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Volume 25 Issue 01

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Volume 25, No. 1
Pages 62 - 77

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Links from Mantle to Microbe at the Lau Integrated Study Site: Insights from a Back-Arc Spreading Center

By Margaret K. Tivey , Erin Becker , Roxanne Beinart, Charles R. Fisher, Peter R. Girguis , Charles H. Langmuir, Peter J. Michael , and Anna-Louise Reysenbach  
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Article Abstract

The Lau Integrated Study Site (ISS) has provided unique opportunities for study of ridge processes because of its back-arc setting in the southwestern Pacific. Its location allows study of a biogeographical province distinct from those of eastern Pacific and mid-Atlantic ridges, and crustal compositions along the ridge lie outside the range of mid-ocean ridge crustal compositions. The Lau ISS is located above a subduction zone, at an oblique angle. The underlying mantle receives water and other elements derived from the downgoing lithospheric slab, with an increase in slab influence from north to south. Water lowers the mantle melting temperature and leads to greater melt production where the water flux is greater, and to distinctive regional-scale gradients along the ridge. There are deeper faulted axial valleys with basaltic volcanism in the north and inflated axial highs with andesites in the south. Differences in igneous rock composition and release of magmatic volatiles affect compositions of vent fluids and deposits. Differences in vent fluid compositions and small-scale diffuse-flow regimes correlate with regional-scale patterns in microbial and megafaunal distributions. The interdisciplinary research effort at the Lau ISS has successfully identified linkages between subsurface processes and deep-sea biological communities, from mantle to microbe to megafauna.

Citation

Tivey, M.K., E. Becker, R. Beinart, C.R. Fisher, P.R. Girguis, C.H. Langmuir, P.J. Michael, and A.-L. Reysenbach. 2012. Links from mantle to microbe at the Lau Integrated Study Site: Insights from a back-arc spreading center. Oceanography 25(1):62–77, https://doi.org/10.5670/oceanog.2012.04.

References

Bachraty, C., P. Legendre, and D. Desbruyères. 2009. Biogeographic relationships among deep-sea hydrothermal vent faunas at global scale. Deep Sea Research Part I 56:1,371–1,378, https://doi.org/10.1016/j.dsr.2009.01.009.

Baker, E.T., F. Martinez, J.A. Resing, S.L. Walker, N.J. Buck, and M.H. Edwards. 2010. Hydrothermal cooling along the Eastern Lau Spreading Center: No evidence for discharge beyond the neovolcanic zone. Geochemistry Geophysics Geosystems 11, Q08004, https://doi.org/10.1029/2010GC003106.

Baker, E.T., J.A. Resing, S.L. Walker, F. Martinez, B. Taylor, and K. Nakamura. 2006. Abundant hydrothermal venting along melt-rich and melt-free ridge segments in the Lau back-arc basin. Geophysical Research Letters 33, L07308, https://doi.org/10.1029/2005GL025283.

Bezos, A., S. Escrig, C.H. Langmuir, P.J. Michael, and P.D. Asimow. 2009. Origins of chemical diversity of back-arc basin basalts: A segment-scale study of the Eastern Lau Spreading Center. Journal of Geophysical Research 114, B06212, https://doi.org/10.1029/2008JB005924.

Carlson, R.L., and C.N. Herrick. 1990. Densities and porosities in the oceanic crust and their variations with depth and age. Journal of Geophysical Research 95:9,153–9,170, https://doi.org/10.1029/JB095iB06p09153.

Cavanaugh, C., Z. McKiness, I.L.G. Newton, and F.J. Stewart. 2006. Marine chemosynthetic symbioses. The Prokaryotes 1:475–507, https://doi.org/10.1007/0-387-30741-9_18.

Conder, J.A., and D.A. Wiens. 2007. Rapid mantle flow beneath the Tonga volcanic arc. Earth and Planetary Science Letters 264:299–307, https://doi.org/10.1016/j.epsl.2007.10.014.

Crawford, W.C., J.A. Hildebrand, L.M. Dorman, S.C. Webb, and D.A. Wiens. 2003. Tonga Ridge and Lau Basin crustal structure from seismic refraction data. Journal of Geophysical Research 108(B4), 2195, https://doi.org/10.1029/2001JB001435.

Desbruyères, D., A.M. Alayse-Danet, S. Ohta, and the Scientific Parties of biolauand starmer Cruises. 1994. Deep-sea hydrothermal communities in southwestern Pacific back-arc basins (the North Fiji and Lau Basins): Composition, microdistribution and food web. Marine Geology 116:227–242, https://doi.org/10.1016/0025-3227(94)90178-3.

Dubilier, N., C. Bergin, and C. Lott. 2008. Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nature Reviews Microbiology 6(10):725–740, https://doi.org/10.1038/nrmicro1992.

Dunn, R.A., and F. Martinez. 2011. Contrasting crustal production and rapid mantle transitions beneath back-arc ridges. Nature 469:198–202, https://doi.org/10.1038/nature09690.

Escrig, S., A. Bezos, S.L. Goldstein, C.H. Langmuir, and P.J. Michael. 2009. Mantle source variations beneath the Eastern Lau Spreading Center and the nature of subduction components in the Lau Basin–Tonga arc system. Geochemistry Geophysics Geosystems 10, Q04014, https://doi.org/10.1029/2008GC002281.

Ferrini, V.L., M.K. Tivey, S.M. Carbotte, F. Martinez, and C. Roman. 2008. Variable morphologic expression of volcanic, tectonic, and hydrothermal processes at six hydrothermal vent fields in the Lau back-arc basin. Geochemistry Geophysics Geosystems 9, Q07022, https://doi.org/10.1029/2008GC002047.

Fisher, C.R., J.J. Childress, A.J. Arp, J.M. Brooks, D.L. Distel, J.A. Dugan, H. Felbeck, L.W. Fritz, R.R. Hessler, K.S. Johnson, and others. 1988b. Variation in the hydrothermal vent clam Calyptogen magnifica at the Rose Garden vent on the Galapagos spreading center. Deep Sea Research Part I 35:1,811–1,831, https://doi.org/10.1016/0198-0149(88)90051-9.

Fisher, C.R., J.J. Childress, A.J. Arp, J.M. Brooks, D. Distel, J.A. Favuzzi, H. Felbeck, R. Hessler, K.S. Johnson, M.C. Kennicutt II, and others. 1988a. Microhabitat variation in the hydrothermal vent mussel Bathymodiolus thermophilus at the Rose Garden vent on the Galapagos Rift. Deep Sea Research Part I 35:1,769–1,791, https://doi.org/10.1016/0198-0149(88)90049-0.

Fisher, C.R., K. Takai, and N. Le Bris. 2007. Hydrothermal vent ecosystems. Oceanography 20(1):14–23, https://doi.org/10.5670/oceanog.2007.75.

Flores, G.E., R.C. Hunter, Y. Liu, A. Mets., S. Schouten, and A.-L. Reysenbach. 2011. Hippea jasoniae sp. nov. and Hippea alviniae sp. nov., thermoacidophilic Deltaproteobacteria isolated from deep-sea hydrothermal vent deposits. International Journal of Systematic and Evolutionary Microbiology, http://dx.doi\.org/10.1099/ijs.0.033001-0.

Flores, G.E., I.D. Wagner, Y. Liu, and A.-L. Reysenbach. In Press. Distribution, abundance, and diversity patterns of the thermoacidophilic “Deep-sea Hydrothermal Vent Euryarchaeota 2” (DHVE2). Frontiers in Extreme Microbiology.

Fornari, D.J., K.L. Von Damm, J.G. Bryce, J.P. Cowen, V. Ferrini, A. Fundis, M.D. Lilley, G.W. Luther III, L.S. Mullineaux, M.R. Perfit, and others. 2012. The East Pacific Rise between 9°N and 10°N: Twenty-five years of integrated, multidisciplinary oceanic spreading center studies. Oceanography 25(1):18–43, https://doi.org/10.5670/oceanog.2012.02.

Fornari, D.J., and the WHOI TowCam Group. 2003. A new deep-sea towed digital camera and multi-rock coring system. Eos, Transactions American Geophysical Union 84(8):69, https://doi.org/10.1029/2003EO080001.

Fouquet, Y., U. Von Stackelberg, J.L. Charlou, J.P. Donval, J. Erzinger, J.P. Foucher, P. Herzig, R. Mühe, S. Soakai, M. Wiedicke, and H. Whitechurch. 1991. Hydrothermal activity and metallogenesis in the Lau back-arc basin. Nature 349:778–781, https://doi.org/10.1038/349778a0.

Fouquet, Y., U. von Stackelberg, J.L. Charlou, J. Erzinger, P.M. Herzig, R. Muhe, and M. Wiedicke. 1993. Metallogenesis in back-arc environments: The Lau Basin example. Economic Geology 88:2,154–2,181, https://doi.org/10.2113/gsecongeo.88.8.2154.

Gartman, A., M. Yücel, A.S. Madison, D.W. Chu, S. Ma, C.P. Janzen, E.L. Becker, R.A. Beinart, P.R. Girguis, and G.W. Luther III. 2011. Sulfide oxidation across diffuse flow zones of hydrothermal vents. Aquatic Geochemistry 17:583–601, https://doi.org/10.1007/s10498-011-9136-1.

German, C.R., D.R. Yoerger, M. Jakuba, T.M. Shank, C.H. Langmuir, and K. Nakamura. 2008. Hydrothermal exploration with the Autonomous Benthic Explorer. Deep-Sea Research Part I 55:203–219, https://doi.org/10.1016/j.dsr.2007.11.004.

Glazer, B.T., and O.J. Rouxel. 2009. Redox speciation and distribution within diverse iron-dominated microbial habitats at Loihi Seamount. Journal of Geomicrobiology 26:606–622, https://doi.org/10.1080/01490450903263392.

Hannington, M.D., C.E.J. de Ronde, and S. Petersen. 2005. Sea-floor tectonics and submarine hydrothermal systems. Pp. 111–141 in 100th Anniversary Volume of Economic Geology. J.

Hedenquist, J.F.H. Thompson, R.J. Goldfarb, and J.P. Richards, eds, Society of Economic Geologists, Littleton, CO.

Harding, A.J., G.M. Kent, and J.A. Collins. 2000. Initial results from a multichannel seismic survey of the Lau back-arc basin. Eos, Transactions, American Geophysical Union 81:Fall meeting supplement Abstract T61C-16.

Harmon, N., and D.K. Blackman. 2010. Effects of plate boundary geometry and kinematics on mantle melting beneath the back-arc spreading centers along the Lau Basin. Earth and Planetary Science Letters 298:334–346, https://doi.org/10.1016/j.epsl.2010.08.004.

Henry, M.S., J.J. Childress, and D. Figueroa. 2008. Metabolic rates and thermal tolerances of chemoautotrophic symbioses from Lau Basin hydrothermal vents and their implications for species distributions. Deep-Sea Research Part A 55:679–695, https://doi.org/10.1016/j.dsr.2008.02.001.

Hsu-Kim, H., K.M. Mullaugh, J.J. Tsang, M. Yücel, and G.W. Luther III. 2008. Formation of Zn- and e-sulfides near hydrothermal vents at the Eastern Lau Spreading Center: Implications for sulfide bioavailability to chemoautotrophs. Geochemical Transactions 9:6, https://doi.org/10.1186/1467-4866-9-6.

Ishibashi, J., J.E. Lupton, T. Yamaguchi, J. Querellou, T. Nunoura, and K. Takai. 2006. Expedition reveals changes in Lau Basin hydrothermal system. Eos, Transactions, American Geophysical Union 87(2):13, https://doi.org/10.1029/2006EO020001.

Jacobs, A.M., A.J. Harding, and G.M. Kent. 2007. Axial crustal structure of the Lau back-arc basin from velocity modeling of multichannel seismic data. Earth and Planetary Science Letters 259:239–255, https://doi.org/10.1016/j.epsl.2007.04.021.

Kelley, D.S., S.M. Carbotte, D.W. Caress, D.A. Clague, J.R. Delaney, J.B. Gill, H. Hadaway, J.F. Holden, E.E.E. Hooft, J.P. Kellogg, and others. 2012. Endeavour Segment of the Juan de Fuca Ridge: One of the most remarkable places on Earth. Oceanography 25(1):44–61, https://doi.org/10.5670/oceanog.2012.03.

Kessel, R., M.W. Schmidt, P. Ulmer, and T. Pettke. 2005. Trace element signature of subduction-zone fluids, melts and supercritical liquids at 120–180 km depth. Nature 437:724–727, https://doi.org/10.1038/nature03971.

Kristall, B., D.S. Kelley, M.D. Hannington, and J.R. Delaney. 2006. Growth history of a diffusely venting sulfide structure from the Juan de Fuca Ridge: A petrological and geochemical study. Geochemistry Geophysics Geosystems 7, Q07001, https://doi.org/10.1029/2005GC001166.

Langmuir, C.H., A. Bezos, S. Escrig, and S.W. Parman. 2006. Chemical systematics and hydrous melting of the mantle in back-arc basins. Pp. 87–146 in Back-Arc Spreading Systems: Geological, Biological, Chemical, and Physical Interactions. D.M. Christie, C.R. Fisher, S.-M. Lee, and S. Givens, eds, Geophysical Monograph Series, vol. 166, American Geophysical Union, Washington, DC.

Langmuir, C., S. Humphris, D. Fornari, C. Van Dover, K. Von Damm, M.K. Tivey, D. Colodner, J.-L. Charlou, D. Desonie, C. Wilson, and others. 1997. Hydrothermal vents near a mantle hot spot: The Lucky Strike vent field at 37°N on the Mid-Atlantic Ridge. Earth and Planetary Science Letters 148:69–91, https://doi.org/10.1016/S0012-821X(97)00027-7.

Lau Workshop Report. 2006. Ridge 2000 Workshop Report: Lau Integrated Studies Site Focus Workshop. Available online at: http://www.ridge2000.org/science/meetings/index.php (accessed January 12, 2012).

Le Bris, N., B. Govenar, C. Le Gall, and C.R. Fisher. 2006. Variability of physico-chemical conditions in 9°50’N EPR diffuse flow vent habitats. Marine Chemistry 98:167–182, https://doi.org/10.1016/j.marchem.2005.08.008.

Lee, H.S., S.G. Kang, S.S. Bae, J.K. Lim, Y. Cho, Y.J. Kim, J.H. Jeon, S.S. Cha, K.K. Kwon, H.T. Kim, and others. 2008. The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. Journal of Bacteriology 190:7,491–7,499, https://doi.org/10.1128/JB.00746-08.

Luther, G.W. III, A. Gartman, M. Yücel, A.S. Madison, T.S. Moore, H.A. Nees, D.B. Nuzzio, A. Sen, R.A. Lutz, T.M. Shank, and C.R. Fisher. 2012. Chemistry, temperature, and faunal distributions at diffuse-flow hydrothermal vents: Comparison of two geologically distinct ridge systems. Oceanography 25(1):234–245, https://doi.org/10.5670/oceanog.2012.22.

Luther, G.W. III, T.F. Rozan, M. Taillefert, D.B. Nuzzio, C. Di Meo, T.M. Shank, R.A. Lutz, and S.C. Cary. 2001. Chemical speciation drives hydrothermal vent ecology. Nature 410:813, https://doi.org/10.1038/35071069.

Martinez, F., K. Okino, Y. Ohara, A.-L. Reysenbach, and S.K. Goffredi. 2007. Back-arc basins. Oceanography 20(1):116–127, https://doi.org/10.5670/oceanog.2007.85.

Martinez, F., B. Taylor, E.T. Baker, J.A. Resing, and S.L. Walker. 2006. Opposing trends in crustal thickness and spreading rate along the back-arc Eastern Lau Spreading Center: Implications for controls on ridge morphology, faulting, and hydrothermal activity. Earth and Planetary Science Letters 245:655–672, https://doi.org/10.1016/j.epsl.2006.03.049.

Moore, J.G., J.N. Batchelder, and C.G. Cunningham. 1977. CO2-filled vesicles in mid-ocean basalt. Journal of Volcanology and Geothermal Research 2:309–327, https://doi.org/10.1016/0377-0273(77)90018-X.

Moore, T.S., T.M. Shank, D.B. Nuzzio, and G.W. Luther III. 2009. Time-series chemical and temperature habitat characterization of diffuse flow hydrothermal sites at 9°50’N East Pacific Rise. Deep Sea Research Part II 56:1,616–1,621, https://doi.org/10.1016/j.dsr2.2009.05.008.

Mottl, M.J., J.S. Seewald, C.G. Wheat, M.K. Tivey, P.J. Michael, G. Proskurowski, T.M. McCollom, E. Reeves, J. Sharkey, C.F. You, and others. 2011. Chemistry of hot springs along the Eastern Lau Spreading Center. Geochimica et Cosmochimica Acta 75:1,013–1,038, https://doi.org/10.1016/j.gca.2010.12.008.

Pearce, J.A., R.J. Stern, S.H. Bloomer, and P. Fryer. 2005. Geochemical mapping of the Mariana arc-basin system: Implications for the nature and distribution of subduction components. Geochemistry Geophysics Geosystems 6, Q07006, https://doi.org/10.1029/2004GC000895.

Peate, D.W., T.F. Kokfelt, C.J. Hawkesworth, P.W. VanCalsteren, J.M. Hergt, and J.A. Pearce. 2001. U-series isotope data on Lau Basin glasses: The role of subduction-related fluids during melt generation in back-arc basins. Journal of Petrology 42:1,449–1,470, https://doi.org/10.1093/petrology/42.8.1449.

Podowski, E.L., S. Ma, G.W. Luther III, D. Wardrop, and C.R. Fisher. 2010. Biotic and abiotic factors affecting distributions of megafauna in diffuse flow on andesite and basalt along the Eastern Lau Spreading Center, Tonga. Marine Ecology Progress Series 418:25–45, https://doi.org/10.3354/meps08797.

Podowski, E.L., T.S. Moore, K.A. Zelnio, G.W. Luther III, and C.R. Fisher. 2009. Distribution of diffuse flow megafauna in two sites on the Eastern Lau Spreading Center, Tonga. Deep-Sea Research Part I 56:2,041–2,056, https://doi.org/10.1016/j.dsr.2009.07.002.

Ramirez-Llodra, E., T.M. Shank, and C.R. German. 2007. Biodiversity and biogeography of hydrothermal vent species: Thirty years of discovery and investigations. Oceanography 20(1):30–41, https://doi.org/10.5670/oceanog.2007.78.

Reysenbach, A.-L., and G.E. Flores. 2008. Electron microscopy encounters with unusual thermophiles helps direct genomic analysis of Aciduliprofundum boonei. Geobiology 6:331–336, https://doi.org/10.1111/j.1472-4669.2008.00152.x.

Reysenbach, A.-L., Y. Liu, A.B. Banta, T.J. Beveridge, J.D. Kirshtein, S. Schouten, M.K. Tivey, K.L. Von Damm, and M.A. Voytek. 2006. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447, https://doi.org/10.1038/nature04921.

Ryan, W.B.F., S.M. Carbotte, J.O. Coplan, S. O’Hara, A. Melkonian, R. Arko, R.A. Weissel, V. Ferrini, A. Goodwillie, F. Nitsche, and others. 2009. Global multi-resolution topography synthesis. Geochemistry Geophysics Geosystems 10, Q03014, https://doi.org/10.1029/2008GC002332.

Shank, T.M., D.J. Fornari, K.L. Von Damm, M.D. Lilley, R.M. Haymon, and R.A. Lutz. 1998. Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50’N, East Pacific Rise). Deep Sea Research Part II 45:465–515, https://doi.org/10.1016/S0967-0645(97)00089-1.

Slobodkin, A.I., A.-L. Reysenbach, G.A. Slobodkina, R.V. Baslerov, N. Kostrikina, I. Wagner, E. Bonch-Osmolovskaya. 2011. Thermosulfurimonas dismutans gen. nov., sp. nov. a novel extremely thermophilic sulfur-disproportionating bacterium from a deep-sea hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology, https://doi.org/10.1099/ijs.0.034397-0.

Slobodkina, G.B., A.-L. Reysenbach, A. Panteleeva, N. Kostrikina, I. Wagner, E. Bonch-Osmolovskaya, and A.I. Slobodkin. 2011. Deferrisoma camini gen. nov., sp. nov. a novel moderately thermophilic dissimilatory Fe(III)-reducing bacterium from a deep-sea hydrothermal vent that forms a distinct phylogenetic branch in Deltaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, https://doi.org/10.1099/ijs.0.038372-0.

Smith, G.P., D.A. Wiens, K.M. Foscher, L.M. Dorman, S.C. Webb, and J.A. Hildebrand. 2001. A complex pattern of mantle flow in the Lau backarc. Science 292:713–716. https://doi.org/10.1126/science.1058763.

Speer, K., and A.M. Thurnherr. 2012. The Lau Basin Float Experiment (LAUB-FLEX). Oceanography 25(1):284–285, https://doi.org/10.5670/oceanog.2012.27.

SRK Consulting Report for Nautilus Minerals. 2008. 2008 Exploration Program Papua New Guinea, Tonga, Fiji, Solomons Islands and New Zealand, Nautilus Minerals Inc. Available online at: http://www.nautilusminerals.com/i/pdf/2008NautilusExplorationNI43-101Report.pdf (accessed January 12, 2012).

Stolper, E., and S. Newman. 1994. The role of water in the petrogenesis of Mariana Trough magmas. Earth and Planetary Science Letters 121:293–325, https://doi.org/10.1016/0012-821X(94)90074-4.

Takai, K., T. Nunoura, J.-I. Ishibashi, J. Lupton, R. Suzuki, H. Hamasaki, Y. Ueno, S. Kawagucci, T. Gamo, Y. Suzuki, and others. 2008. Variability in the microbial communities and hydrothermal fluid chemistry at the newly discovered Mariner hydrothermal field, southern Lau Basin. Journal of Geophysical Research 113, G02031, https://doi.org/10.1029/2007JG000636.

Tivey, M.K., P. Craddock, J. Seewald, V. Ferrini, S. Kim, M. Mottl, A. Sterling, A.-L. Reysenbach, C.G. Wheat, and the Scientific Party of TUIM05MV. 2005. Characterization of six vent fields within the Lau Basin. Eos, Transactions, American Geophysical Union 86(52):Fall Meeting Supplement Abstract T31A-0477.

Tivey, M.K., and J.R. Delaney. 1986. Growth of large sulfide structures on the Endeavour Segment of the Juan de Fuca Ridge. Earth and Planetary Science Letters 77:303–317, https://doi.org/10.1016/0012-821X(86)90142-1.

Tivey, M.K., D.S. Stakes, T.L. Cook, M.D. Hannington, and S. Petersen. 1999. A model for growth of steep-sided vent structures on the Endeavour Segment of the Juan de Fuca Ridge: Results of a petrologic and geochemical study. Journal of Geophysical Research 104:22,859–22,883, https://doi.org/10.1029/1999JB900107.

Turner, I.M., C. Peirce, and M.C. Sinha. 1999. Seismic imaging of the axial region of the Valu Fa Ridge, Lau Basin: The accretionary processes of an intermediate back-arc spreading ridge. Geophysical Journal International 138:495–519, https://doi.org/10.1046/j.1365-246X.1999.00883.x.

Waite, T.J., T.S. Moore, J.J. Childress, H. Hsu-Kim, K.M. Mullaugh, D.B. Nuzzio, A.N. Paschal, J. Tsang, C.R. Fishers, and G.W. Luther III. 2008. Variation in sulfur speciation with shellfish presence at a Lau Basin diffuse flow vent site. Journal of Shellfish Research 27:163–168, https://doi.org/10.2983/0730-8000(2008)27[163:VISSWS]2.0.CO;2.

Yücel, M., A. Gartman, C.S. Chan, and G.W. Luther III. 2011. Hydrothermal vents as a kinetically stable source of iron-sulphide-bearing nanoparticles to the ocean. Nature Geoscience 4:367–371, https://doi.org/10.1038/NGEO1148.

Zhou, H., J. Li, and Q. Yang. 2008. Microbiological oxidation of sulfide chimney promoted by warm diffusing flow in CDE hydrothermal field in Eastern Lau Spreading Center. Eos, Transactions, American Geophysical Union 89(48):Fall Meeting Supplement Abstract B51D-0405.

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