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A B S T R A C T . D uring the European Com m issions Fram ew orkSix Program m e, HERMES, we investigated three m ain areas along

the European margin, each characterized by the presence of seep-related structures exhibiting different intensity o f activity and

biological diversity. These areas are: (1) the N ordic m argin with the H âkon Mosby m ud volcano and m any pockm arks, (2) the Gulf

of Cádiz, and (3) the eastern M editerranean with its hundreds of m ud volcanoes and brine pool structures. One of the m ain goals

of the HERMES project was to unravel the biodiversity associated with these seep-associated ecosystems, and to understand their

driving forces and functions, using an integrated approach. Several m ultidisciplinary research cruises to these three areas provided

evidence of high variability in ecosystem processes and associated biodiversity at different spatial scales, illustrating the “hotspot”

nature of these deep water systems.

I N T R O D U C T I O N

Soon after the discovery of the spec

tacular hydrotherm al vent com m unities

30 years ago, other types of chemo-

synthetic assemblages—so-called “cold

seeps”—were found along continental

m argins during submersible dives to

the deep G ulf of Mexico (Pauli et ah,

1984), subduction zones off O regon in

the eastern Pacific (Suess et a l , 1985),

and trenches off Japan in the western

Pacific (Juniper and Sibuet, 1987). Cold

seeps are now am ong the m ost geologi

cally diverse and widely distributed of

the deep-sea reducing environm ents

explored to date, and new sites are

still being discovered every year. Since

their initial discovery, active seeps

have been reported from shallow to

hadai (> 6000-m) depths (Sibuet and

Olu-Le Roy, 2002; Levin, 2005, and

references therein), along other active

and passive margins, and from all parts

of the global ocean, even Antarctic

regions (Dom ack et a l, 2005). It is only

during the last decade that m ore intense

observation of the European continental

m argins using in situ video and photog

raphy w ith adapted deep submersibles

provided evidence for a wide range of

active cold-seep ecosystems associated

w ith fluid, gas, and m ud escape struc

tures. These structures include pock

m arks (seafloor depressions), brine lakes,

and elevated or flat m ud volcanoes.

As with hot vents, cold seeps are

characterized by the flow of reduced

chemical com pounds from the sub

surface to the seafloor, but they are not

directly associated w ith high therm al

anomalies. M ost know n cold seeps

are associated with reduced environ

m ents that are linked indirectly to gas

hydrates or to hydrocarbon reservoirs.

Hence, in contrast to the m ajority of

m arine deep-water ecosystems, which

depend on photosynthetically derived

food (phytoplankton and plant m ate

rial), m ethane and other hydrocarbon

seeps are colonized by specific anaerobic

subsurface microbiota; these organisms

use hydrocarbons as an energy source

(Sloan, 1990) to transform seawater

sulfate, thus producing high fluxes of

hydrogen sulfide (Jorgensen and Boetius,

2007). Chem osynthetic m icroorgan

isms are the p rim ary producers in seep

food webs, depending on such reduced

chemicals as m ethane and sulfide as

their energy sources.

Similar to their hydrotherm al vent

counterparts, m ost cold seeps support

highly productive ecosystems (high

biomass) that consist o f specialized

m etazoan com m unities dom inated by

a few adapted taxa that can cope with

elevated concentrations of chemical

com pounds and low oxygen levels at

and below the sedim ent-w ater interface.

O ther harsh conditions, such as high

concentrations of hydrocarbons or

high-salinity brines, m ay locally reduce

faunal diversity (M acDonald et a l , 2004;

Bergquist et a l , 2005). A m ong the m ost

rem arkable of the fauna exploiting the

abundant chemical energy of seeps are

the sym biont-bearing invertebrate spe

cies, often sim ilar or related to the fauna

Oceanography M arch 2009 111

found at hydrotherm al vents. These

large taxa, such as vesicomyids (clams),

bathym odiolids (mussels), and siboglin-

ids (form erly know n as Pogonophora or

tube worm s), and some motile species

such as shrim ps and gastropods, cluster

in areas where fluids rich in reduced

chemicals reach the seafloor (Sibuet and

Olu, 1998; Sibuet and Olu-LeRoy, 2002;

Bergquist et a l , 2003; Van Dover et ah,

2003; Cordes et a l , 2007).

D uring HERMES, three m ain areas

harboring prom inent seep ecosystems

were investigated, including the N ordic

m argin and its H âkon Mosby m ud vol

cano, the G ulf o f Cádiz, and the eastern

M editerranean. After a short in troduc

tion of the three m ain study areas, which

are m ore extensively discussed elsewhere

(see Foucher et a l , this issue), we p ro

vide an overview of the m ain results

from biodiversity studies perform ed dur

ing HERMES. An integrated approach

com bined detailed habitat m apping and

characterization of associated fauna.

Both sym biont-bearing and associated

nonsym biotic fauna were investigated,

as well as different size classes, from fish

and large invertebrates (megafauna), to

small endofaunal organism s (meio- and

m acrofauna), including the very specific

seep-related m icrobial com m unities. In

addition to biodiversity patterns in rela

tion to the high habitat heterogeneity

w ithin a region, sim ilarities in com m uni

ties am ong regions are currently under

investigation in order to gain better

insight into the biology, biodiversity, and

biogeography of seep-associated biota

along Europe’s continental margins.

HE R ME S C O L D SEEP

S T U D Y SITES

Along the N ordic m argin, the highly

active H âkon Mosby m ud volcano

(72°N) at 1280-m water depth on the

Barents Sea slope south of Svalbard, was

the target o f several m ultidisciplinary

cruises (Figures 1A, 2). The Storegga

slide at 64°N and associated Nyegga

pockm arks were also visited (Figure 1A).

Hâkon Mosby m ud volcano was first

observed in 1989 during a side-scan

sonar survey (Vogt et ah, 1997). An

expedition in 1995 m easured very

high tem perature gradients in the sedi

m ents, recovered m ethane hydrate from

2-m subbottom depth and sampled

siboglinid polychaetes, suggesting active

chem osynthesis (Vogt et a l , 1997). The

concentric structure of the m ud volcano

can be divided into several subhabitats

characterized by different biogeochem i

cal sedim ent conditions (de Beer et ah,

2006; N iem ann et ah, 2006b).

The Storegga area is well know n for

its giant Holocene slide, one of the larg

est ever m apped on continental m argins

(Pauli et a l , 2008). O n the northeastern

flank o f the Storegga slide, complex

pockm arks are located in the so-called

Nyegga area at 740-m water depth. These

pockm arks are circular in plan view and

feature up to 190-m-long ridges of car

bonate rock (Hovland et a l, 2005).

Ann Vanreusel ([email protected]) is Professor, Marine Biology Research Croup, Uniuersiteit Cent, Cent, Belgium. Ann C. Andersen

is Professor, Uniuersité Pierre et Marie Curie (UPMC), and a researcher in Equipe Ecophysiologie: Adaptation et Evolution Moléculaires,

UMR 7744 - Centre national de la recherche scientifique (CNRS) - UPMC, Station Biologique, Roscoff, France. Antje Boetius is Head, Microbial

Habitat Croup, M ax Planck Institute fo r Marine Microbiology, and Professor, Jacobs University Bremen, Germany. Douglas Connelly

is a researcher in the Geology and Geophysics Group, National Oceanography Centre, University o f Southam pton, Southam pton, UK.

Marina R. Cunha is Professor, Centro de Estudos do A m biente e do M ar (CESAM), D epartem ento de Biologia, Universidade de Aveiro,

Campus Universitario de Santiago, Aveiro, Portugal. Carole Decker is PhD Candidate, Deep-Sea Ecosystem Department, Institut français

de recherche pour l'exploitation de la m er (Ifremer), Centre de Brest, Plouzané, France. Ana Hilario is a postdoctoral researcher a t CESAM,

Departem ento de Biologia, Universidade de Aveiro, Campus Universitario de Santiago, Aveiro, Portugal. Konstantinos Ar. Kormas is

Assistant Professor, D epartm ent o f Ichthyology and Aquatic Environment, University o f Thessaly, Nea Ionia, Greece. Loïs Maignien is

PhD Candidate, Laboratory o f Microbial Ecology and Technology (LabMET) and Renard Center fo r Marine Geology (RCMG), Uniuersiteit

Cent, Cent, Belgium. Karine Olu is a researcher in the Deep-Sea Ecosystem Department, Ifremer, Centre de Brest, Plouzané, France.

Maria Pachiadaki is PhD Candidate, D epartm ent o f Chemistry, University o f Crete, Heraklion, Greece. Benedicte Ritt is PhD Candidate,

Deep-Sea Ecosystem Departm ent, Ifremer, Centre de Brest, Plouzané, France. Clara Rodrigues is PhD Candidate, CESAM, Departemento

de Biologia, Universidade de Aveiro, Campus Universitario de Santiago, Aveiro, Portugal. Jozée Sarrazin is a researcher in the Deep-Sea

Ecosystem Departm ent, Ifremer, Centre de Brest, Plouzané, France. Paul Tyler is Professor, National Oceanography Centre, University o f

Southam pton, Southam pton, UK. Saskia Van Caever is a postdoctoral researcher in the Marine Biology Research Group, Uniuersiteit Cent,

Cent, Belgium. Heleen Vanneste is PhD Candidate, School o f Ocean and Earth Science, University o f Southam pton, UK.

112 Oceanography Vol. 22, No.1

mailto:[email protected]

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Figure 1. ( to p left) O verview m ap. (A) N ordic

m argin: Flâkon M osby m u d volcano, S toregga

slide, a n d N yegga area in th e n o rth iden tified on

th e m ap. Vicking cruise © ifrem er 2000. (B) G ulf o f

Cádiz: Sim plified geological m a p a fte r M ed ia ldea

e ta l . (2004), show ing th e loca tions o f know n m u d v o lcanoes (com pila tion o f Kenyon e t al., 2000,

2003, 2006; A k h m e tzh an o v e t al., 2007) w ith th e ir

g eochem ical charac te ris tics as d e te rm in e d so far

(com pila tion o f Som oza e t al., 2003; N iem ann

e t al., 2006a; S tadn itska ia e t al., 2006; Flaeckel

e t al., 2007; a n d Flensen e t al., 2007). M u d vo lcano fields: G R D = G uadalquiv ir D iapiric Ridge; Tasyo;

SPM =Spanish M o ro ccan M argin; D PM =D eep-

Po rtuguese M argin. (C) Eastern M ed ite rran ean

Sea: Seep sites visited d u rin g th e M ed ite rran ean

D eep-Sea Ecosystem s (M EDECO) cruise in 2007,

includ ing th e N apoli a n d A m sterdam m u d volcanoes as well as d iffe ren t areas in th e Nile D eep Sea

Fan. MEDECO cruise © Ifrem er 2007

MOTH


u n s u r e 14 '44 'trE

rwao"N

T ÎW N

T 2 ? 0 ' 1 D "N

Î ^ 'D - N - ■

%■ m *

ñ 4y «

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d l l ;

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it

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Figure 2. OTUS im age o f th e Flâkon M osby m u d v o lcano in th e n o rth . A rea covered by

op tica l su rvey (OTUS cam era), rep resen tin g 30% o f a 400 x 400-m area. F o o tp rin ts o f

each p h o to are georeferenced . Vicking cruise © Ifrem er2006

The G ulf of Cádiz is located between

Iberia and Africa on the A tlantic side,

between 9°W and 6045'W, and 34°N

and 37°15'N. The hydrography of the

study area is complex, w ith the influ

ence of M editerranean outflow water on

the shallower eastern m ud volcanoes,

and evidence for input of h igh-nutrient

A ntarctic Interm ediate Water in the

deeper western regions (Van Aken,

2000). The area has a com plex tectonic

h istory and is now dom inated by thick

sedim entary deposits. Since their initial

discovery in the area in 1999 (Kenyon

et al., 2000), a large num ber of m ud vol

canoes have been identified, located in

four m ain fields and exhibiting different

but generally very localized hydrocar

bon seepage (N iem ann et a l , 2006b;

Figure IB). The presence of carbonate

chim neys indicates past activity. At m ost

of them , the m ajority o f the m ethane is

consum ed w ithin the sedim ents, and

does not reach the hydrosphere.

Different seep sites are also pres

ent in the eastern M editerranean Sea

(Figure 1C), where intense emission

of m ethane occurs from the center of

active m ud volcanoes and along related

faults (M EDINAUT/M EDINETH 2000,

Charlou et a l, 2003; D upré et al., 2007).

D uring the last decade, three major

areas were the focus of m ultidisciplinary

cruises using submersibles: the Olimpi

m ud volcano field, located on the

M editerranean Ridge south of Crete

(Mascle et a l , 1999); the A naxim ander

M ountains, south of Turkey, caught up

in the plate convergence between Africa

and Eurasia (W oodside et a l , 1998); and

the seafloor of the Nile Deep Sea Fan

(Nile delta turbidic system; Loncke et al.,

2004). The Olimpi m ud volcano field and

A naxim ander M ountain areas, located at

depths between 1700 m and 2000 m, are

characterized by strong com pressional

tectonic processes superim posed by

faulting. They harbor large conical m ud

volcanoes several kilom eters across but

only a few hundred m eters high. Fresh

m ud flows, brines, clasts, and carbonate

crusts were observed on their surface,

depending on the current activity o f the

volcano (Ziffer et a l , 2005). In a passive

m argin context, the Nile deep turbidic

system displays m any fluid-releasing

structures on the seafloor, including m ud

volcanoes, m ud pies, and pockm arks

(Loncke et a l , 2004).

M A P P I N G H A B I T A T

H E T E R O G E N E I T Y A T

C O L D SEEPS

Cold seeps are characterized by the

patchy occurrence of sulfide and/or

m ethane-dependent biota, including

m icrobial m ats and sym biont-bearing

invertebrates (Bivalvia, Polychaeta) that

can form small clusters or spread over

large fields in high densities. This high

spatial variability at scales of tens to h u n

dreds of m eters has been attributed to

the m agnitude of fluid flow and the cor

related chemical depth profiles (H enry

et al., 1992; Barry et a l , 1997; Olu et al.

1997; Sahling et a l , 2002; Levin et a l ,

2003; de Beer et al., 2006). Low net flow

rates appear to provide sufficient m eth

ane from depth to fuel the near-surface

biological com m unities while still allow

ing downward transport and m ixing of

oxygen- and sulfate-rich seawater in the

upper few centim eters o f the sedim ent

(de Beer et a l , 2006). More intense fluid

flow is associated w ith altered pore-

water com position and elevated sulfide


concentrations extending to the sedi

m ent surface, thus allowing the growth

of m icrobial m ats (Tryon and Brown,

2001; Levin et a l , 2003).

To understand the spatial and tem

poral scales at which seep ecosystem

processes change, a crucial initial phase

in seep research is m apping the size and

distribution of different habitats and

identifying the associated com m unities

(Sibuet and Olu-Le Roy, 2002). A great

step forward in the precision of habitat

m apping has been achieved in the last

few years with use of rem otely operated

vehicles (ROVs), which allows regular

transects over long distances in com

bination with m ore precise positioning

m ethods. There is also rapid progress in

optical cam era resolution and data p ro

cessing using Geographic Inform ation

System (GIS)-supported image analysis.

O n the H âkon Mosby m ud volcano,

the concentric d istribution of habitats

around a central crater, apparently not

colonized, was first described from

towed video systems and observations

by submersibles (Milkov et al., 1999;

G ebruk et a l, 2003).

The first predictive habitat map was

based on ROV video m osaics processed

by Jerosch et al. (2007) using geostatisti-

cal analysis. These authors estim ated

the percent coverage for each targeted

habitat: m ud apparently devoid of life in

the center, surrounded by areas densely

inhabited by m icrobial mats, particularly

in the south; and hum m ocky outer parts

colonized dom inantly by siboglinids.

D uring the HERMES Vicking cruise

(2006), a new habitat m apping survey

was conducted (Figure 2) by m eans of

parallel transects at 8-m altitude above

the seafloor, using the black and white

high sensibility cam era OTUS m ounted

on the ROV Victor 6000 survey module.

At this altitude, each picture covers a

surface of ~ 64 m 2 (Figure 3A, B). The

new habitat m ap suggests changes in the

colonization of m ud flows by m icrobial

m ats and siboglinids between 2003

(Jerosch et a l , 2007) and 2006 (recent

work of authors Olu, Fabri, Deep-Sea

Ecosystem D epartm ent of Ifremer, and

others). A sim ilar spatial organization of

habitats (central seep area surrounded

by m icrobial m ats and siboglinid fields

in the external ring) was also observed

at small individual pockm arks along the

Storegga slide and in the Nyegga area,

but at a m uch smaller scale (decim eter to

meter) (recent w ork of author Olu).

In 2007, the MEDECO cruise

aboard RV Pourquoi pas? visited sev

eral different seep sites in the eastern

M editerranean, four of which were the

focus of systematic ecological studies at

different spatial scales: the Napoli m ud

volcano south of Crete, the A m sterdam

m ud volcano south of Turkey, and a

pockm ark field and the Cheops m ud

volcano located in the Nile delta. Five

different habitats were recognized by the

presence of visible features such as key

megafaunal taxa (Bivalvia, Siboglinidae)

or m icrobial mats on the seafloor. More

extensive habitat and m egafaunal dis

tribu tion surveys on the Napoli m ud

volcano (33°43.7777'N, 24°40.9495'E;

1750-1934-m depth) were based on

regularly spaced transects at 10-m alti

tude with each OTUS picture covering a

surface of - 100 m 2. This survey showed

that num erous brine pools characterized

the southeast sector (Figure 3C), cor

responding to depressions on the m icro-

bathym etric map. Small tubeworm s

were rarely observed. The n o rthern part

showed a m ore disturbed environm ent,

colonized by siboglinids. A bundant

em pty bivalve shells were lying on the

seafloor, possibly indicating the extinc

tion of previous bivalve-dom inated

com m unities (recent w ork of authors

Olu and Sarrazin).

E N D O S Y M B I O N T - B E A R I N G

C H E M O S Y N T H E T I C F A U N A

Megafaunal species com prise organ

isms larger than 2 cm that are generally

visible on seafloor optical images. Cold

seep ecosystems provide niches for

chem o-synthetic com m unities based on

reduced com pounds such as m ethane

and sulfide, which are energy sources

for CO,-fixing symbiotic bacteria. These

symbioses between invertebrates and

sulfur-oxidizing and/or m ethanotrophic

bacteria are only found in highly reduced

environm ents, and are an obvious exam

ple of how cold seep ecosystems add

biodiversity to m arine deep-water life.

D uring our HERMES research, we were

able to identify the dom inant chemosyn-

thetic symbioses on Europe’s continental

m argins, but m ost likely m uch more

rem ain to be discovered.

At the H âkon Mosby m ud volcano,

m egafauna are dom inated by sibo

glinids (tubeworm s) that lack both

m outh and gut and live in symbiosis

w ith sulfur-oxidizing bacteria stored

inside their bodies (Lösekann et al.,

2008). W ide areas in the periphery of

this m ud volcano are covered with the

curled brownish tubes of the species

Sclerolinum contortum (Figure 3D), bu r

ied up to 70-cm deep in soft sedim ent. In

some areas, clusters of the straight black

tubes of Oligobrachia haakonmosbiensis

webbi (Smirnov, 2000) stand erect about

5 cm above the seafloor. Both species are

also found further south on pockm arks


Figure 3. Exam ple o f OTUS p h o to s show ing (A) m icrobial m a ts an d zoarcid fishes an d (B) a p a tch o f siboglin id po lychaetes. P h o to size is 64 m 2. Vicking cruise © Ifrem er2006. (C) A brine poo l on th e su m m it o f th e Napoli m u d volcano. MEDECO 2007

©Ifremer. (D ) View o f a w ide field o f siboglin id po lychaetes a t Flâkon M osby m u d volcano. The cu rled b row nish Sclerolinum

su rro u n d s a large s p o t o f black, s tra ig h t Oligobrachia tu b es. An o ran g e sea s ta r lies in fro n t o f a Sclerolinum p a tch covered by

w hitish bacterial filam ents. Vicking cruise © Ifrem er2006

at the Storegga slide and at Nyegga,

where they su rround every dark spot of

m ethane seepage (recent w ork of author

A ndersen). M any small symbiont-

bearing bivalves belonging to the family

Thyasiridae have been sam pled on these

sites, especially in siboglinid fields at the

Hâkon Mosby m ud volcano, whereas

num erous larger Vesicomyidae shells

have also been observed at the Storegga

and Nyegga pockm arks (recent w ork of

authors Decker and Olu).

At Nyegga, 1-m -high pillow structures

covered with a carpet of siboglinids are

know n as “subm arine pingoes;” they

are described by Hovland and Svensen

(2006) as local hydrate (ice) accum ula

tions. However, during the HERMES

Vicking cruise in 2006, observation

and sam pling by ROV Victor 6000

showed the pingoes to be com posed

of m ud accum ulations w ith entangled

Sclerolinum, soft enough to be sampled

by blade core. In all the explored areas,

Sclerolinum seem to dom inate, whereas

Oligobrachia has a discrete, highly patchy

distribution (recent w ork o f authors

A ndersen and Olu). The factors that con

trol the spatial d istribution of these two

species rem ain unclear. The local sedi

m ent chemistry, the penetration of the

worm s into the seabed, and som e of the

worm s’ physiological adaptations con

cerning their hem oglobins seem to differ

between the two species, and m ay affect

their habitat selection (recent w ork of

author Andersen). However, other fac

tors such as their reproduction and dis

persal m ay also play a role. Filam entous


bacteria often cover their tubes and the

spaces between tubes provide shelter to

a highly diversified m acrofauna, particu

larly between the tw isted creeping tubes

of Sclerolinum. Sclerolinum can therefore

be com pared to other habitat-providing

species such as deep-water corals, as it

harbors a great epifaunal biodiversity on

the otherw ise barren soft sedim ents of

the Norwegian deep margin.

In contrast to the H âkon Mosby

m ud volcano, where perm anently high

fluxes of reduced com pounds are read

ily indicated by the presence of large

aggregations of siboglinids and bacterial

mats, the m ud volcanoes in the G ulf of

Cádiz do no t show evidence of dense

aggregations of living chem osynthetic

megafauna. An initial ROV transect at

1100-m depth on the D arw in m ud vol

cano during a sam pling cam paign with

RRS James Cook in 2007 revealed a mass

of mytilids identified as Bathymodiolus

mauritanicus (Figure 4A) on the top

of this m ud volcano. However, m ost

of this accum ulation com prised em pty

shells. Further along the transect, rock

exposures (Figure 4B) and vast carbon

ate outcrops (Figure 4C) were observed

w ith bo th live and dead mussels w ithin

cracks in the carbonates. These obser

vations suggest that the D arw in m ud

volcano had once been very active and

that the release of m ethane was sufficient

to support a considerable population of

mytilids. Cessation of seep activity prob

ably leads to the death of the population.

This event took place relatively recently

as m any of the shells rem ained intact

and articulated. A small area (about

100 cm 2) of soft, blue-grayish-colored

sedim ent (Figure 4D) was observed

in the northw est corner of the m ud

volcano that, when disturbed, released

considerable quantities of m ethane, but

contained no obvious chem osynthetic

fauna. O ther megafauna, not directly

chem osynthesis-dependent, consisted

of stylasterine corals attached to the car

bonate cap (Figure 4E), scavenging crabs

(Figure 4F), and corals (Figure 4G).

Aside from the dead mytilid fields,

the chem osynthetic species o f the Gulf

of Cádiz live m ostly buried inside the

sedim ents, a distribution that is p rob

ably related to the shallow (< 30 cm)

depth of the sulfide/m ethane gradient.

The m ost com m on species include

siboglinid polychaetes (Siboglinum spp.)

and solemyid bivalves (Acharax sp.,

Petrasma sp.), bu t also other frenu-

late (Polybrachia, Spirobrachia,

Bobmarleya, Lamellisabella) (Figure 5)

and bivalve taxa (Lucinoma, Thyasira,

Bathymodiolus, Vesicomyidae) (Génio

et al., 2008; H ilário and Cunha, 2008;

Rodrigues et a l , 2008). The first results

of stable isotope analyses (ô13C, ô15N,

ô34S) support the occurrence of chem os

ynthetic production in these species,

with th io trophy (H,S) being the m ain

m etabolic pathway in the benthic food

Figure 4. B athym etry an d h a b ita ts asso c ia ted w ith th e Darw in m u d volcano: (A) B athym odiolus m auritanicus, (B) rock exposure, (C) c a rb o n a te o u tc ro p s , (D) soft, b lue-gray ish-co lored sed im en t,

(E) s ty laste rine corals, (F) scaveng ing crabs, a n d (G) corals a t ta c h e d to an u p tu rn e d p iece o f car

b o n a te crust.

7.193032’W


web (recent w ork of author Rodrigues

and colleagues).

The first data on M editerranean cold

seep com m unities were acquired during

the French-D utch MEDINAUT cruise

(1998). Chem osynthetic com m unities

from the Olim pi and A naxim ander m ud

fields were m ostly concentrated near the

sum m its of the volcanoes, where fluid

expulsion is concentrated (Olu-Fe Roy

et ah, 2004). The com m unities were

dom inated by small-sized bivalves from

four families com m on to cold seep

environm ents (Mytilidae, Vesicomyidae,

Thyasiridae), or to shallower sulfidic-

rich habitats (Fucinidae). However,

large-size bivalve genera typical o f cold

seeps (Bathymodiolus and Calyptogena)

were absent. Siboglinids of the O bturata

group (genus Lamellibrachia) were found

nearby or in close relation to carbonate

crusts (Figure 6A). Differences in the

biological activity can be related to the

variability and intensity of fluid expul

sions between the volcanoes (Olu-Fe Roy

et ah, 2004), as supported by variable

m ethane concentrations m easured above

the seafloor (Charlou et a l , 2003). Small

Siboglinidae of the Frenulata group

(Siboglinum sp.) were also collected.

D uring the HERMES BIONIF cruise

to the Nile Deep Sea Fan in 2006, new

samples from the three dom inant

sym biont-bearing m acrofaunal species

were collected. The clam Lucinoma aff.

kazani was found w ithin the sediments,

the mytilid Idas sp. was attached to

different hard substrata (crusts, tubes,

urchins), and siboglinid tubeworm s

occurred either on reduced sedim ents

(Am on m ud volcano) or on carbonate

crusts (central pockm ark area). Symbiotic

associations have been described for

Lucinoma aff. kazani and for the small

mytilid Idas sp., the latter harboring an

exceptional num ber of symbionts in its

gills (D uperron et a l , 2006, 2007).

" N O N S Y M B I O T I C ” M E G A F A U N A

The m egafauna at seeps also include

m any nonsym biont-bearing species,

which profit in m any different ways

from the large biom ass and productiv

ity o f chem osynthetic megafauna. They

are attracted by the heterogeneity of the

habitats, the abundance of prey, or pos

sibly to the elevated topographic posi

tion provided by m ud volcanoes. At the

Hâkon Mosby m ud volcano, the m ost

abundant species in the megafaunal size

class is the fish of the Zoarcidae family,

Lycodes squamiventer (G ebruk et a l,

2003) (Figure 6B). Image analysis from

the Vicking cruise (2006) confirm ed

previous observations of G ebruk et al.

(2003) on the d istribution of this zoarcid

fish: they show the highest abundances

in the m ost active area of the volcano,

and are particularly associated with

microbial m ats (recent w ork o f authors

Olu and Decker). Zoarcidae is the typical

fish family encountered at hydrotherm al

vents and cold seeps, w ith some endem ic

species likely having adapted to the

toxic environm ent.

O n the Storegga slide and in Nyegga

pockm arks, nonsym biotic m egafauna

are m uch m ore abundant and diverse,

probably for two reasons. First, the cold

seeps are m uch smaller com pared to

the H âkon Mosby m ud volcano, they

are sparsely distributed, and m ethane

concentrations in seawater are quite

low (J.F. Charlou, M arine Geosciences

D epartm ent, Ifremer, pers. com, 2008).

Second, the water depth is shallower

(600-1000 m) and the Storegga slide

is likely to be a site of high detritus

input that favors the presence of sus

pension and deposit feeders. The very

large ophiurid Gorgonocephalus sp.

(Figure 6C), reaching up to 0.5-m diam

eter, is the m ost striking species of this

background megafauna, bu t abundant

comatules, crinoids, and pedonculate

sponges were also observed.

In the G ulf o f Cádiz, several

nonchem osynthetic species were

observed associated w ith different m ud

volcanoes at various water depths. In

contrast to the shallower m ud volca

noes, the Carlos Ribeiro m ud volcano

at 2200-m water depth has a more

diverse nonchem osynthetic- dep endent

Figure 5. F renulata co llec ted d u rin g TTR17 cruise in th e G ulf o f Cádiz: (a) Siboglinum sp. (from Darwin m u d volcano), (b) Polybrachia sp. 1 (from P orto m u d volcano), (c) Polybrachia sp. 2 (from Sagres m u d

volcano), a n d (d ) Polybrachia sp. 3 (from Soloviev m u d volcano). Photos by A n a Hilario


Figure 6. (A) Lamellibrachia from th e pock m ark area in th e Nile D eep Sea Fan. MEDECO cruise © Ifrem er2007. (B) Lycodes squ a m iven ter (Z oarcidae) in a p a tch w ith siboglin id tu b e w o rm s a t th e Flâkon M osby m u d volcano. ARKXXII cruise

© M ARUM , University o f Bremen. (C) Richness o f th e back g ro u n d m egafau n a on S torrega slide, w ith th e g ian t o p h iu rid

G orgonocephalus sp. Vicking cruise © Ifrem er 2006. (D) U nusual large spec im ens o f th e sponge Rhizaxinella pyrifera on

N apoli m u d volcano. MEDECO cruise @ lfremer 2007

megafauna. The m ud volcano center

consists of series of concentric ridges

that support very few m egafauna except

siboglinid tubeworm s (Figure 7A)

and a mobile echinothurid sea urchin

found close to the “eye” of the volcano

(Figure 71). Most o f the m ore extensive

m egafauna com prise suspension-feeding

cnidarians situated at the periphery of

the m ud volcano, including poriferans

(Figure 6B), the sea pen Umbellula

(Figure 7C), and dense gorgonian bushes

(Figure 7F, G). Further off the m ud

volcano the enigm atic athecate hydroid

Monocaulus (Figure 7D) was observed.

At som e tim e in the past, m ud over

flowed the volcanos crest and slid down

its southeast side, where huge num bers

of deposit-feeding holothurians were

observed (Figure 7H).

In the eastern M editerranean, poly

chaetes are abundant around the Napoli

brine lakes and on the active sites on

A m sterdam m ud volcano. O ther associ

ated species include unusually large

specim ens of the Suberitidae poriferan

Rhizaxinella pyrifera (Figure 6D) that

was sam pled on Napoli m ud volcano.

Crustaceans such as galatheids, shrim ps,

and Chaceon mediterraneus crabs were

equally abundant at all sites. Farge densi

ties o f Echinus sp. were observed at active

sites, suggesting some sort of depen

dence on fluid emission (Olu-Fe Roy

et al. 2004; recent w ork o f authors Ritt,

Olu, and Sarrazin).

S M A L L - S I Z E D E N D O F A U N A

Since their discovery, m uch seep research

has focused on the chemosynthetic

megafauna as well as the associated

m icrobiota. Infaunal organisms, usually

of smaller size (macro- and meiofauna),

such as nem atodes, harpacticoid cope-

pods, polychaetes, am phipods, tanaids,

gastropods, ostracods, and kinorhynchs,

have been studied to a m uch lesser

extent. The HERMES project aimed at

painting a full picture of seep biodiversity

by investigating all size classes o f the b en

thos. The m acrofaunal and meiofaunal

com m unities at active cold seeps on the

N ordic m argin and in the G ulf o f Cádiz

and the eastern M editerranean were

studied for the first tim e, and analysis


I 8.42210VW 1 3.419487’W

Figure 7. B athym etry a n d fau n a asso c ia ted w ith Carlos Ribeira m u d volcano: (A) Siboglinid po lychaetes, (B) Porifera, (C) th e seapen U mbellula, (D) a th e c a te hydro id M onocaulus,

(F, G) gorgon ian bushes, (FI) h o lo th u rian s in high nu m b ers , an d (I) e ch in o th u rid sea urchin.

of the samples is currently ongoing.

Initial results from the N ordic margin,

including different habitats found on

the H âkon Mosby m ud volcano (in its

center, m icrobial mats and siboglinid

polychaete fields) as well as the Storegga

and Nyegga cold seeps, show that the

m acrofauna (those between 500 pm

and 1-2 cm) are generally dom inated

by polychaetes. A quantitative analysis

revealed highly contrasting densities

am ong the habitats (recent w ork of

authors Decker, Van Gaever, and Olu);

the highest abundances were associ

ated with siboglinid fields (from 6700

to 56,000 ind. n r 2). M acrofauna were

m uch less abundant in the m icrobial

mats (1000 to 1600 ind. n r 2) and

even less abundant in the central area

(55-170 ind. n r 2). Great discrepancies

am ong habitats were also observed in

the taxonom ic diversity, because only

a few species are able to colonize the

m ore sulfidic and oxygen-depleted

sedim ents at the m icrobial m at sites.

There, the m acrofauna were dom i

nated by a polychaete belonging to the

genus Capitella (Figure 8A), whose

shallow-water species from the Capitella

capitata complex is adapted to organic

and sulfide-rich environm ents and is

used as an indicator o f pollution. In

contrast, Siboglinidae fields were colo

nized by a higher taxonom ic diversity

with at least seven polychaete families

(M. M orineaux, Deep-Sea Ecosystem

D epartm ent, Ifremer, pers. com., 2008)

and other groups, including poriferans,

molluscs (Bivalvia, G astropoda), and

crustaceans (Am phipoda, Tanaidacea,

Isopoda). Similar differences in com

m unity structure and dom inant taxa

am ong habitats were observed in the

Storegga and Nyegga pockm arks (recent

work of authors Decker, Van Gaever,

and Olu). Ongoing w ork on dom inant

taxa will com pare Storegga/Nyegga and

Hâkon Mosby m ud volcano com m uni

ties at higher taxonom ic levels to test

the influence of geographic patterns

com pared to habitat influence on the

structure of communities.

Significant differences in diversity

and abundance of the meiofaunal

com m unities (organisms passing

through a 1-mm sieve and retained on

a 32-pm sieve) associated with differ

ent habitats were also found. The bare,

m uddy sedim ents from the active center

yielded the lowest nem atode densities,

but unusually high benthic copepod

abundance (271 ± 37 ind. 10 cm 2;

Van Gaever et a l , 2006). In contrast, one

single nem atode species, Halomonhystera

disjuncta Bastian 1865 (Figure 8B), pre

viously described from shallow-water

habitats, was found in extremely high

abundances (> 11,000 ind. 10 cm 2;

Van Gaever et a l , 2006) in the bacte

rial sedim ent-covering Beggiatoa mats.

Biomarker fatty acid and stable carbon

isotope analyses of H. disjuncta revealed

that this species was thriving on chemo-

synthetically derived food sources, in

particular, on the Beggiatoa bacteria

(recent w ork of author Van Gaever and

colleagues). The uncom m on ovovi-

viparous reproduction of H. disjuncta


at H âkon Mosby m ud volcano has been

identified as an im portant adaptation

of parents to secure the survival and

development of their brood in this anoxic

environm ent. This nem atode species

was not found on the adjacent Storegga

slide or in the Nyegga area, nor in any of

the other cold seeps studied in the Gulf

of Cádiz or the eastern M editerranean.

Here, the reduced sedim ents host a

very impoverished nem atode assem

blage, in term s of both diversity and

density, that is dom inated by one or

two species belonging to the genera

Terschellingia, Thalassomonhystera,

Sabatieria or Desmodora (Van Gaever

et a l , in press). At least three of these

dom inant species (i.e., Halomonhystera

disjuncta, Terschellingia longicaudata

De M an 1907, and Sabatieria mortenseni

Ditlevsen 1921) were already described

as com m on inhabitants of intertidal,

organically enriched mudflats. Seep

sedim ents that are strongly affected by

reduced fluids and characterized by

harsh environm ental conditions (such

as oxygen depletion, toxic sulfide levels)

generate a habitat that is difficult for

m ost o f the typical deep-sea nem atode

species to exploit. Only some oxygen-

stress-resistant, shallow-water nem atode

species with an extensive geographical

range are able to thrive in these deep-

sea reduced environm ents. In contrast,

the seep sedim ents colonized by sibo

glinid polychaetes display very diverse

nem atode com munities, highly similar

in term s of generic diversity com pared to

the surrounding background sediments.

Siboglinidae are know n to strongly

affect the geochemical conditions in the

sedim ent surrounding the tube through

their intense ventilation activity (Julian

et a l , 1999; Bergquist et a l , 2002).

Consequently, well-oxygenated sedim ent

down to 5-cm depth is created (de Beer

et a l , 2006), providing a suitable habitat

for a wide range of nem atode species.

Siboglinidae fields and “control” samples

of deep-sea sedim ents yield comparable

highly diverse nem atode assemblages, but

a shift in dom inant families and genera

was detected (Van Gaever et a l, in press).

The endobenthic com m unity of the

m ud volcanoes in the G ulf o f Cádiz dis

plays wide variability in species com posi

tion and structure. Densities com m only

vary from a few hundred to thousands

per square meter, bu t local patches of

greater than 20,000 ind. n r 2 often occur.

The shallower m ud volcanoes of the

M oroccan field (200-1000-m depth)

show higher densities and num ber of

species b u t a low degree of endemicity,

while the few samples taken from the

Portuguese field (2000-3000-m depth)

show lower densities and species num ber

but suggest that endem icity is clearly

higher at these deeper m ud volcanoes as

m any of the species collected (including

the chem osynthetic ones) do not m atch

the available descriptions of sim ilar taxa.

In the eastern M editerranean, differ

ent habitats were selected for systematic

sam pling (recent w ork of authors Ritt,

Sarrazin, and colleagues). Prelim inary

results on the Napoli m ud volcano

show that the “Lamellibrachia habi

tat” has higher m acrofaunal densities

(5133 ± 3993 ind. n r 2) than the “bivalve

habitat,” where the highest density

reaches only -2 1 1 7 ± 226 ind. n r 2

(recent w ork o f authors Ritt and

Sarrazin). Despite lower faunal density,

the latter habitat exhibits a higher taxo

nom ic richness. Characterization of the

physico-chem ical conditions is no t yet

Figure 8. Small-sized e n d o fa u n a w ith (A) th e po ly ch aete Capitella sp. a n d (B) th e n e m a to d e H alom onhystera disjuncta.


finalized but a significant difference in

oxygen penetration in the sedim ents was

m easured—lim ited to a few millim eters

into the sedim ent in the “Lamellibrachia

habitat” but reaching several tens of m il

lim eters in the “bivalve habitat” (recent

w ork o f authors Ritt and Sarrazin). At

the rim of the A m on m ud volcano, a

m uddy brine flow characterized by

blackish sulfidic sedim ents was sampled.

Prelim inary results from analyses of the

m acrofauna from the BIONIL cruise

(RV M eteor/Quest, 2006) show that this

particular habitat (only fauna > 1 m m

have been sorted so far) exhibits a high

abundance of polychaetes in addition to

the presence of three families of bivalves

(Lucinidae, Thyasiridae, Vesicomyidae)

typical of chem osynthetic or reduced

habitats. Species richness on this p rob

ably short-lived habitat appears to be

lower than on other seep habitats studied

in this region. O n the pockm ark area

(1700 m, Nile Delta), the “reduced

sedim ent” sample contained a high

abundance of dorvilleid polychaetes,

characteristic o f reduced habitats.

Overall, the prelim inary results

obtained during the BIONIL (2006) and

M EDECO cruise (2007) show a vast he t

erogeneity o f habitats and faunal assem

blages, even w ithin tens to hundreds of

m eters w ithin different geological struc

tures. More data need to be analyzed

to highlight faunal and environm ental

sim ilarities am ong sim ilar habitats

(bivalve, siboglinid) sam pled from differ

ent m ud volcanoes.

M I C R O B I A L C O M M U N I T I E S

A T C O L D SEEPS

Similar to hot vents, cold seeps support

an enorm ous biom ass of free-living

and symbiotic m icrobial life that is

nourished by the oxidation of m ethane,

higher hydrocarbons, and sulfide. In fact,

m ethane-fueled m icrobial com m unities

in anoxic sedim ents above gas hydrates

and gas vents have the highest biomass

know n to occur in m arine ecosystems,

with up to IO12 cells per cm 3 (Boetius

et ah, 2000). Because of their distinct

m etabolic abilities, which are adapted

to the exploitation of reduced chemical

com pounds, m ethanotrophs, hydro

carbon degraders, and sulfate-reducing

and sulfide-oxidizing bacteria are the

key functional groups at cold seep eco

systems (Jorgensen and Boetius, 2007).

Unfortunately, environm entally relevant

representatives of these functionally

relevant bacterial and archaeal clades

have not yet been isolated, bu t a variety

of nucleic acid and m em brane lipid-

based m olecular identification m ethods

have been instrum ental in HERMES

investigations of the m icrobial diversity

of European cold seeps. The m ain groups

at cold seeps can be sum m arized as

follows. H ydrocarbon degradation is

usually dom inated by sulfate-reducing

bacteria of the D eltaproteobacteria

(Knittel et al., 2003). In contrast to m ost

other seafloor habitats, cold seep sedi

m ents host a h igh proportion of archaea,

m ainly m ethanotrophic and m ethano-

genic Euryarchaeota and uncultured

Crenarchaeota (Knittel et a l , 2005). The

m icroorganism -m ediated anaerobic

oxidation of m ethane (AOM) with

sulfate is the dom inant process at cold

seep ecosystems and the cause of the

observed high sulfide fluxes. The organ

isms m ediating AOM are anaerobic

m ethanotrophic (ANME) archaea that

form consortia with sulfate-reducing

Deltaproteobacteria o f the Desulfosarcina

(Boetius et a l , 2000) or Desulfobulbus

groups (Lösekann et al., 2007).

A key indicator com m unity o f active

cold seep ecosystems is m icrobial mats,

some of which cover hundreds of m eters

of seafloor, for example, at the H âkon

Mosby m ud volcano (N iem ann et a l,

2006b). These mats typically consist of

giant, vacuolated sulfur-oxidizing bac

teria, such as Beggiatoa, Thioploca and

Thiomargarita spp., which exploit the

high AOM -derived sulfide fluxes at the

seafloor (Figure 9). Such bacteria can use

internally stored nitrate to oxidize sulfur

and fix carbon dioxide for growth, thus

coupling the carbon, nitrogen, and sulfur

cycles in seep sedim ents. Their diversity

is m uch higher than anticipated, and

each population has distinct adaptations

to enable the use of the steep gradients of

sulfide, nitrate, and oxygen that develop

in the m ethane-rich sedim ents (Preisler

et ah, 2007). M icrobial m ats at seeps

are often very patchy and m ainly white

(caused by the reflection of the intracel

lular sulfur granules), but they are also

found in shades of yellow, orange, or

grey. Thiotrophic mats usually com prise

a diverse m ixture of m ostly bacterial

taxa, bu t are dom inated by large fila

m entous sulfide-oxidizing bacteria or by

small thiotrophic Epsilonproteobacteria

such as Arcobacter (Om oregie et ah,

2007). Some of these “giant” sulfide-

oxidizing microbes, such as the filam en

tous Beggiatoa bacteria, have a gliding

m ovem ent with which they position

themselves w ithin a steep gradient of

oxygen and sulfide (Preisler et a l , 2007);

others depend on a flux of sulfide to the

bottom -w ater interface.

Lösekann et al. (2007) describe in

detail the relationship am ong the bacte

rial mats and the m ethanotrophic and

sulfate-reducing bacteria found at the


Figure 9. M acroscop ic an d m icroscop ic im ages o f m icrobial m a ts a t co ld seep ecosystem s. (U p p e r panel, left) Thiom argarita m a t

in a fau lt su rro u n d in g th e A m on m u d volcano. © M ARUM /M PI. (M idd le) Thin filam en tous m a ts a t th e c e n te r o f th e A m on m u d

volcano. © M ARU M /M PI (R ight) Thick filam en to u s m a ts su rro u n d in g th e c e n te r o f th e Flâkon M osby m u d volcano. © IfremeriAW I.

The m icrog raphs in th e low er panel show th e respec tive m a t-fo rm in g th io tro p h ic bacteria. (Left) Sphere-like v acuo late Thiom ar

garita cell. (M idd le) G ian t filam en to u s v acuo late g a m m a p ro teo b ac te ria . (R ight) Thin filam en to u s v a cuo late Beggiatoa cells. © Stefanie Griinke, M PI/AW I

Hâkon Mosby m ud volcano. Briefly,

in the active volcano center, the m ain

m ethane-consum ing process was bac

terial aerobic oxidation. In this zone,

aerobic m ethanotrophs belonging to

three bacterial clades closely affiliated

w ith M ethylobacter and M ethylophaga

species accounted for 56 ± 8% of total

cells. In sedim ents below the Beggiatoa

mats encircling the center o f the Hâkon

Mosby m ud volcano, m ethanotrophic

archaea of the ANME-3 clade dom inated

the AOM. They form cell aggregates

with sulfate-reducing bacteria o f the

D esulfobulbus (DBB) branch, com pris

ing 94% ± 2% of the total m icrobial

biom ass at 2 -3 cm below the surface.

At the outer rim of the m ud volcano,

the seafloor is colonized by siboglin

ids. Here, bo th aerobic and anaerobic

m ethane oxidizers were found in lower

abundances, but distributed over a m uch

larger vertical and horizontal zone.

M icrobial diversity was higher at this site

com pared to the central and Beggiatoa-

covered part o f the H âkon Mosby m ud

volcano. Obviously, m icrobial diversity

and com m unity structure are closely

related to different fluid-flow regimes

at the H âkon Mosby m ud volcano, p ro

viding distinct niches for aerobic and

anaerobic m ethanotrophs.

M ud volcanism in the G ulf o f Cádiz

is characterized by a wide diversity of

processes and environm ental settings,

such as different types of fluid m igra

tion pathways, tectonic activity and/or

salt diapirism, m igration velocity, fluid

com position and alteration processes,

depth, sea bottom tem perature (from

4°C to 13°C if under the influence of the

M editerranean outflow water), and the

presence of gas hydrate. Because these

param eters create a wide array of unique

ecological niches for the seep m icrobial

com m unities, the Gulf of Cádiz is an

ideal natural laboratory for exploring the

diversity and activity of seep m icrobes in

relation to their environm ent. In the Gulf

of Cádiz, overall AOM activity is typical

for low to m oderately active seeps. For

instance, m axim um m ethane turnover

is typically around 20 nm ol cm3 day

at bo th Captain A ryutinov and Carlos

Ribeiro m ud volcanoes (N iem ann et al.,

2006a; recent w ork of author M aignien

and colleagues). However, some m ud

volcanoes deviate from this trend: at the

D arw in m ud volcano, thick carbonate

crusts and plates seal m ethane escape

routes. Discrete AOM hotspots have

been observed at the rim of the crater,

suggesting a relocalization of seep activ

ity. In these hotspots, AOM activity is

one order higher than at Carlos Ribeiro

m ud volcano and was found to sustain


the development of white bacterial mats.

In contrast, salt diapir-driven m ud volca

noes such as M ercator have hypersaline

pore water that probably inhibits m icro

bial activity, which was found to be one

order of m agnitude lower than at Carlos

Ribeiro m ud volcano, although m ethane

and sulfate are present in large am ounts.

Interestingly, these environm ental setting

variations and AOM activity are reflected

by diverse m icrobial com m unity com

positions. Inventories of archaeal and

bacterial phylotypes in m ethane-rich

sedim ents reveal that the three m icrobial

consortia know n to perform this reaction

(ANME-1, -2, and -3) are active with dif

ferent distribution patterns (Figure 10).

A nother major feature of m ud volcanoes

from the G ulf o f Cádiz is the very deep

origin of m igrating fluid and m ud reach

ing the surface (Hensen et a l , 2007).

HERMES w ork also shed some light

on the bacterial and archaeal diversity of

the m ud volcanoes at the Anaxim ander

M ountains, eastern M editerranean Sea.

The A naxim ander M ountains comprise a

group of three m ain m ountains between

the Cyprus and Hellenic arcs (Zitter

et al., 2005). The first gas hydrate sam

pling in the Anaxim ander M ountains

took place in 1996 at the Kula m ud

volcano (W oodside et a l, 1997,1998).

Today, hydrates have also been sampled

from four other m ud volcanoes in the

area. High seafloor m ethane fluxes are

associated with the m ud volcanoes as

well as with the accompanying cold

vents and seeps (Charlou et a l, 2003),

and the available gas provides energy

for rich benthic com munities, includ

ing chem osynthetic symbiotic fauna

(Olu-Le Roy et a l, 2004). Carbonate

crusts derived from anaerobic oxidation

of m ethane are form ed in these environ

m ents (Aloisi et al., 2002). O f the five

know n m ud volcanoes in the province,

m icrobial diversity data exist only for

prokaryotes (Bacteria and Archaea) from

the A m sterdam (ca. 2030 m) and Kazan

(ca. 1700 m) m ud volcanoes. Based on

16S rRNA gene diversity, the Am sterdam

m ud volcano harbors a rather diverse

bacterial community. Shannon diversity

index H ’ (a tool for com paring two dis

tinct habitats by com bining the quantifi

able term s of species richness and species

equitability; high H values indicate more

diverse com m unities—an H value of 0

indicates a com m unity with one species)

varies between 3.33 (carbonate crusts)

and 5.93 (sediments) (Heijs et a l , 2006,

2008; recent w ork of author Pachiadaki

and colleagues). The m ost abundant

phylotypes in carbonate crusts are

related to Actinobacteria, Clostridia, and

A lpha-, G am m a- and D eltaproteobacteria

as previously described (Heijs et al.,

2006). Regarding sediments, the m ajor

ity o f the phylotypes are closely related

to gas hydrate bearing sedim ents

(Knittel et a l , 2005). High num bers

of D eltaproteobacteria phylotypes

are present, as well as Actinobacteria,

Acidobacteria, A lpha-, G am m a-, Epsilon-

and Deltaproteobacteria, Firmicutes,

Cytophaga-Flexibacter group, and can

didate division WS3. Several phylotypes

have also been found from the Chloroflexi

and candidate division JS1. More rare

phylotypes are related to Planctomycetes,

Firmicutes (Bacilli), Bacteriodetes, and

candidate divisions OD1, OP8, OP 11,

and GN06. (Heijs et al., 2008; recent work

of Pachiadaki and colleagues).

Archaeal com m unities show lower

diversity with FI’ (base e) values rang

ing from 2.14 to 2.68 for sedim ents

while in carbonate crusts FI’ is 2.93

(Heijs et al., 2006, 2008; recent w ork

of author Pachiadaki and colleagues).

Most of the archaeal sequences found

in A m sterdam m ud volcano carbon

ate crusts belong to the Crenarchaeota,

M arine Group I (MGI). The rem ainder

of the crenarchaeal sequences fall into

a hitherto unclassified novel group of

Crenarchaeota whose related sequences

have previously been obtained from

deep-sea sedim ents (Vetriani et al.,

1999). The euryarchaeal sequences are

related to novel Therm oplasm ata or

M ethanosarcinales. The latter are affili

ated to ANM E-2 sequences (Heijs et a l ,

2008; recent w ork of author Pachiadaki

Figure 10. D iversity o f a nae rob ic ox ida tion o f m e th a n e (A O M ) c o m m u n itie s from th e G ulf o f Cádiz

m u d vo lcanoes show n w ith flu o rescen t in s itu hybrid ization im aging. (Left) ANME-2 ty p e aggregates

w ith m u ltip le archaeal cores s u rro u n d e d by b ac ter ia as o b serv ed in th e C arlos R ibeiro m u d vo lcano

AOM zone. (M idd le) ANM E-2 ty p e c lusters w ith a single archeal co re in a shallow m icrobial c o m m u

n ity o f th e Darw in m u d volcano. (R ight) ANME-1 ty p e o f archaeal filam en ts d o m in a te th e M erca to r

m u d vo lcano m icrobial com m unity . M icrobial cells are s ta in ed w ith th e archaeal specific p ro b e A rch915 (red ) an d DAPI s ta in in g (blue).


and colleagues), while all three groups—

ANME-1, ANM E-2, and ANM E-3—

have been found in A m sterdam m ud

volcano sedim ents. O ther sequences are

related to Methanomicrobiales, m arine

benthic group D (M BG-D), and the

Thermoplasmata. In com parison, the

sedim ents o f the Kazan m ud volcano

harbored less diverse bacterial assem

blages. The H ’ index varied between

2.52 and 3.63. The Kazan phylotypes

are related to the Acidobacteria,

Actinobacteria, Bacilli, Clostridia,

Chloroflexi, Spirochaetes, Nitrospira,

Planctomycetes, A lpha-, Gamma- and

Deltaproteobacteria, OP11, WS3, and a

few unclassified Bacteria (Heijs et a l ,

2007; Kormas et a l , 2008; recent w ork


Archaeal diversity was also lower, vary

ing between 1.63 and 2.57. The occur

ring phylotypes are related to MGI,

novel Crenarchaeota, Halobacteriales,

Methanosarcinales, Thermoplasmata,

and unclassified Archaea (Heijs et al.,

2007; Kormas et a l , 2008; recent w ork


Further w ork on the m icrobial biodiver

sity o f eastern M editerranean m ud vol

canoes and pockm arks of the Nile Deep

Sea Fan is underway, focusing on the

variety o f m icrobial mats and associated

com m unities (Om oregie et al., 2007).

O U T L O O K

Seeps, vents, and other reduced ecosys

tem s contain a variety o f organism s with

unique functions related to chemoau-

totrophy, respiration, detoxification,

m ineral precipitation and dissolution,

attachm ent, and sensing (chemotaxis).

A m ong the m ost rem arkable observa

tions regarding different size groups

and taxa, from bacteria to fish, are the

high heterogeneities from sm all to large

scales. Every seep region along the

European m argin is different in term s

of com m unity com position and biodi

versity, and high patchiness and other

differences are observed w ithin regions.

However, m any questions rem ain in the

quest to unravel the diversity, function

ing, and genom ic capacity o f chem osyn

thetic organisms, including free-living

m icrobes and symbiotic associations

with invertebrates. Chem osynthetic

habitats are isolated and highly fractured

ecosystems in which the organism s

require distinct environm ental features

and cues to m aintain their populations

(tem perature, presence of sulfide and

C H 4, hard ground, particle flux). The

life history of animals and m icrobes

restricted to chem osynthetic ecosystems

and their dispersal rem ains a key lim ita

tion in understanding the interconnec

tivity and resilience of these dynam ic

ecosystems. Interconnectivity can be

studied at different geographical scales

as well as am ong vents, seeps and other

habitats, which requires a com bination

of biological, oceanographic, and b io

geographic studies, including population

biology using genom ic m arkers to assess

gene flow. Furtherm ore, in a changing

ocean it becom es critical to assess varia

tions in biodiversity across all habitats

in order to distinguish between natural

and anthropogenic effects. The first

long-term observatories at cold seeps are

planned, and will provide data on the

link between environm ental fluctuations

and the fate of the benthic ecosystem.

A C K N O W L E D G E M E N T S

First, we would like to thank M yriam

Sibuet who was one of the initiators

of the HERMES project and the first

leader o f the Cold Seep Workpackage.

We also want to thank Phil Weaver and

Vikki G unn, respectively, the coordi

nator and m anager of the HERMES

project, which was funded under the

European Com m issions Fram ework

Six Program m e (EC contract no.

GOCE-CT-2005-511234). We acknowl

edge the captains, the crews, ROV teams,

and chief scientists o f the cruises:

• ARKTIS XIX/3b (2003): Polarstern

(M ichael Klages);

• BIONIL (2006): Meteor (Antje

Boetius);

• Vicking (2006): Pourquoi pas?,

Victor 6000 (Hervé Nouzé);

• M EDECO (2007): Pourquoi pas?,

Victor 6000 (Jozée Sarrazin and

Catherine Pierre). EZ

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