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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.

 

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.

 

In deep‐sea environments, plant remains of several origins are found, including branches, twigs, leaves, and wood pieces, among others. As most of the deep‐sea bottoms are oligotrophic and nutrient‐limited, plant remains provide an oasis of localized organic enrichment and a substrate for colonization. Sunken wood was suggested to play an important evolutionary role in the diversification of chemosynthetic ecosystems, possibly representing stepping stones for the colonization between vent and seep ecosystems. In order to understand colonization processes of the Pacific Costa Rican meio‐epifaunal assemblages associated with sunken wood, a field experiment was conducted on Mound 12 (8°55.778′N, 84°18.730′W) at ~1,000 m water depth. Woodblocks were placed in four different habitats (Mussel beds, tube worms, near mussel beds, rubble bottoms), and different local environmental conditions (seepage‐active and seepage‐inactive sites). Seven experimental Douglas fir woodblocks (each 1,047 cm²in surface area) were deployed from the R/V Atlantis using the manned submersibleAlvinin February 2009 and recovered after 10.5 months in January 2010. Sample processing and analyses led to a data set of abundance (total 9,951 individuals) and spatial distribution of nine meio‐epifaunal higher taxa/groups. Meio‐epifaunal densities on individual woodblocks ranged from 3 to 26 ind.10 cm². Copepods accounted for the highest abundances (75.1%), followed by nauplii larvae (11.7%) and nematodes (9.8%). The maximum number of individuals (26.3 ind.10 cm⁻²) was found in blocks placed in seepage‐inactive areas (near active mussel beds) in contrast to 2.9 ind.10 cm⁻²in active areas (within a mussel bed). A hierarchical cluster analysis grouped blocks according to seepage activity and not to habitat, but tests of similarity showed no significant differences in higher taxon composition and abundances, probably owing either to substrate homogeneity or low sample size. Copepods were the most abundant representatives, suggesting that this group is one of the most successful in colonizing in the early stage of succession, in this case while hardwood substrates are not yet decomposed or bored by bivalves.

 

Climate change manifestation in the ocean, through warming, oxygen loss, increasing acidification, and changing particulate organic carbon flux (one metric of altered food supply), is projected to affect most deep‐ocean ecosystems concomitantly with increasing direct human disturbance. Climate drivers will alter deep‐sea biodiversity and associated ecosystem services, and may interact with disturbance from resource extraction activities or even climate geoengineering. We suggest that to ensure the effective management of increasing use of the deep ocean (e.g., for bottom fishing, oil and gas extraction, and deep‐seabed mining), environmental management and developing regulations must consider climate change. Strategic planning, impact assessment and monitoring, spatial management, application of the precautionary approach, and full‐cost accounting of extraction activities should embrace climate consciousness. Coupled climate and biological modeling approaches applied in the water and on the seafloor can help accomplish this goal. For example, Earth‐System Model projections of climate‐change parameters at the seafloor reveal heterogeneity in projected climate hazard and time of emergence (beyond natural variability) in regions targeted for deep‐seabed mining. Models that combine climate‐induced changes in ocean circulation with particle tracking predict altered transport of early life stages (larvae) under climate change. Habitat suitability models can help assess the consequences of altered larval dispersal, predict climate refugia, and identify vulnerable regions for multiple species under climate change. Engaging the deep observing community can support the necessary data provisioning to mainstream climate into the development of environmental management plans. To illustrate this approach, we focus on deep‐seabed mining and the International Seabed Authority, whose mandates include regulation of all mineral‐related activities in international waters and protecting the marine environment from the harmful effects of mining. However, achieving deep‐ocean sustainability under the UN Sustainable Development Goals will require integration of climate consideration across all policy sectors.

 

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. 

Stomatopoda, commonly known as mantis shrimps, are notable for their enlarged second maxillipeds encompassing the raptorial claw. The form of the claw can be used to divide them into two basic groups: smashers and spearers. Previous phylogenetic studies of Stomatopoda have focused on morphology or a few genes, though there have been whole mitochondrial genomes published for 15 members of Stomatopoda. However, the sampling has been somewhat limited with key taxa not included. Here, nine additional stomatopod mitochondrial genomes were generated and combined with the other available mitogenomes for a phylogenetic analysis. We used the 13 protein coding genes, as well as 12S rRNA, 16S rRNA genes, and included nuclear 18S rRNA gene sequences. Different rooting options were used for the analyses: (1) single and multiple outgroups from various eumalocostracan relatives and (2) a stomatopod-only dataset, with Hemisquilla californiensis used to root the topologies, based on the current hypothesis that Hemisquilla is the sister group to the rest of Stomatopoda. The eumalocostracan-rooted analyses all showed H. californiensis nested within Stomatopoda, raising doubts as to previous hypotheses as to its placement. Allowing for the rooting difference, the H. californiensis outgroup datasets had the same tree topology as the eumalocostracan outgroup datasets with slight variation at poorly supported nodes. Of the major taxonomic groupings sampled to date, Squilloidea was generally found to be monophyletic while Gonodactyloidea was not. The position of H. californiensis was found inside its superfamily, Gonodactyloidea, and grouped in a weakly supported clade containing Odontodactylus havanensis and Lysiosquillina maculata for the eumalocostracan-rooted datasets. An ancestral state reconstruction was performed on the raptorial claw form and provides support that spearing is the ancestral state for extant Stomatopoda, with smashing evolving subsequently one or more times. 

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. 

The bathyal serpulid Laminatubus alvini ten Hove & Zibrowius, 1986 was described from the periphery of hydrothermal vents of the Galapagos Rift and has been recorded from other vent communities of the East Pacific Rise (EPR). Here we assessed the biodiversity of serpulids collected from eastern Pacific hydrothermal vents and methane seeps using DNA sequences and morphology. Laminatubus alvini showed little genetic variation over a wide geographic range from the Alarcon Rise vents in southern Gulf of California (~23°N), to at least a point at 38°S on the EPR. Specimens from several methane seeps off Costa Rica and the Gulf of California (Mexico) differed markedly from those of Laminatubus alvini on DNA sequence data and in having seven thoracic chaetigers and lacking Spirobranchus-type special collar chaetae, thus fitting the diagnosis of Neovermilia. However, phylogenetic analysis of molecular data showed that L. alvini and the seep specimens form a well-supported clade. Moreover, among the seep specimens there was minimally a ~7% distance in mitochondrial cytochrome b sequences between a shallow-water (1000 m) seep clade restricted to Costa Rica and a deep-water clade (1800 m) from Costa Rica to Gulf of California. We describe the seep taxa here as morphologically indistinguishable L. paulbrooksi n. sp. and L. joycebrooksae n. sp. 

Benthic animals profoundly influence the cycling and storage of carbon and other elements in marine systems, particularly in coastal sediments. Recent climate change has altered the distribution and abundance of many seafloor taxa and modified the vertical exchange of materials between ocean and sediment layers. Here, we examine how climate change could alter animal-mediated biogeochemical cycling in ocean sediments. The fossil record shows repeated major responses from the benthos during mass extinctions and global carbon perturbations, including reduced diversity, dominance of simple trace fossils, decreased burrow size and bioturbation intensity, and nonrandom extinction of trophic groups. The broad dispersal capacity of many extant benthic species facilitates poleward shifts corresponding to their environmental niche as overlying water warms. Evidence suggests that locally persistent populations will likely respond to environmental shifts through either failure to respond or genetic adaptation rather than via phenotypic plasticity. Regional and global ocean models insufficiently integrate changes in benthic biological activity and their feedbacks on sedimentary biogeochemical processes. The emergence of bioturbation, ventilation, and seafloor-habitat maps and progress in our mechanistic understanding of organism–sediment interactions enable incorporation of potential effects of climate change on benthic macrofaunal mediation of elemental cycles into regional and global ocean biogeochemical models.