• Aucun résultat trouvé

Molecular phylogeny of common cibicidids and related rotaliida (foraminifera) based on small subunit rDNA sequences

N/A
N/A
Protected

Academic year: 2022

Partager "Molecular phylogeny of common cibicidids and related rotaliida (foraminifera) based on small subunit rDNA sequences"

Copied!
16
0
0

Texte intégral

(1)

MOLECULAR PHYLOGENY OF COMMON CIBICIDIDS AND RELATED ROTALIIDA (FORAMINIFERA) BASED ON SMALL SUBUNIT

R

DNA SEQUENCES

MAGALISCHWEIZER1,2,4, JANPAWLOWSKI3, TANJA KOUWENHOVEN2ANDBERT VAN DERZWAAN2 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 planoconvexCibicides and biconvexCibicidoides, 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, andC. 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,Cibicidessp. and C. refulgensclearly 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 lobatuluspossibly comprises two genetically distinct populations, one in the Mediterranean and the other in the North Atlantic.

INTRODUCTION

IMPORTANCE OFCIBICIDIDS INECOSYSTEMS ANDPALEOECOLOGY

This study focuses on six morphospecies of cibicidids commonly found in Recent marine environments:Cibicides refulgensde Montfort, 1808,Cibicidoides kullenbergi(Park- er), 1953, C. lobatulus (Walker and Jacob), 1798, C.

pachyderma (Rzehak), 1886, C. ungerianus (d’Orbigny), 1846 andC. 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;

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, andC. ungerianusare 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 lobatulushave been recorded down to 1000 m (e.g., McCorkle and others, 1997; Holbourn and Henderson, 2002) and liveC. ungerianusare 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, asCibicidoides mundulus).Cibicidoides wuellerstorfiis 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- storfiare 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, whereasC. 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;

Scho¨nfeld, 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.

lobatulusand 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

4Correspondence author: E-mail: magali.schweizer@erdw.ethz.ch

1Geological Institute, ETHZ, Sonneggstrasse 5, 8092 Zurich, Switzerland

2Department of Earth Sciences, Utrecht University, Budapestlaan 4, 3584 CD Utrecht, The Netherlands

3Department of Zoology and Animal Biology, University of Geneva, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland

300

(2)

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 likeCibicidoides wueller- storfiandC. kullenbergiare 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 THEGENERACIBICIDESANDCIBICIDOIDES

The generaCibicidesde Montfort, 1808 andCibicidoides 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 toCibicidoides 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

FIGURE1. SEM images and light photomicrographs (i, j, m) of the studied specimens of cibicidids:a–hC. lobatulus,i, jC. kullenbergi,k, lC.

ungerianus,m, nC. refulgens,oCibicidessp. from Antarctic,pC. pachyderma,qC. wuellerstorfi. Except n and o, all pictures correspond to DNA samples. Scale bar5100mm.

(3)

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

FIGURE2. Representations of (a) water depths and (b) sediment depths at which the six studied morphospecies are commonly found: Bathymetric zones: shelf 50–200 m, slope5200–3000 m, and abyss .3000 m. (Kennett, 1982). The sediment layer interface is not clear (‘‘fluffy’’ layer represented by confetti) between+1 and21 cm. Dashed lines represent depths were the species are less abundant and less typical.

FIGURE3. SEM images of epibiotic cibicidids:aCibicidessp. fixed on a scallop shell, McMurdo Sound, Antarctica,bcibicidids fixed on a small bivalve, Svalbard,ccibicidids (mainlyC. ungerianus) fixed on a tunicate, Bergen area,dcibicidid fixed on an agglutinated foraminifer, Bergen area.

(4)

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 THECLASSIFICATION OFCIBICIDIDS

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 PseudotruncatulinaAndreae, 1884 were synonymized with it after the beginning of the 20th century.LobatulaFleming, 1828 and Heterolepa Franzenau, 1884 were also put in synonymy withCibicidesby Galloway and Wissler (1927), but later considered valid by Loeblich and Tappan (1987).

Fontbotia, created forF. wuellerstorfiby 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.Cibicidoideswas later elevated to genus rank (Loeblich and Tappan, 1955). The distinction between CibicidesandCibicidoideson 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) assignedCibicides andCibicidoides 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

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 likePlanorbulina, Hyalinea,Rupertina(Fig. 5a, b, d) andPlanorbulinellaare 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 thatCibicidesandPlanorbulina might be stages in the life cycle of a single genus. Molecular phylogenies based on partial (Schweizer and others, 2005;

Pawlowski and others, 2007; Ujiie´ 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, whereasPlanorbulina, 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 SAMPLECOLLECTION

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

FIGURE4. Terminology used to describe the cibicidid test:amorphological features;blateral form.

(5)

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,

ANDSEQUENCING

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

FIGURE5. Genera thought to be closely related morphologically or genetically to cibicidids:aPlanorbulina mediterranensis,bHyalinea balthica, cHanzawaiasp.,dRupertina stabilis,eMelonis barleeanus,fPullenia subcarinata,gChilostomella ovoidea. Scale bar5200mm.

(6)

(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.

PHYLOGENETICANALYSIS

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

TABLE1. Geographical and water depth information and GenBank accession numbers of the cibicidids sampled.

Species DNA# Locality Depth Latitude Longitude

GenBank accession number

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,

DQ205366

DQ195541, 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

Cibicidessp. 1075 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ195564

Cibicidessp. 1838 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ195566,

DQ195567

Cibicidessp. 1839 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E DQ205368 DQ195544,

DQ195565

Cibicidessp. 2068 McMurdo Sound, Antarctica ,30 m 77u359S 163u329E AJ514839

Cibicidoides kullenbergi C86 Nazare´ Canyon, Portugal 338 m 39u399N 09u159W DQ408652

Cibicidoides kullenbergi C87 Nazare´ 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 Nazare´ Canyon, Portugal 151 m 39u399N 09u179W DQ408553 DQ195553,

DQ195563

Cibicidoidessp. 2524 North Atlantic - - - DQ408651

Cibicidoidessp. 5227 Weddell Sea, Antarctica 4700 m 64u609S 43u029W FJ705900

Cibicidoidessp. 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, DQ205374

DQ195549, 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

(7)

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 withMelonisas a sister group and a weak statistical support (data not shown), or they are polyphyletic withMelonisbranching 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 (Blu¨mel 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 Melonisat 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 ungerianusandC. wuellerstorfiare closely related sister groups (92% BS/1.00 PP), and this

TABLE2. 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

Buliminellasp. Madagascar 5041 FJ705909/ FJ705917

Buliminellasp. Madagascar 5096 FJ705908/ FJ705916

Cassidulina laevigata Oslo Fjord, Norway 2509 FJ705907/ FJ705915

Chilostomellasp. Bay of Biscaye, France F272 FJ705904

Epiphytic rotaliid Bergen, Norway F20 FJ705892

Epistominella exigua Weddell Sea, Antarctica 5222 FJ705897

Glabratellinasp. Mediterranean F316 FJ705895

Globobulimina turgida Oslo Fjord, Norway 3601 FJ705890

Hanzawaiasp. 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

Globocassidulinasp. 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

(8)

clade is sister toC. lobatulus(94%BS/1.00 PP). In the C.

lobatulus clade, sequences from the Mediterranean are clearly separated from the North Atlantic ones with several differentiated regions. Moreover, a close look at the

alignment shows that the North Atlantic sequences can be divided into three separate groups (Fig. 8) on the basis of the variable regions F4 and V7 (regions detailed in Schweizer and others, 2008).

FIGURE6. 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.

(9)

FIGURE7. 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 cladePullenia–Oridorsalis–Chilostomellaand bootstrap values for ML analysis and PP values for BA are indicated at the nodes.

(10)

DISCUSSION

RELATIONSHIPSBETWEENCIBICIDIDS ANDOTHERROTALIIDS

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

(Hyalinea,Planorbulinella,Planorbulina,Rupertina) belong to clade 2 (see below), whereas the cibicidids form a group in clade 3 withMelonisandHanzawaia(Fig. 6).

As the test morphology ofHanzawaiaresembles that of the cibicidids, they were previously grouped together (Haynes, 1981). The placement ofMelonis 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

FIGURE8. Alignments of diverging regions situated in F4 (a) and V7 (b) for North AtlanticC. lobatulus.

(11)

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 andMelonis(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 (exceptRupertina, 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 (possiblyNeoconor- binaor Gavelinopsis). The newly added sequence of F329, which is a trueRosalina(region s14-sB similar to published sequences), is separated from these and branches with Discorbis (Fig. 6). The new complete SSU sequence of Glabratellinaconfirms the position of the Glabratellacea in clade 2 (Schweizer, 2006, p. 26; Ujiie´ 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 ofGlabratellina(Fig. 6).

ARECIBICIDIDSMONOPHYLETIC?

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 ofMelonisandHanzawaia(Figs. 6, 7).

Three main clades of cibicidids can be distinguished with phylogenetic analyses: (1)Cibicidessp. andC. 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 betweenCibicidesandCibicidoidesbased 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 theC. ungerianusspecimens 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 morphospeciesCibicides refulgensis 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. BecauseC. refulgens is the type species of Cibicides, we propose ascribing the other cibicidid species toCibicidoides. Because the phylo- genetic analyses show that Cibicidoides lobatulus, C.

wuellerstorfi, andC. ungerianusare closely related (Figs. 6, 7), the generaLobatulaandFontbotiacan be synonymized with Cibicidoides as suggested by Galloway and Wissler (1927) and Sen Gupta (1989), respectively. Additionally, there is no reason to placeCibicidoides wuellerstorfiin the genusPlanulina, especially because of its close relationship withC. ungerianusandC. lobatulus.

WHICHSPECIESCANBERECOGNIZED? 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, showCibicidoidessp. 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. AlthoughC. wuellerstorfiand 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.

(12)

Cibicides refulgensde 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 fromC. lobatulus(Figs. 6, 7). In addition, cryptic speciation between Mediterranean and Antarctic popula- tions ofC. refulgensis 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 scallopAdamussium colbeckiSmith, 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 ofC. refulgensis in the Mediterranean region, this name will be retained for the Mediterranean species, whereas the Antarctic one is currently referred to as Cibicidessp.

Cibicidoides pachyderma(Rzehak), 1886 andC.

kullenbergi(Parker), 1953

Cibicidoides pachydermahas also been referred to, albeit incorrectly, as C. pachydermus (see synonymy in the Appendix). As explained by Stainforth (1949), the species namepachyderma, derived from the Greek adjectivepaxuz (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 sampledCibici- doides pachydermaand 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- bergifrom its type locality in the central part of the North Atlantic Ocean are therefore needed for molecular analyses to assess whetherC. kullenbergiis 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.

kullenbergi, contrary to the inferences of Jonkers (1984) and van Morkhoven and others (1986). Its test is distinguished from those of otherCibicidoides 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.

lobatuluscomprises 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.

TheCibicidoides lobatulusmorphospecies 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 thatC. 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 ofC. lobatulusis 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 intoCibicides

(13)

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, andMelonisinto 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 ungerianusandC. wuellerstorfiare confirmed as bona fide species by molecular analyses, whereas C.

pachydermaand the ‘‘Utrecht’’C. kullenbergiare probably infraspecific morphotypes. The morphospeciesC. refulgens and possibly C. lobatuluscomprise 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.

lobatulusandC. 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 Brattstro¨m 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 forChilostomella, 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.).

REFERENCES

ALEXANDER, S. P., and DELACA, T. E., 1987, Feeding adaptations of the foraminiferan Cibicides refulgens living epizoically and parasitically on the Antarctic scallop Adamussium colbecki:

Biological Bulletin, v. 173, p. 136–159.

ALMOGI-LABIN, A., SCHMIEDL, G., HEMLEBEN, C., SIMAN-TOV, R., SEGL, M., and MEISCHNER, D., 2000, The influence of the NE winter monsoon on productivity changes in the Gulf of Aden, NW Arabian Sea, during the last 530 ka as recorded by foraminifera:

Marine Micropaleontology, v. 40, p. 295–319.

ALTENBACH, A. V., and SARNTHEIN, M., 1989, Productivity record in benthic foraminifera, in Berger, W. H., Smetacek, V. S., and Wefer, G. (eds.), Productivity of the Ocean: Present and Past:

John Wiley and Sons, Chichester, p. 255–269.

BILLUPS, K., and SCHRAG, D. P., 2003, Application of benthic foraminiferal Mg/Ca ratios to questions of Cenozoic climate change: Earth and Planetary Science Letters, v. 209, p. 181–195.

BRADY, H. B., 1884, Report on the foraminifera dredged by H.M.S.

Challenger during the years 1873–1876. Reports of the Scientific Results of the Voyage of H.M.S. Challenger, 1873–1876: Zoology, v. 9, p. 1–814.

BROTZEN, F., 1936, Foraminiferen aus dem schwedischen untersten Senon von Eriksdal in Schonen: A˚ rsbok Sveriges Geologiska Underso¨kning, v. 30, p. 1–206.

CIMERMAN, F., and LANGER, M. R., 1991, Mediterranean foraminif- era, v. 30: Slovenska Akademija Znanosti in Umetnosti, Ljubljana, 118 p.

COOPER, S. C., 1965, A new morphologic variation of the foraminifer Cibicides lobatulus: Contributions from the Cushman Foundation for Foraminiferal Research, v. 16, p. 137–140.

CORLISS, B. H., 1991, Morphology and microhabitat preferences of benthic foraminifera from the Northwest Atlantic Ocean: Marine Micropaleontology, v. 17, p. 195–236.

CUSHMAN, J. A., 1928, Foraminifera: Their Classification and Economic Use: Harvard University Press, Cambridge, MA, 401 p.

———, 1931, The Foraminifera of the Atlantic Ocean, 8: Rotaliidae, Amphisteginidae, Calcarinidae, Cymbaloporettidae, Globorotalii- dae, Anomalinidae, Planorbulinidae, Rupertiidae and Homotre- midae: United States National Museum Bulletin, v. 104, p. 1–144.

DEN DULK, M., 2000, Benthic foraminiferal response to late Quaternary variations in surface water productivity and oxygen- ation in the northern Arabian Sea: Geologica Ultraiectina, v. 188, p. 1–205.

DEUTSCHCONGER, S., GREEN, H. W., II, and LIPPS, J. H., 1977, Test ultrastructure of some calcareous foraminifera: Journal of Foraminiferal Research, v. 7, p. 278–296.

D’ORBIGNY, A., 1846, Foraminife`res Fossiles du Bassin Tertiaire de Vienne (Autriche). Paris: Gide et Cie.

FONTANIER, C., JORISSEN, F. J., LICARI, L., ALEXANDRE, A., ANSCHUTZ, P., and CARBONEL, P., 2002, Live benthic foraminif- eral faunas from the Bay of Biscay: faunal density, composition and microhabitats: Deep-Sea Research I, v. 49, p. 751–785.

———, ———, CHAILLOU, G., DAVID, C., ANSCHUTZ, P., and LAFON, V., 2003, Seasonal and interannual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay: Deep- Sea Research I, v. 50, p. 457–494.

GALLOWAY, J. J., 1933, A Manual of Foraminifera: Principia Press, Bloomington, IN, 483 p.

———, and WISSLER, S. G., 1927, Pleistocene foraminifera from the Lomita quarry, Palos Verdes Hills, California: Journal of Paleontology, v. 1, p. 38–87.

GALTIER, N., GOUY, M., and GAUTIER, C., 1996, SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny: Computer Applications in the Biosciences, v. 12, p. 543–548.

GONZALEZ-DONOSO, J. M., and LINARES, D., 1970, Datos sobre los foraminiferos del Tortonense de Alcala la Real (Jaen): Revista Espan˜ola de Micropaleontologı´a, v. 2, p. 235–242.

GUINDON, S., and GASCUEL, O., 2003, A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood:

Systematic Biology, v. 52, p. 696–704.

GUPTA, A. K., 1994, Taxonomy and bathymetric distribution of Holocene deep-sea benthic foraminifera in the Indian Ocean and the Red Sea: Micropaleontology, v. 40, p. 351–367.

HAGEMAN, J., 1979, Benthic foraminiferal assemblages from Plio- Pleistocene open bay to lagoonal sediments of the western Peloponnesus (Greece): Utrecht Micropaleontological Bulletins, v. 20, p. 1–171.

HAYNES, J. R., 1981, Foraminifera: Macmillan, London, 433 p.

HOFKER, J., 1956, Foraminifera dentata: foraminifera of Santa Cruz and Thatch-Island Virginia-Archipelago, West Indies: Spolia Zoologica Musei Hauniensis, v. 15, p. 1–237.

HOLBOURN, A. E., and HENDERSON, A. S., 2002, Re-illustration and revised taxonomy for selected deep-sea benthic foraminifera:

(14)

Palaeontologia Electronica, v. 4, p. 34. 628KB; http://palaeo- electronica.org/paleo/2001-2/foram/issue2-01.htm

———, KUHNT, W., SIMO, J. A., and LI, Q., 2004, Middle Miocene isotope stratigraphy and paleoceanographic evolution of the northwest and southwest Australian margins (Wombat Plateau and Great Australian Bight): Palaeogeography, Palaeoclimatol- ogy, Palaeoecology, v. 208, p. 1–22. doi:10.1016/j.palaeo.

2004.02.003.

HOLZMANN, M., PILLER, W., and PAWLOWSKI, J., 1996, Sequence variations in the large-subunit ribosomal RNA gene ofAmmonia (Foraminifera, Protozoa) and their evolutionary implications:

Journal of Molecular Evolution, v. 43, p. 145–151.

HUELSENBECK, J. P., and RONQUIST, F., 2001, MRBayes: Bayesian inference of phylogenetic trees: Bioinformatics, v. 17, p. 754–755.

INTERNATIONALCOMMISSION ONZOOLOGICALNOMENCLATURE, 2000, International Code of Zoological Nomenclature: International Trust for Zoological Nomenclature, London, 123 p.

JONKERS, H. A., 1984, Pliocene benthonic foraminifera from homog- enous and laminated marls on Crete: Utrecht Micropaleontolog- ical Bulletins, v. 31, p. 1–180.

———, LIRIO, J. M., DELVALLE, R. A., and KELLEY, S. P., 2002, Age and environment of Miocene–Pliocene glaciomarine deposits, James Ross Island, Antarctica: Geological Magazine, v. 139, p. 577–594.

KAIHO, K., 1994, Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen levels in the modern ocean: Geology, v. 22, p. 719–722.

KENNETT, J. P., 1982, Marine Geology: Prentice Hall, Englewood Cliffs, NJ, 813 p.

KOUWENHOVEN, T. J., 2000, Survival under stress: benthic foraminif- eral patterns and Cenozoic biotic crises: Geologica Ultraiectina, v. 186, p. 1–206.

LANAVE, C., PREPARATA, G., SACCONE, C., and SERIO, G., 1984, A new method for calculating evolutionary substitution rates: Journal of Molecular Evolution, v. 20, p. 86–93.

LANGER, M., 1988, Recent epiphytic foraminifera from Vulcano (Mediterranean Sea): Revue de Pale´obiologie, v. spe´c. 2, p. 827–832.

LEAR, C. H., ELDERFIELD, H., and WILSON, P. A., 2000, Cenozoic deep-sea temperatures and global ice volume from Mg/Ca in benthic foraminiferal calcite: Science, v. 287, p. 269–272.

LICARI, L., and MACKENSEN, A., 2005, Benthic foraminifera off West Africa (1uN to 32uS): do live assemblages from the topmost sediment reliably record environmental variability?: Marine Micropaleontology, v. 55, p. 205–233.

LOEBLICH, A. R., JR., and TAPPAN, H., 1955, Revision of some Recent foraminiferal genera: Smithsonian Miscellaneous Collections, v. 128, no. 5, p. 1–37.

———, and ———, 1964, Sarcodina, Chiefly Thecamoebians and Foraminiferida,inMoore, R. C. (ed.), Treatise on Invertebrate Paleontology, New York, Geological Society of America/Univer- sity of Kansas, 900 p.

———, and ——— , 1987, Foraminiferal Genera and Their Classification: Van Nostrand Reinhold, New York, 970 p.

———, and ——— , 1992, Present status of foraminiferal classification,inTakayanagi, Y., and Saito, T. (eds.), Studies in Benthic Foraminifera. Proceedings of the Fourth International Symposium on Benthic Foraminifera, Sendai, 1990. Tokai University Press, Tokyo, p. 93–102.

LOHMANN, G. P., 1978, Abyssal benthonic foraminifera as hydro- graphic indicators in the western South Atlantic Ocean: Journal of Foraminiferal Research, v. 8, p. 6–34.

LUTZE, G. F., and THIEL, H., 1989, Epibenthic foraminifera from elevated microhabitats: Cibicidoides wuellerstorfi and Planulina ariminensis: Journal of Foraminiferal Research, v. 19, p. 153–158.

MACKENSEN, A., HUBBERTEN, H.-W., BICKERT, T., FISCHER, G., and FU¨ TTERER, D. K., 1993, Thed13C in benthic for a foraminiferal tests ofFontbotia wuellerstorfi(Schwager) relative to thed13C of dissolved inorganic carbon in southern ocean deep water:

implications for glacial ocean circulation models: Paleoceanogra- phy, v. 8, p. 587–610.

MCCORKLE, D. C., CORLISS, B. H., and FARNHAM, C. A., 1997, Vertical distributions and stable isotopic compositions of live (stained) benthic foraminifera from the North Carolina and California continental margins: Deep-Sea Research I, v. 44, p. 983–1024.

MEAD, G. A., 1985, Recent benthic foraminifera in the polar front region of the Southwest Atlantic: Micropaleontology, v. 1, p. 221–248.

MIAO, Q., and THUNELL, R. C., 1993, Recent deep-sea benthic foraminiferal distributions in the South China and Sulu seas:

Marine Micropaleontology, v. 22, p. 1–32.

MONTFORT, P. D.DE, 1808, Conchyliologie Syste´matique et Classifi- cation Me´thodique des Coquilles, 1. Paris: F. Schoell.

MURRAY, J. W., 1971, An Atlas of British Recent Foraminiferids:

Heinemann Educational Books, London, 244 p.

———, 1991, Ecology and Paleoecology of Benthic Foraminifera.

Harlow: Longman, 397 p.

NYHOLM, K.-G., 1961, Morphogenesis and biology of the foraminifer Cibicides lobatulus: Zoologiska Bidrag Fran Uppsala, v. 33, p. 157–196.

ONOFRIO, S. D’, 1959, Foraminifera di una carota sottomarina del medio Adriatico: Giornale di Geologia. Annali del Museo Geologico di Bologna, v. 2a, 27 (1956–1957), p. 147–194.

PAWLOWSKI, J., 2000, Introduction to the molecular systematics of foraminifera: Micropaleontology, v. 46, suppl. 1, p. 1–12.

———, FAHRNI, J., LECROQ, B., LONGET, D., CORNELIUS, N., EXCOFFIER, L., CEDHAGEN, T., and GOODAY, A. J., 2007, Bipolar gene flow in deep-sea benthic foraminifera: Molecular Ecology, v. 16, p. 4089–4096.

PFLUM, C. E., and FRERICHS, W. E., 1976, Gulf of Mexico Deep-Water Foraminifers: Cushman Foundation for Foraminiferal Research, Special Publication 14, p. 1–125.

PHLEGER, F. B., PARKER, F. L., and PEIRSON, J. F., 1953, North Atlantic foraminifera: Reports of the Swedish Deep-Sea Expedi- tion, v. 7, p. 1–122.

POSADA, D., and CRANDALL, K. A., 1998, MODELTEST: testing the model of DNA: Bioinformatics, v. 14, p. 817–818.

RATHBURN, A. E., CORLISS, B. H., TAPPA, K. D., and LOHMANN, K. C., 1996, Comparison of the ecology and stable isotopic composition of living (stained) benthic foraminifera from the Sulu and South China seas: Deep-Sea Research I, v. 43, p. 1617–1646.

———, and DE DECKKER, P., 1997, Magnesium and strontium compositions of Recent benthic foraminifera from the Coral Sea, Australia and Prydz Bay, Antarctica: Marine Micropaleon- tology, v. 32, p. 231–248.

REISS, Z., 1958, Classification of lamellar foraminifera: Micropaleon- tology, v. 4, p. 51–70.

REVETS, S. A., 1996, The Generic Revision of the Anomalinidae, Alabaminidae, Cancrisidae and Gavelinellidae: Cushman Founda- tion for Foraminiferal Research, Special Publication 34, p. 57–113.

RODRIGUEZ, F., OLIVER, J. F., MARTIN, A., and MEDINA, J. R., 1990, The general stochastic model of nucleotide substitution: Journal of Theoretical Biology, v. 142, p. 485–501.

RZEHAK, A., 1886, Die Foraminiferenfauna der Neogenformation der Umgebung von Ma¨hr-Ostrau: Verhandlungen des Naturforschen- den Vereins in Bru¨nn, v. 24, p. 77–126.

SCHMIEDL, G., PFEILSTICKER, M., HEMLEBEN, C., and MACKENSEN, A., 2004, Environmental and biological effects on the stable isotope composition of Recent deep-sea benthic foraminifera from the Mediterranean Sea: Marine Micropaleontology, v. 51, p. 129–152.

SCHNITKER, D., 1969, Cibicides, Caribeanella and the polyphyletic origin ofPlanorbulina: Contributions from the Cushman Foun- dation for Foraminiferal Research, v. 20, p. 67–69.

SCHO¨ NFELD, J., 2002, A new benthic foraminiferal proxy for near- bottom current velocities in the Gulf of Cadiz, northeastern Atlantic Ocean: Deep-Sea Research I, v. 49, p. 1853–1875.

SCHWAGER, C., 1866, Fossile Foraminiferen von Kar Nicobar, Reise der O¨ sterreichischen Fregatte Novara um die Erde in den Jahren 1857, 1858, 1859 unter den Befehlen des Commodore B. von Wu¨llerstorf-Urbair: Geologischer Theil, Geologische Beobach- tung, v. 2, p. 187–268.

SCHWEIZER, M., 2006, Evolution and molecular phylogeny ofCibicides andUvigerina(Rotaliida, foraminifera): Geologica Ultraiectina, v. 261, p. 1–167.

———, PAWLOWSKI, J., DUIJNSTEE, I. A. P., KOUWENHOVEN, T. J., and ZWAAN, G. J. VAN DER, 2005, Molecular phylogeny of the foraminiferal genusUvigerinabased on ribosomal DNA sequenc- es: Marine Micropaleontology, v. 57, p. 51–67.

Références

Documents relatifs

joli (jolie), pretty mauvais (mauvaise), bad nouveau (nouvelle), new petit (petite), little vieux (vieille), old.. ordinal

[r]

À l'aide d'un logiciel de géométrie dynamique, construis cette pyramide.. Tu vérifieras progressivement, à l'aide du logiciel, les résultats des

[r]

Abstract – Sequence data from the mitochondrial 16S rDNA of 34 species from 22 genera of stingless bees plus outgroup sequences from 11 species of other corbiculate bees were used

Species names written in bold designate new sequences, the other ones were taken from GenBank (accession numbers in brackets)... 3.4 and 4.7), some taxa which are only represented

Phylogenetic analysis of our data suggests that besides the genus Uvigerina, the clade of Uvigerini- dae also includes at least some members of the genera Rectuvigerina and

Together, GMYC delimitations corroborate all previous genetic type delimitations supported as genuine species using the patristic distance approach, with the exception