Daniel Desbruyères

A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: dispersal vs. environmental controls

Until 1985, seven vent fields were described from the Mid-Atlantic Ridge (MAR). An eighth field, Mount Saldanha (36° N), discovered in 1998, showed unusual geological and biological settings. Vent sites on the MAR exhibit varied environmental conditions, resulting from depth variation of the axis and associated physical parameters, and different source rocks. These could be considered as first order (i.e. most dominant) factors affecting the composition of vent communities on the MAR, in contrast to the East Pacific Rise (EPR) where geographical isolation appears to be a major determinant of faunal differences. In this paper, the geological setting and vent fluid composition of the fields are considered together with their community composition to tentatively ascertain the order of a hierarchy between dispersal and environmental control. The deepest fields (>3000 m) are rather stable systems. The shallower fields, especially Rainbow and Menez Gwen, present some evidence of instability in time and space. The variability in fluid composition is related to phase separation processes (boiling/distillation of subsurface vent fluids) and to the nature of the basement rocks. Depending on depth, phase separation produces gas-enriched and metal-depleted fluids (Menez Gwen, Lucky Strike) or metal-enriched brines (Rainbow, TAG). In addition, high methane content characterises the fluids formed in ultramafic rocks (Rainbow, Logatchev) compared to basaltic rocks. The discrepancy in mineral particulate fluxes at Lucky Strike and Menez Gwen, on one hand, and TAG and Rainbow, on the other, is correlated to the predominance of the vapour or brine phase. The semi-quantitative description of the faunal composition of the different vent fields displays a continuum from Rimicaris-dominated to Bathymodiolus-dominated assemblages. Rather than geographic or bathymetric zonation, this gradation appears to be related to the metal content of the fluids. In addition, the penetration of non vent species into the vent environment increases with decreasing hydrostatic pressure and/or metal content in the fluids. Similarity analysis between vent communities shows that similarity is strongest between Menez Gwen and Lucky Strike (the shallowest fields), less significant between these sites and Rainbow, and weakest for Snake Pit. The inverse relationship between filter feeding organisms and metal concentration in vent fluids could result from a hindrance of mussel bed development by particulate or toxic metal fluxes, and has to be further investigated. Conversely, high metal and particulate content would less affect the more mobile Rimicaris populations. Considering specific similarities of endemic fauna between the four best known hydrothermal vents, the distance between vent fields appears to be a first order parameter. Nevertheless, within the proximity of the Azores Triple Junction area, and in the absence of geographical discontinuity, the similarity between fields stays rather low suggesting faunal islands that have distinct composition and habitat requirements.

Biology and ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal dweller of an extreme deep-sea environment: A synthesis of current knowledge and recent developments

Abstract Alvinella pompejana, the “Pompeii worm” lives on active hydrothermal edifices at deep-sea vents of the East Pacific Rise. The physical and chemical patterns of its microhabitat were determined from temperature probe measurements, temperature time series, and on-board and shore-based chemical analyses based on discrete sampling (pH, H2S, CO2, CH4, S2O2-3, Ca, Mg, Cu, Cd, Zn). The microhabitat is characterised by high temporal and microscale spatial variability, with temperature values in the range of 20°–45°C at the immediate periphery of tubes but reaching higher, still undetermined, values inside the tubes. The difference observed between in vitro temperature limits for the stability of biomolecules and metabolic rates, and suggested in situ conditions seems to indicate a significant protective role of biological interfaces (tubes and cuticle). Temporal instability possibly also plays an important role in the ability for these worms to colonise such an extreme habitat. The functional role of dominant epibiotic bacteria is discussed in the light of recent biochemical and molecular data: the tube-worm–bacteria system can be considered as a symbiotic entity where carbon is probably metabolised and recycled. Sulphide detoxification occurs by oxidation at the gill level and possibly at the intracellular haemoglobin level. Heavy metals, ingested or absorbed, are trapped in spherocrystals and bound to metallothionein-like proteins. Anatomical, physiological and molecular adaptations to hypoxia allow the worm to successfully colonise the chimneys. A. pompejana lives in an ephemeral environment and must reproduce and disperse accordingly. It is a gonochoric species that displays a pseucopulatory behaviour allowing transfer of sperm to female spermathecae, thus avoiding dispersion of the gametes. The size of the oocytes suggests a lecithotrophic or benthic development. The population size structure is polymodal, indicating discontinuous recruitment. Population genetics data indicate the occurrence of a microscale level of population differentiation that does not increase with increasing geographical distances, thus suggesting the occurrence of a metapopulation-like system and/or the possibility that enzyme loci evolve under stabilising selective driving forces inherent to the vents’ highly variable conditions.

Deep-sea hydrothermal communities in Southwestern Pacific back-arc basins (the North Fiji and Lau Basins): Composition, microdistribution and food web

Abstract During the year 1989, two diving cruises of the French deep-sea submersible Nautile were devoted to the study of hydrothermal vent biology in spreading centers of two Southwestern Pacific back-arc basins (Lau Basin and North Fiji Basin). In both cases, two major active sites were visited: White Lady and Mussel Valley in the North Fiji Basin and Hine Hina and Vai Lili in Lau Basin. The faunal associations clustered around active vents are dominated by two species of snails Ifremeria nautilei and Alviniconcha hessleri and one or two species of mytilids belonging to Bathymodiolus. These species are associated with chemoautolithotrophic bacteria in intracellular symbiosis as detected by the activity of the Calvin-Benson cycle diagnostic enzyme RuBPcase. Pedunculate and sessile barnacles dominated the outer rim of the site and are analogs of the fiter-feeding serpulids living in the EPR sites. The hot extremes of the sites are poorly or not colonized by alvinellids or other taxa. In the Lau Basin, “cold seep” sites are found at the periphery of active hot or warm ventsand are dominated by vestimentiferans and pogonophorans. No major differences were seen between associations of the two back-arc basins at the generic level with the exeption of the abundance of synaptid holothurians associated with Bathymodiolus in side the “Mussel Valley” site.

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Nutritional relations of deep-sea hydrothermal fields at the Mid-Atlantic Ridge: a stable isotope approach

Nutritional relations among invertebrates from the hydrothermal vent fields at the Mid Atlantic Ridge (MAR) were studied via the carbon and nitrogen stable isotope approach. A large number of specimens of different vent species from different MAR vent fields were analysed, providing a general picture of the community structure. The isotopic composition at each vent field presents the same general trend. There is an obvious dichotomyof the trophic structure, with the mussels being significantlydepleted in 13 C and shrimps being significantlyenriched in 13 C. MAR and Pacific vent fields present the same picture, despite a different species composition. Primaryconsumers are divided into main groups according to their d 13 C signature: >� 15 (shrimps) and o� 20% (mussels). Vent predators are tightlylinked to one or the other group, but a mixed diet cannot be excluded. Bathyal species are top predators, making incursions into the vent fields to profit from the large biomass. Taking into account the above associations, a descriptive trophic model was elaborated. At the base of the food chain the chemolithotrophic bacteria predominate. Four trophic levels were then distinguished: primaryconsumers, feeding onlyon bacteria; mixotrophs feeding on bacteria and small invertebrates; vent predators feeding onlyon small invertebrates; and finallytop predators that are mainlyconstituted bydeep-sea fauna. r 2002 Elsevier Science Ltd. All rights reserved.

Phylogenetic characterization of the bacterial assemblage associated with mucous secretions of the hydrothermal vent polychaete Paralvinella palmiformis.

As part of an ongoing examination of microbial diversity associated with hydrothermal vent polychaetes of the family Alvinellidae, we undertook a culture-independent molecular analysis of the bacterial assemblage associated with mucous secretions of the Northeastern Pacific vent polychaete Paralvinella palmiformis. Using a molecular 16S rDNA-based phylogenetic approach, clone libraries were constructed from two samples collected from active sulfide edifices in two hydrothermal vent fields. In both cases, clone libraries were largely dominated by epsilon-Proteobacteria. Phylotypes belonging to the Cytophaga-Flavobacteria and to the Verrucomicrobia were also largely represented within the libraries. The remaining sequences were related to the taxonomic groups Fusobacteria, Green non-sulfur bacteria, Firmicutes, gamma- and delta-Proteobacteria. To our knowledge, this is the first report of the presence of Verrucomicrobia, Fusobacteria and green non-sulfur bacteria on hydrothermal edifices. The potential functions of the detected bacteria are discussed in terms of productivity, recycling of organic matter and detoxification within the P. palmiformis microhabitat.

Time-series of temperature from three deep-sea hydrothermal vent sites

Abstract Temperature time-series have been recorded with THYDRO, a new multi-probe temperature recorder, in three different hydrothermal vent sites: 13°N on the East Pacific Rise (EPR), the Lau Back-Arc Basin, and the North-Fiji Basin. The probes were placed on clumps of living animals (molluscs and polychaetes) for periods of up to 47 h, in zones where hydrothermal fluids mix with seawater. Spatial variability of temperature was often very important, thus demonstrating the necessity of a thorough study of the hydrothermal microenvironment. Temporal variability was analysed through standard spectral analysis methods. Several periodicities are superimposed, ranging from tens of seconds to ten of hours. The origin of these periods is discussed, and although the tidal cycle seems to be of greater importance in the driving forces of these variations, other periods exist that may be generated by the turbulent mixing occurring in this environment, and/or by variations in the hydrothermal fluid discharge. Aperiodic phenomena were also noted and, therefore, random processes should not be neglected. Consequences of the encountered variabilities on the vent fauna are also discussed, especially for Alvinella species that live in the studied zone and must have developed adaptive responses.

Evidence of a recent magma dike intrusion at the slow spreading Lucky Strike segment, Mid‐Atlantic Ridge

[1] Mid-ocean ridge volcanic activity is the fundamental process for creation of ocean crust, yet the dynamics of magma emplacement along the slow spreading Mid-Atlantic Ridge (MAR) are largely unknown. We present acoustical, seismological, and biological evidence of a magmatic dike intrusion at the Lucky Strike segment, the first detected from the deeper sections (>1500 m) of the MAR. The dike caused the largest teleseismic earthquake swarm recorded at Lucky Strike in >20 years of seismic monitoring, and one of the largest ever recorded on the northern MAR. Hydrophone records indicate that the rate of earthquake activity decays in a nontectonic manner and that the onset of the swarm was accompanied by 30 min of broadband (>3 Hz) intrusion tremor, suggesting a volcanic origin. Two submersible investigations of high-temperature vents located at the summit of Lucky Strike Seamount 3 months and 1 year after the swarm showed a significant increase in microbial activity and diffuse venting. This magmatic episode may represent one form of volcanism along the MAR, where highly focused pockets of magma are intruded sporadically into the shallow ocean crust beneath long-lived, discrete volcanic structures recharging preexisting seafloor hydrothermal vents and ecosystems. INDEX TERMS: 3035 Marine Geology and Geophysics: Midocean ridge processes; 7280 Seismology: Volcano seismology (8419); 8149 Tectonophysics: Planetary tectonics (5475); 4259 Oceanography: General: Ocean acoustics; 9325 Information Related to Geographic Region: Atlantic Ocean; KEYWORDS: Mid-Atlantic Ridge, earthquake, hydroacoustic

Biogeography Revisited with Network Theory: Retracing the History of Hydrothermal Vent Communities

Defining biogeographic provinces to understand the history and evolution of communities associated with a given kind of ecosystem is challenging and usually requires a priori assumptions to be made. We applied network theory, a holistic and exploratory method, to the most complete database of faunal distribution available on oceanic hydrothermal vents, environments which support fragmented and unstable ecosystems, to infer the processes driving their worldwide biogeography. Besides the identification of robust provinces, the network topology allowed us to identify preferential pathways that had hitherto been overlooked. These pathways are consistent with the previously proposed hypothesis of a role of plate tectonics in the biogeographical history of hydrothermal vent communities. A possible ancestral position of the Western Pacific is also suggested for the first time. Finally, this work provides an innovative example of the potential of network tools to unravel the biogeographic history of faunal assemblages and to supply comprehensive information for the conservation and management of biodiversity.

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.