Fig. 1

22 Pages·2004·1.25 MB·English

ARTICLE IN PRESS
Deep-SeaResearchI51(2004)1915–1936
www.elsevier.com/locate/dsr
Cold seep communities in the deep eastern Mediterranean
Sea: composition, symbiosis and spatial distribution on
mud volcanoes
Karine Olu-Le Roya,(cid:1), Myriam Sibueta, Aline Fiala-Me´dionib, Serge Gofasc,
Carmen Salasc, Andre´ Mariottid, Jean-Paul Fouchere, John Woodsidef
aDe´partementEnvironnementProfond,IFREMERCentredeBrest,BP70,29280Plouzane´,France
bObservatoireOce´anologiquedeBanyuls,Universite´P.&M.Curie,66650Banyuls-sur-mer,France
cDeptBiologı´aAnimal,FacultaddeCiencias,UniversitatdeMa´laga,E-29071Ma´laga,Spain
dUniversite´P.M.Curie,LaboratoiredeChimieIsotopique,75252Paris,Cedex,France
eDe´partementGe´osciencesMarines,IFREMERCentredeBrest,BP70,29280Plouzane´,France
fCentreforMarineEarthSciences,VrijeUniversiteit,DeBoelelaan1085,1081HV,Amsterdam,TheNetherlands
Received4November2003;receivedinrevisedform8July2004;accepted8July2004
Availableonline20October2004
Abstract
Two mud volcano fields were explored during the French–Dutch MEDINAUT cruise (1998) with the submersible
NAUTILE,onesouthofCretealongtheMediteraneanRidgeatabout2000mdepth(Olimpimudfield)andtheother
south of Turkey between 1700 and 2000m depth (Anaximander mud field) where high methane concentrations were
measured.Chemosyntheticcommunitieswereobservedandsampledonsixmudvolcanoesandalongafaultscarp.The
communities were dominated by bivalves of particularly small size, belonging to families commonly found at seeps
(Mytilidae, Vesicomyidae, Thyasiridae) and to Lucinidae mostly encountered in littoral sulfide-rich sediments and at
theshallowestseeps.SiboglinidpolychaetesincludingalargevestimentiferanLamellibrachiasp.werealsoassociated.
Atleastfourbivalvespeciesandonesiboglinidareassociatedwithsymbioticchemoautotrophicbacteria,asevidenced
byTransmissionElectronicMicroscopyandisotopicratiomeasurements.Amongthebivalves,amytilidharborsboth
methanotrophicandsulfide-oxidizingbacteria.Videospatialanalysisofthecommunitydistributiononthreevolcanoes
shows that dense bivalve shell accumulations (mainly lucinids) spread over large areas, from 10% to 38% of the
explored areas (2500–15000m2) on the different volcanoes. Lamellibrachia sp. had different spatial distribution and
variable density in the two mud volcano fields, apparently related with higher methane fluxes in the Anaximander
volcanoesandmaybewiththeinstabilityduetobrinesintheOlimpiarea.Theabundanceandrichnessoftheobserved
chemosyntheticfaunaandthesizeofsomeofthespeciescontrastwiththepovertyofthedeepeasternMediterranean.
(cid:1)
Correspondingauthor.Fax:[phone].
E-mailaddress:[email protected](K.Olu-LeRoy).
0967-0637/$-seefrontmatterr2004ElsevierLtd.Allrightsreserved.
doi:10.1016/j.dsr.2004.07.004
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1916 K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936
Thepresenceofaspecializedfauna,withsomemolluskgeneraandspeciessharedwithotherreducedenvironmentsof
the Mediterranean, butnotdominated bythe large bivalves usually foundat seeps, isdiscussed.
r2004Elsevier Ltd. Allrights reserved.
Keywords:Coldseeps;Chemosynthesis;Symbiosis;Siboglinids;Bivalves;Spatialdistribution
1. Introduction vesicomyid bivalves (Barry et al., 1996). Finally a
mud volcano (Haakon Mosby Mud Volcano) has
Communitiesofbenthicanimalsassociatedwith been described in the Norwegian Sea (Vogt et al.,
cold seeps have been discovered in recent decades 1997; Milkov et al., 1999). The mud volcano
at several places on active and passive continental chemosynthetic communities include bivalves
marginsofthePacificandAtlantic oceans(seefor (mainlyvesicomyidsandmytilids)andpolychaetes
review Sibuet and Olu, 1998; Sibuet and Olu-Le Siboglinidae1(vestimentiferansandperviatepogo-
Roy, 2002). Mud volcanoes, geological structures nophorans), that dominate both Barbados and
where mud and fluid are seeping through the Louisiana slope cold seep communities. Lucinid
seafloor, are one of the most common environ- and thyiasirid infaunal clams occur at the shal-
mentsfavoringtheirdevelopment.Mudvolcanism lowestseepsites,generallyassociatedwithsubsur-
isaphenomenontypicallydrivenbyoverpressured face lithification (Olu et al., 1996; MacDonald et
sediment in subduction zones and by salt tecton- al., 1990a). The Haakon Mosby Mud volcano
ism in passive margins (Milkov, 2000; Bohrmann chemosyntheticcommunityischaracterizedbythe
etal.,2002).Largequantitiesofmethaneareoften absence of bivalves and dominance of small-sized
released at the surface of the mud volcanoes Siboglinidae polychaetes (Frenulata) (Milkov et
(Ginsburgetal.,1999;Martinetal.,1997;Vogtet al., 1999). East Pacific cold seep sites are char-
al.,1997;MEDINAUT/MEDINETH,2000;Mac- acterized by the absence of Mytilidae, except on
Donald et al., 2000; Charlou et al., 2003). The theCostaRicaprism(Bohrmannetal.,2002)that
methane is produced either through biological has been attributed to less methane availability
degradation of organic matter in the upper (Barry et al., 1996; Sibuet and Olu, 1998).
sediments or through migration of thermogenic Chemosynthetic communities have been recently
gas from deeper hydrocarbon deposits. At cold discovered on mud volcanoes at two distinctive
seeps, archae and bacteria consortia use this settings in the eastern Mediterranean Sea south of
methane and produce sulfides in the sediment by Crete (Mediterranean Ridge) and south of Turkey
chemoautotrophic processes (Masuzawa et al., (Corselli and Basso, 1996; Woodside et al., 1998;
1992; Boetius et al., 2000; Pancost et al., 2000) MEDINAUT/MEDINETH, 2000) (Fig. 1). Some
whereas symbiotic bacteria use methane or sulfide shellshavebeenpreviouslysampledbydredgesand
to sustain high biomass production in large size cores; preliminary identification indicated lucinids
invertebrates (review in Fiala-Me´dioni and Fel- and vesicomyids (Corselli and Basso, 1996), and
beck, 1990; Fisher, 1990). Such ecosystems have onelucinidspecieshasrecentlybeendescribedfrom
been described on mud volcanoes along passive these collections (Salas and Woodside, 2002).
and active margins, for example on the Barbados Nevertheless the species composition and extent
accretionary prism (Jollivet et al., 1990; Olu et al., of the chemosynthetic community had not been
1996,1997),intheGulfofMexico(MacDonaldet
al., 1989, 1990a; Carney, 1994; Neurauter and
Roberts, 1994; MacDonald et al., 2003), and on 1AccordingtoMcHugh(1997);RouseandFauchald(1997);
Southward(1999),theperviatepogonophorans(Frenulataand
the Costa Rica accretionary prism (Bohrmann et
Monilifera) and the vestimentiferans (Obturata), at one time
al., 2002). A circular structure considered to be a
regardedasselfstandingphyla,aretobeincludedinPolychaete
mud volcano in Monterey Bay is colonized by familySiboglinidae.
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K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936 1917
studied prior to the MEDINAUT submersible
cruise, realized in 1998. Dives and video observa-
tions revealed exceptionally large fields of bivalve
shells,andlivinglargesiboglinids(vestimentiferans),
though less abundant, were also observed in
association with carbonate crusts. In this paper, we
first describe the composition of the seep fauna and
symbiosis in four species associated with methane
releaseonseveralmudvolcanoessouthofCreteand
Turkey, and outline the main features of the
chemosynthetic fauna in the deep Mediterranean,
with hypothesis for colonization processes. The
spatial distribution of the benthic megafauna colo-
nizing the volcanoes is mapped based on video
processingandthesefeaturesarecomparedbetween
several mud volcanoes in relation with environmen-
talpatterns.Thispaperdescribesforthefirsttimea
diverse chemosynthetic community in the deep
Mediterranean.Thesenewdataincreaseourknowl-
edge of cold seep community structure on mud
volcanoesandthebiogeographyofcoldseepspecies.
2. Geological setting
Intense emission of methane occurs at Mediter-
aneanmudvolcanoesandalongrelatedfaultsystems
(MEDINAUT/MEDINETH, 2000; Charlou et al.,
2003).TheOlimpiMudVolcanofield(OMVarea)is
located on the Mediterranean Ridge (Cita et al.,
1996; Mascle et al., 1999), the accretionary prism
associated with subduction along the Hellenic Arc
south of Greece (Fig. 1a and 1b). The otherarea of
mudvolcanoesistheAnaximanderMountains(AM
area; Fig. 1a and 1c) formed by an older group of
continental fragments now caught up in the plate
convergencebetweenAfricaandEurasia(Woodside
et al., 1998). The OMV and AM settings have in
common strong compressionaltectonicswith super-
Fig. 1. (a) Location map showing the Olimpi Mud Volcano posed faulting. The mud volcanoes are conical
field (OMV) and Anaximander Mountains (AM) in their topographic features several km across and on the
general Eastern Mediterranean context (from MEDINAUT/
order of 100m high, while a few have relatively flat
MEDINETH, 2000). (b) Detailed position of the mud
summit areas with low relief. Fresh mud flows were
volcanoes in the Olimpi area (OMV), Napoli, Milano,
Maidstone and Moscow were investigated during the diving observedonsomevolcanoes,whereasothersmaylie
MEDINAUT cruise. (c) Bathymetric map of Anaximander dormant for a relatively long time before reactivat-
mountains (AM) with the four geological structures (Amster- ing. An extensive field of gas hydrate was sampled
dam, Kula, Kazan, Faulted Ridge) investigated by Nautile
on both Amsterdam and Kula mud volcanoes.
duringtheMEDINAUTcruise.
Largemethaneconcentrationsmeasuredinthewater
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1918 K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936
Fig. 2. (a) Brine lake on Napoli mud volcano, (b) Lucinid shells and echinids, on Kazan mud volcano, (c) Lamellibrachia sp. on
Amsterdammudvolcano,(d)SeaurchinsandsmallsizeLamellibrachiasp.betweencarbonatecrusts.
column above the mud volcanoes indicate intense stone and Moscow mud volcanoes, and the
degassing(MEDINAUT/MEDINETH,2000;Char- Anaximander mud field south of Turkey (351300
lou et al., 2003). Brine pools rich in methane occur N, 301E, 1700–2000m depth) with the Kula,
on some mud volcanoes such as Napoli (Fig. 2a). Kazan and Amsterdam mud volcanoes and the
Anaerobic methane oxidation by a consortium of Faulted Ridge. Two brine lake areas were sur-
ArchaeaandBacteriahasbeenevidencedinthemud veyed, one related to the mud field in the Olimpi
volcano sediments (Pancost et al., 2000). Carbonate area (Nadir brine lakes) and the other in the
crusts, formed by oxidation of methane from mud Urania area south of Greece (Urania brines).
flowsattheseafloor(Aloisietal.,2000)bymethane- Benthic species of chemosynthetic communities
consuming Archaea (Aloisi et al., 2002), form were collected on 6 volcanoes among 7 explored
pavements up to several tens of centimeters thick, (Napoli, Milano, Maidstone, Amsterdam, Kazan,
round slabs, and circular mounds on the central and Kula) and along the Faulted Ridge, using
most active part of the mud volcanoes. When the different sampling devices (Table 1). Nevertheless,
crusts are absent, mud flows are presumed to be as only a few samples were taken by cores, no
freshly erupted. quantitative data are available to estimate densi-
ties or for statistically valuable comparison of
species richness or diversity between sites. Speci-
3. Methods mens were formalin fixed on board and sorted in
the laboratory (Centob, Ifremer DRO-EP) and
3.1. Dives and sampling identified by specialists for each group.
Two ‘‘mud fields’’ were explored during the 3.2. Transmission electronic microscopy
MEDINAUT cruise (Dutch–French collabora-
tion) with the submersible Nautile: the Olimpi Small pieces of gills were fixed in 3% glutar-
mudfieldsouthofCrete(about341N,251E,about aldehyde in 0.4M Nacl, buffered with 0.1M
2000m depth) with the Napoli, Milano, Maid- cacodylate pH 7.4 and post-fixed in 1% osmium
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K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936 1919
Table1
NumberofdivesandfaunasamplingrealizedonthedifferentgeologicalstructuressurveyedbyNautileduringtheMedinautcruise,
andsubsequentvideoanalyses
Area Structurename Numberofdives Bottomtime Faunasampling Videoanalysis
Olimpi Napoli(M.v.) 4 20h06 8BT,1BC,1TC X
Milano(M.v.) 3 15h39 5BT,2BC X
Maidstone(M.v.) 1 1h00 1BT
Moscow(M.v.) 1 5h25
Nadir(B.l.) 1 6h54
Anaximander Amsterdam(M.v.) 4 20h39 7BT,2TC X
Kazan(M.v.) 2 10h40 6BT,1TC X
Kula(M.v.) 1 5h23 1BT
FaultedRidge 1 5h12 4BT,1TC
Urania Urania(B.l.) 1 3h05
ThevolcanoesNapoli,AmsterdamandKazanhavebeenstudiedindetail.AdditionaldatafromMilanovolcano(videodata)and
Faultyridge(samplingdata)havebeenincluded.
M.v.=Mudvolcano,B.l.=Brinelake.
BT:bottomgrab,BC:boxcore,TC:tubecore.
tetroxidefor1hinthesamebuffer.Thespecimens for submersible data processing. Large siboglinids
were dehydrated through a graded ethanol series (vestimentiferans) were enumerated every 30s and
andembeddedinAraldite.Semi-thinsectionswere an average density was computed along contin-
stained with toluidine blue. Ultra-thin sections uous tracks with a sampling unit of about 50m2,
were contrasted with uranyl acetate and lead following the method described in Olu et al.
citrate, and observed under a Hitachi H600 (1997). Their densities were mapped along the
transmission electron microscope. dive tracks, and the mean density on the whole
activesurveyedareaofeachvolcanowasestimated
3.3. Isotopic ratios by dividing the total number of individuals by the
total active area explored. The active area is
Stable carbon and nitrogen isotope analyses of defined as the area where living siboglinids were
the tissues were made on samples frozen and observed. In order to test if the density is
stored in liquid nitrogen then freeze dried and significantly different between two sites, means
acidified in the laboratory. The acidified samples were compared using the Kolmogorov–Smirnov
were combusted to CO and N using standard testasthedatadidnotfitthenormaldistribution.
2 2
methods before being passed through a mass Thepatternsofdistribution(patchyorregular)are
spectrophotometer (Finnigan Delta E). Carbon compared by the variance/mean ratios of the
results are reported relative to PDB (PeeDee densities with the sampling unit of 50m2. A
Belemnite) and nitrogen relative to atmospheric different method was used to map bivalve shells
molecular nitrogen. alongthetracks,becausethespeciesaresmalland
partially or totally buried. Three categories were
3.4. Video analysis delimited: bivalve clusters (dense aggregations on
restricted areas from 0.1 to 1m2), bivalve fields
A video study was made of chemosynthetic (dense aggregations from 10 to more than 50m2)
communities observed around seeps at three mud and scattered bivalves (on areas from 10 to more
volcanoes (Table 1). Dive tracks were plotted on than 100m2). Dense aggregations (clusters or
bathymetric maps using the Adelie software, an fields)aremostlycontinuouslayersonthebottom
extension of ArcView GIS developed at Ifremer (Fig. 2b). The surface of each aggregation was
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1920 K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936
estimatedusingtheempiricalrelationshipbetween striata Sturany (1896) (Fig. 3) were collected on
the submersible altitude and the surface covered Amsterdam and Kazan mud volcanoes in the
bythecamerafield.Crabs, fishes,shrimpsandsea Anaximander area. Four of the five bivalve
urchins were enumerated, abundance of each species, I. perplexum, I. modiolaeformis, M. amor-
group was mapped, and the mean densities were pha, and T. striata were described from the same
estimated for each volcano. dredge sampling in the Nile delta by Sturany
(1896).
4. Results and discussion: community composition 4.1.2. Gastropods
Numerous gastropods, all less than 2cm were
4.1. The fauna sampled on mud volcanoes collected at the five main sites (Table 2b). A total
of 11 species in eight families has been collected.
4.1.1. Bivalves All the species were present in the Anaximander
The sampled bivalves belong to five species in area, whereas only four species (only one living)
four families, Mytilidae, Vesicomyidae, Lucinidae were sampled in the Olimpi area. Empty shells of
andThyasiridae.Numbersofspecimensandshells the Turridae Taranis moerchi (Malm, 1861) were
sampled for each species at the main sites are collected at all the sites and were particularly
indicated in Table 2a. The Mytilidae Idas mod- abundant in the Kazan samples (176 shells in one
iolaeformis (Sturany, 1896) (Fig. 3) appears to be grab). The Trochidae include Putseysia wiseri
relatively ubiquitous in both Olimpi and Anaxi- (Calcara, 1841) sampled on the five sites, with
mander areas as it was sampled at all the sites, dominance of dead individuals, but a few living
except on the Kula volcano where only one grab ones in both areas, and Clelandella n. sp., also
was taken. common but with living specimens only in the
Shell lengths of sampled specimens are com- Anaximander area. The limpet Lepetella sp.
prised between 2 and 17mm. The Vesicomyidae collected on Kazan, is likely living on polychaete
Isorropodon perplexum Sturany (1896) (revised by tubes (maybe on Lamellibrachia sp.), as other
vonCoselandSalas,2002)(Fig.3)wassampledat species of this genus, and Odostomia sp. is likely
the five well-explored sites. Nevertheless, no living commensal of the abundant polychaetes as this is
specimens were collected in the Olimpi area and an obligate way of life (Fretter and Graham,
onlyafewonAmsterdamandKazan (Anaximan- 1962). A few specimens of Lurifax vitreus (Ware´n
der area) whereas the shells and dislocated valves and Bouchet, 2001), recently described from
are very numerous (15 live specimens and more hydrothermal sites on the Mid Atlantic Ridge,
than 1000 valves sampled on Amsterdam). This were interestingly sampled on Amsterdam.
specieswasreportedfromshellstakenbycoreson
Napoli dome by Corselli and Basso (1996) as 4.1.3. Polychaetes Siboglinidae and others
Vesicomya sp. Shell lengths of our specimens All the sampled siboglinids of the Obturata
ranged from 2 to 14mm. The Lucinidae, Myrtea group (Vestimentifera) belong to the same, likely
amorpha (Sturany, 1896) (Fig. 3), was collected at newspeciesofLamellibrachia(E.Southward,pers.
the five main sites and on Kula mud volcano. com.). Specimens were of various sizes (up to
Living specimens were only be found in the 80cm long) and were observed on various
Anaximander area on Kazan and Kula. A second substrata. However, they were always near or in
Lucinidae is the recently described species Lucino- closerelationtocarbonatecrusts(e.g.inmudwith
ma kazani Salas and Woodside (2002) sampled smallcrustfragments,orattachedundercrusts,or
only in the Anaximander zone, with a few living infracturesinsidelargesizeblocks)(Fig.2cand3).
juveniles on Kazan (Fig. 3). Shells of M. amorpha Theysometimesoccupied sinuoustubularhollows
were of small size (8–20mm in length) whereas in carbonate crusts, which form when methane-
Lucinoma is larger (up to 40mm). Finally, living charged mud flows are oxidized at the seafloor
and dead specimens of the Thyasiridae Thyasira (Fig. 3 and Aloisi et al., 2000). This species has
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Table2
SampledfaunaonthedifferentmudvolcanoesandFaultyRidge
Olimpiarea Anaximanderarea Relationto
seeps
Napoli Milano Amsterdam Kazan Faultedridge
(a)Bivalves
Idasmodiolaeformis L L L L/D L ?Endemic
Myrteaamorpha D D D L/D D ?Endemic
Lucinomakazani — — D L(juv)/D D ?Endemic
Isorropodon D D L/D L/D D ?Endemic
perplexum
Thyasirastriata — — L/D L/D — ?Endemic
Yoldiellasp. R Vagrant
(b)Gastropods
Taranismoerchi D D D D D ?Colonist
Putseysiawiseri L/D D L/D L/D D Colonist
Clelandellan.sp. D D L/D L/D L/D ?Colonist
Akritogyraconspicua R L/D L/D L/D ?Colonist
Lurifaxvitreus L/D Endemic
Odostomian.sp. D ?Colonist/
endemic
Drilliolaloprestiana R Vagrant
Benthomangelia R Vagrant
macra
Xylodisculasp. D ?Vagrant
Benthonellatenella D D Vagrant
Lepetellasp.(limpets) L Onvestim.
tubes
Napoli Milano Amsterdam Kazan
(c)Othergroups
Porifera:Rhizaxinellapyrifera X
Actiniaria R
Nemertina X
Nematoda X X X X
Polychaeta X X X
Polychaeta:Serpulidae X X
Polychaeta:Siboglinidae X X X X
(vestimentifera):
Lamellibrachiasp.
Polychaeta:Siboglinidae X X X X
(Monilifera):Siboglinumsp.
Echiurida:Bonelliaviridis X
Aplacophora:Falcidenssp. X X
Amphipoda X X X
Decapoda:Munidopsis X
marionis
Munidopsisacutispina X
Chaceonmediterraneus X X
Tanaidacea:Paranarthrura X
intermedia
Echinodermata:Echinussp. D X
L—livingspecimens,D—deadones,juv.—juveniles,X—presence,R—rare.
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1922 K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936
Fig. 3. Invertebrate species sampled on Mediterranean mud volcanoes, known or assumed to be associated with chemautotrophic
symbiotic bacteria. Bivalve shells and tubes of Lamellibrachia sp. attached in a close relationship with carbonate concretion. I.
modiolaeformis:15mmlong,I.perplexum:14mm,L.kazani:40mm,M.amorpha:20mm,T.striata:10mm.PhotosPatrickBriand
(Ifremer).
been sampled on each volcano and at Faulted Tubes of another family of Polychaetes were
Ridge. The exception was the Maidstone mud also observed in abundance during dives, espe-
volcano, where it was not observed during the 1-h cially on Napoli and Amsterdam mud volcanoes.
dive. Small Siboglinidae of the Monilifera goup Unfortunately, they were not sampled living and
werecollectedonNapoli,Milano,Amsterdamand could not be identified to a genus or species.
Kazan mud volcanoes. Most of them belong to a
probably new species of Siboglinum sp., that is 4.1.4. Other phyla
different from the only species described in The other groups are listed in Table 2c.
Mediterranean, S. carpinei (Ivanov, 1970) from Exceptional large specimens of the Suberitidae
west of Corsica (E. Southward, pers. comm.). sponge Rhizaxinella pyrifera (Delle Chiaje, 1828),
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K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936 1923
common in the bathyal Mediterranean, were hosting number of bacteria. Similar observations
sampled on the Napoli mud volcano (J. Vacelet, were made with scanning electron microscopy
pers.com.).However,thesampledspecimenshave (SEM) on the gills of L. kazani by Salas and
anunusuallylargesizeprobablylinkedtotheirlife Woodside (2002). Observations of the mytilid I.
at seeps. Among Crustaceans, the galatheids were modiolaeformis (Fig. 4c) show that the great
sampled at active sites on Kazan, and the large majority of its gill cells contain two distinct
crab, Chaceon mediterraneus (Manning and morphological types of symbionts. The first type
Holthuis, 1989) (D. Guinot, pers. com.) was consists of small (mean diameter: 0.35mm) coc-
sampled on the Napoli and Amsterdam mud coids or short rods, resembling to the sulfide-
volcanoes The Echinoidea Echinus sp. (M. Sibuet, oxidizing symbionts already observed in Bath-
pers.com.)wereobservedinlargedensityatactive ymodiolus thermophilus from the Pacific hydro-
seep sites, together with bivalves and Lamellibra- thermal vents (Fiala-Me´dioni and Felbeck, 1990).
chiasp.andbetweencarbonatecrusts(Fig.2band The second type are large (mean diameter:
2d), intheAnaximander area. They occurasdead 1.25mm) coccoid-shaped bacteria looking type I
individuals around Napoli volcano brine lakes. methylotrophs with stacked intracytoplasmic
membranes as observed in B. puteoserpentis
4.2. Nutritional strategies (Cavanaugh et al., 1992; Robinson et al., 1998)
or B. azoricus (Fiala-Medioni et al., 2002) and
4.2.1. Symbiotic species identified as methanotrophic symbionts.
The bivalves and siboglinids colonizing the two 13C/12C and 15N/14N isotopic ratios were
mud volcano areas belong to families which are determined on the same tissues as observed in
typicalcomponentofcoldseeps,wheretheylivein TEM. Carbon isotopic ratios on gills of M.
symbiosis with chemoautotrophic bacteria (Sibuet amorpha and I. perplexum and Lamellibrachia sp.
and Olu, 1998; Sibuet and Olu-Le Roy, 2002). trophosome (Table 3) are in the range of those of
Table3summarizestransmissionelectronicmicro- other symbiotic chemosynthetis-based bivalves or
scopy (TEM) observations and isotopic 13C/12C siboglinids hosting sulfide-oxydizing symbionts,
ratios of the presumed symbiotic species sampled found in different vent or cold seep sites (Van
in the Anaximander area. TEM analysis of Dover and Fry, 1989; Kennicutt et al., 1992;
transversal sections of gill filaments of the lucinid Fisher, 1995).Theisotopicratiosmeasuredonthe
M. amorpha (Fig. 4a) and of the vesicomyid I. mytilid I. modiolaeformis sampled on the Kazan
perplexum (Fig. 4d), as well as of the trophosome m.v. are more depleted than those of the
ofthesiboglinidLamellibrachiasp.(Fig. 4b)show lucinids and vesicomyids; ranging from – 44.2%
that they are mainly composed of bacteriocytes to –44.6% : they reflect more likely the presence
Table3
CarbonisotoperatiosandresultsfromTEMobservationsofdifferentspeciesoftheseepcommunity
Species d13C d15N TEMobservations
Idasmodiolaeformis (cid:2)44.2%to(cid:2)44.6% 0.2%to0.4% Sulfur-oxidizingsymbionts
ProbablytypeImethylotroph
Isorropodonperplexum (cid:2)29.3%to(cid:2)30.1% –1.6%to1.9% Sulfur-oxidizingsymbionts
Myrteaamorpha (cid:2)27.7%to(cid:2)30.5% (cid:2)1.0%to1.4% Sulfur-oxidizingsymbionts
Lucinomakazani Intracellularsymbiontsa
Lamellibrachiasp. (cid:2)23.6%to(cid:2)26.6% –0.8%to0.2% Sulfur-oxidizingsymbionts
Echinussp. (cid:2)36.12%(muscle) Noobservation
(cid:2)42.05%(stomach)
Rhizaxinellapyriferab (cid:2)27.6to(cid:2)28.1% Nosymbionts
aSalasandWoodside(2002).
bFiala-Me´dioniandVacelet(unpublished).
ARTICLE IN PRESS
1924 K.Olu-LeRoyetal./Deep-SeaResearchI51(2004)1915–1936
Fig.4. Transmissionelectronmicrographsofendosymbioticbacteriaontransversalsections:(a)TEMshowingbacteriocytesinthegill
ofM.amorpha;(b)TEMofbacteriainthetrophosomeofLamellibrachiasp.;(c)TEMofmethylotrophicandsulfur-oxidizingbacteria
inthegillofmytilidI.modiolaeformis;(d)TEMshowingbacteriocyteswithsulfur-oxidizingbacteriainthegillofI.perplexum;b:
bacteriocyte;ic.:intercalarycell;sb:sulfur-oxidizingbacteria;mb:methylotrophicbacteria.Scalebars:1mm.
of methylotrophic symbionts which may use Perviate siboglinids (‘‘pogonophorans’’) are
methane as energy source as the cold seep mussel known to be associated with methylotrophic or
B. childressi, (d13C=–37.5% to – 67.1% ) (Nelson sulfur-oxidizing symbionts (Southward et al.,
and Fisher, 1995; Kennicutt et al., 1992). The 1981, 1986; Southward, 1982). This probably the
15N/14NisotopicratiosmeasuredinM.amorpha,I. caseofthesampledSiboglinumsp.Thyasiridaeare
modiolaeformis,I.perplexumandLamellibrachiasp. knownfromcoastalreducedenvironmentsorcold
are also within the range of values reported from seeps to be associated with thioautotrophic sym-
other symbiotic organisms (2.0% to –12.9%). bionts and maybe another undetermined type of