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Volume 22 Issue 01

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Volume 22, No. 1
Pages 110 - 127


Biodiversity of Cold Seep Ecosystems Along the European Margins

Ann Vanreusel Ann C. AndersenAntje Boetius Marina R. CunhaCarole DeckerAna HilarioKonstantinos A. KormasLoïs Maignien Karine OluMaria Pachiadaki Benedicte RittClara Rodrigues Jozée SarrazinPaul Tyler Saskia Van GaeverHeleen Vanneste
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Article 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 mud volcano and many pockmarks, (2) the Gulf of Cádiz, and (3) the eastern Mediterranean with its hundreds of mud volcanoes and brine pool 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 ecosystem processes and associated biodiversity at different spatial scales, illustrating the “hotspot” nature of these deep water systems.


Vanreusel, A., A.C. Andersen, A. Boetius, D. Connelly, M.R. Cunha, C. Decker, A. Hilario, K.A. Kormas, L. Maignien, K. Olu, M. Pachiadaki, B. Ritt, C. Rodrigues, J. Sarrazin, P. Tyler, S. Van Gaever, and H. Vanneste. 2009. Biodiversity of cold seep ecosystems along the European margins. Oceanography 22(1):110–127, https://doi.org/10.5670/oceanog.2009.12.


Akhmetzhanov, A.M., M. Ivanov, N.H. Kenyon, and A. Mazzini. 2007. Deep-water cold seeps, sedimentary environments and ecosystems of the Black and Tyrrhenian Sea and the Gulf of Cádiz. Preliminary results of investigations during the TTR-15 cruise, RV Professor Logachev, June–August 2005, Intergovernmental Oceanographic Commission, Paris, 99 pp. plus appendices.

Aloisi, G., I. Bouloubassi, S.K. Heijs, R.D. Pancost, C. Pierre, J.S. Sinninghe Damste, J.C. Gottschal, L.J. Forney, and J.-M. Rouchy. 2002. CH4-consuming microorganisms and the formation of carbonate crusts at cold seeps. Earth and Planetary Science Letters 203:195–203.

Barry, J.P., R.E. Kochevar, and C.H. Baxter. 1997. The influence of pore-water chemistry and physiology on the distribution of vesicomyid clams at cold seeps in Monterey Bay: Implications for patterns of chemosynthetic community organization. Limnology and Oceanography 42:318–328.

Bergquist, D.C., C. Fleckenstein, J. Knisel, B. Begley., I.R. MacDonald, and C.R. Fisher. 2005. Variations in seep mussel bed communities along physical and chemical environmental gradients. Marine Ecology Progress Series 293:99–108.

Bergquist, D.C., I.A. Urcuyo, and C.R. Fisher. 2002. Establishment and persistence of seep vestimentiferan aggregations from the upper Louisiana slope of the Gulf of Mexico. Marine Ecology Progress Series 241:89–98.

Bergquist, D.C., T. Ward, E.E. Cordes, T. McNelis, S. Howlett, R. Koisoff, S. Hourdez, R. Carney, and C.R. Fisher. 2003. Community structure of vestimentiferan-generated habitat islands from Gulf of Mexico cold seeps. Journal of Experimental Marine Biology and Ecology 289:197–222.

Boetius, A., K. Ravenschlag, C. Schubert, D. Rickert, F. Widdel, A. Gieseke, R. Amann, B.B. Jørgensen, U. Witte, and O. Pfannkuche. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626.

Charlou, J.L., J.P. Donval, T. Zitter, N. Roy, P. Jean-Baptiste, J.-P. Foucher, J. Woodside, and The MEDINAUT Scientific Party. 2003. Evidence of methane venting and geochemistry of brines on mud volcanoes of the eastern Mediterranean Sea. Deep-Sea Research Part I 50:941–958.

Cordes, E.E., S.L. Carney, S. Hourdez, R.S. Carney, J.M. Brooks, and C.R. Fisher. 2007. Cold seeps of the deep Gulf of Mexico: Community structure and biogeographic comparisons to Atlantic equatorial belt seep communities. Deep-Sea Research Part I 54:637–653.

de Beer, D., E. Sauter, H. Niemann, U. Witte, and A. Boetius. 2006. In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano. Limnology and Oceanography 51:1,315–1,331.

Duperron, S., C. Bergin, F. Zielinski, A. Blazejak, A. Pernthaler, Z.P. McKiness, E. DeChaine, C.M. Cavanaugh, and N. Dubilier. 2006. A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environmental Microbiology 8:1,441–1,447.

Duperron, S., A. Fiala-Medioni, J.C. Caprais, K. Olu, and M. Sibuet. 2007. Evidence for chemoautotrophic symbiosis in a Mediterranean cold seep clam (Bivalvia: Lucinidae): comparative sequence analysis of bacterial 16S rRNA, APS reductase and RubisCO genes. FEMS Microbiology Ecology 59:64–70.

Dupré, S., J. Woodside, J.-P. Foucher, G. de Lange, J. Mascle, A. Boetius, V. Mastalerz, A. Stadnitskaia, H. Ondreas, C. Huguen, and others. 2007. Seafloor geological studies above active gas chimneys off Egypt (Central Nile Deep Sea Fan). Deep-Sea Research Part I 54:1,146–1,172.

Domack, E., S. Ishman, A. Leventer, S. Sylva, V. Willmott, and B. Huber. 2005. A chemotrophic ecosystem found beneath Antarctic ice shelf. Eos, Transactions, American Geophysical Union 86:269–276.

Gebruk, A.V., E.M. Krylova, A.Y. Lein, G.M. Vinogradov, E. Anderson, N.V. Pimenov, G.A. Cherkashev, and K. Crane. 2003. Methane seep community of the Håkon Mosby mud volcano (the Norwegian Sea): Composition and trophic aspects. Sarsia 88:394–403.

Génio, L., S.B. Johnson, R.C. Vrijenhoek, M.R. Cunha, P.A. Tyler, S. Kiel, and C.T.S. Little. 2008. New record of “Bathymodiolusmauritanicus Cosel 2002 from the Gulf of Cádiz (NE Atlantic) mud volcanoes. Journal of Shellfish Research 27:53–61.

Haeckel, M., C. Berndt, V. Liebetrau, P. Linke, A. Reitzi, J. Schonfield, and H. Vanneste. 2007. Genesis and rates of fluid flow at the Mercator mud volcano, Gulf of Cádiz. Geochimica et Cosmochimica Acta 71:A367.

Heijs, S.K., G. Aloisi, I. Bouloubassi, R.D. Pancost, C. Pierre, J.S. Sinninghe-Damsté, J.C. Gottschal, J.D. van Elsas, and L.J. Forney. 2006. Microbial community structure in three deep-sea carbonate crusts. Microbial Ecology 52:451–462.

Heijs, S.K., R.R. Haese, P.W. van der Wielen, L.J. Forney, and J.D. van Elsas. 2007. Use of 16S rRNA gene based clone libraries to assess microbial communities potentially involved in anaerobic methane oxidation in a Mediterranean cold seep. Microbial Ecology 53:384–398.

Heijs, S.K., A.M. Laverman, L.J. Forney, P.R. Hardoim, and J.D. van Elsas. 2008. Comparison of deep-sea sediment microbial communities in the eastern Mediterranean. FEMS Microbiology Ecology 63:362–377.

Henry, P., J.P. Foucher, X. Le Pichon, M. Sibuet, K. Kobayashi, P. Tarits, N. Chamot-Rooke, T. Furuta, and P. Shultheiss. 1992. Interpretation of temperature measurements from the Kaiko-Nankai Cruise: Modeling of fluid flow in clam colonies. Earth and Planetary Science Letters 109:355–371.

Hensen, C., M. Nuzzo, E. Hornibrook, L.M. Pinheiro, B. Bock, V.H. Magalhaes, and W. Bruckmann. 2007. Sources of mud volcano fluids in the Gulf of Cádiz: Indications for hydrothermal imprint. Geochimica et Cosmochimica Acta 71:1,232–1,248.

Hilário, A., and M.R. Cunha. 2008. On some frenulate species (Annelida: Polychaeta: Siboglinidae) from mud volcanoes in the Gulf of Cádiz (Northeast Atlantic). Scientia Marina 72:361–371.

Hovland, M., and H. Svensen. 2006. Submarine pingoes: Indicators of shallow gas hydrates in a pockmark at Nyegga, Norwegian Sea. Marine Geology 228:15–23.

Hovland, M., H. Svensen, C.F. Forsberg, H. Johansen, C. Fichler, J.H. Fosså, F. Jonsson, and H. Rueslåtten. 2005. Complex pockmarks with carbonate-ridges off mid-Norway: Products of sediment degassing. Marine Geology 218:191–206.

Jerosch, K., M. Schlüter, J.-P. Foucher, A.G. Allais, M. Klages, and C. Edy. 2007. Spatial distribution of mud flows, chemoautotrophic communities, and biogeochemical habitats at Håkon Mosby mud volcano. Marine Geology 243:1–17.

Jorgensen, B.B., and A. Boetius. 2007. Feast and famine–Microbial life in the deep-sea bed. Nature Microbiology Reviews 5:770–781.

Julian, D., F. Gaill, E. Wood, A.J. Arp, and C.R. Fisher. 1999. Roots as a site of hydrogen sulphide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia sp. Journal of Experimental Biology 202:2,245–2,257.

Juniper, S.K., and M. Sibuet. 1987. Cold seep benthic communities in Japan subduction zones: Spatial organization, trophic strategies and evidence for temporal evolution. Marine Ecology Progress Series 40:115–126.

Kenyon, N.H., M.K. Ivanov, A.M. Akhmetzhanov, and G.G. Akhmanov. 2000. Multidisciplinary study of geological processes on the North East Atlantic and western Mediterranean margins. Preliminary results of geological and geophysical investigations during the TTR-9 cruise of R/V Professor Logachev, June–July 1999, Intergovernmental Oceanographic Commission, Paris, 102 pp. plus appendices.

Kenyon, N.H., M.K. Ivanov, A.M. Akhmetzhanov, and G.G. Akhmanov. 2003. Interdisciplinary geoscience research on the North East Atlantic margin, Mediterranean Sea and Mid-Atlantic Ridge. Preliminary results of investigations during the TTR-12 cruise of RV Professor Logachev, June–August 2002, Intergovernmental Oceanographic Commission, Paris, 112 pp. plus appendices.

Kenyon, N.H., M. Ivanov, A.M., Akhmetzhanov, and E.V. Kozlova. 2006. Interdisciplinary geoscience studies of the Gulf of Cádiz and western Mediterranean basins. Preliminary results of investigations during the TTR-14 cruise, RV Professor Logachev, July–September 2004, Intergovernmental Oceanographic Commission, Paris, 115 pp. plus appendices.

Knittel, K., A. Boetius, A. Lemke, H. Eilers, K. Lochte, O. Pfannkuche, P. Linke, and R. Amann. 2003. Activity, distribution, and diversity of sulfate reducers and other bacteria above gas hydrate (Cascadia Margin, OR). Geomicrobiology Journal 20:269–294.

Knittel, K., T. Lösekann, A. Boetius, R. Kort, and R. Amann. 2005. Diversity and distribution of methanotrophic archaea at cold seeps. Applied and Environmental Microbiology 71:467–479.

Kormas, K.A., A. Meziti, A. Dählmann, G.J. de Lange, and V. Lykousis. 2008. Characterization of methanogenic and prokaryotic assemblages based on mcrA and 16S rRNA gene diversity in sediments of the Kazan Mud Volcano (Mediterranean Sea). Geobiology 6:450–460.

Levin, L.A. 2005. Ecology of cold seep sediments: Interactions of fauna with flow, chemistry and microbes. Oceanography and Marine Biology–An Annual Review 43:1–46.

Levin, L.A., W. Ziebis, G.F. Mendoza, V.A. Growney, M.D. Tryon, K.M. Brown, C. Mahn, J.M. Gieskes, and A.E. Rathburn. 2003. Spatial heterogeneity of macrofauna at northern California methane seeps: Influence of sulfide concentration and fluid flow. Marine Ecology Progress Series 265:123–139.

Loncke, L., and J. Mascle. 2004. Mud volcanoes, gas chimneys, pockmarks and mounds in the Nile deep-sea fan (Eastern Mediterranean): Geophysical evidences. Marine and Petroleum Geology 21:669–689.

Lösekann, T., K. Knittel, T. Nadalig, B. Fuchs, H. Niemann, A. Boetius, and R. Amann. 2007. Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby mud volcano, Barents Sea. Applied and Environmental Microbiology 73:3,348–3,362.

Lösekann, T., A. Robador, H. Niemann, K. Knittel, A. Boetius, and N. Dubilier. 2008. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby mud volcano, Barents Sea). Environmental Microbiology 10(12):3,237–3,254, doi:10.1111/j.1462-2920.2008.01712.x.

MacDonald, I.R., G. Bohrmann, E. Escobar, F. Abegg, P. Blanchon, V. Blinova, W. Brückmann, M. Drews, A. Eisenhauer, X. Han, and others. 2004. Asphalt volcanism and chemosynthetic life in the Campeche Knolls, Gulf of Mexico. Science 304:999–1,002.

Mascle, J., C. Huguen, J. Benkhelil, N. Chamot-Rooke, E. Chaumillon, J.-P. Foucher, R. Griboulard, A. Kopf, G. Lamarche, A. Volkonskaia, and others. 1999. Images may show start of European-African plate collision. Eos, Transactions, American Geophysical Union 80:421.

Medialdea, T., R. Vegas, L. Somoza, J.T. Vázquez, A. Maldonado, V. Díaz-del-Río, A. Maestro, D. Córdoba, and M.C. Fernández-Puga. 2004. Structure and evolution of the “Olistostrome” complex of the Gibraltar Arc in the Gulf of Cádiz (eastern Central Atlantic): Evidence from two long seismic cross-sections. Marine Geology 209:173–198.

Milkov, A., P. Vogt, G. Cherkashev, G. Ginsburg, N. Chernova, and A. Andriashev. 1999. Sea-floor terrains of Haakon Mosby Mud Volcano as surveyed by deep-tow video and still photography. Geo-Marine Letters 19:38–47.

Niemann, H., J. Duarte, C. Hensen, E. Omoregie, V.H. Magalhães, M. Elvert, L. Pinheiro, A. Kopf, and A. Boetius. 2006a. Microbial methane turnover at mud volcanoes of the Gulf of Cádiz. Geochemica Cosmochemica Acta 70:5,336–5,335.

Niemann, H., T. Lösekann, D. de Beer, M. Elvert, T. Nadalig, K. Knittel, R. Amann, E.J. Sauter, M. Schlüter, M. Klages, and others. 2006b. Novel microbial communities of the Haakon Mosby mud volcano and their role as methane sink. Nature 443:854–858.

Olu, K., F. Lance, M. Sibuet, P. Henry, A. Fiala-Médioni, and A. Dinet. 1997. Cold seep communities as indicators of fluid expulsion patterns through mud volcanoes seaward of the Barbados accretionary prism. Deep-Sea Research Part II 44:811–841.

Olu-Le Roy, K., M. Sibuet, S. Gofas, A. Fiala-Médioni, J.-P. Foucher, and J. Woodside. 2004. Cold seep communities in the deep eastern Mediterranean Sea: Composition and spatial distribution on mud volcanoes. Deep-Sea Research Part I 51:1,915–1,936.

Omoregie, E.O., V. Mastalerz, G. de Lange, K.L. Straub, A. Kappler, H. Røy, A. Stadnitskaia, J.-P. Foucher, and A. Boetius. 2007. Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren mud volcano (Nile Deep Sea Fan, eastern Mediterranean). Applied Environmental Microbiology 74:3,198–3,215.

Paull, C.K., B. Hecker, R. Commeau, R.P. Freeman-lynde, C. Neumann, W.P. Corso, S. Golubic, J.E. Hook, E. Sikes, and J. Curray. 1984. Biological communities at the Florida Escarpment resemble hydrothermal vent taxa. Science 226:965–967.

Paull, C.K., W. Ussler III, W.S. Holbrook, T.M. Hill, R. Keaten, J. Mienert, H. Haflidason, J.E. Johnson, W.J. Winters, and T.D. Lorenson. 2008. Origin of pockmarks and chimney structure on flanks of the Storegga slide, offshore Norway. Geo-Marine Letters 28:43–51.

Preisler, A., D. de Beer, A. Lichtschlag, G. Larvik, A. Boetius, and B. Joergensen. 2007. Biological and chemical sulfide oxidation in a Beggiatoa inhabited sediment. ISME Journal 1:341–353.

Rodrigues, C.F., P.G. Oliver, and M.R. Cunha. 2008. Thyasiroidea (Mollusca: Bivalvia) from the mud volcanoes of the Gulf of Cádiz (North-east Atlantic). Zootaxa 1572:41–56.

Sahling, H., D. Rickert, R.W. Lee, P. Linke, and E. Suess. 2002. Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific. Marine Ecology Progress Series 231:121–138.

Sibuet, M., and K. Olu. 1998. Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Research Part II 45:517–567.

Sibuet, M., and K. Olu-Le Roy. 2002. Cold seep communities on continental margins: Structure and quantitative distribution relative to geological and fluid venting patterns. Pp. 235–251 in Ocean Margin Systems. G. Wefer, D. Billett, D. Hebbeln, B.B. Jørgensen, M. Schlüter, and T. Van Weering, eds, Springer-Verlag, Berlin Heidelberg.

Sloan, E.D. 1990. Natural-gas hydrate phase-equilibria and kinetics: Understanding the state-of-the-art. Revue de l’Institut Francais du Petrole 45:245–266.

Suess E., B. Carson, S.D. Ritger, J.C. Moore, L.D. Kulm, and G.R. Cochrane. 1985. Biological communities at vent sites along the subduction zone off Oregon. Pp. 475–484 in The Hydrothermal Vents of the Eastern Pacific: An Overview. M.L. Jones, ed., Bulletin of the Biological Society of Washington, volume 6.

Smirnov, R.V. 2000. Two new species of Pogonophora from the arctic mud volcano off northwestern Norway. Sarsia 85:141–150.

Somoza, L., V. Díaz-del-Río, R. León, M. Ivanov, M.C. Fernández-Puga, J.M. Gardner, F.J. Hernández-Molina, L.M. Pinheiro, J. Rodero, A. Lobato, and others. 2003. Seabed morphology and hydrocarbon seepage in the Gulf of Cádiz mud volcano area: Acoustic imagery, multibeam and ultra-high resolution seismic data. Marine Geology 195:153–176.

Stadnitskaia, A., M.K. Ivanov, V. Blinova, R. Kreulen, and T.C.E. Weering. 2006. Molecular and carbon isotopic variability of hydrocarbon gases from mud volcanoes in the Gulf of Cádiz, NE Atlantic. Marine and Petroleum Geology 23:281–296.

Tryon, M.D., and K.M. Brown. 2001. Complex flow patterns through Hydrate Ridge and their impact on seep biota. Geophysical Research Letters 28:2,863–2,866.

Van Aken, H.M. 2000. The hydrography of the middle-latitude Northeast Atlantic Ocean II: The intermediate water masses. Deep-Sea Research Part I 47:789–824.

Van Dover, C., P. Aharon, J.M. Bernhard, E. Caylor, M. Doerries, W. Flickinger, W. Gilhooly, S.K. Goffredi, K. Knick, S.A. Macko, and others. 2003. Blake Ridge methane seep: Characterization of a soft-sediment, chemosynthetically based ecosystem. Deep-Sea Research Part I 50:281–300.

Van Gaever, S., L. Moodley, D. de Beer, and A. Vanreusel. 2006. Meiobenthos at the Arctic Håkon Mosby mud volcano with a parental caring nematode thriving in sulphide-rich sediments. Marine Ecology Progress Series 321:143–155.

Van Gaever, S., K. Olu, S. Derycke, and A. Vanreusel. In press. Metazoan meiofaunal communities at cold seeps along the Norwegian margin: Influence of habitat heterogeneity and evidence for connection with shallow-water habitats. Deep-Sea Research Part I.

Vetriani, C., H.W. Jannasch, B.J. MacGregor, D.A. Stahl, and A.-L. Reysenbach. 1999. Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Applied and Environmental Microbiology 65:4,375–4,394.

Vogt, P.R., A. Cherkashev, G.D. Ginsburg, G.I. Ivanov, K. Crane, A.Y. Lein, E. Sundvor, N.V. Pimenov, and A.V. Egorov. 1997. Haakon Mosby mud volcano: A warm methane seep with seafloor hydrates and chemosynthesis-based ecosystem in late Quaternary Slide Valley, Bear Island Fan, Barents Sea passive margin. Eos, Transactions, American Geophysical Union 78:187–189.

Woodside, J.M., M.K. Ivanov, and A.F. Limonov. 1997. Neotectonics and fluid flow through the seafloor sediments in the Eastern Mediterranean and Black Seas. Part I: Eastern Mediterranean Sea. IOC Technical Series 48:1–128.

Woodside, J.M., M.K. Ivanov, A.F. Limonov, and Shipboard Scientists of the Anaxiprobe expeditions. 1998. Shallow gas and gas hydrates in the Anaximander Mountains region Eastern Mediterranean Sea. Pp. 177–193 in Gas hydrates: Relevance to World Margin Stability and Climate Change. J.-P. Henriet and J. Mienert, eds, Special Publication 137, Geological Society, London.

Zitter, T.A.C., C. Huguen, and J.M. Woodside. 2005. Geology of mud volcanoes in the eastern Mediterranean from combined sidescan sonar and submersible surveys. Deep-Sea Research Part I 52:457–475.

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