Deep-Sea Research I 49 (2002) 991–1005

Lucinoma kazani n. sp. (: ): evidence of a living benthic community associatedwith a coldseep in the Eastern Mediterranean Sea

C. Salasa,*, J. Woodsideb a Department of Biolog!ıa , Facultad de Ciencias, Universidad de Malaga,! 29071- Malaga! Spain b Centre for Marine Earth Sciences, Free University, De Boelelaan, 1085, 1081 HV Amsterdam, Netherlands

Received23 August 2001; accepted19 February 2002

Abstract

Lucinoma kazani, a new deep-water species of Lucinidae from the Eastern Mediterranean Basin, is described and illustrated. The material was collected in the Anaximander Mountains, between Rhodes and Cyprus, Eastern Mediterranean. The first living specimens were collected during the Dutch ANAXIPROBE project in the Kazan volcano, at a depth of 1709 m. Later, during the MEDINAUT programme, both living specimens and shells were collected from several mud volcanoes at different depths in the Anaximander Mountains. This bivalve holds symbionts in the ctenidia, as do all previously studied Lucinidae. The type of habitat of this new species is gas-saturated mud, with high levels of methane, which diffuses upwards into a low-oxygen deep-water. Therefore, we consider this as evidence of a living cold seep community in the Eastern Mediterranean Sea. r 2002 Publishedby Elsevier Science Ltd.

Keywords: Bivalve; Lucinoma; Cold seep; Anaximander mountain; Eastern Mediterranean Sea

1. Introduction releasedby warming of Mediterranean bottom- waters (Pancost et al., 2000). Moreover, massive Mudvolcanoes in the MediterraneanSea eruptions at mud volcanoes could also suddenly appear to have originatedby tectonic compression release large quantities of methane, a potent resulting in the extrusion of methane-rich sedi- greenhouse gas. ments (mudbreccias) (Cita et al., 1996; Limonov Trenches andaccretionary prisms delimit the et al., 1996; Woodside and Volgin, 1996; Wood- subduction zones, which define the edge of the side et al., 1998). This mud volcanism is of African plate today. The roughly 1500 km long particular interest, because it is known that Mediterranean Ridge is an accretionary prism of methane, storedas gas hydrates in subsurface marine sediments extending from western Greece sediments here (Woodside et al., 1998), could be to southern Turkey anddelimitedto the south by a thrust front at the southern edge of the subduction *Corresponding author. zone andto the north by the Hellenic Trench. It E-mail address: [email protected] (C. Salas). formedas a result of compressional forces

0967-0637/02/$ - see front matter r 2002 Publishedby Elsevier Science Ltd. PII: S 0967-0637(02)00010-9 992 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 generatedby the subductionof the African plate of the Dutch ANAXIPROBE project andthe beneath the Aegean plate (McKenzie, 1972; international Training Through Research pro- McClusky et al., 2000; Cita andCamerlenghi, gramme aboardthe Russian research vessel R/V 1992; MEDINAUT/MEDINETH Shipboard Gelendzhik (Woodside et al., 1997). The principal Scientific Parties, 2000). The collision of the objective of ANAXIPROBE was to determine the African andEuropean plates, with the subduction origin andsubsequent development of the Anaxi- of the oceanic part of the African plate below mander Mountains by mapping and sampling Europe causes hydrothermal vents in the Aegean them. These seamounts (Fig. 1) lie just south of Sea (Dandoet al., 1999) andcoldseeps andmud southwestern Turkey between Rhodes and Cy- volcanoes on the crest of the Mediterranean Ridge prus, andare thought to be the southwardrifted (Cita et al., 1996). geological extension of Turkey. The sampling The limestone blocks andlenses collectively strategy included the coring and dredging of ejecta groupedunder the informal name of ‘‘ Calcari a from a number of mudvolcanoes that were Lucina’’ (usually abbreviatedCAL in the paleon- discovered in 1995, as an unexpected result of a tological literature) have been recently re-inter- programme of detailed multibeam bathymetry pretedas constructions linkedto chemosynthetic (SimradEM-12D from the French research vessel processes involving CH4 andH 2S venting/seepage L’Atalante), which was also a part of the (Terzi, 1993; Terzi et al., 1994; Taviani, 1997). ANAXIPROBE project. These megafaunal communities are dominated by Two expeditions to the Eastern Mediterranean bivalves, such as large lucinids together with Sea to study the mud volcanism were carried out mytilids and vesicomyids, which occur within the within the MEDINAUT programme in the Miocene in the Apennine chain (Taviani, 1994, Anaximander Mountains, following ANAXIP- 1996; Amadesi et al., 1997; Conti and Fontana, ROBE. The first one, on the French research ship 1997). Conti andFontana (1998) also studiedthe Nadir, in November andDecember of 1998, used different settings of Lucina limestones to distin- the submersible Nautile to examine andtake site- guish, on the basis of the new fieldandcomposi- specific samples, confirming the association of tional data, between autochthonous (primary) and faults, mudvolcanoes, andmethane release. allochthonous (secondary) lucinid bearing depos- During this cruise additional shells and valves of its. Recently such a chemosynthetic environment the new species of Lucinoma were also collectedin has been discovered in the Pliocene of the Stirone the Anaximander Mountains. The second cruise River, N. Italy (Taviani et al., 1997) andthe took place in August 1999 aboardthe Russian Quaternary of the Eastern Mediterranean ‘‘Napoli R/V Professor Logachev with the objective to take Dome’’ (Corselli andBasso, 1996). Both of them cores to greater depths than those collected by the are considered deep-water cold seep communities. Nautile, together with measurement of methane in The purpose of this paper is to describe a living the water above the mudvolcanoes (MEDI- bivalve of the family Lucinidae collected from NAUT/MEDINETH ShipboardScientific Parties, deep mud volcanoes in the Anaximander Moun- 2000). tains (Eastern Mediterranean Ridge) (Fig. 1), which holds bacteriocytes with symbiotic bacteria 2.1. Geological setting in the gills. This confirms the presence of a living benthic community associatedwith a coldseep in Mudvolcanoes in the AnaximanderMountains the Eastern Mediterranean Sea. (Fig. 1) erupt a matrix-supportedbreccia, contain- ing rock clasts pluckedfrom formations lying well beneath the seafloor, andare thus a simple way of 2. Material and methods obtaining samples from the rocks forming the seamounts. The mudvolcanoes are drivenby The first samples with living material were gas andoverpressuredliquids,but it was still collected in 1996 during a combined expedition a surprise to discover active gas vents (and C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 993

Fig. 1. Location of survey area. clathrates) there, with their characteristic benthic bottom topography in the Eastern Anaximan- communities (Woodside et al., 1997, 1998). Kazan der Mountains. It has a diameter of over 2 km mudvolcano is the site where most of the material anda height of 40–50 m. The sample Anaxi- of Lucinoma sp. was collectedandthe only site at probe 234G was obtainedfrom a gravity core which living material has been found. Measured taken on Kazan andcontaining about 120 cm concentrations of methane in the water column of relatively recent mudbreccia (i.e. there was just above Kazan mudvolcano range from 0.1 to no oxidized mud breccia near the surface and 0.9 ml/l (J.L. Charlou, pers. comm., 1999). Accord- only a few centimetres of overlying pelagic ing to Pancost et al. (2000), indirect evidence for sediments). The mud breccia was highly methane oxidation derives from the widespread saturatedin gas (probably methane; studies occurrence of authigenic carbonate in mudbreccia of the gas are in progress) andcontained samples andabundant 13C-depleted carbonate many fragments of soft sediments and hard crusts at the sediment–water interface (d13C values rocks up to 7 cm in size. are as low as 95%). In addition, multiple cores (2) Faulted Ridge: FaultedRidge was originally collected during the Medineth cruise, in the assumedto be a fault escarpment with debris Eastern Mediterranean Ridge, including the Ka- flows near the base andgas seeps andmud zan mudvolcano (Pancost et al., 2000), indicate volcanic eruptions (‘fissure’ eruption) near that methane concentration increases with depth the top. Observations from Nautile during by as much as four orders of magnitude in the the 1998 MEDINAUT expedition confirmed upper 1 m of the mudbreccias. the presence of a fault escarpment with about Among the various sampling locations were the 500 m of vertical rock outcrop (out of a total following four of relevance to this paper: height of over 1000 m), a slope below the steepest upper part, andubiquitous gas seeps (1) Kazan Mud Volcano: Kazan mudvolcano lies on the cliff face andabove. The sample on the edge of a plateau in an area of rough Anaxiprobe 209D was taken in a dredge haul 994 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005

from the southern slope of the ridge. 200–300 m across at the summit. Gas hydrates Although the dredge started at the bottom were sampledfrom Kula mudvolcano during of the ridge in 1854 m of water and proceeded the 1996 ANAXIPROBE expedition of R/V up slope to a depth of 1165 m, it is likely that Gelendzhik (Woodside et al., 1998) and the the benthic community sampledwas nearer 1999 MEDINAUT sampling expedition of the top than the bottom (i.e. closer to 1200 m R/V Professor Logachev, andso were shells in depth than to 1800 m) because (a) it was not andtube worms. buried deeply in the dredged mud, (b) debris (4) Amsterdam Mud Volcano: Amsterdam is the flows down slope would make it difficult for largest mud volcano studied. It is about 3 km benthic to survive lower on the slope, in diameter and rather flat, with a relief of and(c) most of the gas seeps andthe shells are about 20 m, except for a small actively venting on upper steps in the topography according to parasitic cone on the western side, which has a observations from Nautile during the subse- diameter of about 350 m and a height of about quent MEDINAUT expedition. Moreover, 90 m. Large volumes of eruptedmaterial have along the summit of the ridge, several pock- flowed downhill to the south from Amsterdam marks andacoustic wipe-outs suggest that gas to fill a small basin with over 12 km3 of mud is escaping there. The ridge itself is interpreted breccia. Concentrations of methane in the to be fault-controlled, with gas seeps taking water column above Amsterdam are as high place along the fault at fractures in the as 13.5 ml/l and, gas hydrates were sampled outcrop or at bedding plains of the sedimen- from the central area of the mudvolcano tary rocks. Tube worms also found in dredge during the 1999 MEDINAUT expedition of 209D were identified as vestimentiferans of R/V Professor Logachev. the genus Lamellibrachia (E. Southward, pers. comm., 1996). They were attachedto a large The lucinidmaterial was collectedby differ- piece of rock with irregular holes running ent bottom sampling techniques at different through it, which were inferredto be gas locations in the Anaximander Mountains during escape structures. The rock, which incorpo- the ANAXIPROBE Programme expedition on ratedfragments of mollusc shells, was R/V Gelendzhik (Woodside et al., 1997). The main shown to be a methane-derived carbonate sampling device was a large diameter (14 cm crust at the location of active gas venting. The internal diameter) gravity corer with a length of worms were attachedat one endto the walls 6.6 m anda weight of about 1500 kg. The of the holes, andthe other endprojected secondary sampling device was a pipe dredge with about 20 cm beyondthe holes. Diagenetic a diameter of 75 cm and a length of 1 m. pyrite was present in siltstone clasts from dredge 209D, and there was also a smell of 2.2. Material examined of Lucinoma kazani n. sp. hydrogen sulphide gas from the mud and clasts. ANAXIPROBE Programme (3) Kula Mud Volcano: Several small mudvolca- St. 209D (35125.900N–30124.550Eto35127.100N– noes lie on a triangular plateau of limited 30124.610E; 1854–1165 m deep; Faulted Ridge): extension at the northern corner of the eastern One complete shell (38.4 mm length 35.0 mm Anaximander Mountains. Kula is the largest, height), selectedas holotype, in MNHN, Paris. measuring about 1600 m across andabout St. 234G (35125.730N–30133.640E; 1709 m deep; 100 m high. It is remarkably circular and Kazan MudVolcano): One live collectedspecimen dome shaped rather than conical. Observa- (37 mm length 33.4 mm height), selectedas tions from Nautile indicate that it has resumed paratype, in MNHN, Paris. Two shells (24.2 mm activity in the recent geological past after a length 23.7 mm; 33.7 mm length 29.1 mm long periodof dormancy.Recent mudflows height), both selectedas paratypes, in NMNH, are observedonly over a small area about Leiden. C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 995

MEDINAUT Programme scanning electron microscope, with LINK ANA- St. MN10 (33143.50N–241410E; 1700 m deep; LITICAL 6508 electronic microsonde and with Kazan mudvolcano): 5 living juveniles and90 LINK ANALITICAL EXL for the detection of valves. light elements andmicroanalysis. For the elemen- St. MN12 (33143.50N–241410E; 1700 m deep; tal analysis, the pieces of gills were coatedby Kazan mudvolcano): 4 juvenile shells and33 argon sputteredsilver insteadof gold,because the valves. peak generatedby goldwouldmask the sulphur St. MN9 (35127.10N–30124.40E; 1300 m deep; peak in the spectrum. FaultedRidge):1 shell and6 valves. St. MN11 (351260N–30127.50E; 1630 m deep; 3. Systematics Kula mudvolcano): 1 valve. St. MN13 (351200N–30116.50E; 2030 m deep; 3.1. Family Lucinidae Amsterdam mud volcano): 5 valves. Comparative material examined(all from Genus Lucinoma Dall, 1901 MNHN, Paris, except where otherwise stated): Type species: Lucina filosa Stimpson, 1851, by Lucinoma borealis: Palermo (Italy), coll. Lamy: original designation. 1 shell; Messina (Italy), coll. Lamy: 2 shells; The species collectedin the Anaximander Ajaccio (Corsica), coll. Jousseaume: 3 shells; Mountains is referredto the genus Lucinoma, a Portugal, Algarve, Sagres (37100.70N, 08155.00W, taxon originally introduced as subgenus of Pha- 12–17 m): several juvenile specimens; Brittany, coides Blainville 1825. Shells are usually large, Finistere," Pointe Noire: 1 shell, leg. Gofas; Ros- lentiform, concentrically lamellose or striatedand coff: 1 shell, leg. Gofas; Western Norway, Storres with periostracum. The cardinal teeth are well oilfield, 25–34 m: 11 specimens, leg. AKVAPLAN- developed, with 2a (LV) and 3b (RV) bifid; the NIVA Programme (Swedish Museum of Natural lateral teeth are obsolete or absent. The inner History, Stockholm); Azores, ‘‘Biacores’’- expedi- margin is entire, andthere is no pallial sinus. tion st. 81 (39100.50N, 28104.50W, 142 m): 1 In European waters, the genus Lucinoma is juvenile specimen and1 valve. representedby only one species L. borealis (Linne,! Lucinoma ignota Locard(= L. borealis ): Gulf of 1767), which ranges from the north of Norway Cadiz ( Southern Spain): 1 valve, syntype from (Hisaeter, 1986) to Morocco (Pasteur-Humbert, ‘‘Talisman’’ 1883 sta. 2 (361530N, 081320W, 99 m). 1962) andMauritania (Cosel, pers. comm.), and Lucinoma filosa (Stimpson, 1851): Philadelphia: into the Western Mediterranean, where it is rare 1 shell, leg. Cope; South of Newfoundland, 323– (Lamy, 1920, p. 198). There are no records from 322 m: 7 shells, leg. von Cosel. the Eastern Mediterranean even in the better surveyedareas such as the Levantine coast (Barash 2.3. Preparation for SEM observation andDanin, 1992), Greece (Zenetos, 1996), or Malta (Cachia et al., 1993). To observe the location of the bacteriocytes in the ctenidia and the bacterial morphology by 3.2. Lucinoma kazani new species (Figs. 2 and 3, scanning electron microscopy (SEM), small pieces 6–8, 12–14 and 17) of gills of L. kazani andof L. borealis were taken. The gill tissues were washedin distilledwater and Type material: Holotype: One shell (38.4 mm dehydrated through a graded ethanol series; the length 35.0 mm height), from ANAXIPROBE samples were then critical-point dried. After this, 96, St. 209D, deposited in Museum! National the pieces of gills were mountedon stubs, coated d’Histoire Naturelle, Paris, (MNHN). Paratypes: by argon-sputtered gold-palladium, to be viewed a live collectedspecimen (37 mm length 33.4 mm in the SEM andphotographed. height) from ANAXIPROBE 96, St. 234G, depo- The qualitative andquantitative compositional sitedin MNHN; two shells (24.2 mm length 23.7 analysis were carriedout in a JEOL JSM-6400 mm height; 33.7 mm length 29.1 mm height) 996 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005

Fig. 2. Lucinoma kazani n. sp., internal view of the holotype, Fig. 4. Lucinoma borealis (Linne,! 1767), internal view of a left valve. Actual length 38.4 mm. specimen from subtidal sands near Pointe du Minou, Brittany, left valve. Actual length 31 mm.

Fig. 3. Lucinoma kazani n. sp., internal view of the holotype, right valve. Actual length 38.4 mm. Fig. 5. Lucinoma borealis (Linne,! 1767), internal view of a from ANAXIPROBE 96, St. 234G, deposited in specimen from subtidal sands near Pointe du Minou, Brittany, National Museum of Natural History, Leiden. right valve. Actual length 31 mm. Type locality: Anaximander Mountains, south of southwestern Turkey, Eastern Mediterranean longer than high; inequilateral. Posterior margin Sea (35125.900N–30124.550Eto35127.100N– curved, antero-dorsal margin forming an obtuse 30124.610E; 1854–1165 m deep). angle, ventral margin gently curved. Umbos Description: Shell medium-size, convex, thick somewhat prominent directed inwards and proso- andsolid,equivalve. Outline subcircular, slightly gyrous, just in front of the vertical midline. A C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 997

Fig. 9. Lucinoma borealis (Linne,! 1767), same specimen as Figs. 4 and5, external view of the left valve. Fig. 6. Lucinoma kazani n. sp., holotype, external view of the left valve.

Fig. 10. Lucinoma borealis (Linne,! 1767), same specimen as Figs. 4 and5, dorsalview.

Fig. 7. Lucinoma kazani n. sp., holotype, dorsal view.

Fig. 11. Lucinoma borealis, prodissoconch of a juvenile from Fig. 8. Lucinoma kazani n. sp., prodissoconch of a juvenile shell Algarve. Scale bar=100 mm. from MEDINAUT expedition, Kazan mud volcano St. MN10. Scale bar=100 mm. slight and ill-defined radial depression from the Sculpture of fine andirregularly spacedcon- beginning of ligament to the postero-ventral centric lamellae, more prominent near the ventral corner and another one less defined, almost margin. Outer surface of shell white. Periostracum parallel to the anterior dorsal margin. thin, cream on the umbos, brownish-beige from 998 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005

Fig. 15. Lucinoma borealis, SEM pictures of a critical-point dried fragment of the gills, general view of the gill’s edge in transverse section. Scale bar=1 mm. Fig. 12. Lucinoma kazani n. sp., SEM pictures of a critical- point dried fragment of the gills, general view of the gill’s edge in transverse section. Scale bar=1 mm.

Fig. 16. Lucinoma borealis, SEM pictures of a critical-point Fig. 13. Lucinoma kazani n. sp., SEM pictures of a critical- dried fragment of the gills, bacteriocytes. Scale bar=10 mm. point dried fragment of the gills, several bacteriocytes. Scale bar=10 mm.

length of the anterior dorsal margin and brownish in colour. Prodissoconch semicircular, relatively large (240 mm in diameter) without particular sculpture and very eroded by the reduced environment (Fig. 8). Hinge plate relatively narrow, slightly curved. Right valve with two cardinals, the anterior (3a) simple andthe posterior (3b) bifid;one small knob-like anterior lateral (Ia); posterior lateral obsolete. Left valve with two cardinals, the anterior one (2a) bifidandthe posterior one (4b) simple; a knob-like anterior lateral (IIa), rather prominent; posterior lateral obsolete. Well delimited adductor muscle scars; the Fig. 14. Lucinoma kazani n. sp., SEM pictures of a critical- point dried fragment of the gills, an open bacteriocyte showing anterior one longer than the posterior one and the symbiotic bacteria. Scale bar=10 mm. relatively large, with the proximal part sunken in the hinge plate, under the anterior lateral; and with a rather long ventral extension, slightly diverging the middle part of the valve to the margins. from the pallial line. Posterior adductor scar Ligament external, long andsunken, reaching subelliptical in outline. Small andelliptical ante- almost to the posterior margin. Escutcheon not rior pedal muscle scar, close to the anterior front visible. Lunule well delimited, lanceolate, E2/3 the of the anterior adductor muscle scar. Pallial line C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 999 well defined and beginning near the anterior Inner margin of the valves smooth. Long andfine border of the anterior adductor scar. Inside of pallial bloodvessel impressions, crossing obliquely the shell white, with oblique scars about the the valves from the postero-dorsal to the antero- middle of the valves, and with slight ridges ventral side. reflecting the exterior depressions of the shell. Anatomy: An elongatedcylindricalfoot, with a small posterior heel, is present. Ctenidia large and thickened, composed only of the inner demibranchs. Labial palps minute. Fig. 12 (SEM level) shows a transversal section in part of the large demibranch of L. kazani with the bacteriocytes, which contain the intracellular symbionts. These can be observedin Fig. 13 as bulges set very close each other. Fig. 14 shows one open bacteriocyte, in which the intracellular symbionts (bacteria) can be observed. The size of the observedbacteria ranges between ca. 1 and 3 mm, showing different shapes, from round to elliptical forms. The qualitative andquantitative compositional analysis of some of these symbionts from different bacteriocytes (Table 1) shows a percentage of organic carbon higher than 90% and a percentage of sulphur lower than 1%, thus indicating that they are living organisms and not sulphur deposits. The symbionts are smaller than the cystine-rich granules (up to 6.5 mm) described in Codakia orbicularis by Frenkiel andMou eza. (1995). No mantle gills, either near the anterior adductor or near a mantle septum, have been observed. Mantle edge smooth along most of its extension, fusedonly a short distance anterior to the inhalant aperture. The mantle folds are blunt andbear a single row of minute papillae on each Fig. 17. Lucinoma kazani n. sp. Posterior mantle apertures of a side of the inhalant aperture; there are no papillae paratype from Kazan mudvolcano, Anaxiprobe sta.234G. aroundthe exhalant aperture (Fig. 17). The ‘‘ex- Exhalant aperture (Ea) andinhalant aperture (Ia). halant siphon’’ (according to the terminology of

Table 1 Qualitative andquantitative elemental analysis of bacteria from several bacteriocytes of the ctenidiaof Lucinoma kazani n. sp.

Elements Ba 1 Ba 2 Ba 3 Ba 4 Ba 5 Ba 6 Ba 7 Ba 8

C 93.43 96.15 93.35 95 90.8 93.95 95.45 96.46 O 5.2 2.1 5.4 3.3 7.75 3.6 2.43 1.02 Ca 0.51 0.67 0.36 0.53 0.41 1.01 0.91 1.26 Si 0.11 0.07 0.12 0.13 0.19 0.12 0.1 0.1 P 0.31 0.45 0.24 0.35 0.42 0.44 0.42 0.5 S 0.34 0.4 0.43 0.49 0.34 0.66 0.49 0.55 Mg 0.11 0.16 0.21 0.24 0.2 0.1 1000 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005

Allen, 1958) is retracted, giving the appearance of Cadiz (Southern Spain) and agree with Lamy a funnel turnedinwardson the preservedspeci- (1920) that it is L. borealis. men. The gills of the two species seem to be different, Distribution: The species is known only from the L. kazani having shorter andlarger ctenidiathan Anaximander Mountains, Eastern Mediterranean L. borealis (Fig. 15). However, according to Basin. Hentschel et al. (2000), the phenotype of the gills Habitat: The live specimens were taken on the of the Lucinoma aequizonata changes, in colour Kazan mudvolcano at a depth of 1700–1709 m, in andsize, in relation to their ability to dispose of a mudbreccia deposit that was highly saturatedin sulphur from the environment. So, it couldbe that gas andcontainedmany fragments of soft the phenotypic differences of the gills between sediments and hard rocks up to 7 cm in size. Other L. kazani and L. borealis were relatedto their shells and valves were dredged from the southern nutritional condition. Both species hold symbionts slope of FaultedRidge, a fault escarpment in bacteriocytes, inside the ctenidial cells, but the exposing several hundreds of metres of vertical bacteriocytes are set very close together in rock outcrop with gas seeps evident at bedding L. kazani (Fig. 13), whereas in L. borealis they planes andfractures. They were found,in the are more separatedby intercalary cells (Fig. 16). upper part of a dredge haul which started at a The labial palps of L. kazani are smaller than depth of 1854 m and finished at 1165 m, in rocks those of L. borealis, but the feet in the two species with irregular holes running through them, which are rather similar, with a moderately pronounced were inferredto be authigenic carbonates with gas heel. escape structures. The posterior apertures, derived from the fusion Etymology: The name refers to the Kazan mud of the inner folds of the mantle, are different. The volcano in the Anaximander Mountains, the mud inhalant aperture in L. kazani shows extremely volcano at which living specimens were found small papillae in both sides of the middle fold (Figs. 2 and3, 6–8, 12–14 and17). (Fig. 17), but in L. borealis there are large papillae, as illustratedby Allen (1958, p. 434) andconfirmed on our specimens from Norway. Moreover, the 4. Discussion mantle folds in L. borealis are large andappressed to each other, whereas in our specimen of 4.1. Taxonomic comparison L. kazani these are blunt andremain apart on either side of the aperture. The exhalant apertures The shell of L. kazani resembles that of L. are more similar in the two species; they have no borealis (Figs. 4–5, 9–11), but the umbos are more papillae andappear as a funnel with a rounded prominent and directed more inwards and for- aperture, directed inwards on the fixed specimens wards; the lunule is distinctly broader and better but capable of being stretchedout a long distance delimited; the hinge plate is slightly larger and less in living specimens (Allen, 1958, p. 438). However, curvedthan in L. borealis. The hinge is also the extension of the exhalant aperture along the different, L. kazani having a rather prominent, margin is greater in L. borealis. knob-like anterior lateral in each valve, whereas The habitats of the two species are also quite these are obsolete in L. borealis. Another impor- different. According to Jeffreys (1863), Lucinoma tant difference is the anterior adductor scar, which borealis in the British Isles lives in muddy gravel is broader in L. kazani, with the proximal part and sand, from spring tide low-water mark to 82 nearly twice the size of a L. borealis of comparable fathoms (ca. 150 m), andin one locality off the size. Moreover, the angle between the ventral Mull of Galloway in 110–145 fathoms (ca. 200– extension of the anterior adductor and the pallial 265 m). Allen (1958) reports this species from line is greater (ca. 251) than in L. borealis (ca. 151). Zostera beds at low-water mark in the Roscoff We have examinedthe figuredsyntype of Lucina area, France, andin the sublittoral zone (Ply- ignota Locard, 1898, described from the Gulf of mouth Sound, Firth of Clyde, and Bay of C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 1001

Mentone, British Isles). Dando et al. (1986) found Hand, 1984; Schweimanns and Felbeck, 1985; L. borealis in Zostera beds at shallow depth, in Dando et al., 1985, 1986; Reid and Brand, 1986; medium sand sediment (Salcombe estuary, south Distel andFelbeck, 1987; Cary et al., 1989; coast of Devon), in fine sand(Yealm estuary), and Hickman, 1994) has stimulatedthe interest in the in muddy sediments and black mud (Plymouth basic biology of living lucinids and in their Sound). The species is very abundant in fjords phylogeny. According to Taylor and Glover (Tunberg, 1984), in coarse shell sandandin silty (2000) bacteria have been reportedfrom at least fine sandat shallow depth.Along the West coast 30 species of Lucinidae, representing 18 different of Brittany (France), L. borealis may reach genera from several clades. densities of 1500 specimens per m2 in some Dando et al. (1985) have found that Lucinoma seagrass beds (Monnat, 1970, cited in Le Pennec borealis, Myrtea spinifera (Montagu, 1803) and et al. 1988). There are records from deep water Thyasira flexuosa (Montagu, 1803), living in a (Dautzenberg andFischer, 1906: 1530 m) from the community with the pogonophoran Siboglinum Azores; however, these are basedon valves fiordicum Webb, hadenzymes characteristic of the collectedaroundvolcanic islandswith very steep symbiosis in their ctenidia. Subsequentely, Dando slopes, andspecimens have been carrieddown- et al. (1986) studied the gills of L. borealis and slope. Conversely, L. kazani is a genuine deep- observedthe presence of numerous prokaryotes in water species, with living specimens collectedin specializedcells (bacteriocytes) in the subfilamen- bathyal depths. tar region of the gills, together with high concen- Among the species of lucinids indicated from the trations of elemental sulphur andof a c-type different Italian ‘‘Calcari a Lucina’’ deposits cytochrome. Recently, Gros et al. (2000) have (Conti, 1997), Dentilucina persolida Sacco, 1901, described sulphur-oxidizing endosymbiosis in the from the flysch deposits of Outer Marnoso- lucinid Divaricella quadrisulcata (d’Orbigny, 1842), Arenacea (proximal facies), Parma Foothills, from Guadeloupe Island. resembles Lucinoma kazani in outline andsculp- Bacteria from the ctenidia of Lucinoma borealis, ture, but the anterior adductor muscle scar of Myrtea spinifera, Thyasira flexuosa and T. sarsi D. persolida shows greater similarity to that of (Philippi, 1845) were isolatedandculturedby Lucinoma borealis, being longer, narrower and WoodandKelly (1989). The bacteria were either more parallel to the pallial line than the anterior autotrophs, obtaining energy from oxidation of adductor muscle scar of L. kazani. inorganic sulphur compounds or methylotrophs, Corselli andBasso (1996) founda Quaternary using methanol or methylamine as the source of coldseep Molluscan thanatocoenosis on the top of carbon andenergy. WoodandKelly proposedthat the Napoli Dome, a mudvolcano locatedon the these bacteria are symbiotic with the animals, but Eastern Mediterranean Ridge, at about 1950 m Hickman (1994) pointedout that the authors were depth. The valves collected have been identified by unable to demonstrate that the bacteria were the authors as Myrtea sp. (Lucinidae), Vesicomya housedwithin the ctenidia.On the other hand, sp. 1 and Vesicomya sp. 2 (Vesicomyidae), Cary et al. (1989) indicated that cultivations in belonging to two families typical of coldseep vitro of the symbionts were not successful, and communities. However, they mention that though symbiont-free hosts were not as yet available. living specimens might be present, they were not This metabolic pathway andthe methano- actually foundon the Napoli Dome. trophic nature of the symbionts have been demonstrated only for a seep-mussel from the 4.2. Symbiosis in Lucinidae Louisiana slope (Fisher et al., 1987). These authors testeda variety of animals from the same area, The presence of symbiotic sulphide-oxidizing which harbour chemosynthetic bacteria (the seep- bacteria in all the species of Lucinidae that have mussel, 2 vestimentiferans, 1 pogonophoran, 2 been investigated(Felbeck et al., 1981; Cava- vesicomyids and 1 lucinid), for the presence of naugh, 1983; Berg andAlatolo, 1984; Fisher and methanol deshidrogenase activity, and only the gill 1002 C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 tissue from the mytilidcontaineddetectable levels tions aroundthe vents (Dandoet al., 1995; of this enzyme; therefore, only the mytilidsym- Thiermann et al., 1997). Therefore, living chemo- bionts are capable of methylotrophy. symbiotic communities in the Mediterranean seem The presence of symbionts in the ctenidia of the to be restrictedto coldseep environments (such as new species (Figs. 12–14) is consistent with: (1) all foundin the AnaximanderMountains, present the studied Lucinidae, which are symbiotic with paper) or shallower reducing sediments (such as sulphur-oxidizing bacteria (Reid and Brand, 1986; the substrate of marine sea grasses). Hickman, 1994); in particular L. borealis (Dando et al., 1985, 1986; WoodandKelly, 1989); (2) the habitat of this new species, gas-saturatedmudwith Acknowledgements inferredor observedhigh levels of sulphideand low-oxygen deep-water, is usually occupied by We gratefully acknowledge the funding pro- symbiotic organisms, including the lucinids. In this vided to the second author by the Netherlands case the gas releasedupwardsin the Kazan mud Geosciences Foundation (Stichting GOA) to carry volcano is methane (J. L. Charlou, 1999, pers. out the ANAXIPROBE Project (GOA Project comm.), but in most cases the methane appears to 750.195.02) andthe Training Through Research be associatedwith the zone of sulphate reduction, cruise TTR-6 during which the samples were resulting in the generation of inorganic carbon and obtained. In this regard, we thank also the hydrogen sulphide. Such geochemical profiles are scientists, officers, andcrew of R/V Gelendzhik expectedif methane is oxidizedby a consortium of andespecially M.K. Ivanov andhis team from methanogens andsulphate-reducingbacteria (Pan- Moscow State University. We are indebted to the cost et al., 2000). Moreover, the cores obtained captains andcrews of the R/V Nadir, submersible during the 1999 Medineth cruise on the Eastern Nautile andR/V Prof. Logachev. The MEDI- Mediterranean Ridge indicate that sulphate re- NAUT expedition was a jointly funded French– ducers are abundant and active in the sediments Dutch research project carriedout on boardR/V from mudvolcanoes (Pancost et al., 2000); and(3) Nadir andthe submersible Nautile. The authors the presence in the community of vestimentiferans, are grateful to Jean Paul Foucher (co-chief which are obligate symbiotic metazoans (Childress scientist of the project together with J. Woodside), et al. 1984; Fisher andChildress, 1984; Jones, Myriam Sibuet (responsible for biological sam- 1985), typical of coldseep andvent communities. ples) andall the shipboardscientific party, who Therefore, the occurrence of living endosym- took the biological samples andgas measurements biont-bearing organisms, such as Lucinoma kazani during the MEDINAUT cruises. J.L. Charlou is described here and Vestimentiferans (studies in thankedfor the data on concentration of methane progress by E. Southwards, pers. comm.) in the in the water column above Kazan mudvolcano. Anaximander Mountains is evidence of a living MEDINAUT was partially supportedby the coldseep community in the Eastern Mediterra- Research Council for Earth andLife Sciences nean basin. (ALW) with financial aidfrom the Netherlands Extant faunal assemblages that are specific of Organisation for Scientific Research (NWO) on hydrothermal vents have not been found to date in the Dutch side and by Ifremer on the French side. the Mediterranean, although fossil hydrothermal We are also indebted to Jose! Pascual andAntonio vent fauna are reportedin ancient massive Ramirez (University of Malaga)! for the qualitative sulphide deposits on Cyprus (Dando et al., andquantitative elemental analysis on the SEM 1999). Recent hydrothermal sites in the Mediter- preparations. The first author thanks M. Segonzac ranean are scatteredandsituatedin shallow water (CENTOB, French National Sorting Center, (o200 m). It is likely that the animals which IFREMER, Brest) andM. Sibuet (DRO/EP normally inhabit the nearshore reducing sediments Ecologie Abyssale; IFREMER, Brest) for entrust- are unable to tolerate the prevailing high tempera- ing her with the study of the collected material. tures, salinities, andsulphideandmetal concentra- Karine Olu is thankedfor the preparation and C. Salas, J. Woodside / Deep-Sea Research I 49 (2002) 991–1005 1003 transfer of additional bivalve samples. H.C. Salas Relic Basins: Products, Processes and Causes. International is grateful to Prof. D. Doumenc (Laboratoire de FieldWorkshop to be heldin Bologna andnearby Biologie des Invertebr! es! Marins et Malacologie, Apennines, June 23–26, pp. 1–16. Conti, S., Fontana, D., 1997. Luciniddepositsfrom MNHN, Paris) for the facilities provided her different geological settings of the Northern Apennines. during her stay in his department during the In: COLD-E-VENT. Hydrocarbon Seepage and Chemo- present study. 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