Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes

Two mud volcano fields were explored during the French–Dutch MEDINAUT cruise (1998) with the submersible NAUTILE, one south of Crete along the Mediteranean Ridge at about 2000 m depth (Olimpi mud field) and the other south of Turkey between 1700 and 2000 m depth (Anaximander mud field) where high methane concentrations were measured. Chemosynthetic communities were observed and sampled on six mud volcanoes and along a fault scarp. The communities were dominated by bivalves of particularly small size, belonging to families commonly found at seeps (Mytilidae, Vesicomyidae, Thyasiridae) and to Lucinidae mostly encountered in littoral sulfide-rich sediments and at the shallowest seeps. Siboglinid polychaetes including a large vestimentiferan Lamellibrachia sp. were also associated. At least four bivalve species and one siboglinid are associated with symbiotic chemoautotrophic bacteria, as evidenced by Transmission Electronic Microscopy and isotopic ratio measurements. Among the bivalves, a mytilid harbors both methanotrophic and sulfide-oxidizing bacteria. Video spatial analysis of the community distribution on three volcanoes shows that dense bivalve shell accumulations (mainly lucinids) spread over large areas, from 10% to 38% of the explored areas (2500–15000 m²) on the different volcanoes. Lamellibrachia sp. had different spatial distribution and variable density in the two mud volcano fields, apparently related with higher methane fluxes in the Anaximander volcanoes and maybe with the instability due to brines in the Olimpi area. The abundance and richness of the observed chemosynthetic fauna and the size of some of the species contrast with the poverty of the deep eastern Mediterranean. The presence of a specialized fauna, with some mollusk genera and species shared with other reduced environments of the Mediterranean, but not dominated by the large bivalves usually found at seeps, is discussed.     

Mud volcanoes in the Mediterranean Sea are hot spots of exclusive meiobenthic species

Mud volcanoes are cold seeps, in which the escape of gas and fluids associated with mud creates 3-D bottom structures that enhance the spatial heterogeneity and potentially alter the functioning of the benthic ecosystems. We investigated a complex system of mud volcanoes of the Mediterranean Sea characterised by the presence of different structures (i.e., isolated domes, domes surrounded by moats, clustered domes, and ridges) displaying different levels of seepage. We hypothesize that the combined effects of seafloor heterogeneity (i.e., different 3-D structures as revealed by detailed topographic analysis), fluid emissions and trophic characteristics of these systems can influence the structural and functional biodiversity of meiofauna (with special focus on the nematodes). We found that sediments affected by intensive seepage displayed the lowest faunal abundances and number of higher taxa. However, mud volcanoes without emissions, but characterized by a high structural complexity (such as the ridges), were associated with the highest meiofaunal abundances and number of higher taxa. Mud volcanoes hosted also a remarkable abundance of rare taxa specifically associated with these structures (e.g., acarians, cumaceans, tanaids, cladocerans and hydroids) and absent in slope sediments (used as a control). Each mud-volcano area displayed a different nematode species composition. Overall 76 nematode species (from a total of 235) were exclusively associated with mud-volcano structures, whilst 29 were exclusively encountered in slope sediments. We conclude that the presence of mud volcanoes, for their contribution to increase spatial heterogeneity and for the extreme conditions associated with gas emissions, promotes higher levels of beta diversity, thus enhancing the regional (gamma) benthic diversity. These findings provide new insights on the factors controlling meiobenthic biodiversity in mud volcanoes and clues for future action of conservation of the biodiversity specifically associated with these habitats.     

深海化能生态系统双壳纲共生体系互作机制研究进展

双壳纲贝类在深海特殊生境——热液、冷泉及有机沉落生态系统中分布广泛,并且在其体内常含有化能共生细菌为贝类提供营养物质。双壳纲贝类与化能共生菌形成的共生体系对于其适应深海还原性生境至关重要。近40 a来随着海洋科考力度加大,深海化能生境的神秘面纱被逐渐揭开,越来越多的深海物种被发现,双壳纲贝类无疑是这些化能生态系统中的优势物种。在此,我们对常见的深海化能共生双壳纲贝类与其内共生菌的互作研究进行总结,主要双壳纲门类包含贻贝科（Mytilidae）、囊螂科（Vesicomyidae）、蛏螂科（Solemyidae）、索足蛤科（Thyasiridae）和满月蛤科（Lucinidae）,梳理归纳的内容包括深海化能生态系统的发现、“双壳纲贝类—内共生菌”共生体系的组成、共生体系的营养互作、共生体系的建立与维持以及对未来研究的展望。对这些研究内容的总结有利于进一步加深我们对深海特殊生命系统中共生互作机制的认识。     

Blake Ridge methane seeps: characterization of a soft-sediment,chemosynthetically based ecosystem

Observations from the first submersible reconnaissance of the Blake Ridge Diapir provide the geological and ecological contexts for chemosynthetic communities established in close association with methane seeps. The seeps mark the loci of focused venting of methane from the gas hydrate reservoir, and, in one location (Hole 996D of the Ocean Drilling Program), methane emitted at the seafloor was observed forming gas hydrate on the underside of a carbonate overhang. Megafaunal elements of a chemosynthetically based community mapped onto dive tracks provide a preliminary overview of faunal distributions and habitat heterogeneity. Dense mussel beds were prominent and covered 20×20 m areas. The nearly non-overlapping distributions of mussels and clams indicate that there may be local (meter-scale) variations in fluid flux and chemistry within the seep site. Preliminary evidence suggests that the mussels are host to two symbiont types (sulfide-oxidizing thiotrophs and methanotrophs), while the clams derive their nutrition only from thiotrophic bacteria. Invertebrate biomass is dominated by mussels (Bathymodiolus heckerae) that reach lengths of up to 364 mm and, to a lesser extent, by small (22 mm length) vesicomyid clams (Vesicomya cf. venusta). Taking into account biomass distributions among taxa, symbiont characteristics of the bivalves, and stable-isotope analyses, the relative importance of methanotrophic vs thiotrophic bacteria in the overall nutrition of the invertebrate assemblage is on the order of 60% vs 40% (3:2).     

Mud volcanoes and gas vents in the Okhotsk Sea area

Gas emissions from mud volcanoes on Sakhalin Island and water-column gas flares arising from cold seeps in the Okhotsk Sea appear to be related. They are likely activated by tectonic movements along the transform plate boundary separating the Okhotsk Sea Plate from the Eurasian and Amur plates. Gas vents (flares) and methane anomalies occur in the waters offshore Sakhalin Island, along with NE-SW-trending mounds and fluid escape structures on the seafloor. The intersection of the NE-striking transverse faults on land with the Central Sakhalin and Hokkaido-Sakhalin shear zones apparently determines the sites of mud volcanoes, a pattern that continues offshore where the intersection with the East Sakhalin and West Derugin shear zones determines the sites of the submarine gas vents.     

New discoveries of mud volcanoes on the Moroccan Atlantic continental margin (Gulf of Cádiz): morpho-structural characterization

During the MVSEIS-08 cruise of 2008, ten new mud volcanoes (MVs) were discovered on the offshore Moroccan continental margin (Gulf of Cádiz) at water depths between 750 and 1,600?m, using multibeam bathymetry, backscatter imagery, high-resolution seismic and gravity core data. Mud breccias were recovered in all cases, attesting to the nature of extrusion of these cones. The mud volcanoes are located in two fields: the MVSEIS, Moundforce, Pixie, Las Negras, Madrid, Guadix, Almanzor and El Cid MVs in the western Moroccan field, where mud volcanoes have long been suspected but to date not identified, and the Boabdil and Al Gacel MVs in the middle Moroccan field. Three main morphologies were observed: asymmetric, sub-circular and flat-topped cone-shaped types, this being the first report of asymmetric morphologies in the Gulf of Cádiz. Based on morpho-structural analysis, the features are interpreted to result from (1) repeated constructive (expulsion of fluid mud mixtures) and destructive (gravity-induced collapse and submarine landsliding) episodes and (2) interaction with bottom currents.     

Cold-seep assemblages on a giant pockmark off West Africa: spatial patterns and environmental control

A giant pockmark colonised by dense cold‐seep assemblages near 3160 m depth along the Congo‐Angola margin has been surveyed by the ROV Victor 6000. The quantitative distribution of chemosynthetic communities was mapped along the dive tracks from a video study using GIS and image mosaicking. Several types of faunal assemblages, either dominated by bivalves of the families Mytilidae (Bathymodiolus sp.) or Vesicomyidae (Calyptogena sp., ‘Vesicomya’ aff. chuni), or by Siboglinidae polychaetes (Escarpia southwardae) were mapped over the 800‐m diameter pockmark area and sampled for fauna, water and sediment. The isotopic analyses (δ¹³C) of tissues from symbiont‐bearing species were within the range typical of nutrition via symbiosis using methane for mussels and sulphide for vesicomyids and siboglinids. The living chemosynthetic communities were distributed on a SW‐NE axis, corresponding to the expression at the sediment surface of a main buried channel providing fluids to the pockmark. The site was characterised by a more active central part in a depression with abundant carbonate concretions where high‐density clusters of siboglinids and mytilids dominate. Large fields of dead and live vesicomyids with a lower mean density were observed in the external areas. The mean coverage of each of the three symbiotic taxa in these two contrasted areas was estimated from mosaic analysis and was up to 30% in the central area dominated by E. southwardae bushes (23%). Symbiont‐bearing species distribution was consistent with methane concentrations in seawater that were generally higher in mytilid beds than in the vicinity of siboglinids and vesicomyids. A Principal Component Analysis performed on environmental factors at the ten sampling sites revealed that 37% of the observed variance in the distribution of symbiont‐bearing species may be explained by variation in both methane and oxygen concentrations, while a Canonical Redundancy Analysis selected methane concentration as the only variable which explains symbiont‐bearing species densities. This spatial distribution of chemosynthetic species at the pockmark scale may reflect temporal patterns of succession of both substrate and fauna, and may be related to different individual pockmarks visible on the microbathymetry mapped using ROV data.     

Composition and spatial organization of a cold seep community on the South Barbados accretionary prism: Tectonic, geochemical and sedimentary context

Deep faunal assemblages were observed on cold seeps, between 1000 and 2000m depth, along the southern termination of the Barbados accretionary prism, during the Caracolante II and Diapicar cruises. Faunal composition and microdistribution of a cold seep community were analyzed at one site using deep-sea photographs and seismic (3.5 Kz) profiles. The community is dominated by large mussels up to 20cm long (possibly related to the genus Bathymodiolus), tiny vesicomyid clams, and vestimentiferan clusters in which animals are up to 2m long. There is a high density of sponges (three species), bryozoans and gorgonians. Other taxa occasionally associated with this assemblage include galatheid crabs, anemones, holothurians and possibly pennatulaceans which are numerous at boundaries of the site. A typical deep-sea fauna of fish, asteroids and ophiuroids is also scattered about the vicinity. This seep community is distributed as a band of discontinuous colonies, 40–50m in width and more than 10km in length. Living colonies alternate with accumulations shells and bare areas. The substratum is hard mud covered by a ferrugineous crust and cemented by carbonates. The early diagenetic character of the bottom and the occurrence of biological assemblages indicate that seepages of sulphur and/or methane, which have been revealed along the decollement zone of the Barbados prism, must diffuse through the sea floor. These biological and geological features are located on the crests of NE-SW anticlinal ridges and mud volcanoes which have been built by diaprism.     

ROV study of a giant pockmark on the Gabon continental margin

A giant, 800-m wide pockmark, called Regab, was discovered along the Equatorial African margin at 3160-m water depth and was explored by remote operated vehicle (ROV) as part of the Zaiango (1998–2000) and Biozaire (2001–2003) projects carried out conjointly by TOTAL and a number of French research institutes. A microbathymetric map obtained using the ROV sensors shows that the pockmark actually consists of a cluster of smaller pockmarks aligned N70 along a 15-m deep depression. Methane was recorded all over the pockmark, the highest values along the axis of the depression where massive carbonate crusts and dense seep communities were also found. Several faunal species belong to the Vesicomyidae and Mytilidae bivalve families, as well as to Siboglinidae (Vestimentifera) tubeworms. Preliminary analyses confirm their association with symbiotic bacteria, thus documenting their dependence on fluid seeps. The pockmark appears to be related to an infilled channel, visible on the seismic data 300 m below the seafloor, which may act as a reservoir for biogenic fluids supplied to the trap from the surrounding sediments.     

Terrestrial methane seeps and mud volcanoes: A global perspective of gas origin

A global database of gas composition and methane stable isotopes of 143 terrestrial mud volcanoes from 12 countries and 60 seeps independent from mud volcanism from eight countries, was compiled and examined in order to provide the first worldwide statistics on the origin of methane seeping at the earth's surface. Sixteen seep data were coupled with their associated subsurface reservoirs.     

Epizooic metazoan meiobenthos associated with tubeworm and mussel aggregations from cold seeps of the northern Gulf of Mexico

The abundance and higher taxonomic composition of epizooic metazoan meiobenthic communities associated with mussel and tubeworm aggregations of hydrocarbon seeps at Green Canyon, Atwater Valley, and Alaminos Canyon in depths between 1400 and 2800?m were studied and compared to the infaunal community of non-seep sediments nearby. Epizooic meiofaunal abundances of associated meiobenthos living in tubeworm bushes and mussel beds at seeps were extremely low (usually <100?ind. 10?cm(-2)), similar to epizooic meiofauna at deep-sea hydrothermal vents, and the communities were composed primarily of nematodes, copepods, ostracods, and halacarids. In contrast, epizooic meiobenthic abundance is lower than previous studies have reported for infauna from seep sediments. Interestingly, non-seep sediments contained higher abundances and higher taxonomic diversity than epizooic seep communities, although in situ primary production is restricted to seeps.     

Seafloor geological studies above active gas chimneys off Egypt (Central Nile Deep Sea Fan)

Four mud volcanoes of several kilometres diameter named Amon, Osiris, Isis, and North Alex and located above gas chimneys on the Central Nile Deep Sea Fan, were investigated for the first time with the submersible Nautile. One of the objectives was to characterize the seafloor morphology and the seepage activity across the mud volcanoes. The seepage activity was dominated by emissions of methane and heavier hydrocarbons associated with a major thermal contribution. The most active parts of the mud volcanoes were highly gas-saturated (methane concentrations in the water and in the sediments, respectively, of several hundreds of nmol/L and several mmol/L of wet sediment) and associated with significantly high thermal gradients (at 10 m below the seafloor, the recorded temperatures reached more than 40 °C). Patches of highly reduced blackish sediments, mats of sulphide-oxidizing bacteria, and precipitates of authigenic carbonate were detected, indicative of anaerobic methane consumption. The chemosynthetic fauna was, however, not very abundant, inhibited most likely by the high and vigorous fluxes, and was associated mainly with carbonate-crust-covered seafloor encountered on the southwestern flank of Amon. Mud expulsions are not very common at present and were found limited to the most active emission centres of two mud volcanoes, where slow extrusion of mud occurs. Each of the mud volcanoes is fed principally by a main narrow channel located below the most elevated areas, most commonly in the centres of the structures. The distribution, shape, and seafloor morphology of the mud volcanoes and associated seeps over the Central Nile Deep Sea Fan are clearly tectonically controlled.     

Phase-reversed seabed reflections in seismic data: examples related to mud volcanoes from the South Caspian Sea

The sediment–water interface is usually marked by an increase in acoustic impedance and is therefore displayed in a seismic section as a positive polarity reflection. Here, we use the term “seabed phase reversal” to describe areas of seafloor which are instead expressed as a negative polarity reflection in seismic data. We describe in detail a number of examples of seafloor phase reversals and use a simple one-dimensional geophysical model to test the hypothesis that they are the result of the presence of gas within the seafloor sediment. Our examples are all related to seismically imaged mud volcanoes located within the South Caspian Sea. Sections of phase-reversed seafloor at the summit area of these volcanoes have been mapped to reveal the existence of seafloor mud pools (salses) and recently erupted mud flows which show a strong similarity to smaller-scale features at onshore volcanoes in Azerbaijan. Synthetic geophysical modelling indicates that under the physical conditions likely to occur when the seabed sediment is gas-bearing, the seafloor will be expressed as a strong negative polarity reflection. Unlike other indicators of seafloor gas, such as pockmarks, which merely record the transient expulsion of fluids from sedimentary basins, seafloor phase reversals indicate the presence of gas in marine sediment at the time of survey acquisition. They therefore are of significance to engineering and site survey operations as well as the identification of biological communities and gas flux calculations.     

Influence of seep emission on the non-symbiont-bearing fauna and vagrant species at an active giant pockmark in the Gulf of Guinea (Congo–Angola margin)

Detailed surveying with an ROV found that a dense and diverse cold-seep community colonises a giant pockmark located at 3200 m depth, 8 km north from the deep Congo channel. Several types of assemblages, either dominated by Mytilidae and Vesicomyidae bivalves or Siboglinidae polychaetes, are distributed on the 800-m diameter active area. The site is characterised by a most active central zone in a depression with abundant carbonate concretions and high methane fluxes where high-density clusters of mussels and siboglinids dominate. In contrast, the peripheral zones display large fields of dead and live vesicomyids on soft sediment, with a lower mean density and lower methane concentration in seawater. The associated megafauna includes Alvinocarididae shrimps, echinoids, holothurians of the family Synaptidae, several species of gastropods, two species of galatheids, and Zoarcidae and Ophidiidae fishes. Multivariate analyses of video transect data show that the distribution of these major megafauna species at the pockmark scale is influenced by the habitat heterogeneity due to fluid or gas emission, occurrence of hydrates, substratum variability and by the presence of large symbiont-bearing species. Several assemblages dominated either by mytilids, vesicomyids, or siboglinids have been sampled for megafauna densities and biomass estimations and stable isotope measurements (δ¹³C and δ¹⁵N) of dominant species and food sources. The highest estimates of megafauna densities have been obtained in mytilid beds. According to their stable isotopes values, non-symbiont-bearing species mainly rely on chemosynthesis-originated carbon, either as primary consumers of chemoautotrophic microorganisms, or at higher trophic level recycling organic matter, or relying on bivalve and tubeworm production. Most of them likely feed on different sources like shrimps, but differences according to habitat have been evidenced. Carbon and nitrogen isotope ratios of galatheids and benthic or benthopelagic fishes captured by trawls at increasing distances from the pockmark provide evidence of the high variability in the proportion of chemosynthesis-originated carbon in their diet, from 15% to 38%, according to the species captured as far as 4 km to the site.     

Acoustic investigations of mud volcanoes in the Sorokin Trough, Black Sea

The Sorokin Trough (Black Sea) is characterized by diapiric structures formed in a compressional tectonic regime that facilitate fluid migration to the seafloor. We present acoustic data in order to image details of mud volcanoes associated with the diapirs. Three types of mud volcanoes were distinguished: cone-shaped, flat-topped, and collapsed structures. All mud volcanoes, except for the Kazakov mud volcano, are located above shallow mud diapirs and diapiric ridges. Beyond the known near-surface occurrence of gas hydrates, bottom simulating reflectors are not seen on our seismic records, but pronounced lateral amplitude variations and bright spots may indicate the presence of gas hydrates and free gas.     

The influence of geological, geochemical, and biogenic habitat heterogeneity on seep biodiversity

Cold seeps are among the most heterogeneous of all continental margin habitats. Abiotic sources of heterogeneity in these systems include local variability in fluid flow, geochemistry, and substrate type, which give rise to different sets of microbial communities, microbial symbiont-bearing foundation species, and associated heterotrophic species. Biogenic habitats created by microbial mats and the symbiotic species including vesicomyid clams, bathymodiolin mussels, and siboglinid tubeworms add an additional layer of complexity to seep habitats. These forms of habitat heterogeneity result in a variety of macrofaunal and meiofaunal communities that respond to changes in structural complexity, habitat geochemistry, nutrient sources, and interspecific interactions in different ways and at different scales. These responses are predicted by a set of theoretical metacommunity models, the most appropriate of which for seep systems appears to be the 'species sorting' concept, an extension of niche theory. This concept is demonstrated through predictable patterns of community assembly, succession, and beta-level diversity. These processes are described using a newly developed analytical technique examining the change in the slope of the species accumulation curve with the number of habitats examined. The diversity response to heterogeneity has a consistent form, but quantitatively changes at different seep sites around the world as the types of habitats present and the size-classes of fauna analyzed change. The increase in beta diversity across seep habitat types demonstrates that cold seeps and associated biogenic habitats are significant sources of heterogeneity on continental margins globally.     

Gouge marks on deep-sea mud volcanoes in the eastern Mediterranean: Caused by Cuvier's beaked whales?

Enigmatic seafloor gouge marks at depths of 1700–2100 m have been observed from submersible during geological survey work studying mud volcanoes in the eastern Mediterranean Sea. The marks consist of a central groove (about 10 cm deep and 1–2 m long), superimposed on a broader bowl-shaped depression (1–2 m long by about 50 cm wide) with raised rims (up to 10 cm high) to either side of the central groove. We discuss the potential biological causes of these marks, and conclude that they are probably created by Cuvier's beaked whales (Ziphius cavirostris) during foraging dives to these depths. The mud volcanoes have a comparatively rich and diverse benthic ecology associated with methane-rich fluid seeps and thus could be the base of food chains that reach top predators like the deep-diving whales. The characteristic high acoustic backscatter of the mud volcanoes would facilitate their detection by the echolocation system of these whales.     

Cold seeps of the deep Gulf of Mexico: Community structure and biogeographic comparisons to Atlantic equatorial belt seep communities

Quantitative collections of tubeworm- and mussel-associated communities were obtained from 3 cold seep sites in the deep Gulf of Mexico: in Atwater Valley at 1890 m depth, in Alaminos Canyon at 2200 m depth, and from the Florida Escarpment at 3300 m depth. A total of 50 taxa of macro- and megafauna were collected including 2 species of siboglinid tubeworms and 3 species of bathymodiolin mussels. In general, the highest degree of similarity was between communities collected from the same site. Most of the dominant families at the well-characterized upper Louisiana slope seep sites of the Gulf of Mexico were present at the deep sites as well; however, there was little overlap at the species level between the upper and lower slope communities. One major difference in community structure between the upper and lower slope seeps was the dominance of the ophiuroid Ophioctenella acies in the deeper communities. The transition between upper and lower slope communities appears to occur between 1300 and 1700 m based on the number of shared species with the Barbados seeps at either end of this depth range. Seep communities of the deep Gulf of Mexico were more similar to the Barbados Accretionary Prism seep communities than they were to either the upper slope Gulf of Mexico or Blake Ridge communities based on numbers of shared species and Bray–Curtis similarity values among sites. The presence of shared species among these sites suggests that there is ongoing or recent exchange among these areas. An analysis of bathymodioline mussel phylogeography that includes new collections from the west coast of Africa is presented. This analysis also suggests recent exchange across the Atlantic equatorial belt from the Gulf of Mexico to the seeps of the West Nigerian margin.     

Trace metals in bivalve molluscs from Thailand

Capture fisheries and aquaculture provide a large quantity of bivalve molluscs for human consumption in Thailand each year. The existing information on trace elements in these bivalves is fragmentary and contradictory. This paper reports data for eight metals (cadmium, chromium, copper, iron, lead, nickel, mercury and zinc) in the four major species marketed. These are the clam Pahia undulata, the cockle Anadara granosa, the green mussel Perna viridis and the rock oyster Crassostrea commercialis. The bivalves analysed were taken at markets or in the field to cover as many of the major sources as possible. The results indicate no major threat to public health from trace elements in these species from Thailand and lend confidence to the expansion of aquaculture operations. In particular, the levels of lead found in the samples analysed are considerably lower than those previously reported by other authors.