EMENDATION OF CIBICIDES ANTARCTICUS (SAIDOVA, 1975) BASED ON MOLECULAR, MORPHOLOGICAL, AND ECOLOGICAL DATA
MAGALI SCHWEIZER1,2,6, SAMUELS. BOWSER3, SERGEIKORSUN4ANDJANPAWLOWSKI5 ABSTRACT
Shallow water Antarctic cibicidids are traditionally identified as Cibicides refulgens orCibicidoides lobatulus. However, a recent phylogenetic study based on SSU rDNA sequence data has demonstrated that these Antarctic cibicidids form a well- supported clade that branches sister to Mediterranean C.
refulgensand is only distantly related toC. lobatulus. Based on these DNA sequences, and a detailed scanning electron microscopic examination of material from Explorers Cove (McMurdo Sound), we place Antarctic cibicidids in a separate speciesCibicides antarcticus(Saidova, 1975), which is emended here with molecular, morphological, and ecological features.
INTRODUCTION
Cibicidids (Cibicidesde Montfort, 1808, andCibicidoides Thalmann, 1939) inhabit well-oxygenated marine environ- ments with stable physico-chemical conditions, from the shelf to the abyssal plains, usually on elevated substrates or at the water-sediment interface (Lutze and Thiel, 1989;
Mackensen and others, 2006; Schweizer and others, 2009).
These taxa play an important role in paleoenvironmental reconstructions because they are often used as proxies (e.g., for depth, temperature, or oxygen).
Among the shallow-water cibicidids from Antarctica, planoconvex specimens are usually attributed toCibicides refulgens de Montfort, 1808, or Cibicidoides lobatulus (Walker and Jacob, 1798) (e.g., Heron-Allen and Earland, 1922; Wiesner, 1931; Anderson, 1975; Osterman and Kellogg, 1979; Finger and Lipps, 1981; Mullineaux and DeLaca, 1984; Alexander and DeLaca, 1987; Bernhard, 1987; Mackensen and others, 1990; Gooday and others, 1996; Jonkers and others, 2002; Majewski, 2005). Recently, a phylogenetic study of cibicidids based on Small Subunit (SSU) rDNA sequences has shown that Antarctic speci- mens, previously identified morphologically as Cibicides refulgens,are in fact a distinct species, well separated from typical MediterraneanC. refulgens (Schweizer and others, 2009). No name was given to this newly identified phylospecies. However, Saidova (1975) described a new species,Lobatula antarctica, for cibicidids collected on the Antarctic shelf. Here, we equate the morphology of specimens obtained from McMurdo Sound with those of
L. antarctica, and emend the species description with ecological and molecular data.
MATERIAL AND METHODS
Scallops (Adamussium collbeckiSmith) were collected in Explorers Cove; McMurdo Sound, Ross Sea, Antarctica (Fig. 1) by SCUBA divers from 15–30-m water depth.
Several of the numerous cibicidids attached to the scallop shells were detached with a steel needle. After cleaning with a brush in filtered sea water, six of these specimens were used for DNA investigations (Schweizer and others, 2009).
Others were air dried, coated with gold, and examined with a Philips XL30 Scanning Electron Microscope (SEM) (Fig. 2). Shell fragments with fixed cibicidids were also coated and examined with the SEM (Fig. 3).
SYSTEMATICS
Cibicidids are closely related toHanzawaiaAsano, 1944, and Melonisde Montfort, 1808, and all were included in the family Cibicididae Cushman, 1927 (Schweizer and others, 2009). In the traditional morphologic classification, the Cibicididae belong to the superfamily Planorbulinacea Schwager, 1877, within the order Rotaliida Delage and He´rouard, 1896 (Loeblich and Tappan, 1987; Sen Gupta, 2002). Recent phylogenetic analyses (Schweizer and others, 2008) have shown, however, that the Planorbulinacea were polyphyletic because the Cibicididae did not group with other investigated members of this superfamily such asHyalineaHofker, 1951,PlanorbulinellaCushman, 1927, orPlanorbulina d’Orbigny, 1826. Therefore we prefer not to attribute the Cibicididae to any superfamily until more molecular phylogenetic data become available.
The generic attribution of the species antarcticus to Cibicidesagrees with data published in Schweizer and others (2009). In the same article, molecular data confirmed that Lobatula Fleming, 1828, and Fontbotia Gonza´lez-Donoso and Linares, 1970, were synonyms ofCibicides, as suspected earlier by Galloway and Wissler (1927) and Sen Gupta (2002). However, molecular data also showed that cibicidids should be grouped in at least two genera, Cibicides and Cibicidoides, that are both distinguishable by differences in wall-porosity diameter instead of the biconvex-planoconvex shape of the test (Schweizer and others, 2009).
Supergroup RHIZARIA Cavalier-Smith, 2002 Phylum FORAMINIFERA d’Orbigny, 1826 Order ROTALIIDA Delage and He´rouard, 1896
Family CIBICIDIDAE Cushman, 1927 GenusCibicidesde Montfort, 1808 Type species:Cibicides refulgensde Montfort, 1808
Cibicides antarcticus(Saidova, 1975) Figs. 2.1–2.11
Truncatulina refulgens(de Montfort). Heron-Allen and Earland, 1922, pl. 7, figs. 23, 28.
6Correspondence author: E-mail: [email protected]
1Geological Institute, ETHZ, Sonneggstrasse 5, 8092 Zurich, Switzerland
2Grant Institute of Earth Science, School of GeoSciences, Univer- sity of Edinburgh, West Mains Road, Edinburgh EH9 3JW, United Kingdom
3Wadsworth Center, New York State Department of Health, P.O.
Box 509, Albany, NY 12201, U.S.A.
4Shirshov Institute of Oceanology, Nakhimovsky Pr. 36, Moscow 117997, Russia
5Department of Genetics and Evolution, University of Geneva, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland
340
Cibicides refulgensde Montfort. Wiesner, 1931, p. 136, pl. 22, figs. 268, 269; Anderson, 1975, pl. 10, fig. 3; Finger and Lipps, 1981, pl. 3, fig. 1;
Milam and Anderson, 1981, pl. 9, fig. 5; Alexander and DeLaca, 1987, figs. 2–6; Gazdzicki and Majewski, 2003, pl. 5, figs. 4a–c; Majewski, 2005, fig. 25, 1a–c; Schweizer, 2006, pl. 8, figs. e–j.
Cibicidessp. A of Fillon, 1974, pl. 5, figs. 5–7.
Lobatula antarcticaSaidova, 1975, p. 231, 232, pl. 110, fig. 3.
Cibicides lobatulus(Walker and Jacob). Osterman and Kellogg, 1979, pl. 1, figs. 1–3; Jonkers and others, 2002, figs. 12d–f.
Cibicides antarcticus(Saidova). Mikhalevich, 1991, p. 36, pl. 1, figs. 5a–c;
Mikhalevich, 2004, p. 186, pl. 4, figs. 11, 12.
Cibicidessp. of Schweizer and others, 2009, fig. 1o.
Collecting locality. Specimens were collected on scallop shells from Explorers Cove in McMurdo Sound, Ross Sea, Antarctica (Fig. 1), above 30-m water depth.
Specimen repository.All specimens (Fig. 2) are reposited at the Natural History Museum, Geneva (collection MHNG GEPI 2012-01).
Diagnosis. Large trochospiral test with a flat spiral (attachment) side, a usually high convex–conical umbilical side, and an angular periphery. Chamber porosity rather low, particularly on the umbilical side. Aperture is an arched slit bordered by a lip and situated around the peripheral margin on the umbilical and spiral sides. Agglutinated structures formed around test periphery and pseudopodia.
Description.Tests ofC. antarcticus are trochospiral and planoconvex (the flat spiral side serves as attachment), usually with a well-developed convexity, tending to a conical shape and an angular periphery. Test diameter and height range from 372–1241 mm and 215–585 mm, respectively, and wall pores are ,3 mm in diameter. The sutures are initially flush, but become depressed in the later part of the test. The aperture is an arched slit bordered by a more-or-less marked lip, situated around the peripheral margin on the umbilical side and often extended to the spiral side (e.g., Figs. 2.1–2.5).
Remarks.Saidova’s (1975) description of C. antarcticus fits rather well with our specimens. She collected the type specimens in the Indian sector of Antarctica (station 30, 65u519 S, 111u929 E), where she subsequently reported a
‘‘Lobatula Antarctic community’’ over a depth range of 59–197 m (Saidova, 1998). The species, along with others described by Saidova (1975, Table 8), appears to be endemic because it has been reported only from Antarctic coastal waters. In a compilation of Russian studies in Antarctica, Mikhalevich (2004) estimated that .M of Antarctic species are endemic, with the proportion rising to 80% in some inner-shelf areas. The molecular results available forC. antarcticusand other species (e.g., Habura and others, 2004; Majewski and Pawlowski, 2010) confirm the presence of endemic species in Antarctica, and indicate that more attention should be paid to these Russian studies.
Like our Explorers Cove material, Saidova’s specimens have a large test (1250–1350-mm diameter). Judging from the range of heights that she reports (1100–1200mm), they also have a high profile. However, the side view of her figured specimen (Saidova, 1975, pl. 110, fig. 3) shows a lower profile, suggesting that her material encompassed a similar range of test morphologies as our specimens (Fig. 2). Her tests have flat-spiral and convex-umbilical sides. She similarly reported the aperture ‘‘as a short arch with a thick lip on the umbilical side near the peripheral margin, then bending over the peripheral margin and going as a wide fissure up to the base of the last chamber on the spiral side.’’ She also observed that the sutures were flat and oblique on the spiral side to radial and slightly excavated on the umbilical side, which corresponds to our observations.
Moreover, she described the test as somewhat irregular in form with a lobulate peripheral margin. Our specimens have a rather regular shape, but this discrepancy can be explained by the flatter and more uniform substrate to which the cibicidids attached. In addition, she described the wall as porous, but without specifying if the porosity was important or not.
In Cibicides, the porosity is more discrete than in Cibicidoides (Schweizer and others, 2009); wall pores are numerous and finer, particularly on the umbilical side.
Some tests of C. antarcticus have a lower profile (e.g., Figs. 2.1b, 2.4b, 2.5b), explaining why some specimens were attributed toCibicidoides lobatulus, which has a flattened conical shape. The chambers are sometimes slightly inflated, but never as markedly as forC. lobatulus.
The test ofC. antarcticusis larger than that ofC. refulgens, a typical trait of Antarctic foraminifers (Mikhalevich, 2004), and has a higher profile. Together with the fine wall porosity, these morphologic characteristics clearly distinguish C.
antarcticusfrom other shallow-water cibicidids.
Occurrence. Cibicides antarcticusis definitely known only from Recent sediments in Antarctica.
Molecular phylogeny.Six DNA sequences obtained from four specimens of C. antarcticus were published in Pawlowski and others (2003) and Schweizer and others (2009), and deposited in GenBank under the accession numbers AJ514839, DQ195564-DQ195567, and DQ195544.
The fragment length is 1034 nucleotides with a very low divergence between them (,0.3%). The guanine-cytosine (GC) content is 42.4%.
These sequences and those of the Mediterranean sister groupC. refulgensform a well-characterizedCibicidesclade (Schweizer and others, 2009, Fig. 7) that is clearly separated from theCibicidoidesclade. TheC. refulgensspecimens we
FIGURE1. Map of Antarctica with a star identifying the sampling site at Explorers Cove (77u359S, 163u329E).
FIGURE2. 1–11.Scanning electron micrographs ofCibicides antarcticusfrom Explorers Cove; a5umbilical view, b5apertural view, c5spiral view; scale bar5200mm.
sampled for DNA analysis come from the Gulf of Lions in the Mediterranean Sea, west of the species’ type locality near Livorno, Italy (fide Ellis and Messina, 1940–1960).
Ecology. Cibicides antarcticus is a sessile epibenthic, attached to the surface of scallops and other substrates, such as seaweeds and glacial erratic boulders. Our specimens were collected on the scallop Adamussium colbecki in the same location as the cibicidids described by Mullineaux and DeLaca (1984), Alexander and DeLaca (1987), and Gooday and others (1996). They were firmly cemented to the scallop shell (Fig. 3a), still visible on some detached and cleaned specimens (e.g., Figs. 2.2b, 2.10b), and a shallow pit was observed on the scallop shell after they were removed (Fig. 3d). These cibicidids build agglutinated tubes to protect their pseudopodial network (Figs. 3b, c) as described by Heron-Allen and Earland (1922), Mullineaux and DeLaca (1984), and Alexander and DeLaca (1987). According to the latter researchers, C. antarcticus has several feeding strategies: grazing diatoms and bacteria at the surface of the scallop shell, suspension feeding facilitated by the enlarged pseudopodial network reinforced by agglutinated
tubes, and parasitism by eroding the host shell to feed on the extrapallial cavity.
There are several articles reporting Antarctic cibicidids.
Some only mention the taxonomic name (Anderson, 1975;
Mackensen and others 1990), while others provide detailed description of the morphology and/or ecology: C. antarc- ticusattached to algae with agglutinated tubes (Mikhalevich, 2004),C. lobatulusattached to seaweed (Finger and Lipps, 1991), andC. refulgensattached to scallop shells (Mullineaux and DeLaca, 1984; Alexander and DeLaca, 1987) or other organic and inorganic objects (Heron-Allen and Earland, 1922). There is even an observation ofC. lobatulusfixed to an extinct Pliocene pecten (Jonkers and others, 2002). Most of these cibicidids are probablyC. antarcticus, suggesting that this species has a pan-Antarctic distribution. However, wider sampling elsewhere in Antarctica is needed to determine if there are indeed different species.
ACKNOWLEDGMENTS
We thank Valeria Mikhalevich for providing copies and translation of Saidova’s description ofC. antarcticus, and
FIGURE3. Scanning electron micrographs of Explorers CoveCibicides antarcticusattached to a scallop, with agglutinated tubes (a, b, c) and scar (d) left by the foraminiferal test on the scallop shell.
Ivan Voltsky for imaging the holotype (no. 868 in Saidova’s collection deposited at the Shirshov Institute of Oceanol- ogy, Moscow) and paratypes of C. antarcticus. We also thank Andrew Gooday and an anonymous reviewer for helpful suggestions on the text. United States National Science Foundation grant ANT-0739583 (S.S.B.) is ac- knowledged for support to obtain Explorers CoveCibicides specimens. This study was also supported by the Swiss NSF grants 200020-109639/2 (M.S.) and 3100A0-125372 (J.P.)
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Received 3 February 2012 Accepted 5 August 2012
