Phycologia (2006) Volume 45 (4), 465±477 Published 5 July 2006

Solisphaera gen. nov. (), a new genus from the lower photic zone

JOÈ RG BOLLMANN1*², MARA Y. C ORTEÂ S2,ANNELIES KLEIJNE3³, JETTE B. éSTERGAARD4 AND JEREMY R. YOUNG5 1Geological Institute, Sonneggstrasse 5, ETH ZuÈrich, CH-8092 Zurich, Switzerland 2Departamento de GeologõÂa Marina, Universidad AutoÂnoma de Baja California Sur, UABCS, Carretera al Sur Km. 5.5, C.P. 23080, La Paz, MeÂxico 3Department of Paleoecology and Paleoclimatology, Faculty of Earth Sciences, Vrije Universiteit, De Boelelaan NL-1985, 1081 HV Amsterdam, The Netherlands 4Department of Phycology, Biological Institute, University of Copenhagen, éster Farimagsgade 2D, DK-1353 Copenhagen K, Denmark 5Palaeontology Department, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom

J. BOLLMANN, M.Y. CORTEÂ S,A.KLEIJNE, J.B. éSTERGAARD AND J.R. YOUNG. 2006. Solisphaera gen. nov. (Prymnesiophyceae), a new coccolithophore genus from the lower photic zone. Phycologia 45: 465±477. DOI: 10.2216/05-14.1

Solisphaera gen. nov. (Prymnesiophyceae) is described from the lower photic zone of the Paci®c Ocean, the North Atlantic Ocean and the Gulf of Mexico. Differences in coccolith morphology between Solisphaera and members of Rhabdosphaer- aceae are certainly substantial enough to warrant the erection of a separate genus that should probably be categorised as incertae sedis aff. Rhabdosphaeraceae. The new genus accommodates three new species, S. emidasia sp. nov., S. blagna- censis sp. nov. and S. helianthiformis sp. nov. and the presence of a corona of process-bearing coccoliths around the cell is a key feature that unites the three species in the new genus Solisphaera, while the shape of these coronal coccoliths provides the main character for separating them at species level. A remarkable feature of this genus is the tight interlocking of the coronal coccoliths, in almost all collapsed coccospheres the circle of coronal coccoliths remains intact. This is evidently due to the presence of notches at the base of the process into which the rims of adjacent coccoliths lock. All three species are restricted to the lower photic zone in the areas studied and apparent preferences for different depth levels of S. emidasia and S. blagnacensis, as well as their nutrient and light requirements, have to be con®rmed by further analysis.

KEY WORDS: Solisphaera gen. et sp. nov, Atlantic Ocean, , Gulf of Mexico, lower photic zone, Paci®c Ocean, morphology, taxonomy

INTRODUCTION Thierstein 2001). Typically there are well-developed upper and lower photic zones, with consistently different assem- Recent morphological and genetic studies have demonstrated blages. Characteristic species of the lower photic zone include that the diversity of the coccolithophore community may be Florisphaera profunda Okada & Honjo and Gladiolithus ¯a- considerably underestimated because ®ne scale morphological bellatus (Halldal & Markali) Jordan & Chamberlain. The top variations in some species appear to be also re¯ected in ge- of the lower photic zone varies between environments, often netic variations (Bollmann 1997; Knappertsbusch et al. 1997; corresponding to the depth of the deep chlorophyll maximum SaÂez et al. 2003; Thierstein & Young 2004). In addition, the (DCM) at which the photosynthetic available radiation is 1% number of known coccolithophore species appears to be un- of that at the surface. The DCM is typically located between derestimated because of the limited number of studies focus- 80 to 120 m in the open ocean (Venrick 1973; Bienfang et al. sing on sampling in remote areas such as the subpolar regions 1984). and the central gyres, or on detailed analysis of the vertical There are only a limited number of studies focussing on distribution of coccolithophores (cf. Winter et al. 1994). the vertical community distribution which have sampled thor- The diversity of coccolithophores is highest in low latitude oughly below 100 m (e.g. Okada & Honjo 1973; Venrick oceanic surface waters and more than 120 species have been 1988; Hagino et al. 2000; CorteÂs et al. 2001; Haidar & Thier- reported (Okada & Honjo 1973; Winter et al. 1994; Hagino stein 2001). As a consequence the lower photic zone cocco- et al. 2000; Jordan et al. 2000; CorteÂs et al. 2001). In these lithophore community appears to be described incompletely, areas the coccolithophore assemblages often display depth- although some new species from the lower photic zone have related ecological zones, especially in the oligotrophic central been described during the last decade (Jordan et al. 1991; gyre environments (Okada & Honjo 1973; Winter et al. 1994; Kleijne et al. 1991; Jordan & Chamberlain 1992, 1993; Hag- Jordan & Chamberlain 1997; CorteÂs et al. 2001; Haidar & ino & Okada 1998). In the present paper, we erect a new genus, accommodating * Corresponding author ([email protected]). three new species that were found as a result of detailed sam- ² Present address: Department of Geology, University of Toronto, 22 Russel Street, Toronto, ON, Canada M5S 3B1. pling through the lower photic zone (100±200 m) in the cen- ³ Present address: Duinoord 11, 2224 CA Katwijk aan Zee, The tral equatorial Paci®c Ocean, the North Atlantic Ocean (Ca- Netherlands. nary Islands region) and the Gulf of Mexico.

465 466 Phycologia, Vol. 45 (4), 2006

MATERIAL AND METHODS 33 80 455 232 197

Field sampling No. of analysed specimens NORTH ATLANTIC OCEAN (CANARY ISLANDS REGION): Within the EC-MAST III project CANIGO, a total of 132 samples were spp. were counted F. 65% 64% analysed from several seasonal cruises (September 1995 to 45% 56% 30%

July 1998). These samples cover an east±west temperature and profunda productivity gradient along a 29ЊN transect from the African coast to La Palma (Bollmann et al. 2000; Abrantes et al. Solisphaera

2002). Water samples were collected from vertical sampling ll x x S. pro®les at 9 different water depth levels (0, 10, 25, 50, 75, 100, 125, 150, 200, 300 m) at three locations near the mooring stations LP1 (29Њ45.7ЈN, 17Њ57.3ЈW), JGOFS Time-series helianthiformis Station ESTOC (29Њ10ЈN, 15Њ30ЈW) and EBC2 (28Њ42.05ЈN, 13Њ9.03ЈW). S. 3% 9% x GULF OF MEXICO: Samples were obtained during the Octo- ber 1990 and March 1991 cruises of the R.V. GYRE. Fifteen blagnacensis stations with extended depth pro®les (12 samples, from 5 to 200 m) were studied in detail, as described by Pariente (1997). x x x S. 7% 9% EQUATORIAL PACIFIC OCEAN: The material originates from a 42% 16% 35% 1.50% 0.70% 1% spp. NOAA Spring Cruise during the EqPac Process Study as a emidasia part of the Equatorial Paci®c Ocean Climate Study/Joint Glob- al Ocean Flux Study (EPOCS/JGOFS)ofNSF/NOAA (Murray et al. 1994). Water samples for taxonomy studies were col- ND ND ND 36.56 35.46 36.42 36.26 lected from R.V. MALCOLM BALDRIDGE during Leg 3 from 35.42

Papeete, Tahiti (22 April 1992) via Balboa to Miami, USA 35.37/35.28 34.79/34.74

(24 May 1992). Most samples were collected from vertical 1 Њ

sampling pro®les (0 to 200 m) at stations along the 140 W spp. meridian from 12ЊSto10ЊN. C) Salinity

A summary of samples used in this study is given in Table Њ ND ND ( 17.58 16.99 18.3 16.2 20.6 1 and details of the samples from the Canary Island region 21.24 18.55/16.67 18.28/15.73 can be downloaded from http://www.pangaea.de. Temperature Solisphaera 2 Preparation for scanning electron microscopy (SEM) 60 75 125 150 110 175

NORTH ATLANTIC OCEAN (CANARY ISLANDS REGION): Up to 10 90/100 80/100 80/100 100/120 Sampling litres of seawater were ®ltered onto 47 mm diameter polycar- depth (m) bonate membrane ®lters using inline ®lter gaskets and a low vacuum ®ltration device. Each ®lter membrane was rinsed

with NH4±buffered distilled water (pH 8.5) immediately after ®ltration in order to remove all traces of sea salt. All mem-

branes were stored in plastic petri dishes and oven-dried at 2 May 1992 40Њ to 60ЊC for several hours. For subsequent SEM analyses 21 Sep. 1995 21 Sep. 1995 15 Nov. 1989 14 Oct. 1990 17 Mar. 1992 29 Apr. 1992 29 Apr. 1992 12 May 1992 15 May 1992 a piece of ®lter membrane was mounted on an aluminium stub W W W W W W W W W W

using double sided tape and coated with 15 nm of Gold-Pal- Њ Њ Њ Њ Њ Њ Њ Њ Њ Њ ladium or 2 nm of Platinum for subsequent analysis in various 17.85 89.97 94.60 SEMs at the ETH Zurich and EMPA [for details see Bollmann 17.85 95.56 140.05 140.02 110.01 100.00 140.00 et al. (2002)]. N N N N N S S N N N

GULF OF MEXICO: Samples were collected by vacuum ®ltra- Њ Њ Њ Њ Њ Њ Њ Њ Њ Њ tion onto 0.8±5 ␮m, 25 mm cellulose acetate ®lters. Filters 0.05 0.01 2.99 0.01 0.01 25.40 29.65 were air dried and stored in sealed Petri dishes prior to SEM 29.65 26.33 26.41 examination. Samples examined at the NHM were coated with Gold-Palladium and examined in a FEI XL 30 ®eld emission 5A SEM. 9 23 76 78 83 94 95 799 799

Preparation for transmission electron microscopy (TEM) Data on abundance and environmental parameters of samples containing Nanoplanktonic organisms (Ͻ 20 ␮m fraction) were concen- Of all North AtlanticIndicates data, that only water those samples for from the the type respective localities depths are were listed. mixed Additional before data processing; can ND, be not downloaded determined; from x, http://www.pangaea.de. present; %, relative abundance; spp., a Cruise Station no. Latitude Longitude Date 89G15 90G15 92G03 92/3 92/3 92/3 92/3 92/3 P212/2 P212/2 trated by pre®ltration (mesh size 20 ␮m) followed by gravity 1 2 Gulf of Mexico Equatorial Paci®c Ocean Table 1. North Atlantic Ocean ®ltration using a 2.0 ␮m 47 mm cellulose ®lter membrane. together. Bollmann et al.: Solisphaera gen. nov. 467

One to four litres of seawater were found to provide adequate bricantibus antihelicte dispositis constato; axibus longitudinalibus amounts of material. Organisms concentrated on top of the ad coronam parallelis; extremitatibus coccolithorum contiguorum superpositis, inter se extremitate huius in constrictionem illius ten- ®lter were gently re-suspended and subsequently centrifuged uem connexis. Coccolithi corporis sunt planolithi elliptici vel mul- in order to form a pellet of material. Whole mounts for TEM tanguli, margine ex uno circulo elementorum tangentialium tigilla- were prepared according to well-established procedures torum constato interdum instructi; valde aut leviter calcarei protu- (Moestrup & Thomsen 1980; Thomsen 1982). They were sha- sione interdum muniti. dowcast with chromium at a low angle and examined on a Small coccolithophores with monothecate, probably hemispherical Transmission Electron Microscope (TEM) at the Dept. of Phy- coccospheres; polymorphic with coronal coccoliths and two or more cology, Biological Institute, University of Copenhagen. All types of body coccoliths. The coronal coccoliths form a circular corona around the coccosphere. They are planoliths with an oblong measurements were made on dried material. base and a longitudinally-aligned protrusion, formed of small rhom- bic elements, arranged in an anticlockwise, imbricate pattern. The Classi®cation and terminology coronal coccoliths are arranged with their long-axes parallel to the corona; the ends of adjacent coronal coccoliths overlap and lock We follow the classi®cation of extant Haptophyta of Jordan into a small constriction at the base of the protrusion of the adjacent & Green (1994) and Edvardsen et al. (2000). Terminology coccolith. The body coccoliths are elliptical to polygonal planoliths; used is in accordance with Young et al. (1997) with the ad- they may have a rim constructed of a single cycle of tangential, lath-shaped elements. They are heavily or lightly-calci®ed and may dition of some new terms to describe the peculiar features of bear a protrusion. the new species: TYPE SPECIES (designated here): S. emidasia Bollmann, CorteÂs, ● hemispherical coccosphere ϭ coccosphere with two sides: Kleijne, éstergaard & Young. a domed side (or convex side) and ¯attened/planar side. ETYMOLOGY: sol ϭ sun, sphaera ϭ sphere; the collapsed coccos- ● domal-side body coccoliths ϭ body coccoliths located on phere is reminiscent of a stylized sun.

the domed side of the coccosphere. REMARKS: Only collapsed coccospheres of these species ● ϭ planar-side body coccoliths body coccoliths located on have been found and, therefore, no de®nite cell shape and cell the planar side of the coccosphere. orientation can be given. However, the disposition of the coc- ● ϭ coronal coccoliths coccoliths with a distinctive protru- coliths on the ®lters gives rather strong indications of the sion, that form a circular ring, or corona, around the coc- shape of the living cells. The collapsed coccospheres nearly cosphere. always consist of a ring of protrusion-bearing coccoliths (the coronal coccoliths) surrounding a ®eld of simpler coccoliths. However, the simpler coccoliths may be either (1) a low num- RESULTS ber of heavily-calci®ed non-overlapping planoliths, or (2) nu- merous lightly-calci®ed overlapping planoliths (Figs 1±4). While studying the vertical distribution of the coccolithophore A possible explanation for these observations is that the community from 0 to 200 m water depth in the central equa- coccospheres are hemispherical, with the lightly-calci®ed coc- torial Paci®c Ocean, the North Atlantic Ocean and the Gulf coliths occurring on the domal side and the heavily-calci®ed of Mexico three new coccolithophore species were encoun- coccoliths on the planar side. This shape of a coccosphere tered. The specimens of the three different species possess explains the smaller number of coccoliths on one side of the distinctive coccoliths, unlike those of any previously de- coccosphere and the greater overlap of the coccoliths on the scribed species and genus. Therefore, they are assigned to a other side in collapsed coccospheres. new genus, Solisphaera gen. nov. The presence of a corona In this structure, the continuous ring of interlocked coronal of process-bearing coccoliths around the cell is a key feature coccoliths around the cell may function as a girdle that sta- that unites the species in the genus Solisphaera, while the bilizes a more or less hemispherical shaped coccosphere (Fig. shape of these coronal coccoliths provides the main character 4). for separating them at species level. Solisphaera emidasia Bollmann, CorteÂs, Kleijne, Division HAPTOPHYTA Hibberd 1972 ex Edvardsen & éstergaard & Young sp. nov. Eikrem in Edvardsen et al. 2000 Figs 5±11 Class PRYMNESIOPHYCEAE Hibberd 1976; emend. ␮ Cavalier-Smith in Cavalier-Smith et al. 1996 Coccosphaerae parvae polymorphae (diametro circa 7 m) ex plan- olithis formarum trium constatae. Coccolithi coronarii coccosphaer- Order Hay 1977; emend. Young et ae annulum circumdantes, basi oblonga, protrusione plana trapezi- ϫ ␮ al. 2003 formi longitudinaliter orientata (circa 0.9 1.5 m). Coccosphaera a latere polari tholiformi visa formis duabus planolithorum ellipti- incertae sedis aff. Family RHABDOSPHAERACEAE corum leviter calcareorum (circa 1.2 ϫ 0.9 ␮m) vestita. Planolithi Haeckel 1894 hi margine tenui manifeste distincto constato ex uno circulo ele- mentorum (circa 0.05 ϫ 0.2 ␮m) tangentialium bacilliformium pler- Solisphaera Bollmann, CorteÂs, Kleijne, éstergaard & umque instructi; area centrali ex elementis trapeziformibus (circa 0.1 ϫ 0.4 ␮m) radialiter dispositis constata. Coccosphaera a latere Young gen. nov. polari plano visa planolithis ellipticis (circa 1.5 ϫ 1.0 ␮m), mul- tiangulis valde calcareis vestita. Planolithi hi margine lato constato Coccolithophori parvi coccosphaeris monothecatis probabiliter ex uno circulo elementorum tangentialium rectangularium pler- hemisphaericis, polymorphi, coccolithis et coronariis et corporis, his umque instructi, area centrali ex circulo irregulari elementorum 10± in genera duo pluriave descriptis. Coccolithi coronarii coronam cir- 14 oblongorum fere radialiter dispositorum constata. cularem circum coccosphaeram facientes; sunt planolithi, basi ob- longa protrusione longitudinali ex elementis parvis rhombicis im- Small polymorphic coccosphere (diameter c. 7 ␮m) formed of three 468 Phycologia, Vol. 45 (4), 2006

Figs 1±4. Schematic reconstruction of the coccosphere shape and orientation of Solisphaera spp. Figs 1±2. Collapsed coccospheres of Solisphaera spp. in domal-side pole view, showing the domal (`antapical') side with lightly-calci®ed body coccoliths (Fig. 1) and the planar-side (`apical') pole with heavily-calci®ed coccoliths (Fig. 2). The three new species of the genus Solisphaera are represented by the different shapes of the protrusions of the coronal coccoliths. Fig. 3. Schematic side view of a collapsed coccosphere. The larger coccoliths in the lower part of the drawing represent the heavily-calci®ed coccoliths of the planar (`apical') side. Fig. 4. Tentative reconstruction of a complete coccosphere with ¯agella in side view; the planar (`apical') side is shown as bearing the ¯agellar opening, see discussion.

types of planoliths. Coronal coccoliths form a ring around the coc- HOLOTYPE (designated here): Figs 5, 6. cosphere; they have an oblong base and a ¯at, longitudinally TYPE MATERIAL: ETH SEM stub: P212 St799 150m, ®lter sample aligned, trapezoid protrusion (size c. 0.9 ϫ 1.5 ␮m). Coccosphere collected at the type locality, 21 September 1995. Type repository: in domed-side pole view shows two types of lightly-calci®ed, ellip- Geological Institute, ETH ZuÈrich. tical planoliths (size c. 1.2 ϫ 0.9 ␮m) usually with a well-de®ned narrow rim consisting of a single cycle of tangential, rod-shaped TYPE LOCALITY: North Atlantic Ocean (29.65ЊN, 17.85ЊW, R.V. elements (size c. 0.05 ϫ 0.20 ␮m). The central area consists of c. POSEIDON Cruise P212, station 799 at a depth of 150 m). 20 trapezoid elements (size c. 0.1 ϫ 0.4 ␮m), arranged in a radial ETYMOLOGY: Referring to EMIDAS, the Electronic Microfossil Da- pattern. tabase System (http://www.emidas.ethz.ch) where this form was il- In planar-side pole view, the coccosphere shows heavily-calci®ed, lustrated ®rst, leading to our collaborative description of this new elliptical to polygonal planoliths (size c. 1.5 ϫ 1.0 ␮m) usually with species. a broad rim consisting of a single cycle of tangential, rectangular elements. The central area consists of an irregular cycle of 10±14 DISTRIBUTION: Solisphaera emidasia was con®ned to the lower pho- elongate elements (size c. 0.30±0.50 ϫ 0.10±0.30 ␮m), arranged in tic zone in the North Atlantic Ocean, the central equatorial Paci®c an approximately radial pattern. Ocean and the Gulf of Mexico (Table 1). The known ranges of Bollmann et al.: Solisphaera gen. nov. 469

temperature and salinity of this species are at present c. 15.7±21.2ЊC base (0.9±1.4 ϫ 0.6±0.9 ␮m) with a narrow rim formed by a single and 34.7±37, respectively. cycle of rod-shaped tangential elements and central plate of 10±15 radially-arranged trapezoidal elements. The protrusions are of var- REMARKS: The diameter of the collapsed coccospheres iable size, are aligned longitudinally and are rounded in lateral view. varies from 5 to 8 ␮m. The number of coronal coccoliths The planar-side heavily-calci®ed coccoliths lack protrusions and varies from 13 to 24 and their protrusions are formed of small are of two types: smaller coccoliths with an central, elevated struc- ␮ ture in distal view, formed by the protruding edges of the elements rhombic elements (size c. 0.08±0.25 m), arranged in an an- and larger coccoliths with a ¯at central area. The smaller coccoliths ticlockwise, imbricate pattern (Fig. 11). The apex of the pro- occur in the centre of the collapsed coccosphere; the larger planar trusion appears to be formed of a single row of elements (Fig. coccoliths around the edge. All heavily-calci®ed planar coccoliths 9). There are up to 13 heavily-calci®ed planar-side and 30± are elliptical to polygonal discs (c. 1.4 ϫ 1.0 ␮m) with a broad rim 50 lightly-calci®ed domal-side coccoliths. The rim elements of a single cycle of tangentially arranged rectangular elements. They have a convex central part that consists of an irregular cycle of 10± are often missing from both the lightly-calci®ed and heavily- 14 elongate radially-arranged trapezoidal elements (c. 0.30±0.50 ϫ calci®ed coccoliths, but this does not occur on all specimens 0.10±0.30 ␮m in size). and coccoliths with partial rims occur. We do not know wheth- HOLOTYPE (designated here): Fig. 12; SYNTYPE: Fig. 13. er these coccoliths represent different types of coccoliths or just variable preservation of body coccoliths. (Figs 5, 6, 8, 9). TYPE MATERIAL: ETH SEM stub: P212 St799 150m, ®lter sample collected at the type locality, 21 September 1995. Type repository: Not all coccospheres of S. emidasia show the heavily-cal- Geological Institute, ETH ZuÈrich. ci®ed planar coccoliths, which seems to be the result of the Њ Њ orientation of the coccosphere on the ®lter (Fig. 7). If, for TYPE LOCALITY: North Atlantic Ocean (29.65 N, 17.85 W, R.V. POSEIDON Cruise P212, station 799 at a depth of 150 m). example, coccoliths of the domal side of the coccosphere are lying on top, they will entirely cover the fewer coccoliths of ETYMOLOGY: Referring to ChaÃteau de Blagnac in France, the venue the ¯at side. (See also the remarks on coccosphere shape in of numerous coccolithophore workshops during the CODENET and previous coccolithophore related projects. the generic description; Figs 1±4.) When the heavily-calci®ed planoliths are visible, so in planar pole view, they are often DISTRIBUTION: Solisphaera blagnacensis was found in the lower pho- arranged in a ring along the coronal coccoliths (Fig. 5). Figure tic zone of the North Atlantic Ocean near the Canary Islands and in the central equatorial Paci®c Ocean (Table 1). Rare specimens 10 shows small elliptical unmineralised body-scales (0.17± were also observed in samples from the Western Mediterranean, 0.20 ϫ 0.10±0.13 ␮m) with a raised beaded rim. The form of Alboran Sea. At present this species has been found in water sam- the component elements of the coccoliths in SEM images sug- ples with a temperature of c. 15.7±21.2ЊC and salinity of 34.7±37. gests that they are formed of calcite and this was supported REMARKS: The number of coronal coccoliths varies between by energy-dispersive X-ray analyses which revealed the pres- 11 and 18. The rim of their protrusions appears to be formed ence of calcium carbonate in the periplast of S. emidasia. Po- by a single row of trapezoidal elements (Figs 18, 19; c. 0.15 larising light microscopy observations con®rmed this inter- ϫ 0.25 ␮m). A few heavily-calci®ed planar coccoliths (10± pretation. 14) appear to cover the planar side of the coccosphere, while Solisphaera emidasia was ®rst illustrated as Algirosphaera numerous (40±50) lightly-calci®ed domal coccoliths, each sp. nov. on EMIDAS http://www.emidas.ethz.ch, Image ID: with a small rounded protrusion of varying size cover the 443, 201, 173, 138 and subsequently as `Saturnulus emida- other, domed side of the coccosphere. sius'(nomen nudum) in Young et al. (2003), p. 61, plate 27, The most obvious difference between S. blagnacensis and ®gs 8, 11. S. emidasia is the presence of rounded protrusions on the lightly-calci®ed body coccoliths on the domal side of the coc- Solisphaera blagnacensis Bollmann sp. nov. cosphere. Additional differences are: Figs 12±21 ● The coronal coccoliths of S. blagnacensis bear a protrusion Coccosphaerae parvae (diam. circa 7.5 ␮m) formis quattuor plan- with a rounded, rather than trapezoid-shaped, pro®le and olithorum: (1) coccolithis coronariis aspectu laterali protrusione ro- are more variable in size (compare Figs 12, 14, 15 and Figs tundata instructis et (2±4) formis tribus coccolithorum corporis. 5, 7, 8). Coccolithi lateris tholiformis coccosphaerae leviter calcarei protru- ● The planar-side coccoliths have a more regular structure sionibus humilibus, basi elliptica ad oblonga (0.9±1.4 ϫ 0.6±0.9 ␮m), margine angusto ex uno circulo elementorum bacilliformium than those of S. emidasia (Figs 17, 20, 21). tangentialium constato, area centrali ex elementis 10±15 radialiter ● Planar-side coccoliths consistently occur in the centre of the dispositis trapeziformibus constanti; protrusiones magnitudine var- coccosphere whilst they have often been observed around iabiles longitudinaliter orientatae aspectu laterali rotundatae. Coc- the corona in S. emidasia, and these central planar-side coc- colithi lateris plani coccosphaerae valde calcarei sine protrusioni- bus, illorum duae formae: (1) coccolithi minores aspectu distali coliths have a low central boss. structura centrali elevata ex angulis se procurrentibus elementorum ● The coronal coccoliths and body coccoliths are much more constanti; (2) coccolithi maiores area centrali plana. In coccosphaera similar to each other in S. blagnacensis, than they are in conlapsa, coccolithi minores in centro positi, maiores circum mar- S. emidasia (compare Figs 12, 14, 15 and Figs 5, 7, 8). ginem. Omnes coccolithi lateris plani elliptici ad multanguli (circa 1.4 ϫ 1.0 ␮m), margine lato ex circulo uno elementorum tangen- Energy-dispersive X-ray analyses and polarising light mi- tialiter dispositorum rectangularium constato, area centrali convexa croscopy revealed the presence of calcium carbonate in the ex annulo irregulari elementorum 10±14 elongatorum radialiter dis- positorum trapeziformium (circa 0.3±0.5 ϫ 0.1±0.3 ␮m). periplast of S. blagnacensis. Unmineralised underlayer scales were not observed. Small coccosphere (diameter c. 7.5 ␮m) with four types of planol- iths: coronal coccoliths with a rounded protrusion in lateral view, S. blagnacensis was illustrated for the ®rst-time as Algiros- and three types of body coccoliths. The domal-side lightly-calci®ed phaera sp. nov. on EMIDAS http://www.emidas.ethz.ch, Im- coccoliths have low protrusions. They have an elliptical to oblong age ID: 270, 269 137, 136, 135 and 449 and subsequently as 470 Phycologia, Vol. 45 (4), 2006

Figs 5±11. Solisphaera emidasia sp. nov. Fig. 5. Scanning electron microscope (SEM) image of a collapsed coccosphere in planar (`apical') pole view, displaying 5 types of planoliths: coronal coccoliths [coccoliths with protrusions forming a ring around the coccosphere (cor)], lightly-calci®ed body coccoliths with (lcr) and without (lc) a rim of rod-shaped elements, and heavily-calci®ed body coccoliths with (hcr) and without (hc) such a rim. Scale bar ϭ 2 ␮m. Fig. 6. Detail of Fig. 5, showing lightly-calci®ed domal body coccoliths with and without a rim, and heavily-calci®ed planar coccoliths without a rim. Scale bar ϭ 0.5 ␮m. Fig. 7. SEM image of a collapsed coccosphere in domal (`antapical') pole view, showing coronal coccoliths and lightly-calci®ed body coccoliths. Scale bar ϭ 2 ␮m. Fig. 8. SEM image of a collapsed coccosphere in planar (`apical') pole view, showing coronal coccoliths (cor), a few heavily-calci®ed planar coccoliths and the proximal sides of domal body coccoliths. See Figs 5, 6 for abbreviations. The arrows point to the constrictions at the base of the coronal coccoliths where they interlock. Scale bar ϭ 2 ␮m. Bollmann et al.: Solisphaera gen. nov. 471

`Saturnulus blagnacensis'(nomen nudum) in Young et al. by their twisted, elongated triangular shape (Figs 22, 23, 25). (2003), p. 61, plate 27, ®gs 7, 10. The base of the coronal coccoliths appears to be more or less oblong (Fig. 23), similar to those of S. emidasia. The overall Solisphaera helianthiformis Bollmann, CorteÂs, Kleijne, structure of S. helianthiformis is similar to that of S. emidasia, éstergaard & Young sp. nov. due to the absence of process-bearing body coccoliths (Figs 5±9, 22, 24). However, the twisted triangular shape of the Figs 22±25 protrusions in S. helianthiformis provides an obvious differ- Coccosphaerae parvae polymorphae (diametro circa 8.5 ␮m) ex ence (Figs 22, 23, 25). planolithis formarum tribus constatae. Coccolithi coronarii protru- Solisphaera helianthiformis was illustrated for the ®rst-time ␮ sionibus elongatis tortis triangularibus muniti (usque ad 2.3 m lon- as `unknown' coccolithophore by Pariente (1997), her Plate 3 gis, 0.8 ␮m latis). Coccolithi lateris tholiformis leviter calcarei (cir- ca 1.4 ϫ 1.1 ␮m); sunt planolithi elliptici, margine angusto ex cir- ®g. G and subsequently as `Saturnulus helianthiformis'(no- culo uno elementorum bacilliformium tangentialium constato, area men nudum) in Young et al. (2003), p. 61, plate 27, ®gs 9, centrali ex circa 20 elementis trapeziformibus (circa 0.1 ϫ 0.4 ␮m) 12. in annulo radialiter dispositis. Coccolithi lateris plani valde calcarei Unmineralised underlayer scales were not observed and plani, elliptici ad multanguli (circa 1.5 ϫ 0.1 ␮m). neither energy-dispersive X-ray nor polarising light micros- Small, polymorphic coccosphere (c. 8.5 ␮m in diameter) formed of copy analysis could be performed because of the rarity of the three types of planoliths. Coronal coccoliths bear an elongate, twist- species. However, the appearance of the elements and the ed, triangle-shaped protrusions (up to 2.3 ␮m high ϫ 0.8 ␮m wide). The domal-side lightly-calci®ed coccoliths (c. 1.4 ϫ 1.1 ␮m) are close similarities of them in this species to those of the other elliptical planoliths with a narrow rim of a single cycle of rod- Solisphaera species lead us to predict that the coccoliths are shaped tangential elements. The central area consists of c. 20 trap- formed of calcite. ezoidal elements (c. 0.1 ϫ 0.4 ␮m), arranged in a single, radial cycle. The planar-side heavily-calci®ed coccoliths are elliptical to polygonal and planar (size c. 1.5 ϫ 1.0 ␮m). Ecology and coccolithophore community

HOLOTYPE (designated here): Figs 22±24. The most detailed ecological information on the three new TYPE MATERIAL: ETH SEM stub: P212 St799 150m, ®lter sample species is available from the Canary Island region. Solis- collected at the type locality, 21 September 1995. Type repository: phaera spp. were frequent in most samples from 75 to 200 m Geological Institute, ETH ZuÈrich. water depth and represented the second most abundant taxa Њ Њ TYPE LOCALITY: North Atlantic Ocean (29.65 N, 17.85 W, R.V. of the lower photic zone in this area with an average cell POSEIDON Cruise P212, station 799 at a depth of 150 m). density of about 800 cells lϪ1, after Florisphaera profunda ϭ ϭ ETYMOLOGY: From Latin helianthus sun¯ower, formis formed/ with about 4000 cells lϪ1 and before Gladiolithus ¯abellatus shaped, referring to the collapsed coccosphere resembling a sun- Ϫ1 ¯ower. with about 250 cells l (Figs 26±28). Although the data of the three new species were lumped together while analysing DISTRIBUTION: Solisphaera helianthiformis was found in the lower photic zone of the North Atlantic Ocean near the Canary Islands, the samples, qualitative observations have shown that S. em- the central equatorial Paci®c Ocean and in the Gulf of Mexico (Ta- idasia is the most abundant species, followed by S. blagna- ble 1). At present this species has been found in water samples with censis. In contrast, S. helianthiformis was very rare. At the a temperature of 16.2±18.3ЊC and a salinity of 34.7±37. type locality of S. blagnacensis and S. emidasia (R.V. PO- REMARKS: The number of coronal coccoliths varies between SEIDON Cruise 212 Station 799) the cell density of S. emi- Ϫ 18±28, while 30±50 lightly-calci®ed domal-side body cocco- dasia (2500 cells l 1) was three times higher than that of S. liths cover the remaining part of the coccosphere. The domal- blagnacensis at 125 m water depth. However, at 150 m water Ϫ side body coccoliths resemble the lightly-calci®ed coccoliths depth they were equally abundant (c. 1400 cells l 1, each) of Solisphaera emidasia in their shape, structure and size. In suggesting that S. emidasia is better adapted to `shallower' addition, a few lightly-calci®ed coccoliths without rims are depth levels within the lower photic zone. However, this hy- often seen. It is unclear whether these coccoliths represent pothesis has to be proven by additional analysis. another type of body coccoliths or lightly-calci®ed coccoliths Highest cell densities of up to 7500 cells lϪ1 were encoun- affected by carbonate dissolution or malformation. Heavily- tered during summer and fall cruises, which suggests a sea- calci®ed planar-side coccoliths, as observed for S. emidasia sonal distribution pattern. Solisphaera spp. occurred at 15ЊC and S. blagnacensis are clearly present in this species (see to 20ЊC, with highest cell densities between 17ЊCto19ЊC (Fig. arrow on Fig. 22). However, their ultrastructure and their dis- 29) and salinity from 36 to 37 (Fig. 30). Phosphate concen- tribution on the planar side of the coccosphere remains un- trations varied from 0 to 0.67 ␮mol lϪ1, while cells densities known because of the rareness of this species. higher than 1000 cells lϪ1 occurred only below 0.15 ␮mol lϪ1 The coronal coccoliths of S. helianthiformis can be easily phosphate (Fig. 31). Nitrate concentrations varied from 0 to distinguished from those of S. emidasia and S. blagnacensis 13 ␮mol lϪ1 nitrate and cells densities higher than 1000 cells

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Fig. 9. Transmission electron microscope (TEM) image of a collapsed coccosphere, showing coronal coccoliths, numerous lightly-calci®ed domal body coccoliths with a rim (lcr) and some heavily-calci®ed planar coccoliths with a rim (hcr); the arrow at the lower right points to the single row of elements at the apex of a coronal coccolith. Scale bar ϭ 2 ␮m. Fig. 10. TEM image of unmineralised underlayer scales (us), lightly-calci®ed coccoliths (lcr) and coronal coccoliths (cor). Scale bar ϭ 0.5 ␮m. Fig. 11. Detailed SEM image of coronal coccoliths, showing the rhombic elements of the protrusion, the manner in which they interlock, and the distal surface of the lightly-calci®ed, domal-side, rimmed body coccoliths. Scale bar ϭ 0.2 ␮m. 472 Phycologia, Vol. 45 (4), 2006

Figs 12±17. Solisphaera blagnacensis sp. nov. Fig. 12. Scanning electron microscope (SEM) image of a collapsed coccosphere in domal (`antapical') pole view, showing the ring of coronal coccoliths, lightly-calci®ed domal-side body coccoliths with a rounded protrusion (lcp) and proximal face of heavily-calci®ed planar body coccoliths with rims (hcr). The unlabelled arrows point to the oblong base of the coronal coccoliths. Scale bar ϭ 2 ␮m. Fig. 13. SEM image of a collapsed coccosphere in planar-side (`apical') pole view, showing the heavily-calci®ed non-overlapping planar-side coccoliths. The arrow points to the proximal side of a lightly-calci®ed protrusion-bearing domal-side body coccolith (lcp). Scale bar ϭ 2 ␮m. Fig. 14. SEM image of a collapsed coccosphere in domal-side (`antapical') pole view, showing the coronal coccoliths and the lightly-calci®ed domal-side body coccoliths. Scale bar ϭ 2 ␮m. Fig. 15. SEM image of a collapsed and distorted coccosphere, showing coronal coccoliths and lightly-calci®ed domal-side body coccoliths, as well as the distal face of heavily-calci®ed planar coccoliths on the right side of the coccosphere. Scale bar ϭ 2 ␮m. Bollmann et al.: Solisphaera gen. nov. 473

Figs 18±21. Solisphaera blagnacensis sp. nov. Fig. 18. Detailed scanning electron microscope (SEM) image of a coronal coccolith. The arrow points to the slightly elevated narrow rim. Scale bar ϭ 0.5 ␮m. Fig. 19. Transmission electron microscope (TEM) image of a collapsed coccosphere, showing coronal coccoliths (in lateral view) with a single cycle of trapezoidal elements along the distal margin of the protrusions (arrows). Scale bar ϭ 1 ␮m. Fig. 20. Detailed SEM image of heavily-calci®ed planar-side body coccoliths in distal view, showing a central, elevated structure, formed by the protruding edges of the elements. Scale bar ϭ 0.5 ␮m. Fig. 21. Detailed SEM image of heavily-calci®ed planar-side body coccoliths in distal view and an underlayer of lightly-calci®ed coccoliths apparently with the proximal expression of the protrusion (arrowed). Scale bar ϭ 2 ␮m. lϪ1 occurred only below a concentration of 1.4 ␮mol lϪ1 nitrate the equatorial Paci®c Ocean was made using TEM replicas of (Fig. 32). pre®ltered sample material. Therefore, the results are dif®cult During the Gulf of Mexico study Solisphaera spp. was only to compare with the results obtained from ®lter samples an- present as a rare component of the assemblages (Ͻ 1% of the alysed with the SEM. Nevertheless, in 7 out of 14 samples total assemblage, see also Pariente 1997). The samples con- from the middle and lower photic zone of the Paci®c Ocean, taining Solisphaera spp. were all from the lower photic zone, Solisphaera spp. were found, while 5 samples yielded a suf- where the assemblages were dominated by Florisphaera pro- ®cient number of cells (Ͼ 30) to calculate the relative abun- funda, (Lohmann) Hay & Mohler and Gla- dance of coccolithophore species. From these analyses it is diolithus ¯abellatus (Pariente 1997). evident that S. emidasia, Florisphaera profunda and Gladiol- Abundance analysis of Solisphaera spp. in samples from ithus ¯abellatus were by far the most abundant coccolitho-

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Fig. 16. Detailed SEM image, showing coronal coccoliths and lightly-calci®ed domal-side body coccoliths with a protrusion. The arrows point to the oblong base and the narrow rim of tangential elements. Scale bar ϭ 1 ␮m. Fig. 17. Detailed SEM image of heavily-calci®ed planar-side coccolith in distal view, showing the rim of rectangular elements. Scale bar ϭ 0.5 ␮m. 474 Phycologia, Vol. 45 (4), 2006

Figs 22±25. Solisphaera helianthiformis sp. nov. Fig. 22. Scanning electron microscope (SEM) image of a collapsed coccosphere with many lightly-calci®ed domal-side body coccoliths and a ring of coronal coccoliths. The prominent protrusions of the coronal coccoliths are twisted through Ϯ 45Њ relative to the domal face of the coccosphere. The arrow points to a heavily-calci®ed planar-side body coccolith. Scale bar ϭ 2 ␮m. Fig. 23. High magni®cation SEM image of Fig. 22 showing the interlocking, oblong base of the coronal coccoliths (arrows). Scale bar ϭ 1 ␮m. Fig. 24. High magni®cation SEM image of the two types of domal-side body coccoliths, namely lightly-calci®ed coccoliths with a rim (lcr) and coccoliths without rim (lc). Scale bar ϭ 1 ␮m. Fig. 25. High magni®cation transmission electron microscope (TEM) image of the twisted coronal coccolith protrusions. Scale bar ϭ 1 ␮m. phore species in the lower photic zone of these Paci®c Ocean coccolithophore taxa, for example in many species of the fam- samples (Table 1). Each whole mount examined in the TEM ily Syracosphaeraceae or Rhabdosphaeraceae, is the occur- contained numerous complete cells, while detached coccoliths rence of a few modi®ed coccoliths surrounding the ¯agellar were scattered over the grid surface. Solisphaera blagnacensis opening (the apical or circum-¯agellar coccoliths; Young et and S. helianthiformis were much more infrequently recorded al. 1997). The number of these circum-¯agellar coccoliths is than S. emidasia, and these species always co-occurred with always much lower than the number of body coccoliths. S. emidasia. Furthermore, at the Paci®c Ocean stations Solis- This type of pattern could also be inferred from some spec- phaera spp. occurred at lower salinities (down to a salinity of imens of Solisphaera spp. where a few heavily-calci®ed coc- 34.7) than in the Atlantic Ocean. coliths are often arranged in a radial pattern on the planar side of the coccosphere (e.g., on Fig. 13). These coccoliths are located within the centre of a set of heavily-calci®ed cocco- DISCUSSION liths and they are always smaller than the planar coccoliths covering the reaming planar side of the coccosphere (Fig. 13). So far, no obvious ¯agellar opening has been observed and The smaller coccoliths (`circum-¯agellar coccoliths') may sur- therefore, the relative orientation of the cell is not known. round a ¯agellar opening and therefore, the planar side of the However, there are some indications for the presence of a coccosphere may represent the apical side of the coccosphere, ¯agellar opening in Solisphaera spp. A common feature in as suggested in Figure 4. Bollmann et al.: Solisphaera gen. nov. 475

Figs 26±28. Cell densities of the most abundant lower photic zone taxa in the north Atlantic (Canary Islands) region.

Figs 29±32. Cell densities of Solisphaera spp. with respect to environmental parameters (in Fig. 32 nitrates is the sum of NO2 and NO3). Environmental parameters are from Knoll et al. (1998) and Abrantes et al. (2002).

Taxonomic af®nity coccoliths. The spine-bearing coccoliths may be con®ned to the poles or distributed around the coccosphere, greatly in- Energy-dispersive X-ray analyses and polarising light micros- creasing its outer diameter. Polymorphic, varimorphic, dimor- copy revealed the presence of calcium carbonate in the peri- phic and monomorphic genera occur. The coccoliths are typ- plast of S. emidasia and S. blagnacensis. Solisphaera helian- ically disc-shaped and usually formed of three components. thiformis could not be analysed because it was too rare. How- ever, we are con®dent that all three species are coccolitho- (1) The rim is narrow and slightly elevated and constructed phores from their general morphology and structure. The of two cycles of elements; the outer rim cycle is built of sim- genus Solisphaera is morphologically distinct, and its coccol- ple non-imbricate elements, whilst the inner rim cycle ele- iths do not closely resemble those of any recent or fossil coc- ments show strong obliquity. (2) The radial cycle consists of colithophore genus. Therefore, the allocation of this genus to laths, in an equal number to the rim units, running inwards any existing higher taxa is problematic. from the rim; openings are often present between the laths. In contrast to gross coccolith morphology, coccolith ultra- (3) The lamellar cycle is constructed of numerous small ele- structure provides reliable indications of af®nity (e.g. Perch- ments with a more or less clear anticlockwise helical arrange- Nielsen 1985 a, b; Young et al. 2004). In particular base and ment that may end in a `cuneate cycle' of a few well-formed rim structures have proven consistently reliable indicators of elements. In addition, many species have specialised rhabdo- af®nity. However, in Solisphaera the relatively simple struc- liths with a distal protrusion or process in the central area. ture of the base does not offer any obvious clues of af®nity. This process consists of spirally arranged lath-shaped ele- Conversely the protrusion structure is highly distinctive and ments of the lamellar cycle. suggests an af®nity to the Rhabdosphaeraceae. The family The base of the coccoliths of the three Solisphaera species Rhabdosphaeraceae was reviewed by Kleijne (1992) and Au- apparently lacks the characteristic Rhabdosphaeraceae fea- bry (1999). The family is characterised by motile or nonmotile tures: it shows neither the rim with two cycles of elements cells, typically with both spine-bearing and non±spine-bearing nor the radial cycle of rhabdoliths. The central-area of the 476 Phycologia, Vol. 45 (4), 2006 domal-side body coccoliths consists only of a central cycle of of the samples from the type locality in the Atlantic Ocean. irregularly shaped subradial elements (Figs 6, 12, 24). Gen- Silvia Clavadetscher provided the Latin translation and Peter erally, they have a narrow rim formed of a single cycle of Zeeberg is thanked for suggestions for the Latin names. tangential elements (Figs 6, 10, 16, 22). The structure of the This study was supported by a PhD-grant, funded by the protrusion among members of Solisphaera is highly distinc- Faculty of Science, University of Copenhagen, and a travel tive, and although it shows some similarities to the coccolith grant from the Fiedler Foundation to JBé. This work is a structure of Rhabdosphaeraceae, it is very different from all contribution to the EC-MAST project CANIGO (Subproject other extant coccoliths. The detailed ultrastructure of the pro- 3, `Particle Flux and Oceanography in the Eastern Boundary trusion in Solisphaera species, with its anticlockwise imbri- Current system'), EC contract No. MAS-CT9-0060 and the cate rhombic elements, shows similarities to that of the sac- EC-TMR program CODENET, EC contract No ERB-FRMX- culiform coccoliths of Algirosphaera robusta (Lohmann) Nor- CT97-0113. The Swiss Federal Of®ce for Education ®nan- ris. However, it obviously lacks the complex internal structure cially supported JB (BBW No. 95.0355). of that species (I. Probert, personal communication). An additional similarity to Algirosphaera robusta is the presence of body scales an order of magnitude smaller than REFERENCES the coccoliths, whereas in most other coccolithophores body scales are much closer in size to the coccoliths. If Solisphaera ABRANTES F. , M EGGERS H., NAVE S., BOLLMANN J., PALMA S., SPREN- is related to the Rhabdosphaeraceae then the rhabdolith rim is GEL C., HENDERIKS J., SPIES A., SALGUEIRO E., MOITA T.&NEUER represented by the peripheral cycle of elongate elements that S. 2002. Fluxes of organisms along a productivity gradient in the is visible in some coccoliths of Solisphaera. However, the Canary Islands region (29ЊN); Implications for paleoreconstructions. radial elements are missing and the elements that form the Deep-Sea Research II 49: 3675±3705. protrusion may be comparable to the `lamellar cycle ele- AUBRY M.-P. 1999. Handbook of Cenozoic calcareous nannoplankton. ments'. Radial cycle elements are also missing in all coccol- Book 5: Heliolithae (Zygoliths and Rhabdoliths). Micropaleontolo- gy Press, American Museum of Natural History. 368 pp. iths of Rhabdosphaera and in the antapical spine coccoliths BIENFANG P.K., SZYPER J.P., OKAMOTO M.Y. & NODA E.K. 1984. Tem- of . Thus, a tentative hypothesis could be that the poral and spatial variability of phytoplankton in a subtropical eco- species assigned to Solisphaera are members of Rhabdos- system. Limnology and Oceanography 29: 527±539. phaeraceae in which, as a result of size reduction, the base BOLLMANN J. 1997. Morphology and biogeography of structure has become drastically simpli®ed. However, further coccoliths in Holocene sediments. Marine Micropaleontology 29: detailed observations, especially of the arrangement of ele- 319±350. Â È ments on the proximal face of the body coccoliths, will be BOLLMANN J., CORTES M.Y., LENZ B., LLINAS O., MULLER T. & R EUTER R. 2000. Distribution of living coccolithophores North of the Ca- needed to fully describe the coccolith architecture and the fu- nary Islands: Vertical, seasonal and interannual variations. AGU ture classi®cation of this genus. Fall Meeting, San Francisco, EOS, Vol. 81, No 48, F204, November 2000. Ecology BOLLMANN J., CORTEÂ S M.Y., HAIDAR A.T., BRABEC B., CLOSE A., HOF- MANN R., PALMA S., TUPAS L. & THIERSTEIN H.R. 2002. Techniques The habitat of the three new species is the lower photic zone. for quantitative analyses of calcareous marine phytoplankton. Ma- The apparent adaptation of S. emidasia to `shallower' layers rine Micropaleontology 44: 163±185. and S. blagnacensis to `deeper' layers within the lower photic BRAND L.E. 1994. Physiological ecology of marine coccolithophores. In: Coccolithophores (Ed. by A. Winter & W.G. Siesser), pp. 39± zone as shown for the two Florisphaera profunda varieties, 47. Cambridge University Press, Cambridge. F. profunda var. elongata and F. profunda var. profunda CAVALIER-SMITH T. , A LLSOPP M.T.E.P., HAÈ UBER M.M., GOTHE G., (Quinn et al. 2005) has to be proven by additional analysis. CHAO E.E., COUCH J.A. & MAIER U.-G. 1996. 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