disappearing completely.Peristomal structures always point in distal direction,in the direction of growth, never backward.

A combination of fused peristomes and multipleteeth may lead to the formation of trematophores (Figs.2i-j). These are cupola-shaped sieves over preseptalspaces, which may be supported by single or multiple

Fig. 3 - Toothplates. a-c - Loxostomina amygdalaeformis (Brady): The face is restricted to the immediate surroundings of the aperturewith its toothplate; d-e - Neouvigerina ampullacea (Brady). The aperture with its toothplate, in terminal position, is perched on anarrow neck; f-g - Globocassidulina spp. exhibit a triangular apertural face with v-shaped aperture and toothplate. The specimenfigured in f lacks the ultimate of the biserially enrolled chambers. The relation between the biserial chamber arrangement and the v-shapeof the tooth plate calls for closer investigation.Abbreviations: a - aperture; ad - adapertural depression; n - neck; tp - toothplate.

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pillars. M. Reichel (1984) has produced a very accurateand precise model of such a structure in Rhapydionina.

Lamellar-perforate, small-sized foraminiferaexhibiting bi- or triserial, elongate shells with acomparatively large aperture in terminal position (suchas bolivinids and buliminids) are known to moveactively in the sediment (Wetmore, 1988; Kitazato,1988). Their ambient environment is isotropic but theirmovement is directed in the axis of their elongate shell.Around the terminal aperture there is a face delimitedby approximately circular boundaries and restricted tothe polar front of the elongate shell. This face ischaracterized by low densities or by the absence ofpores, and by an ornamentation of comparatively lowrelief (Figs. 3 a-c). In many cases, the relief of thesefaces has components radiating away from the aperture.They might reflect the flow of pseudopodial protoplasmenveloping the whole shell and forming a kind of hosewithin which the shell glides face foreward. The roleof necks (Fig. 3d) and of ornamental elements disposedin perpendicular direction to the longitudinal elements,such as lateral pseudospines, remains unclear as longas the mechanisms of burrowing in the sediment arenot fully understood.

These burrowing elongate shells all bear in theiraperture a so-called toothplate. The toothplates,however, have a much wider distribution in benthicshells of any shape and from all kinds of habitat. Theirsignificance might therefore reach far beyond

autecological relationships. They consist of half tubesconstructed by the inner lamella (= inner lining; Revets,1989, 1993) attached to an apertural rim and runningmore or less freely from foramen to foramen. In theaperture, they exhibit a serrated hemicircular free rim.Exact definition and delimitation, lamellar nature andmode of construction currently are under somecontroversial debate, but their appearance on theforaminiferal face is very similar: a half tube with aserrated margin extending with one free side as an openloop into the lumen of the aperture (Fig. 3e).Valvulinid and miliolid teeth as well as toothplates dividethe stream of protoplasm extruding from the shell intothe ambient environment. Perhaps they separate ingoingfrom outgoing streams but there are no convincingobservations available on living animals. As to tooth-plates, S. Leutenegger (personal communication) didnot find any differentiation in the fine structure of theprotoplast in the twisted half tube of bolivinids.Consequently we may dismiss any relation to canalsystems housing permanently differentiated ectoplasmin their interlocular spaces. In pseudoplankticforaminifera, after reproduction in the free watercolumn, the young hatchlings leave the mother shellthrough tubular structures running around the floatingchamber (Rückert-Hilbig, 1983). Perhaps thetoothplates of so many infaunal taxa, after reproduction,help to conduct the offspring out of the mother shell,but, again, there are no direct observations.

Fig. 4 - Faces dominated by peristomes (pst). All specimens from the Gulf of Aqaba, recent. SEM graphs from Hottinger et al. (1993),modified. a-c - Monalysium acicularis (Batsch), lateral view (a), oblique end-view (b) showing apertural face with folded peristomes,and oblique view of septal face in broken specimen (c) with foramen carrying strongly folded peristomes; d-e: Coscinospira hemprichiiEhrenberg, lateral view of shell and end-view of apertural face dominated by peristomes fused in the center of the face and subdividingthe aperture; f-g - Fidjiella sp. A in Hottinger et al. (1993), oblique apertural view and end-view of triangular shell face. In this case, itis difficult to distinguish the free edge of the toothplate from the serrated peristomes without opening the shell.

L. Hottinger - The “face” of benthic foraminifera


TYPES OF ORNAMENTATION ON FACES(Figs. 5-7)

Agglutinated foraminiferal shells often exhibit asmooth face extending over the total surface of theshell turned towards the substrate (Fig. 1a). The smoothsurface may appear in strong contrast to the lateralchamber walls bearing below their rough surface aparaporous texture. The face of the shell, covering inbiserial (textulariid) forms the apertural faces of theultimate and the penultimate chamber, is delimited bythe angular break in the chamber outline (Fig. 1b). Somerecent textulariids have been collected in the Gulf ofAqaba glued to a firm substrate. Apparently, their

lifestyle is to some extent sessile or at least poorlymotile. In contrast, the species of Amphistegina showfaces ornamented by strong pustules (Figs. 5-6). Theseare spread over the apertural face of the ultimatechamber and extend over a part of the ventral wall ofthe opposite chamber in the last whorl. The extensionof the face covered by pustules is largest in theshallowest species, A. lobifera, and smallest in thedeepest species A. papillosa. We know from directobservation that A. lobifera inhabits the most turbulentpart of the photic zone and reacts to photoinhibition byactively moving into shade. Thus, A. lobifera mustshow more motility than A. papillosa living at the lowerend of the photic zone and in quiet waters as

Fig. 5 - Reduction of faces in Amphistegina species according to their respective, overlapping depth range. Darkening gray of backgroundsymbolizes depth gradient throughout photic zone. All specimens from Gulf of Aqaba, recent. Details of faces as SEM graphs (x 60).Ventral views of shells (except dorsal view on n) and axial sections as light micrographs (x 30). The sections illustrate the generalflattening trend with depth (Hallock & Hanson, 1979) reflecting the reduction of lamellar thickness as a consequence of reduced waterturbulence. A. aff. radiata is an exception to this trend in spite of its deep habitat but exhibits a strongly reduced face. From Hottingeret al. (1993), modified. a-c - Amphistegina lobifera Larsen; d-f - A. lessonii d’Orbigny; g-i - A. bicirculata Larsen; j-l - A. papillosa Said;m-o - A. aff. radiata in Hottinger et al. (1993).

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documented by the small grain-size of the muddysediments. It is therefore obvious to link thisornamentation to a relative intensity of motility.

Amphisteginids move on a bipolar bundle ofextended rhizopods armed by microtubuli (Fig. 6).Travis & Bowser (1991) explain the movement ofbenthic foraminifers as follows: the tips of the extendedpseudopods are fixed on or in the substrate and in oron the shell. By contraction of the pseudopods, theshell is moved towards the location where thepseudopod tip is fixed to the substrate. Travis andBowser visualise the traction forces by the deformationof a thin rubber sheet used as substrate for Amphisorusin laboratory experiments. My own observationssupport the moving-by-traction-scenario fornummulitids on vertical glass walls, where the climbingforaminifer has to lift the considerable weight of theshell against gravity. In amphisteginids, my observationsin vivo rather suggest that the shell is moved bycoordinated action of parallel pseudopodial strands asif it where a foreign particle or cell organell transportedalong the pseudopodial axis (“membrane domaintransport” according to Travis & Bowser, 1991).However, in both cases, the mechanical forces movingthe shell must be transmitted from the pseudopodialskeleton, the microtubules, to the mechanically

resistant, biomineralized shell in a directionperpendicular to the axis of the pseudopodia bymolecular bridges from the microtubule to the cellmembrane supported by a mechanically resistentsubstrate, the shell wall. The pustules on the aperturalface may thus form anchor surfaces for the forcesmoving the shell.

Other pustular ornaments covering entire faces aremuch smaller in size. Their disposition on the face isradial and independent of the direction and number ofchamber septa extending over the face. Theseornaments occur on small shells, usually with atrochospiral chamber arrangement forming anumbilicus. The flattened umbilical side of the shell isoccupied totally by the shell’s face and its radialoramentation. In many cases, two shells have beenfound glued together face to face, documenting aparticular kind of reproduction, plastogamy, where asmall number of haploid gametes are not released intothe free water column but kept inside the two pairedshells until the zygotes are ready to hatch (Grell, 1967;Goldstein, 1999). Here also, the ornamentation of theface has a mechanical significance for keeping the twopartners together during the act of reproduction (Figs.7a-d).

Fig. 6 - Expansion of pseudopods from amphisteginid face into ambient environment of shell. a - ventral view; b - details of (a) showingcushion of overcrossing pseudopods armed with microtubules between pustules of the shell face. There are some kind of molecularbridges connecting the microtubules with the membrane covering the pseudopod in perpendicular direction. The pseudopodial membraneis mechanically supported by the pustules. By coordinated action of the parallel pseudopods the shell is dragged forewards. Cartoonbased on observation of living Amphistegina in petri dishes, schematic, not to scale; c - dorsal view; d - lateral view; e - TEM micrographof pseudopodial protoplasm with permanently polymerized microtubules in a canal of Assilina ammonoides living in the Gulf of Aqaba(x 24,000). Courtesy S. Reber-Leutenegger. Abbreviations: mem - cell membrane; mt - microtubule; mbr - molecular bridge (perpendicularto axis of microtubules); pust - pustule on face; rzp - rhizopod.



The small-sized shells of Scarificatina (Paleocene;incertae sedis in my view) exhibit an umbilical facewith a single or several straight parallel ridges runningover the entire face and ignoring the pattern of theunderlying ventral, more or less radial sutures of thechambers surrounding narrow umbilical cavities (Fig.7e-g). This is a most unusual pattern in rotaliid smallerforaminifera, raising questions about its function. Acloser look at this umbilical structure reveals the ridgesto delimit by regular lamellar folding on either side aregular row of tubular passages connecting theumbilical cavities with the ambient environment. Theparallel ridges are complemented by much smaller radialribs adorning the face’s periphery. They are extendingin proximal direction by rows of small-sized pustules.

This latter complement of the facial ornament is similarto the ones observed on plastogamic shells andinterpreted the same way. Thus, the canaliferous ridgesmight be interpreted as device to separate and channelgametes towards their place of fecundation in thespaces between the ridges. Loeblich & Tappan (1987)interpreted the ridges as marks of attachment to a firm,ribbed substrate but their material had not revealed theparallel rows of passages produced by the ridges. Theseare certainly not marks of a foreign substrate. To myknowledge there is only one more genus exhibiting alinear pattern extending over the umbilical face of atrochospiral smaller benthic form: Soriella (lowermostEocene). Its architecture however is insufficientlyknown to attempt any interpretation.

Fig. 7 - Radial ornamentation of umbilical faces, linear structures in spiral umbilicus and multiple primary apertures out of alignement.SEM graphs except (g). Scale bars = 0.1 mm.a-b - Glabratellina sp. A in Hottinger et al. (1993), ventral and lateral views. Note intensive ornamentation of umbilical face by radiallyaligned pustules. Gulf of Aqaba, recent; c-d - Discorbinoides sp. A in Hottinger et al. (1993), lateral view of plastogamic pair andumbilical view of single shell showing simple, radial grooves as ornament of the umbilical face in addition to grooved chamber sutures.Gulf of Aqaba, recent; e-g: Scarificatina sp. showing linear, single or multiple, parallel umbilical crests and multiple apertures withperistomes. Mons, Belgium, Paleocene. The exceptionally well preserved material was recovered and placed at my disposal for studyby Yvette Tambareau (Toulouse) to whom I address my sincerest thanks; h - Cincoriola ovoidea Haque, another example of multipleapertures without alignment; axial thin section, light micrograph. Lafarge Quarry, Aquitaine, France, Paleocene.Abbreviations: a - aperture; f - foramen; fol? - surface of foliar (?) origin covering the umbilical cavity; lh - loop hole (connection betweenchamber cavity and interlocular space); p - pore; pst - peristome; rgr - radial grooves; rp - radial pustules; rr - radial ridges; s - septum;sf - septal face; sut - chamber suture; ucr - umbilical crest; uf - umbilical face.

85

THE ROLE OF APERTURES IN SHELLS WITHINTERLOCULAR SPACES (Pl. 2)

Bilamellar spiral shells - producing by their potentialindependence of outer and inner lamella more or lessclosed interlocular spaces - exhibit two independentcavity systems in the shell. The chambers and theirdirect connections through the foramina are filled withvacuolar endoplasm whereas in the interlocular spacespseudopodial ectoplasm circulates and connects theprotoplast with the ambient environment (Hottinger &Dreher, 1974; Hottinger, 1982). In elphidiids, we knowthe foramina to be temporarily closed by organic plugs.These separate each chamber cavity into a metaboliccontainer unit separated from control by the cell nucleusuntil their reopening prior to a new growth process.The number of apertures surpasses the number ofchamber cavities only where the basic body plan(Arthur, 1997) demands the construction of “primary”multiple apertures, in a single interiomarginal row or asareal group, as observed in calcarinids, siderolitids andmost elphidiids or in the genera Scarificatina andCincoriola (Figs. 7e-h) mentioned above. In all theselatter cases of primary multiple apertures, noenlargement of the apertural face beyond ordinarygrowth (folding of enlarged margins, polar torsion) hasbeen observed.

The interlocular spaces may open to the ambientenvironment by slits or canal orifices of circular outline.Their position on the shell surface and their number isindependent of the apertural face, of its size and shape.The orifices of the canal system may be grouped on asingle (ventral) side of shells differentiating their

Fig. 8 - Marginal cord of nummulitids - a peripheral face. All specimens from Gulf of Aqaba, recent. Arrows: direction of shell growth.Scale bars = 0.1 mm. SEM graphs from Hottinger, 1977, modified.a - Heterostegina depressa d’Orbigny: apertural face with masked aperture showing backward extension of specific ornaments towardthe shell periphery; b - Assilina ammonoides (Gronovius), evolute specimen showing an apertural mask in the ultimate, a tunnel in thepenultimate chamber. The base of the apertural face is smooth in evolute, loosely spired specimens; c- A. ammonoides, involutespecimen, broken in axial direction, showing shell periphery formed by a marginal cord and its axial section.Abbreviations: a - aperture; af - apertural face; co - canal orifice; m - mask; mc - marginal cord; s - septum; sf - septal face; sulc - sulcus;t - tunnel; up - umbilical plate.

morphology in respect to their substrate (in mostrotaliids, Pl. 2, figs. 7-21), cover the entire surface ofthe shell (Laffitteina; Pl. 2, figs. 4-6), grouping theorifices on canalicular spines (Calcarina, Siderolites,Wannier, 1980) or on the periphery of the shell. Theelongated, lozenge-shaped ridges alternating in positionon the periphery of a nummulitic shell and forming themarginal cord (Fig. 8) release radial and tangentialbundles of pseudopods from the orifices of the canalsystem - deeply hidden in beween the ridges - at anypoint of the shell’s periphery.

In all these cases, the apertural face loses much ofits significance in non-lamellar, imperforate groups, untilits complete disappearance in forms dominated by asupplemental skeleton (Hottinger et al., 2001). InVacuolispira or Biplanispira (Pellatispirinae) forinstance, primary, bilamellar-perforate chamber wallsmay be built over canal orifices of the supplementalskeleton without any foraminal connection to thenepionic spiral chambers. This is the ultimate, totaldeliverance from the constraints of chamberwisegrowth reflected by a seemingly chaotic architectureof the shell.

GENERAL FEATURES OF AN UMBILICAL FACE(Pl. 2)

The rotaliids s.l. all exhibit faces comprising mostor all of the umbilical (ventral) shell surface as afunctional unit. This is particularly evident in the largestforms, i.e. Dictyoconoides, producing a conical shellof cm size composed of chambers arranged in multiple



spirals (Pl. 2, figs. 1-3). The sparsely perforatedumbilical face is covered by a dense layer of piles, thedorsal side shows regularly perforate chamber wallsornamented only by raised chamber and whorl sutures.Sections reveal the complex architecture extendingbelow the seemingly uniform ornamentation of the faceby piles.

The general architecture characterizing the rotaliidumbilicus and supporting the shell’s faces is composedof the following elements (Pl. 2, figs. 7-11): The ventralchamber wall is extended by a more or less triangularwall called folium covering the sector correspondingto its spiral chamber or more of the umbilical space.The folium may have a differentiated, particular textureexpressed very often by a different perforation pattern.Most of the folia support pustules produced by alocalized inflation of the outer lamella. In overlappingsuccessive folia or in superposed folia of subsequentwhorls, the sites of lamellar inflation may be blueprintedto successive levels producing, thus, the piles oflamellae (“pillars”) which appear on the face as“pustules” (Pl. 2, figs. 2-3).

There are at least three kinds of walls separatingthe chamber lumen from a space below the umbilicalcover, i.e. below the foliar wall. These walls, generallycalled plates, differ in their mode of construction andlamellar composition (Hottinger, 2000, text-fig. 18).Two of them, the umbilical and the coverplates, produceincised sutures on poorly ornamented faces separatingthe folium from the ventral chamber wall. The foliumadmits a retrovert aperture positioned in principlebetween the proximal end of the plate suture (markedby a notch in the proximal radial chamber shoulder)and the adaxial tip of the folium (Pl. 2, figs. 10-12).

Between subsequent spiral chambers, there is anintraseptal space visible on the ventral shell surfaceeither as more or less radial slit or, if subdivided, asrow of canal orifices. Feathering of open intraseptalspaces is frequent (Pl. 2, figs. 7-9).

In most larger rotaliids, the axial zone of theumbilicus is filled with a single, a composed or a multipleplug produced by a single or multiple piles of inflatedlamellae. The adaxial tips of the folia may reach andcover the central umbilical piles (Pl. 2, fig. 18) or admit,at least in the ultimate shell whorl, a circular narrowspace at the center of the face (Pl. 2, figs. 15, 21). Thevarious subfamilies and genera of the rotaliids arecharacterized by differences in proportion andarrangement of these architectural elements and by thegeometry of passages and connections between the shellcavities. However, the umbilical faces of the rotaliidsare very similar: either, the faces are smooth and coveredby uniformly distributed canal orifices, or more or lessevenly covered by pustules with canal orifices hiddenbetween the ornamental protuberances. Langer et al.(1989) have observed smaller, poorly ornamentedspecies of Ammonia to dig into soft substrate by acorkscrew movement. Other, somewhat larger sizedAmmonia species are known to inhabit exclusively soft,fine-grained sediments. Detailed data, however, ondepth of digging or on the mechanisms of the rotatingmovement are not available at present.

Some faces, irrespective of their size, arecharacterized by huge axial umbilical plugs (Pl. 2, figs.20-21). This latter modification of a rotaliid face mightreflect a skipjack device helping to keep the subsphericalshell in appropriate, face-downward position.

EXPLANATION OF PLATE 2

Rotaliid umbilical faces. Light micrographs of fossil shells under water and of thin-sections in transparent light, except SEM micrographs20 and 21. Scale bars = 0.1 mm.

figs. 1-3 - Lockhartiines: Lockhartia haimei (Davies) and Dictyoconoides flemingi Davies & Pinfold showing umbilicus covered withnumerous heads of lamellar piles (“pillars” auctorum) arising each from the tip of a folium and blueprinted throughsuccessive foliar umbilical extensions. Late Paleocene, Salt Range, Pakistan.

figs. 4-6 - Laffitteina bibensis Marie, dorsal and ventral view covered with orifices of an enveloping canal system, and axial section.Early Paleocene, Campo, Spanish Pyrenees.

figs. 7-9 - Rotorbinella or Rotalia sp., a species transitional between the two genera, with incipient feathering of the sunken ventralchamber sutures. Le Quillet, Aquitaine, France, Late Paleocene.

figs. 11-16 - Rotorbinella sp. demonstrating the basic pattern of the rotaliid umbilical face with a freestanding umbilical plug, short foliasupporting each a single pile of lamellae and with a faint notch. There is a single, retrovert foliar aperture. 11-14 from Cuiza,French Pyrenees, Earliest Eocene. 12-13 from Narp (Aquitaine, Southwestern France, Middle Paleocene.

figs. 17-19 - Kathina sp., an early representative of the kathinines, exhibiting foliar extensions fused with each other and with thecentral umbilical pile. Canal orifices represented by slits lacking any ornamentation. As in rotaliines, the dorsal side issmooth, without ornements.

figs. 20-21 - Ammonia pila Billman, Hottinger & Oesterle exhibitig the largest and heaviest umbilical pile known so far in rotaliids,possibly the weight for a skipjack mechanism. From Plio-Pleistocene samples of Kalimantan, Borneo, see Billman et al.(1980).

Abbreviations: a - aperture; chsut - chamber suture; chw - (dorsal) chamber wall; co - canal orifice; f - foramen; fe - feathering of umbilicalchamber sutures; foa - foliar aperture; fol - folium; folu - foliar umbilical extension; isp - interlocular space; lam - lamination visible inlamellar piles; msp - (start of) multiple spiral; n - notch; pil - pile of lamellae; spil - spiral interlocular space; spsut - spiral suture; up -umbilical plate.

87L. Hottinger - The “face” of benthic foraminifera Pl. 2


CONCLUSIONS

1. Delimited by an (usually angular) modificationof shell shape, the surface of the foraminiferal shellturned towards a planar substrate, characterized by acommon differentiation of wall texture and/orornamentation, and including the apertures or canalorifices for the extrusion of pseudopods into the ambientenvironment, is conceived as a functional unit and calledby the general term “face”. This is in contrast to thecurrent, restricted term “apertural face” designating onlythe frontal wall surface of the shell’s ultimate chamberwith its aperture. Similarly, the term “septal face” isrestricted and designates the frontal surface of thechamber wall exposed to the cavity of the followingchamber and often covered by a septal flap of this nextchamber. The marginal cord of the nummulitids isconsidered as a backward extension of the aperturalface over the entire periphery of the shell and thereforemay be called “peripheral face”. The “umbilical face”usually covers the complete ventral surface oftrochospiral benthics including the ventral surface ofall chambers forming the ultimate whorl of the shelland the surface of eventual additional umbilicalstructures such as umbilical plugs or piles.

2. The number of apertures on faces of non-lamellar,imperforate shells increases in proportion with thegrowth of the face during ontogeny and phylogeny.Where chambers are subdivided into chamberlets, thenumber of apertures is proportional to the number ofchamber compartments. Advanced forms show,however, the tendency to accelerate the increase innumbers of apertures with time by a supplementaryenlargement of the apertural face beyond proportionalgrowth: in evolute-discoidal shells by folding a thickenedmargin, in planispiral-involute forms by forming avortex complemented, after transition to annulargrowth, by meandrine supplementary chambers, andin fusiform shells by polar torsion.

3.Valvular teeth are cut out of the frontal wall of theultimate chamber by extending the apertural slit at thebase of the frontal chamber wall into its area. Miliolidteeth are extensions of the miliolid basal layer into thelumen of the aperture. The basal layer is formedexclusively by the inner part of the porcelaneouschamber wall because, by overlaying previouschambers, it is never exposed to the ambientenvironment, only to the protoplasm filling the chamberlumen. Extensions of the inner wall part from free,lateral or peripheral sectors of the chamber areappearing where miliolid teeth occur as pairs in oppositeposition or at the margin of trematophores, where theymay fuse with peristomal structures. Peristomes areextensions of the outer part of the porcelaneous wallincluding its outer cover of tiles. They produce rims orlow walls always directed towards the exterior of theshell and preserved in the interior when overgrown bynew chambers. These structures may be folded and/or fused, subdividing the aperture to form atrematophore.

As to toothplates, their exact lamellar nature isunclear. Toothplates connect subsequent apertures bya half-tube attached with one side to the chamber wall.

The free side is serrated and subdivides the lumen ofthe aperture. Teeth and toothplates obviously subdividethe pseudopodial protoplasm extruding from theaperture but, so far, no ultrastructural differentiationof the protoplasm has been discovered in order tosupport any functional interpretation.

4. Ornaments on the foraminiferal face areinterpreted primarily as reflecting mechanical functionsrelated to motility or to stabilizing the position of pairedshells during plastogamic reproduction. Ornaments mayalso participate in the formation of masks obstructingpartially or totally the aperture in between periods ofchamber construction in the course of ontogeny.

5. In bilamellar-perforate foraminifera, the potentialindependence of outer and inner lamella may be usedto create separate cavity systems connected by separatesystems of communication. The interlocular spacesconnected by canal systems house permanentlydifferentiated pseudopodial ectoplasm and havetherefore much more autecological functions than theapertural communication system between chambercavities related to metabolism and growth processes.This is reflected by the facial morphology extendingover the whole periphery as marginal cord innummulitids or over the entire ventral surface of theumbilicate, trochospiral shells of the rotaliids. Where asupplemental skeleton dominates the shell architecture(Vacuolispira), the apertural face may be lost altogetherand the face, characterised exclusively by orifices ofan enveloping canal system, may cover the entiresurface of the shell (Laffitteina, Calcarina).

ACKNOWLEDGEMENTS

Sincere thanks are due to the reviewer, Dr. Jaroslav Tyszka(Krakow), for a number of very good suggestions for theenhancement of this paper.

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Manuscript received 02 December 2005Revised manuscript accepted 05 June 2006


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The “face” of benthic foraminiferapaleoitalia.org/media/u/archives/075_090_Hottinger.pdf · 2012. 4. 29. · (Hottinger 2005, fig. 5A). Possibly, the interiomarginal, extraumbilical-peripheral