Biodiversity o f
Cold Seep EcosystemsAlong the
E u r oo ea n J\A a r e i n s
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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
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TAS Y O
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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
Oceanography M arch 2009 113
u n s u r e 14 '44 'trE
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T ÎW N
T 2 ? 0 ' 1 D "N
Î ^ 'D - N - ■
%■ m *
ñ 4y «
j .
d l l ;
Û \u V. ' ■
4 1l l i l a !nI t
it
î
i — i— t—« » H» m
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
114 Oceanography Vol. 22, No.1
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
Oceanography M arch 2009 115
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
116 Oceanography Vol. 22, No.1
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
Oceanography M arch 2009 117
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
118 Oceanography Vol. 22, No.1
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
Oceanography M arch 2009 119
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
120 Oceanography Vol. 22, No.1
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.
Oceanography M arch 2009 121
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
122 Oceanography Vol. 22, No.1
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
Oceanography M arch 2009 123
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).
124 Oceanography Vol. 22, No.1
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
of author Pachiadaki and colleagues).
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
of author Pachiadaki and colleagues).
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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