or collective redistirbution other or collective or means this reposting, of machine, is by photocopy article only anypermitted of with portion the approval The O of This article has been published in published been This has article HERMES SPECIAL ISSUE FEATURE , Volume 1, a quarterly 22, Number The O journal of of Cold Seep Along the ceanography Society. © European Margins 2009 by The O

By Ann Vanreusel, Ann C. Andersen, Antje Boetius, Permissionceanography is Society. Allreserved. rights granted to in teaching copy this and research. for use article Republication, systemmatic reproduction, Douglas Connelly, Marina R. Cunha, Carole Decker,

Ana Hilario, Konstantinos A. Kormas, all correspondence to:ceanography Society. Send [email protected] Th e O or Loïs Maignien, Karine Olu, Maria Pachiadaki, Benedicte Ritt, Clara Rodrigues, Jozée Sarrazin, Paul Tyler, Saskia Van Gaever, and Heleen Vanneste ceanography Society, P Box 1931, Rockville, M D 20849-1931, USA. 1931, Rockville, O Box

ROV Victor 6000 taking a water sample above a bush of in the central Deep Fan. Image courtesy of Ifremer/MEDECO Cruise 2007

110 Oceanography Vol.22, No.1 Abstract. During the European Commission’s Framework Six Programme, HERMES, we investigated three main areas along the European margin, each characterized by the presence of seep-related structures exhibiting different intensity of activity and biological diversity. These areas are: (1) the Nordic margin with the Håkon Mosby and many pockmarks, (2) the Gulf of Cádiz, and (3) the eastern Mediterranean with its hundreds of mud volcanoes and structures. One of the main 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 multidisciplinary research cruises to these three areas provided evidence of high variability in processes and associated biodiversity at different spatial scales, illustrating the “hotspot” nature of these deep water systems.

Introduction observation of the European continental (Sloan, 1990) to transform Soon after the discovery of the spec- margins using in situ video and photog- sulfate, thus producing high fluxes of tacular communities raphy with adapted deep submersibles (Jorgensen and Boetius, 30 years ago, other types of chemo- provided evidence for a wide range of 2007). Chemosynthetic microorgan- synthetic assemblages—so-called “cold active cold-seep ecosystems associated isms are the primary producers in seep seeps”—were found along continental with fluid, gas, and mud escape struc- food webs, depending on such reduced margins during submersible dives to tures. These structures include pock- chemicals as and sulfide as the deep (Paull et al., marks (seafloor depressions), brine lakes, their energy sources. 1984), zones off Oregon in and elevated or flat mud volcanoes. Similar to their hydrothermal vent the eastern Pacific (Suess et al., 1985), As with hot vents, cold seeps are counterparts, most cold seeps support and trenches off in the western characterized by the flow of reduced highly productive ecosystems (high Pacific (Juniper and Sibuet, 1987). Cold chemical compounds from the sub- ) that consist of specialized seeps are now among the most geologi- surface to the seafloor, but they are not metazoan communities dominated by cally diverse and widely distributed of directly associated with high thermal a few adapted taxa that can cope with the deep-sea reducing environments anomalies. Most known cold seeps elevated concentrations of chemical explored to date, and new sites are are associated with reduced environ- compounds and low oxygen levels at still being discovered every year. Since ments that are linked indirectly to gas and below the -water interface. their initial discovery, active seeps hydrates or to reservoirs. Other harsh conditions, such as high have been reported from shallow to Hence, in contrast to the majority of concentrations of or hadal (> 6000-m) depths (Sibuet and marine deep-water ecosystems, which high-salinity brines, may locally reduce Olu-Le Roy, 2002; Levin, 2005, and depend on photosynthetically derived faunal diversity (MacDonald et al., 2004; references therein), along other active food ( and plant mate- Bergquist et al., 2005). Among the most and passive margins, and from all parts rial), methane and other hydrocarbon remarkable of the fauna exploiting the of the global , even Antarctic seeps are colonized by specific anaerobic abundant chemical energy of seeps are regions (Domack et al., 2005). It is only subsurface microbiota; these organisms the symbiont-bearing invertebrate spe- during the last decade that more intense use hydrocarbons as an energy source cies, often similar or related to the fauna

Oceanography March 2009 111 found at hydrothermal vents. These Both symbiont-bearing and associated pockmarks were also visited (Figure 1A). large taxa, such as vesicomyids (clams), nonsymbiotic fauna were investigated, Håkon Mosby mud volcano was first bathymodiolids (), and siboglin- as well as different size classes, from observed in 1989 during a side-scan ids (formerly known as Pogonophora or and large invertebrates (megafauna), to sonar survey (Vogt et al., 1997). An tube worms), and some motile species small endofaunal organisms (meio- and expedition in 1995 measured very such as shrimps and gastropods, cluster macrofauna), including the very specific high temperature gradients in the sedi- in areas where fluids rich in reduced seep-related microbial communities. In ments, recovered methane hydrate from chemicals reach the seafloor (Sibuet and addition to biodiversity patterns in rela- 2-m subbottom depth and sampled Olu, 1998; Sibuet and Olu-LeRoy, 2002; tion to the high heterogeneity siboglinid polychaetes, suggesting active Bergquist et al., 2003; Van Dover et al., within a region, similarities in communi- (Vogt et al., 1997). The 2003; Cordes et al., 2007). ties among regions are currently under concentric structure of the mud volcano During HERMES, three main areas investigation in order to gain better can be divided into several subhabitats harboring prominent seep ecosystems insight into the biology, biodiversity, and characterized by different biogeochemi- were investigated, including the Nordic of seep-associated biota cal sediment conditions (de Beer et al., margin and its Håkon Mosby mud vol- along Europe’s continental margins. 2006; Niemann et al., 2006b). cano, the Gulf of Cádiz, and the eastern The Storegga area is well known for Mediterranean. After a short introduc- HERMES Cold Seep its giant slide, one of the larg- tion of the three main study areas, which Study Sites est ever mapped on continental margins are more extensively discussed elsewhere Along the Nordic margin, the highly (Paull et al., 2008). On the northeastern (see Foucher et al., this issue), we pro- active Håkon Mosby mud volcano flank of the Storegga slide, complex vide an overview of the main results (72°N) at 1280-m water depth on the pockmarks are located in the so-called from biodiversity studies performed dur- Barents Sea slope south of Svalbard, was Nyegga area at 740-m water depth. These ing HERMES. An integrated approach the target of several multidisciplinary pockmarks are circular in plan view and combined detailed habitat mapping and cruises (Figures 1A, 2). The Storegga feature up to 190-m-long ridges of car- characterization of associated fauna. slide at 64°N and associated Nyegga bonate rock (Hovland et al., 2005).

Ann Vanreusel ([email protected]) is Professor, Research Group, Universiteit Gent, Gent, Belgium. Ann C. Andersen is Professor, Université Pierre et Marie Curie (UPMC), and a researcher in Equipe Ecophysiologie: Adaptation et Evolution Moléculaires, UMR 7144 - Centre national de la recherche scientifique (CNRS) - UPMC, Station Biologique, Roscoff, France.Antje Boetius is Head, Microbial Habitat Group, Max Planck Institute for Marine , and Professor, Jacobs University Bremen, Germany. Douglas Connelly is a researcher in the Geology and Geophysics Group, National Oceanography Centre, University of Southampton, Southampton, UK. Marina R. Cunha is Professor, Centro de Estudos do Ambiente e do Mar (CESAM), Departemento de Biologia, Universidade de Aveiro, Campus Universitário de Santiago, Aveiro, Portugal. Carole Decker is PhD Candidate, Deep-Sea Ecosystem Department, Institut français de recherche pour l'exploitation de la mer (Ifremer), Centre de Brest, Plouzané, France. Ana Hilario is a postdoctoral researcher at CESAM, Departemento de Biologia, Universidade de Aveiro, Campus Universitário de Santiago, Aveiro, Portugal. Konstantinos Ar. Kormas is Assistant Professor, Department of Ichthyology and Aquatic Environment, University of Thessaly, Nea Ionia, Greece.Loïs Maignien is PhD Candidate, Laboratory of Microbial and Technology (LabMET) and Renard Center for (RCMG), Universiteit Gent, Gent, Belgium. Karine Olu is a researcher in the Deep-Sea Ecosystem Department, Ifremer, Centre de Brest, Plouzané, France. Maria Pachiadaki is PhD Candidate, Department of Chemistry, University of Crete, Heraklion, Greece. Benedicte Ritt is PhD Candidate, Deep-Sea Ecosystem Department, Ifremer, Centre de Brest, Plouzané, France. Clara Rodrigues is PhD Candidate, CESAM, Departemento de Biologia, Universidade de Aveiro, Campus Universitário de Santiago, Aveiro, Portugal. Jozée Sarrazin is a researcher in the Deep-Sea Ecosystem Department, Ifremer, Centre de Brest, Plouzané, France. Paul Tyler is Professor, National Oceanography Centre, University of Southampton, Southampton, UK. Saskia Van Gaever is a postdoctoral researcher in the Marine Biology Research Group, Universiteit Gent, Gent, Belgium. Heleen Vanneste is PhD Candidate, School of Ocean and Earth Science, University of Southampton, UK.

112 Oceanography Vol.22, No.1 Figure 1. (top left) Overview map. (A) Nordic margin: Håkon Mosby mud volcano, Storegga slide, and Nyegga area in the north identified on the map. Vicking cruise ©Ifremer 2006. (B) Gulf of Cádiz: Simplified geological map after Medialdea et al. (2004), showing the locations of known mud volcanoes (compilation of Kenyon et al., 2000, 2003, 2006; Akhmetzhanov et al., 2007) with their geochemical characteristics as determined so far (compilation of Somoza et al., 2003; Niemann et al., 2006a; Stadnitskaia et al., 2006; Haeckel et al., 2007; and Hensen et al., 2007). Mud volcano fields: GRD=Guadalquivir Diapiric Ridge; Tasyo; SPM=Spanish Moroccan Margin; DPM=Deep- Portuguese Margin. (C) Eastern : Seep sites visited during the Mediterranean Deep-Sea Ecosystems (MEDECO) cruise in 2007, including the Napoli and Amsterdam mud volca- noes as well as different areas in the Nile Fan. MEDECO cruise ©Ifremer 2007

Oceanography March 2009 113 2004). The Olimpi mud volcano field and Anaximander Mountain areas, located at depths between 1700 m and 2000 m, are characterized by strong compressional tectonic processes superimposed by faulting. They harbor large conical mud volcanoes several kilometers across but only a few hundred meters high. Fresh mud flows, brines, clasts, and crusts were observed on their surface, depending on the current activity of the volcano (Zitter et al., 2005). In a context, the Nile deep turbidic system displays many fluid-releasing structures on the seafloor, including mud volcanoes, mud pies, and pockmarks (Loncke et al., 2004).

Figure 2. OTUS image of the Håkon Mosby mud volcano in the north. Area covered by Mapping Habitat optical survey (OTUS camera), representing 30% of a 400 x 400-m area. Footprints of Heterogeneity at each photo are georeferenced. Vicking cruise ©Ifremer 2006 Cold Seeps Cold seeps are characterized by the patchy occurrence of sulfide and/or The Gulf of Cádiz is located between of them, the majority of the methane is methane-dependent biota, including Iberia and Africa on the Atlantic side, consumed within the , and microbial mats and symbiont-bearing between 9°W and 6°45'W, and 34°N does not reach the hydrosphere. invertebrates (, Polychaeta) that and 37°15'N. The of the Different seep sites are also pres- can form small clusters or spread over study area is complex, with the influ- ent in the eastern Mediterranean Sea large fields in high densities. This high ence of Mediterranean outflow water on (Figure 1C), where intense emission spatial variability at scales of tens to hun- the shallower eastern mud volcanoes, of methane occurs from the center of dreds of meters has been attributed to and evidence for input of high-nutrient active mud volcanoes and along related the magnitude of fluid flow and the cor- Antarctic Intermediate Water in the faults (MEDINAUT/MEDINETH 2000, related chemical depth profiles (Henry deeper western regions (Van Aken, Charlou et al., 2003; Dupré et al., 2007). et al., 1992; Barry et al., 1997; Olu et al. 2000). The area has a complex tectonic During the last decade, three major 1997; Sahling et al., 2002; Levin et al., history and is now dominated by thick areas were the focus of multidisciplinary 2003; de Beer et al., 2006). Low net flow sedimentary deposits. Since their initial cruises using submersibles: the Olimpi rates appear to provide sufficient meth- discovery in the area in 1999 (Kenyon mud volcano field, located on the ane from depth to fuel the near-surface et al., 2000), a large number of mud vol- south of Crete biological communities while still allow- canoes have been identified, located in (Mascle et al., 1999); the Anaximander ing downward transport and mixing of four main fields and exhibiting different Mountains, south of , caught up oxygen- and sulfate-rich seawater in the but generally very localized hydrocar- in the plate convergence between Africa upper few centimeters of the sediment bon seepage (Niemann et al., 2006b; and Eurasia (Woodside et al., 1998); and (de Beer et al., 2006). More intense fluid Figure 1B). The presence of carbonate the seafloor of the Nile Deep Sea Fan flow is associated with altered pore- chimneys indicates past activity. At most (Nile delta turbidic system; Loncke et al., water composition and elevated sulfide

114 Oceanography Vol.22, No.1 concentrations extending to the sedi- on the ROV Victor 6000 survey module. colonized by siboglinids. Abundant ment surface, thus allowing the growth At this altitude, each picture covers a empty bivalve shells were lying on the of microbial mats (Tryon and Brown, surface of ~ 64 m2 (Figure 3A, B). The seafloor, possibly indicating the extinc- 2001; Levin et al., 2003). new habitat map suggests changes in the tion of previous bivalve-dominated To understand the spatial and tem- colonization of mud flows by microbial communities (recent work of authors poral scales at which seep ecosystem mats and siboglinids between 2003 Olu and Sarrazin). processes change, a crucial initial phase (Jerosch et al., 2007) and 2006 (recent in seep research is mapping the size and work of authors Olu, Fabri, Deep-Sea -bearing distribution of different and Ecosystem Department of Ifremer, and Chemosynthetic Fauna identifying the associated communities others). A similar spatial organization of Megafaunal species comprise organ- (Sibuet and Olu-Le Roy, 2002). A great habitats (central seep area surrounded isms larger than 2 cm that are generally step forward in the precision of habitat by microbial mats and siboglinid fields visible on seafloor optical images. Cold mapping has been achieved in the last in the external ring) was also observed seep ecosystems provide niches for few years with use of remotely operated at small individual pockmarks along the chemo-synthetic communities based on vehicles (ROVs), which allows regular Storegga slide and in the Nyegga area, reduced compounds such as methane transects over long distances in com- but at a much smaller scale (decimeter to and sulfide, which are energy sources bination with more precise positioning meter) (recent work of author Olu). for CO2-fixing symbiotic . These methods. There is also rapid progress in In 2007, the MEDECO cruise symbioses between invertebrates and optical camera resolution and data pro- aboard RV Pourquoi pas? visited sev- sulfur-oxidizing and/or methanotrophic cessing using Geographic Information eral different seep sites in the eastern bacteria are only found in highly reduced System (GIS)-supported image analysis. Mediterranean, four of which were the environments, and are an obvious exam- On the Håkon Mosby mud volcano, focus of systematic ecological studies at ple of how cold seep ecosystems add the concentric distribution of habitats different spatial scales: the Napoli mud biodiversity to marine deep-water life. around a central crater, apparently not volcano south of Crete, the Amsterdam During our HERMES research, we were colonized, was first described from mud volcano south of Turkey, and a able to identify the dominant chemosyn- towed video systems and observations pockmark field and the Cheops mud thetic symbioses on Europe’s continental by submersibles (Milkov et al., 1999; volcano located in the Nile delta. Five margins, but most likely much more Gebruk et al., 2003). different habitats were recognized by the remain to be discovered. The first predictive habitat map was presence of visible features such as key At the Håkon Mosby mud volcano, based on ROV video mosaics processed megafaunal taxa (Bivalvia, Siboglinidae) megafauna are dominated by sibo- by Jerosch et al. (2007) using geostatisti- or microbial mats on the seafloor. More glinids (tubeworms) that lack both cal analysis. These authors estimated extensive habitat and megafaunal dis- mouth and gut and live in the percent coverage for each targeted tribution surveys on the Napoli mud with sulfur-oxidizing bacteria stored habitat: mud apparently devoid of life in volcano (33°43.7777'N, 24°40.9495'E; inside their bodies (Lösekann et al., the center, surrounded by areas densely 1750–1934-m depth) were based on 2008). Wide areas in the periphery of inhabited by microbial mats, particularly regularly spaced transects at 10-m alti- this mud volcano are covered with the in the south; and hummocky outer parts tude with each OTUS picture covering a curled brownish tubes of the species colonized dominantly by siboglinids. surface of ~ 100 m2. This survey showed Sclerolinum contortum (Figure 3D), bur- During the HERMES Vicking cruise that numerous brine pools characterized ied up to 70-cm deep in soft sediment. In (2006), a new habitat mapping survey the southeast sector (Figure 3C), cor- some areas, clusters of the straight black was conducted (Figure 2) by means of responding to depressions on the micro- tubes of Oligobrachia haakonmosbiensis parallel transects at 8-m altitude above bathymetric map. Small tubeworms webbi (Smirnov, 2000) stand erect about the seafloor, using the black and white were rarely observed. The northern part 5 cm above the seafloor. Both species are high sensibility camera OTUS mounted showed a more disturbed environment, also found further south on pockmarks

Oceanography March 2009 115 Figure 3. Example of OTUS photos showing (A) microbial mats and zoarcid and (B) a patch of siboglinid polychaetes. Photo size is 64 m2. Vicking cruise ©Ifremer 2006. (C) A brine pool on the summit of the Napoli mud volcano. MEDECO 2007 ©Ifremer. (D) View of a wide field of siboglinid polychaetes at Håkon Mosby mud volcano. The curled brownishSclerolinum surrounds a large spot of black, straight Oligobrachia tubes. An orange sea star lies in front of a Sclerolinum patch covered by whitish bacterial filaments.Vicking cruise ©Ifremer 2006

at the Storegga slide and at Nyegga, covered with a carpet of siboglinids are distribution (recent work of authors where they surround every dark spot of known as “submarine pingoes;” they Andersen and Olu). The factors that con- methane seepage (recent work of author are described by Hovland and Svensen trol the spatial distribution of these two Andersen). Many small symbiont- (2006) as local hydrate (ice) accumula- species remain unclear. The local sedi- bearing bivalves belonging to the family tions. However, during the HERMES ment chemistry, the penetration of the Thyasiridae have been sampled on these Vicking cruise in 2006, observation worms into the , and some of the sites, especially in siboglinid fields at the and sampling by ROV Victor 6000 worms’ physiological adaptations con- Håkon Mosby mud volcano, whereas showed the pingoes to be composed cerning their hemoglobins seem to differ numerous larger shells of mud accumulations with entangled between the two species, and may affect have also been observed at the Storegga Sclerolinum, soft enough to be sampled their habitat selection (recent work of and Nyegga pockmarks (recent work of by blade core. In all the explored areas, author Andersen). However, other fac- authors Decker and Olu). Sclerolinum seem to dominate, whereas tors such as their reproduction and dis- At Nyegga, 1-m-high pillow structures Oligobrachia has a discrete, highly patchy persal may also play a role. Filamentous

116 Oceanography Vol.22, No.1 bacteria often cover their tubes and the considerable quantities of methane, but siboglinid polychaetes (Siboglinum spp.) spaces between tubes provide shelter to contained no obvious chemosynthetic and solemyid bivalves (Acharax sp., a highly diversified macrofauna, particu- fauna. Other megafauna, not directly Petrasma sp.), but also other frenu- larly between the twisted creeping tubes chemosynthesis-dependent, consisted late (Polybrachia, Spirobrachia, of Sclerolinum. Sclerolinum can therefore of stylasterine attached to the car- Bobmarleya, Lamellisabella) (Figure 5) be compared to other habitat-providing bonate cap (Figure 4E), scavenging crabs and bivalve taxa (Lucinoma, Thyasira, species such as deep-water corals, as it (Figure 4F), and corals (Figure 4G). , Vesicomyidae) (Génio harbors a great epifaunal biodiversity on Aside from the dead mytilid fields, et al., 2008; Hilário and Cunha, 2008; the otherwise barren soft sediments of the chemosynthetic species of the Gulf Rodrigues et al., 2008). The first results the Norwegian deep margin. of Cádiz live mostly buried inside the of stable isotope analyses (δ13C, δ15N, In contrast to the Håkon Mosby sediments, a distribution that is prob- δ34S) support the occurrence of chemos- mud volcano, where permanently high ably related to the shallow (< 30 cm) ynthetic production in these species, fluxes of reduced compounds are read- depth of the sulfide/methane gradient. with thiotrophy (H2S) being the main ily indicated by the presence of large The most common species include metabolic pathway in the benthic food aggregations of siboglinids and bacterial mats, the mud volcanoes in the Gulf of Cádiz do not show evidence of dense aggregations of living chemosynthetic megafauna. An initial ROV transect at 1100-m depth on the Darwin mud vol- cano during a sampling campaign with RRS James Cook in 2007 revealed a mass of mytilids identified as Bathymodiolus mauritanicus (Figure 4A) on the top of this mud volcano. However, most of this accumulation comprised empty shells. Further along the transect, rock exposures (Figure 4B) and vast carbon- ate outcrops (Figure 4C) were observed with both live and dead mussels within cracks in the . These obser- vations suggest that the Darwin mud volcano had once been very active and that the release of methane 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 many of the shells remained intact and articulated. A small area (about 100 cm2) of soft, blue-grayish-colored sediment (Figure 4D) was observed Figure 4. and habitats associated with the Darwin mud volcano: (A) Bathymodiolus mauritanicus, (B) rock exposure, (C) carbonate outcrops, (D) soft, blue-grayish-colored sediment, in the northwest corner of the mud (E) stylasterine corals, (F) scavenging crabs, and (G) corals attached to an upturned piece of car- volcano that, when disturbed, released bonate crust.

Oceanography March 2009 117 web (recent work of author Rodrigues During the HERMES BIONIL cruise class is the fish of the Zoarcidae family, and colleagues). to the Nile Deep Sea Fan in 2006, new Lycodes squamiventer (Gebruk et al., The first data on Mediterranean cold samples from the three dominant 2003) (Figure 6B). Image analysis from seep communities were acquired during symbiont-bearing macrofaunal species the Vicking cruise (2006) confirmed the French-Dutch MEDINAUT cruise were collected. The clam Lucinoma aff. previous observations of Gebruk et al. (1998). Chemosynthetic communities kazani was found within the sediments, (2003) on the distribution of this zoarcid from the Olimpi and Anaximander mud the mytilid Idas sp. was attached to fish: they show the highest abundances fields were mostly concentrated near the different hard substrata (crusts, tubes, in the most active area of the volcano, summits of the volcanoes, where fluid urchins), and siboglinid tubeworms and are particularly associated with expulsion is concentrated (Olu-Le Roy occurred either on reduced sediments microbial mats (recent work of authors et al., 2004). The communities were (Amon mud volcano) or on carbonate Olu and Decker). Zoarcidae is the typical dominated by small-sized bivalves from crusts (central pockmark area). Symbiotic fish family encountered at hydrothermal four families common to cold seep associations have been described for vents and cold seeps, with some endemic environments (, Vesicomyidae, Lucinoma aff. kazani and for the small species likely having adapted to the Thyasiridae), or to shallower sulfidic- mytilid Idas sp., the latter harboring an toxic environment. rich habitats (Lucinidae). However, exceptional number of symbionts in its On the Storegga slide and in Nyegga large-size bivalve genera typical of cold gills (Duperron et al., 2006, 2007). pockmarks, nonsymbiotic megafauna seeps (Bathymodiolus and Calyptogena) are much more abundant and diverse, were absent. Siboglinids of the Obturata “Nonsymbiotic” Megafauna probably for two reasons. First, the cold group (genus Lamellibrachia) were found The megafauna at seeps also include seeps are much smaller compared to nearby or in close relation to carbonate many nonsymbiont-bearing species, the Håkon Mosby mud volcano, they crusts (Figure 6A). Differences in the which profit in many different ways are sparsely distributed, and methane biological activity can be related to the from the large biomass and productiv- concentrations in seawater are quite variability and intensity of fluid expul- ity of chemosynthetic megafauna. They low (J.L. Charlou, Marine Geosciences sions between the volcanoes (Olu-Le Roy are attracted by the heterogeneity of the Department, Ifremer, pers. com, 2008). et al., 2004), as supported by variable habitats, the of prey, or pos- Second, the water depth is shallower methane concentrations measured above sibly to the elevated topographic posi- (600–1000 m) and the Storegga slide the seafloor (Charlou et al., 2003). Small tion provided by mud volcanoes. At the is likely to be a site of high Siboglinidae of the Frenulata group Håkon Mosby mud volcano, the most input that favors the presence of sus- (Siboglinum sp.) were also collected. abundant species in the megafaunal size pension and deposit feeders. The very large ophiurid Gorgonocephalus sp. (Figure 6C), reaching up to 0.5-m diam- eter, is the most striking species of this background megafauna, but abundant comatules, crinoids, and pedonculate were also observed. In the Gulf of Cádiz, several nonchemosynthetic species were observed associated with different mud volcanoes at various water depths. In contrast to the shallower mud volca- noes, the Carlos Ribeiro mud volcano Figure 5. Frenulata collected during TTR17 cruise in the Gulf of Cádiz: (a) Siboglinum sp. (from Darwin mud volcano), (b) Polybrachia sp. 1 (from Porto mud volcano), (c) Polybrachia sp. 2 (from Sagres mud at 2200-m water depth has a more volcano), and (d) Polybrachia sp. 3 (from Soloviev mud volcano). Photos by Ana Hilário diverse nonchemosynthetic-dependent

118 Oceanography Vol.22, No.1 Figure 6. (A) Lamellibrachia from the pockmark area in the Nile Deep Sea Fan. MEDECO cruise ©Ifremer 2007. (B) Lycodes squamiventer (Zoarcidae) in a patch with siboglinid tubeworms at the Håkon Mosby mud volcano. ARKXXII cruise ©MARUM, University of Bremen. (C) Richness of the background megafauna on Storrega slide, with the giant ophiurid Gorgonocephalus sp. Vicking cruise ©Ifremer 2006. (D) Unusual large specimens of the Rhizaxinella pyrifera on Napoli mud volcano. MEDECO cruise @Ifremer 2007

megafauna. The mud volcano center of deposit-feeding holothurians were Small-Sized Endofauna consists of series of concentric ridges observed (Figure 7H). Since their discovery, much seep research that support very few megafauna except In the eastern Mediterranean, poly- has focused on the chemosynthetic siboglinid tubeworms (Figure 7A) chaetes are abundant around the Napoli megafauna as well as the associated and a mobile echinothurid sea urchin brine lakes and on the active sites on microbiota. Infaunal organisms, usually found close to the “eye” of the volcano Amsterdam mud volcano. Other associ- of smaller size (macro- and meiofauna), (Figure 7I). Most of the more extensive ated species include unusually large such as nematodes, harpacticoid cope- megafauna comprise suspension-feeding specimens of the Suberitidae poriferan pods, polychaetes, amphipods, tanaids, cnidarians situated at the periphery of Rhizaxinella pyrifera (Figure 6D) that gastropods, ostracods, and kinorhynchs, the mud volcano, including poriferans was sampled on Napoli mud volcano. have been studied to a much lesser (Figure 6B), the sea pen Umbellula such as galatheids, shrimps, extent. The HERMES project aimed at (Figure 7C), and dense gorgonian bushes and Chaceon mediterraneus crabs were painting a full picture of seep biodiversity (Figure 7F, G). Further off the mud equally abundant at all sites. Large densi- by investigating all size classes of the ben- volcano the enigmatic athecate hydroid ties of Echinus sp. were observed at active thos. The macrofaunal and meiofaunal Monocaulus (Figure 7D) was observed. sites, suggesting some sort of depen- communities at active cold seeps on the At some time in the past, mud over- dence on fluid emission (Olu-Le Roy Nordic margin and in the Gulf of Cádiz flowed the volcano’s crest and slid down et al. 2004; recent work of authors Ritt, and the eastern Mediterranean were its southeast side, where huge numbers Olu, and Sarrazin). studied for the first time, and analysis

Oceanography March 2009 119 with at least seven families (M. Morineaux, Deep-Sea Ecosystem Department, Ifremer, pers. com., 2008) and other groups, including poriferans, molluscs (Bivalvia, ), and crustaceans (Amphipoda, Tanaidacea, Isopoda). Similar differences in com- munity structure and dominant taxa among habitats were observed in the Storegga and Nyegga pockmarks (recent work of authors Decker, Van Gaever, and Olu). Ongoing work on dominant taxa will compare Storegga/Nyegga and Håkon Mosby mud volcano communi- ties at higher taxonomic levels to test the influence of geographic patterns compared to habitat influence on the structure of communities. Significant differences in diversity and abundance of the meiofaunal communities (organisms passing through a 1-mm sieve and retained on Figure 7. Bathymetry and fauna associated with Carlos Ribeira mud volcano: (A) Siboglinid polychaetes, (B) Porifera, (C) the seapen Umbellula, (D) athecate hydroid Monocaulus, a 32-µm sieve) associated with differ- (F, G) gorgonian bushes, (H) holothurians in high numbers, and (I) echinothurid sea urchin. ent habitats were also found. The bare, muddy sediments from the active center yielded the lowest nematode densities, but unusually high benthic copepod of the samples is currently ongoing. mats (1000 to 1600 ind. m-2) and abundance (271 ± 37 ind. 10 cm-2; Initial results from the Nordic margin, even less abundant in the central area Van Gaever et al., 2006). In contrast, one including different habitats found on (55–170 ind. m-2). Great discrepancies single nematode species, Halomonhystera the Håkon Mosby mud volcano (in its among habitats were also observed in disjuncta Bastian 1865 (Figure 8B), pre- center, microbial mats and siboglinid the taxonomic diversity, because only viously described from shallow-water polychaete fields) as well as the Storegga a few species are able to colonize the habitats, was found in extremely high and Nyegga cold seeps, show that the more sulfidic and oxygen-depleted abundances (> 11,000 ind. 10 cm-2; macrofauna (those between 500 µm sediments at the sites. Van Gaever et al., 2006) in the bacte- and 1–2 cm) are generally dominated There, the macrofauna were domi- rial sediment-covering mats. by polychaetes. A quantitative analysis nated by a polychaete belonging to the Biomarker fatty acid and stable carbon revealed highly contrasting densities genus Capitella (Figure 8A), whose isotope analyses of H. disjuncta revealed among the habitats (recent work of shallow-water species from the Capitella that this species was thriving on chemo- authors Decker, Van Gaever, and Olu); capitata complex is adapted to organic synthetically derived food sources, in the highest abundances were associ- and sulfide-rich environments and is particular, on the Beggiatoa bacteria ated with siboglinid fields (from 6700 used as an indicator of pollution. In (recent work of author Van Gaever and to 56,000 ind. m-2). Macrofauna were contrast, Siboglinidae fields were colo- colleagues). The uncommon ovovi- much less abundant in the microbial nized by a higher taxonomic diversity viparous reproduction of H. disjuncta

120 Oceanography Vol.22, No.1 at Håkon Mosby mud volcano has been species to exploit. Only some oxygen- per square meter, but local patches of identified as an important adaptation stress-resistant, shallow-water nematode greater than 20,000 ind. m-2 often occur. of parents to secure the survival and species with an extensive geographical The shallower mud volcanoes of the development of their brood in this anoxic range are able to thrive in these deep- Moroccan field (200–1000-m depth) environment. This nematode species sea reduced environments. In contrast, show higher densities and number of was not found on the adjacent Storegga the seep sediments colonized by sibo- species but a low degree of endemicity, slide or in the Nyegga area, nor in any of glinid polychaetes display very diverse while the few samples taken from the the other cold seeps studied in the Gulf nematode communities, highly similar Portuguese field (2000–3000-m depth) of Cádiz or the eastern Mediterranean. in terms of generic diversity compared to show lower densities and species number Here, the reduced sediments host a the surrounding background sediments. but suggest that endemicity is clearly very impoverished nematode assem- Siboglinidae are known to strongly higher at these deeper mud volcanoes as blage, in terms of both diversity and affect the geochemical conditions in the many of the species collected (including density, that is dominated by one or sediment surrounding the tube through the chemosynthetic ones) do not match two species belonging to the genera their intense ventilation activity (Julian the available descriptions of similar taxa. Terschellingia, Thalassomonhystera, et al., 1999; Bergquist et al., 2002). In the eastern Mediterranean, differ- Sabatieria or Desmodora (Van Gaever Consequently, well-oxygenated sediment ent habitats were selected for systematic et al., in press). At least three of these down to 5-cm depth is created (de Beer sampling (recent work of authors Ritt, dominant species (i.e., Halomonhystera et al., 2006), providing a suitable habitat Sarrazin, and colleagues). Preliminary disjuncta, Terschellingia longicaudata for a wide range of nematode species. results on the Napoli mud volcano De Man 1907, and Sabatieria mortenseni Siboglinidae fields and “control” samples show that the “Lamellibrachia habi- Ditlevsen 1921) were already described of deep-sea sediments yield comparable tat” has higher macrofaunal densities as common inhabitants of intertidal, highly diverse nematode assemblages, but (5133 ± 3993 ind. m-2) than the “bivalve organically enriched . Seep a shift in dominant families and genera habitat,” where the highest density sediments that are strongly affected by was detected (Van Gaever et al., in press). reaches only ~ 2117 ± 226 ind. m-2 reduced fluids and characterized by The endobenthic of the (recent work of authors Ritt and harsh environmental conditions (such mud volcanoes in the Gulf of Cádiz dis- Sarrazin). Despite lower faunal density, as oxygen depletion, toxic sulfide levels) plays wide variability in species composi- the latter habitat exhibits a higher taxo- generate a habitat that is difficult for tion and structure. Densities commonly nomic richness. Characterization of the most of the typical deep-sea nematode vary from a few hundred to thousands physico-chemical conditions is not yet

Figure 8. Small-sized endofauna with (A) the polychaete Capitella sp. and (B) the nematode Halomonhystera disjuncta.

Oceanography March 2009 121 finalized but a significant difference in nourished by the oxidation of methane, groups (Lösekann et al., 2007). oxygen penetration in the sediments was higher hydrocarbons, and sulfide. In fact, A key indicator community of active measured—limited to a few millimeters methane-fueled microbial communities cold seep ecosystems is microbial mats, into the sediment in the “Lamellibrachia in anoxic sediments above gas hydrates some of which cover hundreds of meters habitat” but reaching several tens of mil- and gas vents have the highest biomass of seafloor, for example, at the Håkon limeters in the “bivalve habitat” (recent known to occur in marine ecosystems, Mosby mud volcano (Niemann et al., work of authors Ritt and Sarrazin). At with up to 1012 cells per cm3 (Boetius 2006b). These mats typically consist of the rim of the Amon mud volcano, a et al., 2000). Because of their distinct giant, vacuolated sulfur-oxidizing bac- muddy brine flow characterized by metabolic abilities, which are adapted teria, such as Beggiatoa, Thioploca and blackish sulfidic sediments was sampled. to the exploitation of reduced chemical spp., which exploit the Preliminary results from analyses of the compounds, methanotrophs, hydro- high AOM-derived sulfide fluxes at the macrofauna from the BIONIL cruise carbon degraders, and sulfate-reducing seafloor (Figure 9). Such bacteria can use (RV Meteor/Quest, 2006) show that this and sulfide-oxidizing bacteria are the internally stored nitrate to oxidize sulfur particular habitat (only fauna > 1 mm key functional groups at cold seep eco- and fix carbon dioxide for growth, thus have been sorted so far) exhibits a high systems (Jorgensen and Boetius, 2007). coupling the carbon, nitrogen, and sulfur abundance of polychaetes in addition to Unfortunately, environmentally relevant cycles in seep sediments. Their diversity the presence of three families of bivalves representatives of these functionally is much higher than anticipated, and (Lucinidae, Thyasiridae, Vesicomyidae) relevant bacterial and archaeal clades each population has distinct adaptations typical of chemosynthetic or reduced have not yet been isolated, but a variety to enable the use of the steep gradients of habitats. on this prob- of nucleic acid and membrane lipid- sulfide, nitrate, and oxygen that develop ably short-lived habitat appears to be based molecular identification methods in the methane-rich sediments (Preisler lower than on other seep habitats studied have been instrumental in HERMES et al., 2007). Microbial mats at seeps in this region. On the pockmark area investigations of the microbial diversity are often very patchy and mainly white (1700 m, Nile Delta), the “reduced of European cold seeps. The main groups (caused by the reflection of the intracel- sediment” sample contained a high at cold seeps can be summarized as lular sulfur granules), but they are also abundance of dorvilleid polychaetes, follows. Hydrocarbon degradation is found in shades of yellow, orange, or characteristic of reduced habitats. usually dominated by sulfate-reducing grey. Thiotrophic mats usually comprise Overall, the preliminary results bacteria of the Deltaproteobacteria a diverse mixture of mostly bacterial obtained during the BIONIL (2006) and (Knittel et al., 2003). In contrast to most taxa, but are dominated by large fila- MEDECO cruise (2007) show a vast het- other seafloor habitats, cold seep sedi- mentous sulfide-oxidizing bacteria or by erogeneity of habitats and faunal assem- ments host a high proportion of , small thiotrophic blages, even within tens to hundreds of mainly methanotrophic and methano- such as Arcobacter (Omoregie et al., meters within different geological struc- genic Euryarchaeota and uncultured 2007). Some of these “giant” sulfide- tures. More data need to be analyzed Crenarchaeota (Knittel et al., 2005). The oxidizing microbes, such as the filamen- to highlight faunal and environmental -mediated anaerobic tous Beggiatoa bacteria, have a gliding similarities among similar habitats oxidation of methane (AOM) with movement with which they position (bivalve, siboglinid) sampled from differ- sulfate is the dominant process at cold themselves within a steep gradient of ent mud volcanoes. seep ecosystems and the cause of the oxygen and sulfide (Preisler et al., 2007); observed high sulfide fluxes. The organ- others depend on a flux of sulfide to the Microbial Communities isms mediating AOM are anaerobic bottom-water interface. at Cold Seeps methanotrophic (ANME) archaea that Lösekann et al. (2007) describe in Similar to hot vents, cold seeps support form consortia with sulfate-reducing detail the relationship among the bacte- an enormous biomass of free-living Deltaproteobacteria of the Desulfosarcina rial mats and the methanotrophic and and symbiotic microbial life that is (Boetius et al., 2000) or Desulfobulbus sulfate-reducing bacteria found at the

122 Oceanography Vol.22, No.1 Figure 9. Macroscopic and microscopic images of microbial mats at cold seep ecosystems. (Upper panel, left) Thiomargarita mat in a fault surrounding the Amon mud volcano. ©MARUM/MPI. (Middle) Thin filamentous mats at the center of the Amon mud volcano. ©MARUM/MPI (Right) Thick filamentous mats surrounding the center of the Håkon Mosby mud volcano. ©Ifremer/AWI. The micrographs in the lower panel show the respective mat-forming thiotrophic bacteria. (Left) Sphere-like vacuolateThiomar- garita cell. (Middle) Giant filamentous vacuolate gammaproteobacteria. (Right) Thin filamentous vacuolateBeggiatoa cells. ©Stefanie Grünke, MPI/AWI

Håkon Mosby mud volcano. Briefly, larger vertical and horizontal zone. ecological niches for the seep microbial in the active volcano center, the main Microbial diversity was higher at this site communities, the Gulf of Cádiz is an methane-consuming process was bac- compared to the central and Beggiatoa- ideal natural laboratory for exploring the terial aerobic oxidation. In this zone, covered part of the Håkon Mosby mud diversity and activity of seep microbes in aerobic methanotrophs belonging to volcano. Obviously, microbial diversity relation to their environment. In the Gulf three bacterial clades closely affiliated and community structure are closely of Cádiz, overall AOM activity is typical with Methylobacter and Methylophaga related to different fluid-flow regimes for low to moderately active seeps. For species accounted for 56 ± 8% of total at the Håkon Mosby mud volcano, pro- instance, maximum methane turnover cells. In sediments below the Beggiatoa viding distinct niches for aerobic and is typically around 20 nmol cm3 day mats encircling the center of the Håkon anaerobic methanotrophs. at both Captain Aryutinov and Carlos Mosby mud volcano, methanotrophic Mud volcanism in the Gulf of Cádiz Ribeiro mud volcanoes (Niemann et al., archaea of the ANME-3 clade dominated is characterized by a wide diversity of 2006a; recent work of author Maignien the AOM. They form cell aggregates processes and environmental settings, and colleagues). However, some mud with sulfate-reducing bacteria of the such as different types of fluid migra- volcanoes deviate from this trend: at the Desulfobulbus (DBB) branch, compris- tion pathways, tectonic activity and/or Darwin mud volcano, thick carbonate ing 94% ± 2% of the total microbial salt diapirism, migration velocity, fluid crusts and plates seal methane escape biomass at 2–3 cm below the surface. composition and alteration processes, routes. Discrete AOM hotspots have At the outer rim of the mud volcano, depth, sea bottom temperature (from been observed at the rim of the crater, the seafloor is colonized by siboglin- 4°C to 13°C if under the influence of the suggesting a relocalization of seep activ- ids. Here, both aerobic and anaerobic Mediterranean outflow water), and the ity. In these hotspots, AOM activity is methane oxidizers were found in lower presence of gas hydrate. Because these one order higher than at Carlos Ribeiro abundances, but distributed over a much parameters create a wide array of unique mud volcano and was found to sustain

Oceanography March 2009 123 the development of white bacterial mats. took place in 1996 at the Kula mud and 5.93 (sediments) (Heijs et al., 2006, In contrast, salt diapir-driven mud volca- volcano (Woodside et al., 1997, 1998). 2008; recent work of author Pachiadaki noes such as Mercator have hypersaline Today, hydrates have also been sampled and colleagues). The most abundant pore water that probably inhibits micro- from four other mud volcanoes in the phylotypes in carbonate crusts are bial activity, which was found to be one area. High seafloor methane fluxes are related to Actinobacteria, Clostridia, and order of magnitude lower than at Carlos associated with the mud volcanoes as Alpha-, Gamma- and Deltaproteobacteria Ribeiro mud volcano, although methane well as with the accompanying cold as previously described (Heijs et al., and sulfate are present in large amounts. vents and seeps (Charlou et al., 2003), 2006). Regarding sediments, the major- Interestingly, these environmental setting and the available gas provides energy ity of the phylotypes are closely related variations and AOM activity are reflected for rich benthic communities, includ- to gas hydrate bearing sediments by diverse microbial community com- ing chemosynthetic symbiotic fauna (Knittel et al., 2005). High numbers positions. Inventories of archaeal and (Olu-Le Roy et al., 2004). Carbonate of Deltaproteobacteria phylotypes bacterial phylotypes in methane-rich crusts derived from anaerobic oxidation are present, as well as Actinobacteria, sediments reveal that the three microbial of methane are formed in these environ- Acidobacteria, Alpha-, Gamma-, Epsilon- consortia known to perform this reaction ments (Aloisi et al., 2002). Of the five and Deltaproteobacteria, Firmicutes, (ANME-1, -2, and -3) are active with dif- known mud volcanoes in the province, Cytophaga-Flexibacter group, and can- ferent distribution patterns (Figure 10). microbial diversity data exist only for didate division WS3. Several phylotypes Another major feature of mud volcanoes (Bacteria and Archaea) from have also been found from the Chloroflexi from the Gulf of Cádiz is the very deep the Amsterdam (ca. 2030 m) and Kazan and candidate division JS1. More rare origin of migrating fluid and mud reach- (ca. 1700 m) mud volcanoes. Based on phylotypes are related to , ing the surface (Hensen et al., 2007). 16S rRNA gene diversity, the Amsterdam Firmicutes (Bacilli), Bacteriodetes, and HERMES work also shed some light mud volcano harbors a rather diverse candidate divisions OD1, OP8, OP11, on the bacterial and archaeal diversity of bacterial community. Shannon diversity and GN06. (Heijs et al., 2008; recent work the mud volcanoes at the Anaximander index H’ (a tool for comparing two dis- of Pachiadaki and colleagues). Mountains, eastern Mediterranean Sea. tinct habitats by combining the quantifi- Archaeal communities show lower The Anaximander Mountains comprise a able terms of species richness and with H’ (base e) values rang- group of three main mountains between equitability; high H values indicate more ing from 2.14 to 2.68 for sediments the Cyprus and Hellenic arcs (Zitter diverse communities—an H value of 0 while in carbonate crusts H’ is 2.93 et al., 2005). The first gas hydrate sam- indicates a community with one species) (Heijs et al., 2006, 2008; recent work pling in the Anaximander Mountains varies between 3.33 (carbonate crusts) of author Pachiadaki and colleagues). Most of the archaeal sequences found in Amsterdam mud volcano carbon- ate crusts belong to the Crenarchaeota, Marine Group I (MGI). The remainder of the crenarchaeal sequences fall into a hitherto unclassified novel group of Crenarchaeota whose related sequences have previously been obtained from deep-sea sediments (Vetriani et al., Figure 10. Diversity of anaerobic oxidation of methane (AOM) communities from the Gulf of Cádiz mud volcanoes shown with fluorescent in situ hybridization imaging. (Left) ANME-2 type aggregates 1999). The euryarchaeal sequences are with multiple archaeal cores surrounded by bacteria as observed in the Carlos Ribeiro mud volcano related to novel Thermoplasmata or AOM zone. (Middle) ANME-2 type clusters with a single archeal core in a shallow microbial commu- Methanosarcinales. The latter are affili- nity of the Darwin mud volcano. (Right) ANME-1 type of archaeal filaments dominate the Mercator mud volcano microbial community. Microbial cells are stained with the archaeal specific probe ated to ANME-2 sequences (Heijs et al., Arch915 (red) and DAPI staining (blue). 2008; recent work of author Pachiadaki

124 Oceanography Vol.22, No.1 and colleagues), while all three groups— high heterogeneities from small to large leader of the Cold Seep Workpackage. ANME-1, ANME-2, and ANME-3— scales. Every seep region along the We also want to thank Phil Weaver and have been found in Amsterdam mud European margin is different in terms Vikki Gunn, respectively, the coordi- volcano sediments. Other sequences are of community composition and biodi- nator and manager of the HERMES related to Methanomicrobiales, marine versity, and high patchiness and other project, which was funded under the benthic group D (MBG-D), and the differences are observed within regions. European Commission’s Framework Thermoplasmata. In comparison, the However, many questions remain in the Six Programme (EC contract no. sediments of the Kazan mud volcano quest to unravel the diversity, function- GOCE-CT-2005-511234). We acknowl- harbored less diverse bacterial assem- ing, and genomic capacity of chemosyn- edge the captains, the crews, ROV teams, blages. The H’ index varied between thetic organisms, including free-living and chief scientists of the cruises: 2.52 and 3.63. The Kazan phylotypes microbes and symbiotic associations • ARKTIS XIX/3b (2003): Polarstern are related to the Acidobacteria, with invertebrates. Chemosynthetic (Michael Klages); Actinobacteria, Bacilli, Clostridia, habitats are isolated and highly fractured • BIONIL (2006): Meteor (Antje Chloroflexi, Spirochaetes, Nitrospira, ecosystems in which the organisms Boetius); Planctomycetes, Alpha-, Gamma- and require distinct environmental features • Vicking (2006): Pourquoi pas?, Deltaproteobacteria, OP11, WS3, and a and cues to maintain their populations Victor 6000 (Hervé Nouzé); few unclassified Bacteria (Heijs et al., (temperature, presence of sulfide and • MEDECO (2007): Pourquoi pas?,

2007; Kormas et al., 2008; recent work CH4, hard ground, flux). The Victor 6000 (Jozée Sarrazin and of author Pachiadaki and colleagues). life history of and microbes Catherine Pierre). Archaeal diversity was also lower, vary- restricted to chemosynthetic ecosystems ing between 1.63 and 2.57. The occur- and their dispersal remains a key limita- References ring phylotypes are related to MGI, tion in understanding the interconnec- Akhmetzhanov, A.M., M. Ivanov, N.H. Kenyon, and A. Mazzini. 2007. Deep-water cold seeps, sedimentary novel Crenarchaeota, Halobacteriales, tivity and resilience of these dynamic environments and ecosystems of the Black and Methanosarcinales, Thermoplasmata, ecosystems. Interconnectivity can be Tyrrhenian Sea and the Gulf of Cádiz. Preliminary results of investigations during the TTR-15 and unclassified Archaea (Heijs et al., studied at different geographical scales cruise, RV Professor Logachev, June–August 2005, 2007; Kormas et al., 2008; recent work as well as among vents, seeps and other Intergovernmental Oceanographic Commission, of author Pachiadaki and colleagues). habitats, which requires a combination Paris, 99 pp. plus appendices. Aloisi, G., I. Bouloubassi, S.K. Heijs, R.D. Pancost, C. Further work on the microbial biodiver- of biological, oceanographic, and bio- Pierre, J.S. Sinninghe Damste, J.C. Gottschal, L.J. sity of eastern Mediterranean mud vol- geographic studies, including population Forney, and J.-M. Rouchy. 2002. CH4-consuming and the formation of carbonate canoes and pockmarks of the Nile Deep biology using genomic markers to assess crusts at cold seeps. Earth and Planetary Science Sea Fan is underway, focusing on the gene flow. Furthermore, in a changing Letters 203:195–203. variety of microbial mats and associated ocean it becomes critical to assess varia- Barry, J.P., R.E. Kochevar, and C.H. Baxter. 1997. The influence of pore-water chemistry and physiology communities (Omoregie et al., 2007). tions in biodiversity across all habitats on the distribution of vesicomyid clams at cold in order to distinguish between natural seeps in : Implications for patterns Outlook and anthropogenic effects. The first of chemosynthetic community organization. and Oceanography 42:318–328. Seeps, vents, and other reduced ecosys- long-term observatories at cold seeps are Bergquist, D.C., C. Fleckenstein, J. Knisel, B. Begley., tems contain a variety of organisms with planned, and will provide data on the I.R. MacDonald, and C.R. Fisher. 2005. Variations in seep bed communities along physical unique functions related to chemoau- link between environmental fluctuations and chemical environmental gradients. Marine totrophy, respiration, detoxification, and the fate of the benthic ecosystem. Ecology Progress Series 293:99–108. mineral precipitation and dissolution, Bergquist, D.C., I.A. Urcuyo, and C.R. Fisher. 2002. Establishment and persistence of seep vestimen- attachment, and sensing (chemotaxis). Acknowledgements tiferan aggregations from the upper Louisiana Among the most remarkable observa- First, we would like to thank Myriam slope of the Gulf of Mexico. Marine Ecology Progress Series 241:89–98. tions regarding different size groups Sibuet who was one of the initiators Bergquist, D.C., T. Ward, E.E. Cordes, T. McNelis, S. and taxa, from bacteria to fish, are the of the HERMES project and the first Howlett, R. Koisoff, S. Hourdez, R. Carney, and

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