Myriam Sibuet

Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins

Abstract To date, several cold-seep areas which fuel chemosynthesis-based benthic communities have been explored, mainly by deployment of manned submersibles. They are located in the Atlantic and in the Eastern and Western Pacific oceans and in the Mediterranean Sea, in depths ranging between 400 and 6000 m in different geological contexts in passive and active margins. Our study is based on a review of the existent literature on 24 deep cold seeps. The geographic distribution of seeps, the variations of origin and composition of fluids, and rates of fluid flow are presented as they are important factors which explain the spatial heterogeneity and the biomass of biological communities. Methane-rich fluid of thermogenic and/or biogenic origin is the principal source of energy for high-productive communities; however, production of sulphide by sulphate reduction in the sediment also has a major role. The dominant seep species are large bivalves belonging to the families Vesicomyidae or Mytilidae. Other symbiont-containing species occur belonging to Solemyidae, Thyasiridae, Lucinidae bivalves, Pogonophora worms, Cladorhizidae and Hymedesmiidae sponges. Most of the symbiont-containing cold-seep species are new to science. Different symbiont-containing species rely on sulphide or methane oxidation, or both, via chemoautotrophic endosymbiotic bacteria. A total of 211 species, from which 64 are symbiont-containing species, have been inventoried. Patterns in biodiversity and biogeography are proposed. A large majority of the species are endemic to a seep area and the symbiont-containing species are mainly endemic to the cold-seep ecosystem. A comparison of species found in other deep chemosynthesis-based ecosystems, hydrothermal vents, whale carcass and shipwreck reduced habitats, reveals from the existing data, that only 13 species, of which five are symbiont-containing species occur, at both seeps and hydrothermal vents. The species richness of cold-seep communities decreases with depth. High diversity compared to that on hydrothermal vent sites is found at several seeps. This may be explained by the duration of fluid flow, the sediment substrate which may favour long-term conditions with accumulation of sulphide and the evolution of cold seeps.

Long-term change in the megabenthos of the Porcupine Abyssal Plain (NE Atlantic)

A radical change in the abundance of invertebrate megafauna on the Porcupine Abyssal Plain is reported over a period of 10 years (1989–1999). Actiniarians, annelids, pycnogonids, tunicates, ophiuroids and holothurians increased significantly in abundance. However, there was no significant change in wet weight biomass. Two holothurian species, Amperima rosea and Ellipinion molle, increased in abundance by more than two orders of magnitude. Samples from the Porcupine Abyssal Plain over a longer period (1977–1999) show that prior to 1996 these holothurian species were always a minor component of the megafauna. From 1996 to 1999 A. rosea was abundant over a wide area of the Porcupine Abyssal Plain indicating that the phenomenon was not a localised event. Several dominant holothurian species show a distinct trend in decreasing body size over the study period. The changes in megafauna abundance may be related to environmental forcing (food supply) rather than to localised stochastic population variations. Inter-annual variability and long-term trends in organic matter supply to the seabed may be responsible for the observed changes in abundance, species dominance and size distributions.

Deep-Sea Biodiversity in the Mediterranean Sea: The Known, the Unknown, and the Unknowable

Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.

Cold seep communities as indicators of fluid expulsion patterns through mud volcanoes seaward of the Barbados accretionary prism

Cold seep communities are sustained by massive methane-rich fluid expulsion through mud volcanoes located at about 5000 m in the Barbados Trench. These communities, dependent on chemosynthetic processes, are dominated by a vesicomyid bivalve assumed to be a new species related to the genus Calyptogena, and by large bushes of the sponge Cladorhizidae. Both are associated with symbiotic bacteria and are indicative of methane release in seawater and sulphide production in sediments. Non-symbiotic organisms, such as large fields of filter-feeding polychaetes and high densities of meiofauna are indicative of enhanced biological production in the sediments. The spatial distribution of the bivalve populations was mapped using video observations and a computer method based on a simple calculation of the area covered by a submersible camera. The observation of clam beds of variable densities allows us to define two types of fine-scale fluid expulsion pattern: dense Calyptogena beds (up to 150 ind.m−2) are associated with“vents” with relatively high fluid discharge velocities of about 10 cm s−1 and focused by high permeability conduits, whereas dispersed clams (1–10 ind.m−2) are probably sustained only by slow, diffusive “seepages”. The distribution of the chemosynthetic zones from the centre to the edges of the volcano, highlighting the heterogeneity of the concentric zones from the centre to the edges of the volcano, highlighting the heterogeneity of the fluid expulsion pattern at the scale of the volcano. The spatial distribution of the chemosynthetic communities characterizes the fluid expulsion on several types of volcanoes: two mud volcanoes, identified as diatremes, named Atalante and Cyclope, are flat with a central lake of warm fluid mud that is devoid of life, whereas Calyptogena beds are located in the outer regions. On the two other structures, mounds shaped as cones, all activity is concentrated near the summit and seems to be related to higher flow vents than on diatremes. However, the scarceness of bivalves on the flanks of these volcanoes indicates that low flow seepages are less developed than on diatremes. The high mean clam density and the presence of large Cladorhizidae bushes on the volcano Atalante show that larger quantities of methane are emitted through this structure than on the others, and suggest a more evolved surface, favouring chemosynthetic production, than on the other diatreme, named Cyclope. The level of colonization and the spatial patterns of the chemosynthetic communities, when compared on the different volcanoes, suggest that they are at different stages of activity.

Dual Symbiosis in a Bathymodiolus sp. Mussel from a Methane Seep on the Gabon Continental Margin (Southeast Atlantic): 16S rRNA Phylogeny and Distribution of the Symbionts in Gills

ABSTRACT Deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae) harbor symbiotic bacteria in their gills and are among the dominant invertebrate species at cold seeps and hydrothermal vents. An undescribed Bathymodiolus species was collected at a depth of 3,150 m in a newly discovered cold seep area on the southeast Atlantic margin, close to the Zaire channel. Transmission electron microscopy, comparative 16S rRNA analysis, and fluorescence in situ hybridization indicated that this Bathymodiolus sp. lives in a dual symbiosis with sulfide- and methane-oxidizing bacteria. A distinct distribution pattern of the symbiotic bacteria in the gill epithelium was observed, with the thiotrophic symbiont dominating the apical region and the methanotrophic symbiont more abundant in the basal region of the bacteriocytes. No variations in this distribution pattern or in the relative abundances of the two symbionts were observed in mussels collected from three different mussel beds with methane concentrations ranging from 0.7 to 33.7 μM. The 16S rRNA sequence of the methanotrophic symbiont is most closely related to those of known methanotrophic symbionts from other bathymodiolid mussels. Surprisingly, the thiotrophic Bathymodiolus sp. 16S rRNA sequence does not fall into the monophyletic group of sequences from thiotrophic symbionts of all other Bathymodiolus hosts. While these mussel species all come from vents, this study describes the first thiotrophic sequence from a seep mussel and shows that it is most closely related (99% sequence identity) to an environmental clone sequence obtained from a hydrothermal plume near Japan.

Cold Seep Communities on Continental Margins: Structure and Quantitative Distribution Relative to Geological and Fluid Venting Patterns

Cold seep ecosystems occur on active and passive continental margins. Chemosynthesisbased communities depend on autochtonous and local chemical energy and produce organic carbon in large quantities through microbial chemosynthesis. The high organic carbon production leads to the large size of the fauna and the high biomass of the communities. The remarkable abundance of giant tubeworms (vestimentiferans) and large bivalves (i.e. Vesicomyidae, Mytilidae and others) is one of the most striking features of such communities and one of the best indicators or tracers of fluid emissions at the seafloor. Cold seep communities are known since about 15 years and have shown that the chemoautotrophy and many symbiont containing organisms are not unique to hydrothermal vents. Ecosystem characteristics and functioning in continental margin habitats are incompletely understood and we do not know how detritus and chemosynthesis-based ecosystems interact. There is a clear need of more field investigations. But with progress in deep-sea submersible technology, our understanding continues to grow. Following a recent review that focused on biogeographical trends and comparisons with hydrothermal vent communities (Sibuet and Olu 1998), we review here the ecology of chemosynthesis-based communities from several cold seep areas. Our synthesis addresses biodiversity and abundance fluctuations and distribution patterns linked to geological and fluid venting features. The diversity of the “symbiotic” fauna expressed as species richness decreases with ocean depth. Species composition is an indicator of the biotope variability. The spatial extension of active seep areas is highly variable from hundreds of square meters to several hectares. Three distinct categories of cold seep sites are recognised. The shape, density and biomass of aggregations reflect the intensity of fluid flow, and characterise fluid circulation and different expulsion pathways through geological structures.

Spatial distribution of diverse cold seep communities living on various diapiric structures of the southern Barbados prism

Three sectors of the south Barbados prism between 1000 and 2000 m depth were explored by the French submersible Nautile. Chemosynthesis-based benthic communities were discovered on several structures affected by diapirism, including mud volcanoes, domes and an anticlinal ridge. The communities are associated with the expulsion of methane-rich fluids which is a wide-spread process in the area. These communities are dominated by large bivalves and vestimentiferans which harbour chemoautotrophic symbiotic bacteria. The symbiotic bivalves include two species of Mytilidae and one of Vesicomyidae, with dominance of a methanotrophic mussel. Cartography of the benthic communities, interpretation of thermal measurements and observation of sedimentary patterns have been used to define the life habits of each of the three species of symbiotic bivalves. Each species has a characteristic preference for different conditions of edaphic and fluid flow: the dominant methanotrophic mussel appears to require high velocity vents and hard substratum. The vesicomyids and the other species of mussel are able to take up sulfide from the sediments, and so are associated with low seepages, but also require soft sediment. The three bivalve species are assumed successively to colonize the top of a diapiric ridge, in a succession related to the temporal evolution of fluid flow and sedimentation. The composition of the bivalve assemblages, their densities and biomasses all differ between the several mud volcanoes and domes studied, and these parameters are thought to be related to the spatial and temporal variations of fluid expulsion through the structures, and the lithification processes linked to fluid expulsion. One very active dome is at present colonized by an exceptionally large and dense population of the methanotrophic mussel. In contrast, communities in another area, on the domes and volcanoes that are currently inactive, were colonized by only a few living vesicomyids and mussels, both associated with sulfur-oxydizing bacteria, and there were numerous empty shells. The densities and biomasses of symbiotic bivalves were far greater in the area studied than in a deeper mud volcano field on the same prism that had been studied previously. This is consistent with a report that methane production is greater in the southern region of this accretionary prism than in the northern. Numerous non-symbiotic organisms were observed in and around the areas of the seeps, some are endemic to the seep communities, including some gastropods and shrimps, others are either colonists or vagrants from the surrounding deep-sea floor. Filter feeders were very abundant, and some of these, like the serpulids and large sponges, may also be dependent on the chemosynthetic production. Faunistic composition of both symbiotic and non-symbiotic taxa, of the assemblages around these cold seeps, is closely related to that reported for communities living on hydrocarbon seeps in the Gulf of Mexico.

Temporal patterns among meiofauna and macrofauna taxa related to changes in sediment geochemistry at an abyssal NE Atlantic site

Abstract Two major size classes of the sediment community, meiofauna and macrofauna, and four classes of lipid compounds, fatty acids, alkanes, alcohols and sterols, were investigated using multicorer and USNEL boxcorer samples, collected during six cruises over a two year period (September 1996 to September–October 1998), at the Porcupine Abyssal Plain (∼ 48° 50′N 16° 30′W, 4850 m depth) within the framework of the MAST 3 BENGAL project. This site was known to be subject to seasonality in the input of organic matter to the seafloor. Results are given for each faunal size class in terms of taxonomic structure at the level of phylum, class or order, depending on the taxon, and for the dominant faunal components in terms of density and vertical distribution. For each lipid compound class, results are given in concentration and vertical distribution. The taxonomic structure of each size class did not change within the study period. Total meiofaunal and macrofaunal densities were particularly high, probably reflecting the high quantity and quality of organic matter inputs to the site. The dominant components of the two size classes presented different temporal patterns in their responses to changes in their environment. Populations of meiofaunal species, a foraminiferan and an opheliid polychaete, which inhabit the surface or sub-surface of sediment and feed on phytodetritus, responded with a rapid increase in abundance to a pulse of organic input in summer 1996. The macrofaunal polychaetes showed a lagged response to the same event by slowly increasing in density. Other components of the sediment community, that can live deeper in the sediment, moved down the sediment column, in response to 1) the impoverishment and bioturbation of the surface layer, and 2) the downward mixing of organic matter in the sediment by larger organisms. In this study, different temporal patterns were demonstrated for the first time in different size classes of the sediment community, and in the biological and environmental parameters that were studied simultaneously.

Community structure and spatial heterogeneity of the deep-sea macrofauna at three contrasting stations in the tropical northeast Atlantic

A study of macrofauna community structure and spatial patterns was undertaken at three deep-sea stations during three EUMELI cruises in the tropical northeast Atlantic Ocean. The benthic response to contrasting regimes of organic carbon supply at the eutrophic (E), mesotrophic (M) and oligotrophic (O) stations (1700 m, 3 100 m and 4700 m depth, respectively) was evaluated through qualitative and quantitative analysis of the composition and structure of benthic macrofauna (> 250 μm) and discussed with regard to the biological and physical conditions. The mean densities of the total macrofauna, dominated by the Polychaeta, Tanaidacea, Isopoda and Bivalvia, decreased with increasing depth from 5403 ind. m−2 at station E to 231.5 ind. m−2 at station O. From the 16 taxonomic groups represented at the E and M sites, only eight could be sampled at the O site. The density gradient can be related to the decreasing surface production, food supply and hydrographic conditions between the three stations. The comparison of the high densities encountered at station E with other studies underlines the particular feature of this station subjected to intense upwelling activity resulting in high organic carbon input. The patchy distribution of the macrofauna at stations E and M suggests that both physical and biologically-mediated disturbances create environmental heterogeneity favouring the aggregation of organisms. This process occurs at different observation scales. At a large scale, bottom current and upwelling activity induce high densities and faunal aggregations, displaying a degree of density-dependence. At the local scale, the complexity of the food web induces biologically-mediated disturbances, and the activity of major deposit-feeding taxa, like polychaetes, create sediment microhabitats favouring patchy distribution. Faunal patch sizes are variable among the taxa considered. Most are distributed in patches less than 1 m z. Our work contributes to the understanding of how the deep benthic communities are structured, particularly under the influence of environmental conditions in tropical latitudes.

Interpretation of temperature measurements from the Kaiko-Nankai cruise: Modeling of fluid flow in clam colonies

During the Kaiko-Nankai detailed submersible survey, numerous measurements of the temperature gradient inside the sediment were performed on the deepest active zone of fluid venting, which is situated on the anticline related to the frontal thrust, using the Ifremer T-Naut temperature probe operated from the submersibleNautile. We thus obtained the temperature structure below different types of clam colonies associated with fluid venting. We used the finite element method to model the thermal structure and fluid flow pattern of these vents and to determine the velocity of upward fluid flow through the colonies. On a biological basis, four types of clam colonies are defined. Each biological type has distinctive thermal characteristics and corresponds to a particular fluid flow pattern. Darcian flow velocity in the most active type of colony (type A) is of the order of 100 m/a. The total amount of fluid flowing through colonies in the studied area is estimated to be 200 m3 a−1 per metre width of subduction zone. Most of the flow is vented through type A colonies. This value is more than one order of magnitude too high to be compatible with the amount of water available from steady-state compaction of sediments in the whole wedge. Thermal arguments suggest that downwelling of seawater occurs around type A colonies and that seawater is then mixed with upcoming fluids at a depth of 1 or 2 metres. Furthermore, finite element modeling shows that a salinity difference of a few parts per mil between the upcoming fluids and seawater is sufficient to drive convection around the colonies. As water samples from a few vents indicate that the fluid source should actually be significantly less saline than seawater, we propose that the very high fluid flows measured are a consequence of the dilution of the fluid of deep origin with seawater by a factor of 5 to 10.