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Continental margins host methane seeps, animal falls and wood falls, with chemosynthetic communities that may share or exchange species. The goal of this study was to examine the existence and nature of linkages among chemosynthesis-based ecosystems by deploying organic fall mimics (bone and wood) alongside defaunated carbonate rocks within high and lesser levels of seepage activity for 7.4 years. We compared community composition, density, and trophic structure of invertebrates on these hard substrates at active methane seepage and transition (less seepage) sites at Mound 12 at ~1,000 m depth, a methane seep off the Pacific coast of Costa Rica. At transition sites, the community composition on wood and bone was characteristic of natural wood- and whale-fall community composition, which rely on decay of the organic substrates. However, at active sites, seepage activity modified the relationship between fauna and substrate, seepage activity had a stronger effect in defining and homogenizing these communities and they depend less on organic decay. In contrast to community structure, macrofaunal trophic niche overlap between substrates, based on standard ellipse areas, was greater at transition sites than at active sites, except between rock and wood. Our observations suggest that whale- and wood-fall substrates can function as stepping stones for seep fauna even at later successional stages, providing hard substrate for attachment and chemosynthetic food. 

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. 

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. 

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.