Succession of hydrocarbon seep communities associated with the long-lived foundation species Lamellibrachia luymesi

Cordes, Erik E.; Hourdez, Stéphane; Predmore, Benjamin L.; Redding, Meredith L.; Fisher, Charles R.

doi:10.3354/meps305017

Cited by 86 publications

(131 citation statements)

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“…Aller, 1980Aller, , 1984Aller and Aller, 1998;Meile et al, 2001;Cordes et al, 2005;Dattagupta et al, 2008). However, only a few studies have quantified the influence of the activity of chemosynthetic biota on benthic fluxes at cold seeps (Wallmann et al, 1997;Haese, 2002;Cordes et al, 2005;Haese et al, 2006).…”

Section: Fischer Et Al: Pore Water Geochemistry Of Cold Seeps Offmentioning

confidence: 99%

“…Hensen et al, 2003;Cordes et al, 2005;Haese et al, 2006;Dattagupta et al, 2008). Several studies have demonstrated that the interaction of the transport processes bioirrigation and advection significantly influences pore water profiles and solute fluxes at cold seeps (Wallmann et al, 1997;Haese et al, 2006;Niemann et al, 2006).…”

Section: Schematic Evolution Of the Depth Of The Smt And Sulfate Fluxmentioning

confidence: 99%

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Interaction between hydrocarbon seepage, chemosynthetic communities, and bottom water redox at cold seeps of the Makran accretionary prism: insights from habitat-specific pore water sampling and modeling

et al. 2012

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Abstract. The interaction between fluid seepage, bottom water redox, and chemosynthetic communities was studied at cold seeps across one of the world's largest oxygen minimum zones (OMZ) located at the Makran convergent continental margin. Push cores were obtained from seeps within and below the core-OMZ with a remotely operated vehicle. Extracted sediment pore water was analyzed for sulfide and sulfate concentrations. Depending on oxygen availability in the bottom water, seeps were either colonized by microbial mats or by mats and macrofauna. The latter, including ampharetid polychaetes and vesicomyid clams, occurred in distinct benthic habitats, which were arranged in a concentric fashion around gas orifices. At most sites colonized by microbial mats, hydrogen sulfide was exported into the bottom water. Where macrofauna was widely abundant, hydrogen sulfide was retained within the sediment.Numerical modeling of pore water profiles was performed in order to assess rates of fluid advection and bioirrigation. While the magnitude of upward fluid flow decreased from 11 cm yr −1 to <1 cm yr −1 and the sulfate/methane transition (SMT) deepened with increasing distance from the central gas orifice, the fluxes of sulfate into the SMT did not significantly differ (6.6-9.3 mol m −2 yr −1 ). Depth-integrated rates of bioirrigation increased from 120 cm yr −1 in the central habitat, characterized by microbial mats and sparse macrofauna, to 297 cm yr −1 in the habitat of large and few small vesicomyid clams. These results reveal that chemosynthetic macrofauna inhabiting the outer seep habitats below the core-OMZ efficiently bioirrigate and thus transport sulfate down into the upper 10 to 15 cm of the sediment. In this way the animals deal with the lower upward flux of methane in outer habitats by stimulating rates of anaerobic oxidation of methane (AOM) with sulfate high enough to provide hydrogen sulfide for chemosynthesis. Through bioirrigation, macrofauna engineer their geochemical environment and fuel upward sulfide flux via AOM. Furthermore, due to the introduction of oxygenated bottom water into the sediment via bioirrigation, the depth of the sulfide sink gradually deepens towards outer habitats. We therefore suggest thatin addition to the oxygen levels in the water column, which determine whether macrofaunal communities can develop or not -it is the depth of the SMT and thus of sulfide production that determines which chemosynthetic communities are able to exploit the sulfide at depth. We hypothesize that large vesicomyid clams, by efficiently expanding the sulfate zone down into the sediment, could cut off smaller or less mobile organisms, as e.g. small clams and sulfur bacteria, from the sulfide source.

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Section: Fischer Et Al: Pore Water Geochemistry Of Cold Seeps Offmentioning

confidence: 99%

Section: Schematic Evolution Of the Depth Of The Smt And Sulfate Fluxmentioning

confidence: 99%

Interaction between hydrocarbon seepage, chemosynthetic communities, and bottom water redox at cold seeps of the Makran accretionary prism: insights from habitat-specific pore water sampling and modeling

et al. 2012

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“…It forms 1-2·m tall bush-like aggregations that can contain over one thousand individuals, and provide habitat for a wide variety of heterotrophic fauna Cordes et al, 2005a;Cordes et al, 2005b). L. luymesi grows extremely slowly, and has a lifespan of at least 170-250·years (Bergquist et al, 2000;Fisher et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

The hydrocarbon seep tubeworm Lamellibrachia luymesi primarily eliminates sulfate and hydrogen ions across its roots to conserve energy and ensure sulfide supply

Dattagupta

Miles

Barnabei

et al. 2006

Journal of Experimental Biology

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-1 (Freytag et al., 2001), levels in the sediment underlying them are typically greater than 1.5·mmol·l -1 (Julian et al., 1999). L. luymesi obtains sulfide from the sediment using long, root-like, posterior extensions of its body (Freytag et al., 2001; Julian et Lamellibrachia luymesi (Polychaeta, Siboglinidae) is a deep-sea vestimentiferan tubeworm that forms large bushlike aggregations at hydrocarbon seeps in the Gulf of Mexico. Like all vestimentiferans, L. luymesi obtains its nutrition from sulfide-oxidizing endosymbiotic bacteria, which it houses in an internal organ called the trophosome. This tubeworm has a lifespan of over 170·years and its survival is contingent upon the availability of sulfide during this long period. In sediments underlying L. luymesi aggregations, microbes produce sulfide by coupling sulfate reduction with hydrocarbon oxidation. L. luymesi acquires sulfide from the sediment using a rootlike posterior extension of its body that is buried in the sediment. Its symbionts then oxidize the sulfide to produce energy for carbon fixation, and release sulfate and hydrogen ions as byproducts. It is critical for the tubeworm to eliminate these waste ions, and it could do so either across its vascular plume or across its root. In this study, we measured sulfate and proton elimination rates from live L. luymesi and found that they eliminated approximately 85% of the sulfate produced by sulfide oxidation, and approximately 67% of the protons produced by various metabolic processes, across their roots. On the basis of experiments using membrane transport inhibitors, we suggest that L. luymesi has anion exchangers that mediate sulfate elimination coupled with bicarbonate uptake. Roots could be the ideal exchange surface for eliminating sulfate and hydrogen ions for two reasons. First, these ions might be eliminated across the root epithelium using facilitated diffusion, which is energetically economical. Second, sulfate and hydrogen ions are substrates for bacterial sulfate reduction, and supplying these ions into the sediment might help ensure a sustained sulfide supply for L. luymesi over its entire lifespan.

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“…At present, the chemoautotrophic frenulate worms no longer exist, but the products of seepage, such as carbonate rocks, provide settlement substrates, making this community diverse and densely colonized. This is similar to what has been observed or predicted at lower latitude seeps, where carbonates and the tubes of 10 vestimentiferans provide a substrate for hard bottomed animals such as sponges or cnidarians (Bergquist et al, 2003;Bowden et al, 2013;Cordes et al, 2005). The major difference is that in these studies and models of succession in lower latitude seeps, a major driving force from an active to a senescent or background fauna dominated community, is a cessation or displacement of fluid flow, often accompanied by a decrease in sediment sulfide concentrations.…”

Section: Comparisons To Other Seep Sitesmentioning

confidence: 49%

Geophysical and geochemical controls on the megafaunal community of a high Arctic cold seep

Sen¹,

Åström²,

Hong³

et al. 2018

Preprint

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Cold seep communities around gas hydrate mounds (pingos) in the Western Barents Sea (76°N, 16°E, ~400 m depth) were investigated with high resolution, geographically referenced images acquired with an ROV and towed camera. Four pingos associated with seabed methane release hosted diverse biological communities of mainly non-seep (background) species including commercially important fish and crustaceans, as well as a species new to this area (the snow crab Chionoecetes 15 opilio). We attribute the presence of most benthic community members to habitat heterogeneity and the occurrence of hard substrates (methane derived authigenic carbonates), particularly the most abundant phyla (Cnidaria and Porifera), though food availability and exposure to a diverse microbial community is also important for certain taxa. Only one chemosynthesis based species was confirmed, the siboglinid frenulate polychaete, Oligobrachia haakonmosbiensis. Overall, the pingo communities formed two distinct clusters, distinguished by the presence or absence of frenulates. Methane gas advection through sediments 20 was absent below the single pingo that lacked frenulates, while seismic profiles indicated gas saturated sediment below the other frenulate colonized pingos. The absence of frenulates could not be explained by sediment sulfide concentrations, despite these worms likely containing sulfide oxidizing symbionts. We propose that high levels of seafloor methane seepage linked to sub-surface gas reservoirs support an abundant and active sediment methanotrophic community that maintains high sulfide fluxes and serves as a carbon source for frenulate worms. The pingo currently lacking a sub-surface gas source and lower 25 methane concentrations has lower sulfide flux rates and limited amounts of carbon insufficient to support frenulates. Two previously undocumented behaviors were visible through the images: grazing activity of snow crabs on bacterial mats, and seafloor crawling of Nothria conchylega onuphid polychaetes.Biogeosciences Discuss., https://doi

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Succession of hydrocarbon seep communities associated with the long-lived foundation species Lamellibrachia luymesi

Cited by 86 publications

References 50 publications

Interaction between hydrocarbon seepage, chemosynthetic communities, and bottom water redox at cold seeps of the Makran accretionary prism: insights from habitat-specific pore water sampling and modeling

Interaction between hydrocarbon seepage, chemosynthetic communities, and bottom water redox at cold seeps of the Makran accretionary prism: insights from habitat-specific pore water sampling and modeling

The hydrocarbon seep tubeworm Lamellibrachia luymesi primarily eliminates sulfate and hydrogen ions across its roots to conserve energy and ensure sulfide supply

Geophysical and geochemical controls on the megafaunal community of a high Arctic cold seep

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