Journal of Foraminiferal Research, v. 42, no. 4, p. 340–344, October 2012

EMENDATION OF CIBICIDES ANTARCTICUS (SAIDOVA, 1975) BASED ON MOLECULAR, MORPHOLOGICAL, AND ECOLOGICAL DATA

MAGALI SCHWEIZER1,2,6,SAMUEL S. BOWSER3,SERGEI KORSUN4 AND JAN PAWLOWSKI5

ABSTRACT L. antarctica, and emend the species description with Shallow water Antarctic cibicidids are traditionally identified ecological and molecular data. as Cibicides refulgens or Cibicidoides lobatulus. However, a recent phylogenetic study based on SSU rDNA sequence data MATERIAL AND METHODS has demonstrated that these Antarctic cibicidids form a well- supported clade that branches sister to Mediterranean C. Scallops (Adamussium collbecki Smith) were collected in refulgens and is only distantly related to C. lobatulus. Based on Explorers Cove; McMurdo Sound, Ross Sea, Antarctica these DNA sequences, and a detailed scanning electron (Fig. 1) by SCUBA divers from 15–30-m water depth. microscopic examination of material from Explorers Cove Several of the numerous cibicidids attached to the scallop (McMurdo Sound), we place Antarctic cibicidids in a separate shells were detached with a steel needle. After cleaning with species Cibicides antarcticus (Saidova, 1975), which is emended a brush in filtered sea water, six of these specimens were here with molecular, morphological, and ecological features. 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) INTRODUCTION (Fig. 2). Shell fragments with fixed cibicidids were also Cibicidids (Cibicides de Montfort, 1808, and Cibicidoides coated and examined with the SEM (Fig. 3). Thalmann, 1939) inhabit well-oxygenated marine environ- ments with stable physico-chemical conditions, from the SYSTEMATICS shelf to the abyssal plains, usually on elevated substrates or at the water-sediment interface (Lutze and Thiel, 1989; Cibicidids are closely related to Hanzawaia Asano, 1944, and Mackensen and others, 2006; Schweizer and others, 2009). Melonis de Montfort, 1808, and all were included in the family These taxa play an important role in paleoenvironmental Cibicididae Cushman, 1927 (Schweizer and others, 2009). In the reconstructions because they are often used as proxies (e.g., traditional morphologic classification, the Cibicididae belong to for depth, temperature, or oxygen). the superfamily Planorbulinacea Schwager, 1877, within the Among the shallow-water cibicidids from Antarctica, order Delage and He´rouard, 1896 (Loeblich and planoconvex specimens are usually attributed to Cibicides Tappan, 1987; Sen Gupta, 2002). Recent phylogenetic analyses refulgens de Montfort, 1808, or Cibicidoides lobatulus (Schweizer and others, 2008) have shown, however, that the (Walker and Jacob, 1798) (e.g., Heron-Allen and Earland, Planorbulinacea were polyphyletic because the Cibicididae did 1922; Wiesner, 1931; Anderson, 1975; Osterman and not group with other investigated members of this superfamily Kellogg, 1979; Finger and Lipps, 1981; Mullineaux and such as Hyalinea Hofker, 1951, Planorbulinella Cushman, 1927, DeLaca, 1984; Alexander and DeLaca, 1987; Bernhard, or Planorbulina d’Orbigny, 1826. Therefore we prefer not to 1987; Mackensen and others, 1990; Gooday and others, attribute the Cibicididae to any superfamily until more 1996; Jonkers and others, 2002; Majewski, 2005). Recently, molecular phylogenetic data become available. a phylogenetic study of cibicidids based on Small Subunit The generic attribution of the species antarcticus to (SSU) rDNA sequences has shown that Antarctic speci- Cibicides agrees with data published in Schweizer and others mens, previously identified morphologically as Cibicides (2009). In the same article, molecular data confirmed that refulgens, are in fact a distinct species, well separated from Lobatula Fleming, 1828, and Fontbotia Gonza´lez-Donoso typical Mediterranean C. refulgens (Schweizer and others, and Linares, 1970, were synonyms of Cibicides, as suspected 2009). No name was given to this newly identified earlier by Galloway and Wissler (1927) and Sen Gupta phylospecies. However, Saidova (1975) described a new (2002). However, molecular data also showed that cibicidids species, Lobatula antarctica, for cibicidids collected on the should be grouped in at least two genera, Cibicides and Antarctic shelf. Here, we equate the morphology of Cibicidoides, that are both distinguishable by differences in specimens obtained from McMurdo Sound with those of wall-porosity diameter instead of the biconvex-planoconvex shape of the test (Schweizer and others, 2009).

1 Geological Institute, ETHZ, Sonneggstrasse 5, 8092 Zurich, Supergroup Cavalier-Smith, 2002 Switzerland Phylum d’Orbigny, 1826 2 Grant Institute of Earth Science, School of GeoSciences, Univer- sity of Edinburgh, West Mains Road, Edinburgh EH9 3JW, United Order ROTALIIDA Delage and He´rouard, 1896 Kingdom Family CIBICIDIDAE Cushman, 1927 3 Wadsworth Center, New York State Department of Health, P.O. Genus Cibicides de Montfort, 1808 Box 509, Albany, NY 12201, U.S.A. Type species: Cibicides refulgens de Montfort, 1808 4 Shirshov Institute of Oceanology, Nakhimovsky Pr. 36, Moscow Cibicides antarcticus (Saidova, 1975) 117997, Russia Figs. 2.1–2.11 5 Department of Genetics and Evolution, University of Geneva, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland Truncatulina refulgens (de Montfort). Heron-Allen and Earland, 1922, 6 Correspondence author: E-mail: [email protected] pl. 7, figs. 23, 28.

340 EMENDATION OF CIBICIDES ANTARCTICUS 341

‘‘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 for C. antarcticus and 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 (1100–1200 mm), 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 FIGURE 1. Map of Antarctica with a star identifying the sampling (Fig. 2). Her tests have flat-spiral and convex-umbilical site at Explorers Cove (77u359 S, 163u329 E). sides. She similarly reported the aperture ‘‘as a short arch with a thick lip on the umbilical side near the peripheral Cibicides refulgens de Montfort. Wiesner, 1931, p. 136, pl. 22, figs. 268, margin, then bending over the peripheral margin and going 269; Anderson, 1975, pl. 10, fig. 3; Finger and Lipps, 1981, pl. 3, fig. 1; as a wide fissure up to the base of the last chamber on the Milam and Anderson, 1981, pl. 9, fig. 5; Alexander and DeLaca, 1987, spiral side.’’ She also observed that the sutures were flat and figs. 2–6; Gazdzicki and Majewski, 2003, pl. 5, figs. 4a–c; Majewski, oblique on the spiral side to radial and slightly excavated on 2005, fig. 25, 1a–c; Schweizer, 2006, pl. 8, figs. e–j. Cibicides sp. A of Fillon, 1974, pl. 5, figs. 5–7. the umbilical side, which corresponds to our observations. Lobatula antarctica Saidova, 1975, p. 231, 232, pl. 110, fig. 3. Moreover, she described the test as somewhat irregular in Cibicides lobatulus (Walker and Jacob). Osterman and Kellogg, 1979, form with a lobulate peripheral margin. Our specimens pl. 1, figs. 1–3; Jonkers and others, 2002, figs. 12d–f. have a rather regular shape, but this discrepancy can be Cibicides antarcticus (Saidova). Mikhalevich, 1991, p. 36, pl. 1, figs. 5a–c; explained by the flatter and more uniform substrate to Mikhalevich, 2004, p. 186, pl. 4, figs. 11, 12. which the cibicidids attached. In addition, she described the Cibicides sp. of Schweizer and others, 2009, fig. 1o. wall as porous, but without specifying if the porosity was Collecting locality. Specimens were collected on scallop important or not. shells from Explorers Cove in McMurdo Sound, Ross Sea, In Cibicides, the porosity is more discrete than in Antarctica (Fig. 1), above 30-m water depth. Cibicidoides (Schweizer and others, 2009); wall pores are Specimen repository. All specimens (Fig. 2) are reposited numerous and finer, particularly on the umbilical side. at the Natural History Museum, Geneva (collection Some tests of C. antarcticus have a lower profile (e.g., MHNG GEPI 2012-01). Figs. 2.1b, 2.4b, 2.5b), explaining why some specimens were Diagnosis. Large trochospiral test with a flat spiral attributed to Cibicidoides lobatulus, which has a flattened (attachment) side, a usually high convex–conical umbilical conical shape. The chambers are sometimes slightly side, and an angular periphery. Chamber porosity rather inflated, but never as markedly as for C. lobatulus. low, particularly on the umbilical side. Aperture is an arched The test of C. antarcticus is larger than that of C. refulgens, slit bordered by a lip and situated around the peripheral a typical trait of Antarctic foraminifers (Mikhalevich, 2004), margin on the umbilical and spiral sides. Agglutinated and has a higher profile. Together with the fine wall porosity, structures formed around test periphery and pseudopodia. these morphologic characteristics clearly distinguish C. Description. Tests of C. antarcticus are trochospiral and antarcticus from other shallow-water cibicidids. planoconvex (the flat spiral side serves as attachment), Occurrence. Cibicides antarcticus is definitely known only usually with a well-developed convexity, tending to a from Recent sediments in Antarctica. conical shape and an angular periphery. Test diameter Molecular phylogeny. Six DNA sequences obtained from and height range from 372–1241 mm and 215–585 mm, four specimens of C. antarcticus were published in respectively, and wall pores are ,3 mm in diameter. The Pawlowski and others (2003) and Schweizer and others sutures are initially flush, but become depressed in the later (2009), and deposited in GenBank under the accession part of the test. The aperture is an arched slit bordered by a numbers AJ514839, DQ195564-DQ195567, and DQ195544. more-or-less marked lip, situated around the peripheral The fragment length is 1034 nucleotides with a very low margin on the umbilical side and often extended to the divergence between them (,0.3%). The guanine-cytosine spiral side (e.g., Figs. 2.1–2.5). (GC) content is 42.4%. Remarks. Saidova’s (1975) description of C. antarcticus These sequences and those of the Mediterranean sister fits rather well with our specimens. She collected the type group C. refulgens form a well-characterized Cibicides clade specimens in the Indian sector of Antarctica (station 30, (Schweizer and others, 2009, Fig. 7) that is clearly separated 65u519 S, 111u929 E), where she subsequently reported a from the Cibicidoides clade. The C. refulgens specimens we 342 SCHWEIZER AND OTHERS

FIGURE 2. 1–11. Scanning electron micrographs of Cibicides antarcticus from Explorers Cove; a 5 umbilical view, b 5 apertural view, c 5 spiral view; scale bar 5 200 mm. EMENDATION OF CIBICIDES ANTARCTICUS 343

FIGURE 3. Scanning electron micrographs of Explorers Cove Cibicides antarcticus attached to a scallop, with agglutinated tubes (a, b, c) and scar (d) left by the foraminiferal test on the scallop shell. sampled for DNA analysis come from the Gulf of Lions in tubes, and parasitism by eroding the host shell to feed on the Mediterranean Sea, west of the species’ type locality the extrapallial cavity. near Livorno, Italy (fide Ellis and Messina, 1940–1960). There are several articles reporting Antarctic cibicidids. Ecology. Cibicides antarcticus is a sessile epibenthic, Some only mention the taxonomic name (Anderson, 1975; attached to the surface of scallops and other substrates, Mackensen and others 1990), while others provide detailed such as seaweeds and glacial erratic boulders. Our description of the morphology and/or ecology: C. antarc- specimens were collected on the scallop Adamussium ticus attached to algae with agglutinated tubes (Mikhalevich, colbecki in the same location as the cibicidids described 2004), C. lobatulus attached to seaweed (Finger and Lipps, by Mullineaux and DeLaca (1984), Alexander and 1991), and C. refulgens attached to scallop shells (Mullineaux DeLaca (1987), and Gooday and others (1996). They and DeLaca, 1984; Alexander and DeLaca, 1987) or other were firmly cemented to the scallop shell (Fig. 3a), still organic and inorganic objects (Heron-Allen and Earland, visible on some detached and cleaned specimens (e.g., 1922). There is even an observation of C. lobatulus fixed to an Figs. 2.2b, 2.10b), and a shallow pit was observed on the extinct Pliocene pecten (Jonkers and others, 2002). Most of scallop shell after they were removed (Fig. 3d). These these cibicidids are probably C. antarcticus, suggesting that cibicidids build agglutinated tubes to protect their this species has a pan-Antarctic distribution. However, wider pseudopodial network (Figs. 3b, c) as described by sampling elsewhere in Antarctica is needed to determine if Heron-Allen and Earland (1922), Mullineaux and DeLaca there are indeed different species. (1984), and Alexander and DeLaca (1987). According to the latter researchers, C. antarcticus has several feeding ACKNOWLEDGMENTS strategies: grazing diatoms and bacteria at the surface of the scallop shell, suspension feeding facilitated by the We thank Valeria Mikhalevich for providing copies and enlarged pseudopodial network reinforced by agglutinated translation of Saidova’s description of C. antarcticus, and 344 SCHWEIZER AND OTHERS

Ivan Voltsky for imaging the holotype (no. 868 in Saidova’s LOEBLICH, A. R., and TAPPAN, H., 1987, Foraminiferal Genera and collection deposited at the Shirshov Institute of Oceanol- Their Classification: Van Nostrand Reinhold, New York, v. 2, 1182 p. (imprinted 1988) ogy, Moscow) and paratypes of C. antarcticus. We also LUTZE, G. F., and THIEL, H., 1989, Epibenthic foraminifera from thank Andrew Gooday and an anonymous reviewer for elevated microhabitats: Cibicidoides wuellerstorfi and Planulina helpful suggestions on the text. United States National ariminensis: Journal of Foraminiferal Research, v. 19, p. 153–158. Science Foundation grant ANT-0739583 (S.S.B.) is ac- MACKENSEN, A., GROBE, H., KUHN, G., and FU¨ TTERER, D. K., 1990, knowledged for support to obtain Explorers Cove Cibicides Benthic foraminiferal assemblages from the eastern Weddell Sea between 68 and 73uS: distribution, ecology and fossilization specimens. 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