Karine Olu

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.

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.

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.

Submersible study of mud volcanoes seaward of the Barbados accretionary wedge: sedimentology, structure and rheology

Abstract In 1992, the Nautile went to a mud volcano field located east of the Barbados accretionary wedge near 13 ° 50N. Using nannofossil analysis on cores, we determined the sedimentation rate, and provided a new estimation of the age of the mud volcanoes (750,000 years for the oldest one). Six structures have been explored with the submersible Nautile, and manifestations of fluid venting (chimneys, carbonate cementation and chemosynthetic communities) were observed on all. Sedimentological analysis identifies two sources of diapiric mud. Most mud volcanoes expel mud containing Late Miocene to Quaternary faunae that have the same composition as sediments drilled above the Barbados wedge decollement. One volcano also contains older Oligocene taxa, with a mud composition corresponding to the sedimentary sequence below the decollement. We use diving observations to map the fine-scale morphology, the distribution of chemosynthetic fauna and define two end-member types of structures: mud-pies (flat topped mud volcanoes) and conical mounds. Mud-pies (Atalante and Cyclops) are characterised by the presence of a lake of highporosity mud (70% to 75%) in their central parts. Chemosynthetic benthic communities ( Calyptogena colonies and sponge bushes) are concentrated in the outer parts. Contrasting morphologies of the two mud-pies indicate different stages of activity: Cyclops is growing whereas Atalante is collapsing. Expulsion of water and methane occurs mostly through the mud lake and may be stronger during the collapse phase. On conical mounds there are no mud lakes, fluid venting concentrates near the summit and occurs through carbonate cemented chimneys which form within the sediment. Viscosity measurements have been carried out on mud samples from the two mud-pies and one conical mound. All mud samples have a plastic fluid behaviour, the plastic threshold decreases with porosity, and thixotropy is observed for a porosity of more than 70%. An analogue experiment shows that for this thixotropic mud, shearing in the feeding conduit liquefies the mud which then spreads to form a mud-pie. Conical mounds form when the mud remains plastic. We show that the dissociation of methane hydrate is the cause of the high porosity in mud-pies and confirm that these structures are a consequence of large-scale dissociation of methane hydrate at the base of its stability field. Dissociation of hydrates before and during ascent is only slightly contributing to the pore fluid in conical mounds, but solid hydrates still present in the mud may contribute to its buoyancy.

Biogeography and Potential Exchanges Among the Atlantic Equatorial Belt Cold-Seep Faunas

Like hydrothermal vents along oceanic ridges, cold seeps are patchy and isolated ecosystems along continental margins, extending from bathyal to abyssal depths. The Atlantic Equatorial Belt (AEB), from the Gulf of Mexico to the Gulf of Guinea, was one focus of the Census of Marine Life ChEss (Chemosynthetic Ecosystems) program to study biogeography of seep and vent fauna. We present a review and analysis of collections from five seep regions along the AEB: the Gulf of Mexico where extensive faunal sampling has been conducted from 400 to 3300m, the Barbados accretionary prism, the Blake ridge diapir, and in the Eastern Atlantic from the Congo and Gabon margins and the recently explored Nigeria margin. Of the 72 taxa identified at the species level, a total of 9 species or species complexes are identified as amphi-Atlantic. Similarity analyses based on both Bray Curtis and Hellinger distances among 9 faunal collections, and principal component analysis based on presence/absence of megafauna species at these sites, suggest that within the AEB seep megafauna community structure is influenced primarily by depth rather than by geographic distance. Depth segregation is observed between 1000 and 2000m, with the middle slope sites either grouped with those deeper than 2000m or with the shallower sites. The highest level of community similarity was found between the seeps of the Florida escarpment and Congo margin. In the western Atlantic, the highest degree of similarity is observed between the shallowest sites of the Barbados prism and of the Louisiana slope. The high number of amphi-atlantic cold-seep species that do not cluster according to biogeographic regions, and the importance of depth in structuring AEB cold-seep communities are the major conclusions of this study. The hydrothermal vent sites along the Mid Atlantic Ridge (MAR) did not appear as “stepping stones” for dispersal of the AEB seep fauna, however, the south MAR and off axis regions should be further explored to more fully test this hypothesis.

Large Vesicomyidae (Mollusca: Bivalvia) from cold seeps in the Gulf of Guinea off the coasts of Gabon, Congo and northern Angola

Two new genera and three new species of large Vesicomyidae are described from cold-seep sites on pockmarks and other sulfide-rich environments in the Gulf of Guinea (tropical east Atlantic) off Gabon, Congo (Brazzaville) and northern Angola, from 500 to 4000 m depth: “Calyptogena” (s.l.) regab n. sp., Wareniconcha (n.g.) guineensis (Thiele and Jaeckel 1931), Elenaconcha guiness n.g. n. sp., and Isorropodon atalantae n. sp. For two other species already taken by the R/V Valdivia in 1898, Calyptogena valdiviae (Thiele and Jaeckel 1931) and Isorropodon striatum (Thiele and Jaeckel 1931) new localities were discovered, and the species are rediscussed. E. guiness n.g. n.sp. is also recorded from off Banc d’Arguin, Mauritania, collected by commercial fishing vessels. The vesicomyid species here treated were encountered in different depth ranges along the Gabon–Congo–Angola margin, between 500 and 4000 m depth, and it was found that, in comparison with the dredge samples taken by the Valdivia expedition off southern Cameroon and off Rio de Oro (both at 2500 m), the same species occur in other depth ranges, in some cases with a vertical difference of more than 1000 m. .That means that the species are not confined to a given depth thought being typical for them and that the characteristics of the biotope are likely to play a major role in the distribution of the vesicomyids associated to cold seeps or other reduced environments along the West African margin.

Gigantism in Mytilidae. A new Bathymodiolus from cold seep areas on the Barbados accretionary Prism

Bathymodiolus boomerang n. sp., a very large mussel, is described from deep cold seeps located on a continental margin on the southern end of the Barbados accretionary Prism in the tropical western Atlantic. The exceptional gigantism of this species, which makes it the largest mussel presently known on earth, is related to its life history in a muddy biotope with abundance of nutrients via symbiotic bacteria and a presumed longevity due to adaptation to fluid flow variability.

Phylogeny and Diversification Patterns among Vesicomyid Bivalves

Vesicomyid bivalves are among the most abundant and diverse symbiotic taxa in chemosynthetic-based ecosystems: more than 100 different vesicomyid species have been described so far. In the present study, we investigated the phylogenetic positioning of recently described vesicomyid species from the Gulf of Guinea and their western Atlantic and Pacific counterparts using mitochondrial DNA sequence data. The maximum-likelihood (ML) tree provided limited support for the recent taxonomic revision of vesicomyids based on morphological criteria; nevertheless, most of the newly sequenced specimens did not cluster with their morphological conspecifics. Moreover, the observed lack of geographic clustering suggests the occurrence of independent radiations followed by worldwide dispersal. Ancestral character state reconstruction showed a significant correlation between the characters “depth” and “habitat” and the reconstructed ML phylogeny suggesting possible recurrent events of ‘stepwise speciation’ from shallow to deep waters in different ocean basins. This is consistent with genus or species bathymetric segregation observed from recent taxonomic studies. Altogether, our results highlight the need for ongoing re-evaluation of the morphological characters used to identify vesicomyid bivalves.

High connectivity across the fragmented chemosynthetic ecosystems of the deep Atlantic Equatorial Belt: efficient dispersal mechanisms or questionable endemism?

Chemosynthetic ecosystems are distributed worldwide in fragmented habitats harbouring seemingly highly specialized communities. Yet, shared taxa have been reported from highly distant chemosynthetic communities. These habitats are distributed in distinct biogeographical regions, one of these being the so‐called Atlantic Equatorial Belt (AEB). Here, we combined genetic data (COI) from several taxa to assess the possible existence of cryptic or synonymous species and to detect the possible occurrence of contemporary gene flow among populations of chemosynthetic species located on both sides of the Atlantic. Several Evolutionary Significant Units (ESUs) of Alvinocarididae shrimp and Vesicomyidae bivalves were found to be shared across seeps of the AEB. Some were also common to hydrothermal vent communities of the Mid‐Atlantic Ridge (MAR), encompassing taxa morphologically described as distinct species or even genera. The hypothesis of current or very recent large‐scale gene flow among seeps and vents was supported by microsatellite analysis of the shrimp species Alvinocaris muricola/Alvinocaris markensis across the AEB and MAR. Two nonmutually exclusive hypotheses may explain these findings. The dispersion of larvae or adults following strong deep‐sea currents, possibly combined with biochemical cues influencing the duration of larval development and timing of metamorphosis, may result in large‐scale effective migration among distant spots scattered on the oceanic seafloor. Alternatively, these results may arise from the prevailing lack of knowledge on the ocean seabed, apart from emblematic ecosystems (chemosynthetic ecosystems, coral reefs or seamounts), where the widespread classification of endemism associated with many chemosynthetic taxa might hide wider distributions in overlooked parts of the deep sea.