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Molecular phylogeny of common Cibicidids and related Rotaliida (Foraminifera)

based on small subunit rDNA sequences

Article  in  The Journal of Foraminiferal Research · November 2009

DOI: 10.2113/gsjfr.39.4.300

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Journal of Foraminiferal Research, v. 39, no. 4, p. 300–315, October 2009
MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS AND RELATED ROTALIIDA
(FORAMINIFERA) BASED ON SMALL SUBUNIT RDNA SEQUENCES
MAGALI SCHWEIZER1,2,4, JAN PAWLOWSKI3, TANJA KOUWENHOVEN2
ABSTRACT
To infer the phylogenetic relationships of cibicidids, we
obtained small subunit ribosomal DNA (SSU rDNA)
sequences of six common cibicidid morphospecies. In view
of our results, the placement of cibicidids in different
superfamilies, the distinction between planoconvex Cibicides
and biconvex Cibicidoides, and the erection of genera such as
Fontbotia and Lobatula are unjustified. Moreover, the
superfamily Planorbulinacea, in which cibicidids are often
placed, is polyphyletic and coiling mode cannot be used as a
major taxonomic criterion. Our data suggest that all
cibicidids examined here could be classified in one unique
family, the Cibicididae, that includes Melonis, Hanzawaia,
Cibicides (for C. refulgens), and Cibicidoides for the other
five morphospecies studied (C. kullenbergi, C. lobatulus, C.
pachyderma, C. ungerianus, and C. wuellerstorfi).
Among the six sampled morphospecies, Cibicides refulgens
is least closely related to any of the other cibicidids and forms
a clade consisting of two different species, Cibicides sp. and
C. refulgens clearly separated by geography (Antarctic and
Mediterranean, respectively). The morphospecies Cibici-
doides kullenbergi and C. pachyderma form a single clade
representing the same species. The three other species,
Cibicidoides lobatulus, C. ungerianus, and C. wuellerstorfi
are closely related. Cibicidoides lobatulus possibly comprises
two genetically distinct populations, one in the Mediterranean
and the other in the North Atlantic.
INTRODUCTION
IMPORTANCE OF CIBICIDIDS IN ECOSYSTEMS
AND PALEOECOLOGY
This study focuses on six morphospecies of cibicidids
commonly found in Recent marine environments: Cibicides
refulgens de Montfort, 1808, Cibicidoides kullenbergi (Park-
er), 1953, C. lobatulus (Walker and Jacob), 1798, C.
pachyderma (Rzehak), 1886, C. ungerianus (d’Orbigny),
1846 and C. wuellerstorfi (Schwager), 1866 (Fig. 1). Cibici-
dids are often used in reconstructing marine paleoenviron-
ments by quantifying them in fossil assemblages (e.g.,
Lohmann, 1978; Altenbach and Sarnthein, 1989; Kouwen-
hoven, 2000), and by measuring geochemical proxies such as
stable carbon and oxygen isotopes (e.g., Holbourn and
others, 2004) and Mg/Ca ratios (e.g., Lear and others, 2000;
1
Geological Institute, ETHZ, Sonneggstrasse 5, 8092 Zurich,
Switzerland
2
Department of Earth Sciences, Utrecht University, Budapestlaan 4,
3584 CD Utrecht, The Netherlands
3
Department of Zoology and Animal Biology, University of
Geneva, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland
4
Correspondence author: E-mail: magali.schweizer@erdw.ethz.ch
300
AND BERT VAN DER ZWAAN2
Billups and Schrag, 2003) of their tests. Because many species
of cibicidids have been present since the Miocene and before,
they also hold a potential for evolutionary studies.
Cibicidids occur in a wide range of water depths (depth
zones mentioned here are based on Fig. 8–16 of Kennett,
1982). Among the studied species (Fig. 2a; Schweizer, 2006
and references therein), Cibicides refulgens, Cibicidoides
lobatulus, and C. ungerianus are typical shelf species, found
chiefly from the coast to depths of ,200 m, but all range
deeper. Live Antarctic Cibicides refulgens (5 Cibicides sp.
here) have been reported down to 950 m (Murray, 1991), live
Cibicidoides lobatulus have been recorded down to 1000 m
(e.g., McCorkle and others, 1997; Holbourn and Henderson,
2002) and live C. ungerianus are reported as deep as 550 m in
the Bay of Biscay (Fontanier and others, 2003). Cibicidoides
pachyderma usually inhabits the upper and middle slope
(200–1000 m), whereas C. kullenbergi lives mainly on the
middle and lower slope and the abyssal plain (van
Morkhoven and others, 1986; Holbourn and Henderson,
2002, as Cibicidoides mundulus). Cibicidoides wuellerstorfi is
the deepest-dweller, usually found living below 2000 m.
Cibicidids generally live in well-oxygenated environments
with stable physico-chemical conditions (van der Zwaan,
1982; Kaiho, 1994; Kouwenhoven, 2000). Most have an
epibenthic or shallow-infaunal habitat (Fig. 2b; Schweizer,
2006 and references therein). Among the studied species,
Cibicides refulgens, Cibicidoides lobatulus, and C. wueller-
storfi are known to inhabit elevated microhabitats, prefer-
ably fixed to animals, plants, or hard substrates like pebbles
(Fig. 3a–b). Cibicides refulgens and Cibicidoides lobatulus
tend to attach to a substrate to which they conform in shape
as they grow, whereas C. wuellerstorfi moves freely on its
surface. These three morphospecies are thought to be
suspension feeders because they occur where currents are
strong (Murray, 1971, 1991; Lutze and Thiel, 1989;
Schönfeld, 2002) and oligotrophic conditions prevail, such
as in the deep-sea and at high latitudes (Altenbach and
Sarnthein, 1989; Wollenburg and Mackensen, 1998).
Cibicidoides lobatulus and C. wuellerstorfi have also been
recorded attached to tubeworms in cold seeps (Sen Gupta
and others, 2007; Wollenburg and Mackensen, 2009).
Antarctic C. refulgens (5 Cibicides sp. here) might feed
on diatoms and the extrapallial cavity fluids of a host
pecten (Alexander and DeLaca, 1987). The other cibicidids
generally live at the mud–water interface. However, we
collected Cibicidoides ungerianus in association with C.
lobatulus and fixed on tunicates and other organisms in the
fjords of Bergen, Norway (Fig. 3c–d). Cibicidoides kullen-
bergi and C. pachyderma occur in oligotrophic environ-
ments (Woodruff, 1992; Miao and Thunell, 1993; Almogi-
Labin and others, 2000), but are not restricted to them
(Fontanier and others, 2002; Licari and Mackensen, 2005).
Cibicidids play an important role in the fossil record as
proxies of marine paleoenvironmental conditions, including
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS 301

FIGURE 1. SEM images and light photomicrographs (i, j, m) of the studied specimens of cibicidids: a–h C. lobatulus, i, j C. kullenbergi, k, l C.
ungerianus, m, n C. refulgens, o Cibicides sp. from Antarctic, p C. pachyderma, q C. wuellerstorfi. Except n and o, all pictures correspond to DNA
samples. Scale bar 5 100 mm.

trophic state (Altenbach and Sarnthein, 1989), dissolved
oxygen (Kaiho, 1994), water masses (Lohmann, 1978;
Woodruff and Savin, 1989; Woodruff, 1992; Mackensen
and others, 1993; Yasuda, 1997) and water depth (Pflum
and Frerichs, 1976; Wright, 1978; van der Zwaan and
others, 1999; van Hinsbergen and others, 2005). Due to
their living mode, morphospecies like Cibicidoides wueller-
storfi and C. kullenbergi are thought to build their shells in
equilibrium with bottom-water chemistry. Consequently,
they are widely used in stable oxygen and carbon isotopic
analyses (e.g., Rathburn and others, 1996; McCorkle and
others, 1997; Schmiedl and others, 2004) and in Mg/Ca
paleothermometry (e.g., Rathburn and De Deckker, 1997;
Lear and others, 2000; Billups and Schrag, 2003). To
construct proper down-core isotope curves, it is important
to use a single species (Murray, 1991; Schmiedl and others,
2004). Therefore, the status and recognition of species play
an important role in paleoecologic interpretation.
DEFINITION OF THE GENERA CIBICIDES AND CIBICIDOIDES
The genera Cibicides de Montfort, 1808 and Cibicidoides
Thalmann, 1939 have a test wall of hyaline lamellar calcite,
coarsely perforated on the spiral side; coiling is a low
trochospire with an evolute spiral side and an involute
umbilical side (Fig. 4a). The shape of the axial profile is one
of the important morphological features. Traditional
practice has been to assign biconvex forms to Cibicidoides
and planoconvex forms (Fig. 4b) to Cibicides. However,
infraspecific variation that blurs this distinction is not
uncommon (Mead, 1985; Verhallen, 1991; Gupta, 1994).
Thus, the axial profile might reflect ecological conditions
302 SCHWEIZER AND OTHERS

FIGURE 2. Representations of (a) water depths and (b) sediment depths at which the six studied morphospecies are commonly found: Bathymetric
zones: shelf 5 0–200 m, slope 5 200–3000 m, and abyss . 3000 m. (Kennett, 1982). The sediment layer interface is not clear (‘‘fluffy’’ layer
represented by confetti) between +1 and 21 cm. Dashed lines represent depths were the species are less abundant and less typical.

rather than taxonomic differences. Species that tend to
attach themselves have the planoconvex form, where the
flat side, usually the spiral side, serves as the attachment
face. Vagile specimens are usually biconvex. The aperture,
another taxonomically important feature, is a simple slit
bordered by a lip and located near the peripheral margin on
the umbilical side; it occasionally extends along the spiral
suture on the spiral side (Cushman, 1931; Phleger and
others, 1953; Jonkers, 1984; Verhallen, 1991; den Dulk,
2001; Holbourn and Henderson, 2002). This criterion is

FIGURE 3. SEM images of epibiotic cibicidids: a Cibicides sp. fixed on a scallop shell, McMurdo Sound, Antarctica, b cibicidids fixed on a small
bivalve, Svalbard, c cibicidids (mainly C. ungerianus) fixed on a tunicate, Bergen area, d cibicidid fixed on an agglutinated foraminifer, Bergen area.
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS
FIGURE 4. Terminology used to describe the cibicidid test: a morphological features; b lateral form.
used to separate Cibicides, which sometimes has an
extending aperture, from Cibicidoides (Loeblich and Tap-
pan, 1964, 1987; Mead, 1985). Other criteria to identify
cibicidids are the aspect of the sutures, porosity, and wall
thickness.
HISTORY OF THE CLASSIFICATION OF CIBICIDIDS
The present classification of the cibicidids is entirely
based on morphological characteristics and there is some
confusion about the generic status of the different species.
Cibicides de Montfort, 1808 was described first, and it
remains a valid genus. Truncatulina d’Orbigny, 1826 and
Pseudotruncatulina Andreae, 1884 were synonymized with it
after the beginning of the 20th century. Lobatula Fleming,
1828 and Heterolepa Franzenau, 1884 were also put in
synonymy with Cibicides by Galloway and Wissler (1927),
but later considered valid by Loeblich and Tappan (1987).
Fontbotia, created for F. wuellerstorfi by Gonzalez-Donoso
and Linares (1970), was also recognized by Loeblich and
Tappan (1987), but synonymized with Cibicides by Sen
Gupta (1989). Often referred to as Planulina wuellerstorfi
(see Appendix for references) that generic assignment is
incorrect as the species does not have a partially evolute
umbilical side. Cibicidoides Brotzen, 1936 was originally
designated as a subgenus of Cibicides, and that was
validated by Thalmann (1939) upon the designation of a
subgenotype. Cibicidoides was later elevated to genus rank
(Loeblich and Tappan, 1955). The distinction between
Cibicides and Cibicidoides on the basis of convexity became
widespread at the end of the 1970s.
Many authors have considered the cibicidids as a
monophyletic group and have therefore grouped them
(Cushman, 1928; Galloway, 1933; Hofker, 1956; Reiss,
1958) until Loeblich and Tappan (1964) assigned Cibicides
and Cibicidoides to different superfamilies on the basis of
crystallographic wall structure. The wall structure has since
been considered to be of major importance in foraminiferal
classification (Loeblich and Tappan 1987, 1992), as noted
by Sen Gupta (2002, p. 18), and the division of the
cibicidids among different superfamilies has been main-
tained even though Towe and Cifelli (1967) showed that the
orientation of the calcite crystals is not a valid criterion to
separate hyaline foraminifers. Two concepts of cibicidid
303
classification coexist in recent literature: they are either
united in a single family (Haynes, 1981; Sen Gupta, 2002)
or separated into families belonging to different superfam-
ilies (Loeblich and Tappan, 1987, 1992; Revets, 1996).
In the traditional classifications, genera like Planorbulina,
Hyalinea, Rupertina (Fig. 5a, b, d) and Planorbulinella are
considered to belong to the same superfamily as cibicidids,
but Hanzawaia (Fig. 5c) is either placed within the same
superfamily as cibicidids (Haynes, 1981) or within the
superfamily Chilostomellacea (Loeblich and Tappan, 1964,
1987; Sen Gupta, 2002). Moreover, Nyholm (1961) and
Schnitker (1969) suggested that Cibicides and Planorbulina
might be stages in the life cycle of a single genus. Molecular
phylogenies based on partial (Schweizer and others, 2005;
Pawlowski and others, 2007; Ujiié and others, 2008;
Tsuchiya and others, 2009) and complete (Schweizer and
others, 2008) sequences of the small subunit (SSU) of
ribosomal DNA (rDNA) have shown that Melonis,
Chilostomella, Pullenia (Fig. 5e–g) and Oridorsalis belong
to the same subgroup as cibicidids, whereas Planorbulina,
Planorbulinella and Hyalinea do not seem to be phyloge-
netically close to cibicidids (Schweizer and others, 2005,
2008).
Because of their wide utility as environmental proxies
and their extensive history of taxonomic discussion,
cibicidids are good subjects to investigate cryptic speciation,
morphological plasticity within a genetic species, and
accuracy of morphological criteria used for taxonomy.
Here, we use complete and partial SSU rDNA sequences to
investigate the phylogeny of six common Recent species of
cibicidids (Fig. 1) and to establish their relationships with
other rotaliids.
MATERIAL AND METHODS
SAMPLE COLLECTION
Cibicidids analyzed in this study were collected in the
North Atlantic, the Skagerrak, the Mediterranean, and the
Southern Ocean (Table 1). Shallow-water samples were
taken by SCUBA diving or from intertidal rocks, whereas
sampling of deeper substrates was achieved by boxcoring or
multicoring. The top 1–2 cm of sediment in each core was
collected with a spoon and immediately sieved in order to
304 SCHWEIZER AND OTHERS

FIGURE 5. Genera thought to be closely related morphologically or genetically to cibicidids: a Planorbulina mediterranensis, b Hyalinea balthica,
c Hanzawaia sp., d Rupertina stabilis, e Melonis barleeanus, f Pullenia subcarinata, g Chilostomella ovoidea. Scale bar 5 200 mm.

remove mud. All sieved residues were kept at temperatures
close to those of sampling sites. Live specimens were picked
within a week after sampling, carefully cleaned with a brush
in filtered sea water to avoid contamination by minute
foraminifers present on the shell, and air-dried (see
Schweizer and others, 2005 for details). Most specimens
were imaged with scanning electron microscope (SEM) or a
camera connected to a dissection microscope prior to DNA
extraction (Fig. 1).
DNA EXTRACTION, PCR AMPLIFICATION, CLONING,
AND SEQUENCING
DNA was extracted from single specimens using DOC
lysis buffer or guanidine buffer (Pawlowski, 2000) and from
samples containing multiple specimens by DNeasy Plant
Mini Kit (Qiagen). The SSU rDNA gene was sequenced in
three steps with foraminiferal specific primers (Fig. 2 in
Schweizer and others, 2008). Of the three fragments
obtained, sA-s6 at the 59 end and s14-sB at the 39 end
could be sequenced directly whereas the middle fragment
s6-s14 had to be cloned. Despite many attempts, not all the
studied samples could be amplified for the fragments sA-s6
and s6-s14. The protocol of the amplification and the
sequences of the primers are detailed in Schweizer and
others (2008). Positively amplified products were purified
using High Pure PCR Purification Kit (Roche Diagnostics).
These purified products were either sequenced directly or
cloned. For cloning, the products were ligated with the
pGEM-T Vector (Promega) or the Topo Cloning vector
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS 305

TABLE 1. Geographical and water depth information and GenBank accession numbers of the cibicidids sampled.

GenBank accession number

Species DNA # Locality Depth Latitude Longitude SSU sA-s6 S14-sB

Cibicides refulgens C78 Planier Canyon, France 1000 m 43u029N 05u129E DQ205367 DQ195543
Cibicides refulgens C171 Marseille, France ,10 m 43u189N 05u229E DQ195568,
DQ195569,
DQ195570
Cibicides refulgens C172 Marseille, France ,10 m 43u189N 05u229E DQ205365, DQ195541,
DQ205366 DQ195542
Cibicides refulgens C173 Marseille, France ,10 m 43u189N 05u229E DQ205364 DQ195571,
DQ195540,
DQ195572
Cibicides refulgens C208 Marseille, France ,10 m 43u189N 05u229E DQ195582
Cibicides refulgens C218 Mediterranean - - - FJ705902
Cibicides sp. 1075 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ195564
Cibicides sp. 1838 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ195566,
DQ195567
Cibicides sp. 1839 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ205368 DQ195544,
DQ195565
Cibicides sp. 2068 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E AJ514839
Cibicidoides kullenbergi C86 Nazaré Canyon, Portugal 338 m 39u399N 09u159W DQ408652
Cibicidoides kullenbergi C87 Nazaré Canyon, Portugal 338 m 39u399N 09u159W DQ195575
Cibicidoides lobatulus C2 Sandgerdi, Iceland 0–1 m 64u029N 22u429W DQ195576,
DQ195585
Cibicidoides lobatulus C24 Oslo Fjord, Norway 54 m 59u399N 10u379E DQ408649 DQ195577,
DQ195578,
DQ195579
Cibicidoides lobatulus C35 Oslo Fjord, Norway 54 m 59u399N 10u379E DQ195580
Cibicidoides lobatulus C37 Oslo Fjord, Norway 54 m 59u399N 10u379E DQ195581
Cibicidoides lobatulus C39 Oslo Fjord, Norway 54 m 59u399N 10u379E AY934742,
DQ195586
Cibicidoides lobatulus C40 Oslo Fjord, Norway 54 m 59u399N 10u379E DQ195587
Cibicidoides lobatulus C120 Skagerrak, Sweden 32 m 58u219N 11u249E DQ408650 DQ195561,
DQ195562
Cibicidoides lobatulus C170 Marseille, France ,10 m 43u189N 05u229E DQ408648 DQ195583,
DQ195584
Cibicidoides lobatulus F77 Bergen, Norway 148 m 60u189N 05u129E FJ705919
Cibicidoides lobatulus F182 Bergen, Norway 148 m 60u189N 05u129E FJ705911 FJ705918
Cibicidoides lobatulus 576 Skagerrak, Sweden ,10 m 58u879N 11u159E DQ195573.
DQ195574
Cibicidoides pachyderma C196 Nazaré Canyon, Portugal 151 m 39u399N 09u179W DQ408553 DQ195553,
DQ195563
Cibicidoides sp. 2524 North Atlantic - - - DQ408651
Cibicidoides sp. 5227 Weddell Sea, Antarctica 4700 m 64u609S 43u029W FJ705900
Cibicidoides sp. 5305 Svalbard, Norway 87 m 77u139N 20u279E FJ705901
Cibicidoides ungerianus C29 Oslo Fjord, Norway 195 m 59u389N 10u379E DQ205370 DQ195546
Cibicidoides ungerianus F8 Bergen, Norway 148 m 60u189N 05u129E FJ705920
Cibicidoides ungerianus F180 Bergen, Norway 148 m 60u189N 05u129E FJ705898
Cibicidoides wuellerstorfi C184 Setubal Canyon, Portugal 2774 m 38u129N 09u329W DQ205373, DQ195549,
DQ205374 DQ195558,
AY934741
Cibicidoides wuellerstorfi 2648 Svalbard, Norway - - - DQ195560
Cibicidoides wuellerstorfi 2649 Svalbard, Norway - - - DQ195559
Cibicidoides wuellerstorfi 5660 Weddell Sea, Antarctica 1970 m 61u489S 47u289W FJ705899

(Invitro Gene), and inserted in ultracompetent cells XL2-
Blue MRF9 (Stratagene). Sequencing reactions were pre-
pared using an ABI-PRISM Big Dye Terminator Cycle
Sequencing Kit and analyzed with DNA sequencers ABI-
377 or ABI-PRISM 3100 (Applied Biosystems), all accord-
ing to the manufacturer’s instructions.
PHYLOGENETIC ANALYSIS
The new sequences presented here have been deposited in
the EMBL/GenBank database; their accession numbers are
indicated in Tables 1 and 2. Our data set was completed
with sequences available from the EMBL/GenBank data-
base (accession numbers given in Figures 6 and 7). Two
sequence datasets were analyzed: one with complete and
partial (fragments sA-s6 and s14-sB concatenated) SSU
sequences to assess the position of cibicidids inside the
rotaliids, and a second one with partial SSU sequences
(concatenated sequences of fragments sA-s6 and s14-sB and
other sequences with s14-sB only) of cibicidids and their
close relatives to look at relationships inside their subclade.
The two datasets were aligned manually in separate
alignments using Seaview (Galtier and others, 1996). The
regions which were impossible to align properly were
306 SCHWEIZER AND OTHERS

TABLE 2. List of new SSU sequences with the GenBank accession numbers for non-cibicidid taxa.

Species Locality DNA # Accession number

Bolivina skagerrakensis Bergen, Norway F14 FJ705905/ FJ705914
Buliminella sp. Madagascar 5041 FJ705909/ FJ705917
Buliminella sp. Madagascar 5096 FJ705908/ FJ705916
Cassidulina laevigata Oslo Fjord, Norway 2509 FJ705907/ FJ705915
Chilostomella sp. Bay of Biscaye, France F272 FJ705904
Epiphytic rotaliid Bergen, Norway F20 FJ705892
Epistominella exigua Weddell Sea, Antarctica 5222 FJ705897
Glabratellina sp. Mediterranean F316 FJ705895
Globobulimina turgida Oslo Fjord, Norway 3601 FJ705890
Hanzawaia sp. Bergen, Norway 6863 FJ705903
Nonionella labradorica Oslo Fjord, Norway 3600 FJ705896
Rosalina macropora Sardinia, Italy F329 FJ705891
Rupertina stabilis Svalbard, Norway 5711 FJ705893
Rupertina stabilis Svalbard, Norway 5712 FJ705894
Epistominella exigua Weddell Sea, Antarctica 3623 DQ205386/ DQ195557
Globocassidulina sp. Madagascar 5035 FJ705906/ FJ705913
Planorbulina mediterranensis Golfe du Morbihan, France 142 DQ205361/ AJ504684
Pullenia subcarinata McMurdo Sound, Antarctica 1148 DQ205382/ DQ195555
Pullenia subcarinata McMurdo Sound, Antarctica 1850 DQ205380/ DQ195554
Uvigerina earlandi McMurdo Sound, Antarctica 1994 DQ205390/ AY914568
Uvigerina peregrina Oslo Fjord, Norway U32 DQ205358/ AY914571
Virgulina concava Dunstaffnage, Scotland 3991 FJ705910/ AY934746

removed to obtain two final alignments of 3499 and 2188
sites from which 2481 and 1110 sites respectively (calculated
with Phylo-Win, Galtier and others, 1996) were used for
analyses.
The maximum likelihood (ML) trees were obtained using
PhyML 2.4.4 (Guindon and Gascuel, 2003). To assess the
reliability of internal branches, the bootstrap support (BS)
values were calculated by PhyML, with 100 replicates.
Bayesian analyses (BA) were performed with MrBayes 3.1.1
(Huelsenbeck and Ronquist, 2001). Two independent
analyses were done at the same time with four simultaneous
chains run for 1,000,000 generations, and sampled every
100 generations with 2,500 initial trees discarded as burn-in
after convergence was reached. The posterior probabilities
(PP), calculated during the BA, estimated the reliability of
internal branches. Both ML and BA were performed using
the GTR+I+C model as suggested by MODELTEST 3.7
(Posada and Crandall, 1998) implemented in PAUP*
(Swofford, 1998). The GTR or General Time Reversible
model allows the transition and transversion rates to be
different (Lanave and others, 1984; Rodriguez and others,
1990). To correct for among-site rate variations, the
proportion of invariable sites (I) and the alpha parameter
of gamma distribution (C), with six rate categories, were
estimated by the programs and taken into account in all
analyses.
RESULTS
The first dataset includes complete and partial SSU
sequences of 13 cibicidids, 47 other rotaliids, and two
textulariids taken as an outgroup. The topologies for ML
and BA are slightly different and the two divergent regions
are shown for both analyses (Fig. 6). The same three main
clades appear as in our former analysis (Schweizer and
others, 2008). The statistical support of clade 1 is 64% BS/
1.00 PP (without Globobulimina) and 0.65 PP (with
Globobulimina). The second clade has a statistical support
of 60% BS/1.00 PP and includes the following new taxa: an
unidentified rotaliid (F20), Rupertina stabilis, Glabratellina
sp., and Buliminella sp. The third clade is rather well-
supported (83% BS/0.59 PP). Inside this clade, cibicidids
form a well supported group (77% BS/1.00 PP) with
Hanzawaia and Melonis. The cibicidids form either a
monophyletic group with Melonis as a sister group and a
weak statistical support (data not shown), or they are
polyphyletic with Melonis branching among them (Fig. 6).
The second dataset (Fig. 7) includes 63 sequences of
cibicidids and eight sequences belonging to taxa of the same
subclade. Pullenia, Oridorsalis, and Chilostomella were
taken as the out-group, following the results obtained with
the first phylogenetic analyses (Fig. 6). Some sequences of
Cibicidoides lobatulus (AJ972504, AJ972513, AJ972520,
AJ972524) and C. wuellerstorfi (AJ972561, AJ972565,
AJ972574) are from specimens collected in the East
Greenland Sea (Blümel and others, unpublished data). A
supplementary sequence from an environmental sample
(AB234891, Takishita and others, 2006), closely related to
Melonis, was added to the analysis. Both ML and Bayesian
analyses give the same topology with Hanzawaia and
Melonis at the basis of the clade formed with the cibicidids.
The cibicidid clade is monophyletic with a support of 69%
BS/1.00 PP and is divided into three subclades with high
statistical supports. The first subclade (79% BS/1.00 PP),
represented by the morphospecies Cibicides refulgens, is
clearly separated in two groups (Mediterranean and
Antarctic; the Antarctic specimens are referred to as
Cibicides sp. in Fig. 7). The second subclade (80% BS/
0.98 PP) includes Cibicidoides pachyderma and C. kullen-
bergi without morphospecies separation, and a cibicidid
that was not identified at species level (Cibicidoides sp.
5305). The third subclade (98% BS/1.00 PP) is divided into
two groups: Cibicidoides ungerianus and C. wuellerstorfi are
closely related sister groups (92% BS/1.00 PP), and this
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS 307

FIGURE 6. Molecular phylogeny of rotaliids with complete (new ones in bold) and partial SSU sequences using the ML method (GTR+I+C) with
inserts of the BA tree when divergences were observed, black dots show same nodes in both analyses. Tree is rooted on textulariids and bootstrap
values for ML analysis and PP values for BA are indicated at the nodes.

clade is sister to C. lobatulus (94% BS/1.00 PP). In the C. alignment shows that the North Atlantic sequences can be
lobatulus clade, sequences from the Mediterranean are divided into three separate groups (Fig. 8) on the basis of
clearly separated from the North Atlantic ones with several the variable regions F4 and V7 (regions detailed in
differentiated regions. Moreover, a close look at the Schweizer and others, 2008).
308 SCHWEIZER AND OTHERS

FIGURE 7. Molecular phylogeny of cibicidids with partial SSU sequences (indicated in bold when fragments sA10-s6 and s14-sB are both
represented) using the ML method (GTR+I+C). Tree is rooted on the clade Pullenia–Oridorsalis–Chilostomella and bootstrap values for ML analysis
and PP values for BA are indicated at the nodes.
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS 309

FIGURE 8. Alignments of diverging regions situated in F4 (a) and V7 (b) for North Atlantic C. lobatulus.

DISCUSSION (Hyalinea, Planorbulinella, Planorbulina, Rupertina) belong

RELATIONSHIPS BETWEEN CIBICIDIDS AND OTHER ROTALIIDS
The 15 complete and 12 partial (fragments sA-s6 and s14-
sB) newly added SSU sequences confirm the general
topology of our previous phylogenetic trees, the monophyly
of cassidulinids and uvigerinids, and the polyphyly of
Buliminacea and Nonionacea (Schweizer and others, 2005,
2008). Loeblich and Tappan (1987) include cibicidids in the
superfamily Planorbulinacea. With the SSU rDNA phylog-
eny, it is clear that this superfamily is polyphyletic (Fig. 6
and Schweizer and others, 2005, 2008). Most of its members
to clade 2 (see below), whereas the cibicidids form a group
in clade 3 with Melonis and Hanzawaia (Fig. 6).
As the test morphology of Hanzawaia resembles that of
the cibicidids, they were previously grouped together
(Haynes, 1981). The placement of Melonis with cibicidids
is more surprising because it is planispiral, and coiling mode
has been considered a major criterion in traditional
taxonomies (superfamily level for Haynes, 1981 and Sen
Gupta, 2002; family level for Loeblich and Tappan, 1987).
However, other examples of mixed coiling modes are shown
by the SSU phylogeny, such as the grouping of planispiral
310 SCHWEIZER AND OTHERS
Elphidium with trochospiral Ammonia (Fig. 6). Moreover,
test-shape modelling has shown that only small changes are
needed to transform a planispiral test into a trochospiral
one and vice versa; additionally, trochospiral tests can be
generated with very different parameters giving room to
convergent evolution (Tyszka, 2006). Therefore, we can
imagine that minor mutations in building genes through
generations could transform a trochospiral test into a
planispiral one and vice versa rather easily, which implies
that coiling mode cannot be universally applied to the
Foraminiferida as a major taxonomical criterion. In the
light of these hypotheses, the genera Anomalina and
Anomalinoides could be considered as morphological
intermediates between the planispiral Melonis and the
trochospiral cibicidids because they are thought to be
closely related to cibicidids and they have a very low
trochospire (Haynes, 1981, Loeblich and Tappan, 1987). In
addition, the apertures of cibicidids and Melonis (i.e., a low
interiomarginal slit with a lip; see Figs. 1 and 5e) look
rather similar.
The other Planorbulinacea belong to clade 2, which is
composed of fast-evolving sequences of taxa from relatively
shallow water (except Rupertina, Fig. 6). The accession of
new sequences has shed light on some parts of the topology.
The polyphyly previously observed with sequences of
Rosalina (Schweizer and others, 2008) can be explained by
species misidentification – specimens 3675 and F20 are not
Rosalina, but other epiphytic rotaliids (possibly Neoconor-
bina or Gavelinopsis). The newly added sequence of F329,
which is a true Rosalina (region s14-sB similar to published
sequences), is separated from these and branches with
Discorbis (Fig. 6). The new complete SSU sequence of
Glabratellina confirms the position of the Glabratellacea in
clade 2 (Schweizer, 2006, p. 26; Ujiié and others, 2008).
Moreover, partial sequences of Buliminella, a genus
traditionally classified in the Buliminacea (Haynes, 1981;
Loeblich and Tappan, 1987; Sen Gupta, 2002), appear as a
sister group of Glabratellina (Fig. 6).
ARE CIBICIDIDS MONOPHYLETIC?
Although cibicidids were split by Loeblich and Tappan
(1964, 1987) into different superfamilies on the basis of the
optical properties of their wall microstructure, this criterion
was dismissed as inappropriate for classification of higher
taxa by Towe and Cifelli (1967) and Deutsch Conger and
others (1977). Our molecular results confirm this and agree
with the classifications placing all cibicidids in a single
family (Cushman, 1928; Galloway, 1933; Hofker, 1956;
Reiss, 1958; Haynes, 1981; Sen Gupta, 2002), but with the
addition of Melonis and Hanzawaia (Figs. 6, 7).
Three main clades of cibicidids can be distinguished with
phylogenetic analyses: (1) Cibicides sp. and C. refulgens, (2)
Cibicidoides pachyderma and C. kullenbergi, and (3) C.
ungerianus, C. wuellerstorfi and C. lobatulus (Figs. 6, 7).
This contradicts the traditional taxonomic separation
between Cibicides and Cibicidoides based on the convexity
of the test. Our results confirm that the generic distinction
based on plano- or biconvexity of the test is not
taxonomically relevant; test convexity can be affected by
the specimen’s mode of life (e.g., free vs. attached to hard
substrate), which is why this feature is often observed to
vary within and between populations (Mead, 1985;
Verhallen, 1991; Gupta, 1994). This variability was also
observed among the C. ungerianus specimens collected from
Bergen for this study; for example, F180 is planoconvex
(Fig. 1l) whereas other specimens from the same region
were more biconvex.
Cibicidids share many morphological traits: a perforate
wall made of hyaline lamellar calcite, a trochospiral test
with an evolute spiral side and an involute umbilical side,
and a slit-like, lipped interiomarginal aperture located on
the umbilical side. However, they cannot be all grouped in a
single genus: the morphospecies Cibicides refulgens is well-
separated from the others, sometimes with Melonis in
between (Fig. 6). More Melonis species need to be
sequenced to clarify the position of this genus and its
relation with cibicidids, but it is already clear that C.
refulgens is a genus apart from other cibicidids. Morpho-
logically, C. refulgens is characterized by a finer porosity
compared to other sampled cibicidids. Because C. refulgens
is the type species of Cibicides, we propose ascribing the
other cibicidid species to Cibicidoides. Because the phylo-
genetic analyses show that Cibicidoides lobatulus, C.
wuellerstorfi, and C. ungerianus are closely related (Figs. 6,
7), the genera Lobatula and Fontbotia can be synonymized
with Cibicidoides as suggested by Galloway and Wissler
(1927) and Sen Gupta (1989), respectively. Additionally,
there is no reason to place Cibicidoides wuellerstorfi in the
genus Planulina, especially because of its close relationship
with C. ungerianus and C. lobatulus.
WHICH SPECIES CAN BE RECOGNIZED?
General Considerations
Some sequences of clones belonging to a single specimen,
such as C196 (C. pachyderma) or C170 (C. lobatulus), show
variations in SSU rDNA. This suggests the persistence of
multiple divergent copies of SSU within one individual, as
previously observed and discussed (Holzmann and others,
1996; Pawlowski and others, 2007). On the other hand, a
good example of discrepancy between morphological and
genetic variability is the clade of Cibicidoides sp.–C.
wuellerstorfi–C. ungerianus (Fig. 7). Cibicidoides sp. 2524
and Cibicidoides sp. 5227 branch at the basis of the C.
wuellerstorfi subclade. Their SSU sequences are rather
similar to the ones of C. wuellerstorfi (less than 0.5% of
divergence between them), but analyses of the Internal
Transcribed Spacer (ITS), a much more variable region of
rDNA, show Cibicidoides sp. 2524 to be genetically distinct
from C. wuellerstorfi (unpublished data). Thus, there is
some genetic diversity among deep-sea cibicidids. This
diversity was confirmed morphologically because these
specimens were not recognized as C. wuellerstorfi when
they were visually identified. Although C. wuellerstorfi and
C. ungerianus are certainly different morphospecies, this
clade has less genetic divergence between species than do
the other clades. This shows that it is impossible to make
the distinction between species based only on an arbitrary
threshold value of sequence divergence and that morpho-
logical variability is not always less than genetic variability.
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS
Cibicides refulgens de Montfort, 1808
Cibicides refulgens is often included within Cibicidoides
lobatulus in (paleo-) ecological studies (e.g., Hageman,
1979; Verhallen, 1991) because of their morphological
similarity and the observation of intermediate forms
(Verhoeve, 1971; Hageman, 1979; van der Zwaan, 1982;
Verhallen, 1991; Jonkers and others, 2002). However, our
molecular results clearly show that C. refulgens is well-
separated from C. lobatulus (Figs. 6, 7). In addition, cryptic
speciation between Mediterranean and Antarctic popula-
tions of C. refulgens is evident. Moreover, these populations
differ in ecology: the Mediterranean specimens attach to
seaweeds and feed on diatoms (Langer, 1988), whereas the
Antarctic ones live on the shell of the scallop Adamussium
colbecki Smith, 1902 (Fig. 3a) and feed on diatoms or on
the mantle of their host (Alexander and DeLaca, 1987). On
the basis of these geographical, ecological, and molecular
differences, both populations should be considered as
separate species, and a morphological study is needed to
search for features discriminating them. Because the type
locality of C. refulgens is in the Mediterranean region, this
name will be retained for the Mediterranean species,
whereas the Antarctic one is currently referred to as
Cibicides sp.
Cibicidoides pachyderma (Rzehak), 1886 and C.
kullenbergi (Parker), 1953
Cibicidoides pachyderma has also been referred to, albeit
incorrectly, as C. pachydermus (see synonymy in the
Appendix). As explained by Stainforth (1949), the species
name pachyderma, derived from the Greek adjective paxuz
(thick) and noun to derma (the skin), is a noun in the
nominative singular standing in opposition to the generic
name (International Code of Zoological Nomenclature
[ICZN] 2000, 11.9.1.2.), and therefore remains invariable
(ICZN, 2000, 34.2.1.).
Our phylogenetic analyses show that the sampled Cibici-
doides pachyderma and C. kullenbergi belong to the same
species because they form a single clade (Figs. 6, 7). In the
concept of the Utrecht school (e.g., van der Zwaan, 1982; van
Leeuwen, 1989; van Hinsbergen and others, 2005), both
species are morphologically close, and there are intermediate
forms (see Schweizer, 2006 with descriptions and references
therein). In addition, other authors have a different concept
of C. kullenbergi (e.g., van Morkhoven and others, 1986;
Sprovieri and Hasegawa, 1990; Corliss, 1991; Holbourn and
Henderson, 2002), which is sometimes synonymized with
Cibicidoides mundulus (van Morkhoven and others, 1986;
Holbourn and Henderson, 2002). Specimens of C. kullen-
bergi from its type locality in the central part of the North
Atlantic Ocean are therefore needed for molecular analyses
to assess whether C. kullenbergi is a separate species or if it
should be synonymized with C. pachyderma. For the
specimens in the present study, we retain the senior species
name, C. pachyderma.
Cibicidoides ungerianus (d’Orbigny), 1846
Cibicidoides ungerianus appears as a well-characterized
clade (Fig. 7) distinct from C. pachyderma and C.
311
kullenbergi, contrary to the inferences of Jonkers (1984)
and van Morkhoven and others (1986). Its test is
distinguished from those of other Cibicidoides by its very
coarse porosity and transparency (Fig. 1k–l). The two
specimens collected in Bergen (F8 and F180) are more
closely related to each other than to the specimen from Oslo
Fjord. The Bergen specimens were fixed on tunicates or
algae, whereas the Oslo specimen was collected from
sediment. Supplementary sampling and ITS studies are
needed to elucidate these ecological and genetic differences.
Cibicidoides wuellerstorfi (Schwager), 1866
This deep-sea species is well-characterized both morpho-
logically, with a flat test and sigmoidal glassy sutures
(Fig. 1q), and genetically (Fig. 7). The sampled SSU
sequences are almost identical and the genetic homogeneity
of this cosmopolitan species was confirmed by analyses of
ITS sequences (Pawlowski and others, 2007).
Cibicidoides lobatulus (Walker and Jacob), 1798
It is often difficult to morphologically separate Cibici-
doides lobatulus from Cibicides refulgens, especially when
they occur in association (e.g., Mediterranean specimens
C170 to C173). The commonly used criterion is a higher test
in C. refulgens, but this is not always discriminating; for
example, F77 has a high test (Fig. 1f) although it was
genetically identified as C. lobatulus. Additionally, C.
lobatulus comprises a huge variety of morphotypes, which
were sometimes described as different subspecies or species
(Wood and Haynes, 1957; Nyholm, 1961; Cooper, 1965;
Schnitker, 1969). Some attached specimens have aberrant
shapes reflecting the substrate on which they live, while
vagile specimens have the more regular and typical
appearance.
The Cibicidoides lobatulus morphospecies forms a mono-
phyletic clade in phylogenetic analyses (Fig. 7); however,
there is a clear genetic separation between the Mediterranean
specimen (C170) and specimens from the North Atlantic.
Furthermore, slight differences were noted between the
North Atlantic SSU sequences, which can be divided in three
groups (clades a, b, c) present in different locations (Fig. 8).
Additional investigations with ITS sequences are needed to
confirm these clades, but it is already clear that C. lobatulus
includes a mosaic of genotypes, and there are at least two
geographic populations, one in the Mediterranean and the
other in the North Atlantic, that might represent separate
species. The genetic heterogeneity of C. lobatulus is probably
reflected in its wide morphological plasticity, which will
certainly assist the search for criteria to recognize the
different genotypes involved.
CONCLUSIONS
Current classifications have split the cibicidids into
different genera, families, and superfamilies despite their
similarities in morphology and ecology. Our study clearly
shows that there is no justification for assigning the
analyzed cibicidids to different superfamilies. According
to our data (Figs. 6, 7), there is no justification for
separating biconvex from planoconvex tests into Cibicides
312 SCHWEIZER AND OTHERS
and Cibicidoides, or to retain the genera Fontbotia and
Lobatula, or to transfer Cibicidoides wuellerstorfi to
Planulina. The data justifies placing all these cibicidids,
Hanzawaia, and Melonis into a single family, the Cibicidi-
dae. On the basis of phylogenetic analyses, we propose
retaining at least two cibicidid genera: Cibicides for C.
refulgens and Cibicides sp., and Cibicidoides for C.
lobatulus, C. pachyderma, C. ungerianus, and C. wueller-
storfi.
Cibicidoides ungerianus and C. wuellerstorfi are confirmed
as bona fide species by molecular analyses, whereas C.
pachyderma and the ‘‘Utrecht’’ C. kullenbergi are probably
infraspecific morphotypes. The morphospecies C. refulgens
and possibly C. lobatulus comprise several cryptic species,
and they fit the ‘‘super-species’’ concept that de Vargas and
others (2004) applied to coccolithophores and planktic
foraminifera. The morphological distinction between C.
lobatulus and C. refulgens, and between different genotypes
within both morphospecies, needs to be emended following
more detailed study. Samples from other localities around
the world are clearly needed to test the species definition in
widely distributed cibicidids and to fully answer the
questions addressed in this paper.
ACKNOWLEDGMENTS
We thank E. Alve, S. Agrenius, H. C. de Stigter, C.
Schander and the participants of the course ‘‘Biodiversity
and Ecology of Foraminifera’’ in Bergen, the crews of the R/
V Trygve Braarud, Arne Tiselius, Pelagia and Hans
Brattström for their help in sampling Scandinavian and
Portuguese material, A. Brandt, B. Hilbig, I. Schewe, E.
Fahrbach, P. Lemke, organizers and scientific leaders of
ANDEEP III and ARK XXI/1b cruises and captains and
crew of R/V Polarstern for help in collecting samples from
Arctic Ocean and Weddell Sea, G. Gudmundsson and T.
Cedhagen for help in collecting Icelandic cibicidids, S. S.
Bowser for North Atlantic and Antarctic specimens (U.S.
NSF grant ANT-0739583), J.-P. Gillig, D. Longet and F.
Sinniger for Mediterranean ones, F. Sinniger for samples
from Madagascar, E. Geslin for Chilostomella, C. Berney for
advice in molecular phylogenies, and J. Fahrni, J. Guiard, D.
Berger and the sequencing team of the Botanical Institute
from the University of Zurich for technical assistance. In
addition, we are very grateful to two anonymous reviewers
and K. Finger, the Editor of JFR, for their comments that
considerably improved the manuscript. This study was
supported by the Dutch NWO/ALW (grant 811.32.001 to
M. S.) and Swiss NSF (grants 3100A0-112645 to J. P. and
200020-109639/1 to M. S.).
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APPENDIX 1: TAXONOMIC LIST AND SYNONYMY
Cibicides refulgens de Montfort, 1808
(Fig. 1m–n)
Cibicides refulgens de Montfort, 1808, Conch, Syst., p. 123, pl. on
p. 122.
Truncatulina refulgens (de Montfort) in Brady, 1884, Rep. Voy.
‘‘Challenger’’ Zool., v. 9., p. 659, pl. 92, figs. 7–9.
Cibicides lobatulus (Walker and Jacob) refulgens type in Verhoeve,
1971, PhD Kath. Uni. Leuven, p. 62, pl. 3, fig. 4.
Cibicides lobatulus type refulgens de Montfort in van der Zwaan, 1982,
Utr. Micropal. Bull., v. 25, pl. 7, fig. 4.
in the Angola Basin: Utrecht Micropaleontological Bulletins, v. 38,
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western equatorial Atlantic: evidence from deep-sea benthic
foraminifers: Proceedings of the Ocean Drilling Program,
Scientific Results, v. 154, Government Printing Office, Washing-
ton, D.C., p. 395–431.
Received 18 March 2009
Accepted 24 August 2009
Cibicides refulgens de Montfort in Cimerman and Langer, 1991,
Mediterranean Foram., p. 70–71, pl. 75, figs. 5–9.
Cibicides refulgens de Montfort in Schweizer, 2006, Geol. Ultraiectina,
v. 261, p. 126, pl. 8, figs. a–d, k.
Cibicidoides kullenbergi (Parker), 1953
(Fig. 1i–j)
Cibicides kullenbergi Parker in Phleger and others, 1953, Swed. Deep-
Sea Exped., v. 7, p. 49, pl. 11, figs. 7–8.
Cibicides kullenbergi Parker in van der Zwaan, 1982, Utr. Micropal.
Bull., v. 25, p. 146, pl. 4, fig. 4a–c.
 MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS
Cibicides ungerianus Parker in Jonkers, 1984, Utr. Micropal. Bull., v.
31, pl. 3, fig. 4a–c.
Cibicides kullenbergi Parker in van Leeuwen, 1989, Utr. Micropal.
Bull., v. 38, p. 223, pl. 9, figs. 1–3.
Cibicidoides kullenbergi (Parker) in Corliss, 1991, Mar. Micropal, v. 17,
pl. 1, figs. 6, 8–9.
Cibicides kullenbergi Parker in Gupta, 1994, Micropal., v. 40, pl. 5,
fig. 5.
Cibicides kullenbergi Parker in den Dulk, 2000, Geol. Ultraiectina, v.
188, pl. 6, fig. 4a–c (non 5a–b).
Cibicides kullenbergi Parker in Kouwenhoven, 2000, Geol. Ultraiectina,
v. 186, pl. 1, fig. 4a–c.
Cibicidoides mundulus (Brady, Parker and Jones) in Holbourn and
Henderson, 2002, Paleont. Electron., v. 4, p. 19, fig. 4, 1–9.
Cibicides kullenbergi Parker in Schweizer, 2006, Geol. Ultraiectina, v.
261, p. 124, pl. 4, figs. a–m.
Cibicidoides lobatulus (Walker and Jacob), 1798
(Fig. 1a–h)
Nautilus lobatulus Walker and Jacob in Kanmacher, 1798, Adam’s Ess.
Micr., p. 642, pl. 14, fig. 36.
Truncatulina lobatula (Walker and Jacob) in Brady, 1884, Rep. Voy.
‘‘Challenger’’ Zool., v. 9., p. 660, pl. 92, fig. 10; pl. 93, fig.1.
Cibicides lobatulus (Walker and Jacob) in van der Zwaan, 1982, Utr.
Micropal. Bull., v. 25, p. 146, pl. 7, figs. 1–2.
Lobatulua lobatula (Walker and Jacob) in Loeblich and Tappan, 1987,
Foram. Gen. Classif., pl. 637, figs. 10–13.
Lobatulua lobatula (Walker and Jacob) in Cimerman and Langer, 1991,
Mediterranean Foram., p. 71, pl. 75, figs. 1–4.
Cibicides lobatulus (Walker and Jacob) in Verhallen, 1991, Utr.
Micropal. Bull., v. 40, p. 128–129, pl. 15, figs. 1–2.
Cibicides lobatulus (Walker and Jacob) in Kouwenhoven, 2000, Geol.
Ultraiectina, v. 186, pl. 1, fig. 1a–c.
Cibicides lobatulus (Walker and Jacob) in Holbourn and Henderson,
2002, Paleont. Electron., v. 4, p. 16, fig. 3, 1–3.
Cibicides lobatulus (Walker and Jacob) in Schweizer, 2006, Geol.
Ultraiectina, v. 261, p. 124–125, pl. 5, figs. a–l.
Cibicidoides pachyderma (Rzehak), 1886
(Fig. 1p)
Truncatulina ungeriana (d’Orbigny) in Brady (non d’Orbigny), 1884,
Rep. Voy. ‘‘Challenger’’ Zool., v. 9., p. 664, pl. 94, fig. 9a–c.
Truncatulina pachyderma Rzehak, 1886, Verh. Naturf. Ver. Brünn, v.
24, p. 87, pl. 1, fig. 5a–c.
Cibicides pachydermus (Rzehak) in d’Onofrio, 1959, Giorn. Geol, v. 2a,
p. 180, pl. 11, fig. 12a–c.
Cibicidoides pachyderma (Rzehak) in van Morkhoven and others, 1986,
Cen. Cosmopol. Deep-Water Benth. Foram., p. 68–70, pl. 22, fig.
1a–c.
315
Cibicides pachyderma (Rzehak) in Kouwenhoven, 2000, Geol. Ultra-
iectina, v. 186, pl. 2, fig. 1a–c.
Cibicides pachyderma (Rzehak) in Schweizer, 2006, Geol. Ultraiectina,
v. 261, p. 125, pl. 6, figs. a–p.
Cibicidoides ungerianus (d’Orbigny), 1846
(Fig. 1k–l)
Rotalina ungeriana d’Orbigny, 1846, Foram. Foss. Bass. Tert. Vienne,
p. 157, pl. 8, figs. 16–18.
Truncatulina ungeriana (d’Orbigny) in Brady, 1884, Rep. Voy.
‘‘Challenger’’ Zool., v. 9., p. 644, pl. 94, fig. 9.
Cibicides ungerianus (d’Orbigny) in Verdenius, 1970, Utr. Micropal.
Bull., v. 3, pl. 6, fig. 1.
Cibicides ungerianus (d’Orbigny) in Verhoeve, 1971, Ph.D. Diss. Kath.
Uni. Leuven, p. 65, pl. 3, fig. 6a–c.
Cibicides ungerianus (d’Orbigny) in van der Zwaan, 1982, Utr.
Micropal. Bull., v. 25, p. 147, pl. 6, fig. 2a–b.
Cibicides ungerianus (d’Orbigny) in Jonkers, 1984, Utr. Micropal. Bull.,
v. 31, p. 128–129, pl. 3, figs. 1–4 (rem. figs. 2–4 not typical).
Cibicides ungerianus (d’Orbigny) in Verhallen, 1991, Utr. Micropal.
Bull., v. 40, p. 129, pl. 16, figs. 5–9.
Cibicides ungerianus (d’Orbigny) in Kouwenhoven, 2000, Geol.
Ultraiectina, v. 186, pl. 1, fig. 2a–c.
Cibicides ungerianus (d’Orbigny) in Schweizer, 2006, Geol. Ultraiectina,
v. 261, p. 127, pl. 10, figs. a–m.
Cibicidoides wuellerstorfi (Schwager), 1866
(Fig. 1q)
Anomalina wuellerstorfi Schwager, 1866, Kar Nicobar, Novara Exped.,
Geol Pt., v. 2, p. 258, pl. 7, figs. 105, 107.
Truncatulina wuellerstorfi (Schwager) in Brady, 1884, Rep. Voy.
‘‘Challenger’’ Zool., v. 9., p. 662, pl. 93, fig. 9.
Planulina wuellerstorfi (Schwager) in Phleger and others, 1953, Swed.
Deep-Sea Exped., v. 7, p. 49, pl. 11, figs. 1–2.
Fontbotia wuellerstorfi (Schwager) in Gonzalez-Donoso and Linares,
1970, Rev. Esp. Micropal., v. 2, p. 238, pl. 1, fig. 4a–c.
Planulina wuellerstorfi (Schwager) in van Morkhoven and others, 1986,
Cen. Cosmopol. Deep-Water Benth. Foram., p. 48, 50, pl. 14, figs.
1–2.
Fontbotia wuellerstorfi (Schwager) in Loeblich and Tappan, 1987,
Foram. Gen. and Classif., p. 583, pl. 634, figs. 10–12; pl. 635, figs.
1–3.
Cibicides wuellerstorfi (Schwager) in Sen Gupta, 1989, J. Pal., v. 63,
p. 706, figs. 1–3.
Cibicides wuellerstorfi (Schwager) in Kouwenhoven, 2000, Geol.
Ultraiectina, v. 186, pl. 2, fig. 3a–c.
Planulina wuellerstorfi (Schwager) in Holbourn and Henderson, 2002,
Paleont. Electron., v. 4, p. 25, fig. 5, 6–8.
Cibicides wuellerstorfi (Schwager) in Schweizer, 2006, Geol. Ultra-
iectina, v. 261, p. 127–128, pl. 11, figs. a–l.