skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.


Title: A chemosynthetic ecotone—“chemotone”—in the sediments surrounding deep‐sea methane seeps
Abstract

Ecotones have been described as “biodiversity hotspots” from myriad environments, yet have not been studied extensively in the deep ocean. While physiologically challenging, deep‐water methane seeps host highly productive communities fueled predominantly by chemosynthetic pathways. We hypothesized that the biological and geochemical influence of methane seeps extends into background habitats, resulting in the formation of a “chemotone” where chemosynthesis‐based and photosynthesis‐based communities overlap. To investigate this, we analyzed the macrofaunal assemblages and geochemical properties of sediments collected from “active,” “transition” (potential chemotone), and “background” habitats surrounding five Costa Rican methane seeps (depth range 377–1908 m). Sediment geochemistry demonstrated a clear distinction between active and transition habitats, but not between transition and background habitats. In contrast, biological variables confirmed the presence of a chemotone, characterized by intermediate biomass, a distinct species composition (including habitat endemics and species from both active and background habitats), and enhanced variability in species composition among samples. However, chemotone assemblages were not distinct from active and/or background assemblages in terms of faunal density, biological trait composition, or diversity. Biomass and faunal stable isotope data suggest that chemotones are driven by a gradient in food delivery, receiving supplements from chemosynthetic production in addition to available photosynthetic‐based resources. Sediment geochemistry suggests that chemosynthetic food supplements are delivered across the chemotone at least in part through the water column, as opposed to reflecting exclusivelyin situchemosynthetic production in sediments. Management efforts should be cognisant of the ecological attributes and spatial extent of the chemotone that surrounds deep‐sea chemosynthetic environments.

 
more » « less
Award ID(s):
1634002 1634172
NSF-PAR ID:
10452339
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Limnology and Oceanography
Volume:
66
Issue:
5
ISSN:
0024-3590
Page Range / eLocation ID:
p. 1687-1702
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Methane seeps are highly productive deep‐sea ecosystems reliant on chemosynthetic primary production. They are increasingly affected by direct human activities that threaten key ecosystem services. Methane seepage often generates precipitation of authigenic carbonate rocks, which host diverse microbes, and a dynamic invertebrate community. By providing hard substrate, even after seepage ceases, these rocks may promote a long‐lasting ecological interaction between seep and background communities. We analyzed community composition, density, and trophic structure of invertebrates on authigenic carbonates at Mound 12, a seep on the Pacific margin of Costa Rica, using one mensurative and two manipulative experiments. We asked whether carbonate macrofaunal communities are able to survive, adapt, and recover from changes in environmental factors (i.e., seepage activity, chemosynthetic production, and food availability), and we hypothesized a key role for seepage activity in defining these communities and responses. Communities onin situcarbonates under different seepage activities showed declining density with increasing distance from the seep and a shift in composition from gastropod dominance in areas of active seepage to more annelids and peracarid crustaceans that are less dependent on chemosynthetic production under lesser seepage. Response to changing environmental context was evident from altered community composition following (1) a natural decline in seepage over successive years, (2) transplanting of carbonates to different seepage conditions for 17 months, and (3) defaunated carbonate deployments under different seepage regimes over 7.4 yr. Seep faunas on transplants to lesser seepage emerge and recover faster than transition fauna (characterized by native seep and background faunas, respectively) and are able to persist by adapting their diets or by retaining their symbiotic bacteria. The macrofaunal community colonizing defaunated carbonates deployed for 7.4 yr developed communities with a similar successional stage asin siturocks, although trophic structure was not fully recovered. Thus, macrofaunal successional dynamics are affected by habitat complexity and the availability of microbial chemosynthetic productivity. This multi‐experiment study highlights the interaction between biotic and abiotic factors at methane seeps at different time scales along a spatial gradient connecting seep and surrounding deep‐sea communities and offers insight on the resilience of deep‐sea macrofaunal communities.

     
    more » « less
  2. Methane seeps are highly abundant marine habitats that contribute sources of chemosynthetic primary production to marine ecosystems. Seeps also factor into the global budget of methane, a potent greenhouse gas. Because of these factors, methane seeps influence not only local ocean ecology, but also biogeochemical cycles on a greater scale. Methane seeps host specialized microbial communities that vary significantly based on geography, seep gross morphology, biogeochemistry, and a diversity of other ecological factors including cross-domain species interactions. In this study, we collected sediment cores from six seep and non-seep locations from Grays and Quinault Canyons (46–47°N) off Washington State, USA, as well as one non-seep site off the coast of Oregon, USA (45°N) to quantify the scale of seep influence on biodiversity within marine habitats. These samples were profiled using 16S rRNA gene sequencing. Predicted gene functions were generated using the program PICRUSt2, and the community composition and predicted functions were compared among samples. The microbial communities at seeps varied by seep morphology and habitat, whereas the microbial communities at non-seep sites varied by water depth. Microbial community composition and predicted gene function clearly transitioned from on-seep to off-seep in samples collected from transects moving away from seeps, with a clear ecotone and high diversity where methane-fueled habitats transition into the non-seep deep sea. Our work demonstrates the microbial and metabolic sphere of influence that extends outwards from methane seep habitats. 
    more » « less
  3. Methane seeps provide biogeochemical and microbial heterogeneity in deep-sea habitats. In the Northeast (NE) Pacific Ocean recent studies have found an abundance of seeps at varying spatial separations and within distinct biogeochemical environments ranging in oxygen, depth, and temperature. Here, we examine eight newly discovered seeps and two known seeps covering 800 km and varying across 2000 m water depth to identify: (1) novel megafaunal communities in this geographical region; (2) variations in the microbiome of seep habitats across the margin; (3) spatial and biogeochemical drivers of microbial diversity at seeps. In addition to authigenic carbonates, clam beds, microbial mats, and exposed hydrates - we also observed Siboglinidae tube worm bushes and an anomalous deep-sea barnacle adding to the overall habitats known from the NE Pacific. The microbial communities showed high variability in their spatial distribution and community structure. The seep communities formed distinct groups that included multiple groups of anaerobic methane oxidizing Archaea (ANME; 1, 2ab, 2c, and 3), often co-occurring within one site – however, there were also other sites with clearly dominant members (e.g. ANME-1s at Nehalem Bank). Sulfide oxidizers were dominated by the non-mat forming Campylobacterales and even though vertical gradients in redox potential typify seep sediments, in two cases there was not a significant change in community structure across the top five cm of sediment. We posit that these patterns were driven by ‘bubble-turbation,’ and bioirrigation by megafauna. A surprising latitudinal trend was observed in species diversity and richness with increasing richness significantly correlated to increasing latitude. Overall, our results demonstrate that heterogeneity is ubiquitous in the seep biome, spanning all faunal classes, and that the understanding of seeps and the drivers of the community structure can be improved by studying seeps at a range of spatial scales. 
    more » « less
  4. null (Ed.)
    International Ocean Discovery Program Expedition 385 drilled organic-rich sediments and intruded sills in the off-axis region and axial graben of the northern spreading segment of Guaymas Basin, a young marginal seafloor spreading system in the Gulf of California. Guaymas Basin is characterized by high heat flow and magmatism in the form of sill intrusions into sediments, which extends tens of kilometers off axis, in contrast with the localized volcanism found at most mid-ocean ridge spreading centers. Sill intrusions provide transient heat sources that mobilize buried sedimentary carbon, in part as methane and other hydrocarbons, and drive hydrothermal circulation. The resulting thermal and geochemical gradients shape abundance, composition, and activity of the deep subsurface biosphere of the basin. Drill sites extend over a broad region of Guaymas Basin. Adjacent Sites U1545 and U1546, located ~52 km northwest of the northern Guaymas Basin axial graben, recovered sediment successions to ~540 meters below seafloor (mbsf) (equivalent to the core depth below seafloor, Method A [CSF-A] scale), including a thin sill (a few meters thick) drilled near the bottom of Site U1545 and a massive sill (~355–430 mbsf) at Site U1546 that chemically and physically affects the surrounding sediments. Sites U1547 and U1548, located ~27 km northwest of the axial graben, were drilled to investigate an active sill-driven hydrothermal system evident at the seafloor as an 800 m wide, circular bathymetric high called Ringvent because of its outline of a ring of active vent sites. Ringvent is underlain by a thick sill at shallow depth (Site U1547). Geothermal gradients steepen toward the Ringvent periphery (Holes U1548A–U1548C), and the zones of authigenic carbonate precipitation and of highest microbial cell abundance correspondingly shallow toward the periphery. The underlying sill was drilled several times and yielded diverse igneous rock textures, sediment/sill interfaces, and alteration minerals in veins and vesicles. The Ringvent sill became the target of an integrated, interdisciplinary sampling and research effort that included geological, geochemical, and microbiological components. The thermal, lithologic, geochemical, and microbiological contrasts between the northwestern sites (U1545 and U1546) and the Ringvent sites (U1547 and U1548) form the core scientific observations informing the direct influence of sill-sediment interaction. These observations are supplemented by results from sites that exhibit persistent influence of thermally equilibrated sill intrusions, including supporting long-lived methane cold seeps, as observed at off-axis Sites U1549 and U1552, and the persistent geochemical record of hydrocarbon formation near the sill/sediment contact, as observed at the northern axial trough Site U1550, which confirms observations from Deep Sea Drilling Project (DSDP) Leg 64. Drilling at Site U1551 ~29 km southeast of the axial graben was not successful due to unstable shallow sands, but it confirmed the dominant influence of gravity-flow sedimentation processes southeast of the axial graben. The scientific outcomes of Expedition 385 will (1) revise long-held assumptions about the role of sill emplacement in subsurface carbon mobilization versus carbon retention, (2) comprehensively examine the subsurface biosphere of Guaymas Basin and its responses and adaptations to hydrothermal conditions, (3) redefine hydrothermal controls on authigenic mineral formation in sediments, and (4) yield new insights into the long term influence of sill-sediment interaction on sediments deposited at the earliest stages of seafloor spreading, that is, when spreading centers are proximal to a continental margin. The generally high quality and high degree of completeness of the shipboard data sets present opportunities for inter- and multidisciplinary collaborations during shore-based studies. In comparison to DSDP Leg 64 to Guaymas Basin in 1979, continuous availability of sophisticated drilling strategies (e.g., the advanced piston corer [APC] and half-length APC systems) and numerous analytical innovations greatly improved sample recovery and scientific yield, particularly in the areas of organic geochemistry and microbiology. For example, microbial metagenomics did not exist 40 y ago. However, these technical refinements do not change the fact that Expedition 385 in many respects builds on the foundations of understanding laid by Leg 64 drilling in Guaymas Basin. 
    more » « less
  5. As biodiversity loss accelerates globally, understanding environmental influence over biodiversity–ecosystem functioning (BEF) relationships becomes crucial for ecosystem management. Theory suggests that resource supply affects the shape of BEF relationships, but this awaits detailed investigation in marine ecosystems. Here, we use deep-sea chemosynthetic methane seeps and surrounding sediments as natural laboratories in which to contrast relationships between BEF proxies along with a gradient of trophic resource availability (higher resource methane seep, to lower resource photosynthetically fuelled deep-sea habitats). We determined sediment fauna taxonomic and functional trait biodiversity, and quantified bioturbation potential (BPc), calcification degree, standing stock and density as ecosystem functioning proxies. Relationships were strongly unimodal in chemosynthetic seep habitats, but were undetectable in transitional ‘chemotone’ habitats and photosynthetically dependent deep-sea habitats. In seep habitats, ecosystem functioning proxies peaked below maximum biodiversity, perhaps suggesting that a small number of specialized species are important in shaping this relationship. This suggests that absolute biodiversity is not a good metric of ecosystem ‘value’ at methane seeps, and that these deep-sea environments may require special management to maintain ecosystem functioning under human disturbance. We promote further investigation of BEF relationships in non-traditional resource environments and emphasize that deep-sea conservation should consider ‘functioning hotspots' alongside biodiversity hotspots. 
    more » « less