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There are numerous studies highlighting the impacts of direct and indirect stressors on marine organisms, and multi-stressor studies of their combined effects are an increasing focus of experimental work. Lophelia pertusa is a framework-forming cold-water coral that supports numerous ecosystem services in the deep ocean. These corals are threatened by increasing anthropogenic impacts to the deep-sea, such as global ocean change and hydrocarbon extraction. This study implemented two sets of experiments to assess the effects of future conditions (temperature: 8 °C and 12 °C, pH: 7.9 and 7.6) and hydrocarbon exposure (oil, dispersant, oil + dispersant combined) on coral health. Phenotypic response was assessed through three independent observations of diagnostic characteristics that were combined into an average health rating at four points during exposure and recovery. In both experiments, regardless of environmental condition, average health significantly declined during 24-hour exposure to dispersant alone but was not significantly altered in the other treatments. In the early recovery stage (24 hours), polyp health returned to the pre-exposure health state under ambient temperature in all treatments. However, increased temperature resulted in a delay in recovery (72 hours) from dispersant exposure. These experiments provide evidence that global ocean change can affect the resilience of corals to environmental stressors and that exposure to chemical dispersants may pose a greater threat than oil itself.

Resource extraction from the ocean comes with ecosystem-wide risks, including threats to its biota such as the habitat forming corals that support elevated biomass and biodiversity. Despite catastrophic incidents like theDeepwater Horizonoil spill (DWHOS) disaster that occurred in 2010, offshore oil and gas drilling continues to occur around the world. Previous work investigating the toxicity of oil and the chemical dispersant used in an attempt to mitigate the effects of the DWHOS revealed that the dispersant elicits a stronger, negative physiological response than oil alone. However, little is known regarding the specific ways in which these anthropogenic pollutants impact organisms at the cellular level. To investigate the impacts of each pollutant and their synergistic effects on corals, we analyzed the transcriptional responses of the deep-sea octocoralsCallogorgia deltaandParamuriceatype B3 following 12 h of exposure to oil, dispersant, and mixtures of oil and dispersant. Analyses revealed that the highest levels of significant differential gene expression were found among the treatments containing dispersant, which corresponds to the significant effects observed in physiological experiments. Functional analyses of annotated transcripts further suggest both species- and colony-specific responses to the exposures, likely due to underlying cellular and physiological differences. However, some commonalities were observed among the responses to chemical stress across treatments and species, including immune and cellular stress responses, altered energy metabolism, and oxidative stress, elucidating how corals respond to chemical pollutants. As resource extraction is an ongoing threat, this study demonstrates the importance of considering the varied and diverse responses of biota to anthropogenic disturbances and the implications of introducing chemicals into vulnerable ecosystems like those associated with deep-sea corals.

Summary As agglutinated Foraminifera, Xenophyophores inhabit the deep ocean floor and build their tests from particles of the environment. Despite their diversity and abundance, especially in areas of commercial interest for polymetallic nodules, the role of Xenophyophores in the deep-sea ecosystem and their physiology is still poorly understood. Previous studies hypothesized that their tests provide a habitat for deep-sea microbes. To further investigate Xenophyophores and associated microbes, we analyzed diverse Xenophyophores from the Quepos plateau and seamounts off Costa Rica for their lipid biomarkers and microbial 16S rRNA gene diversity. In our data we identified archaeal glycerol dialkyl glycerol tetraethers with a high content of intact polar lipids and substantial amounts of the thaumarchaeal biomarker Crenarchaeol. This data is suggestive of a thaumarchaeal assemblage, which was independently confirmed through Illumina 16S rRNA amplicon sequencing. The spatial distribution of biomarkers we observed with mass spectrometry imaging in a section through a Xenophyophore test shows a heterogeneity, which we interpret as differences in activity, community composition and/ or growth stages of the archaeal community members. Our lipid biomarker and molecular data suggests that Thaumarchaea are associated with diverse Xenophyophores and that their tests can provide a newly discovered micro-niche for these microbes.

Hidden in plain sight: Methanotrophic feather duster worms redefine the methane seep sphere of influence., Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ13C of −44 to −58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of 13C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150–million year–old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.

Deep-sea methane seeps are dynamic sources of greenhouse gas production and unique habitats supporting ocean biodiversity and productivity. Here, we demonstrate new animal-bacterial symbioses fueled by methane, between two undescribed species of annelid (a serpulidLaminatubusand sabellidBispira) and distinct methane-oxidizing Methylococcales bacteria. Worm tissue δ13C of −44‰ to −58‰ suggested methane-fueled nutrition for both species and shipboard experiments revealed active assimilation of13C-labelled CH4into animal biomass, occurring via engulfment of methanotrophic bacteria across the host epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria, and further explain their enigmatic mass occurrence at 150-million-year-old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep-sea, and by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.

Cold-water corals (CWCs) are important foundation species in the world's largest ecosystem, the deep sea. They support a rich faunal diversity but are threatened by climate change and increased ocean acidification. As part of this study, fragments from three genetically distinct Lophelia pertusa colonies were subjected to ambient pH (pH = 7.9) and low pH (pH = 7.6) for six months. RNA was sampled at two, 4.5, and 8.5 weeks and sequenced. The colony from which the fragments were sampled explained most of the variance in expression patterns, but a general pattern emerged where upregulation of ion transport, required to maintain normal function and calcification, was coincident with lowered expression of genes involved in metabolic processes; RNA regulation and processing in particular. Furthermore, there was no differential expression of carbonic anhydrase detected in any analyses, which agrees with a previously described lack of response in enzyme activity in the same corals. However, one colony was able to maintain calcification longer than the other colonies when exposed to low pH and showed increased expression of ion transport genes including proton transport and expression of genes associated with formation of microtubules and the organic matrix, suggesting that certain genotypes may be better equipped to cope with ocean acidification in the future. While these genotypes exist in the contemporary gene pool, further stresses would reduce the genetic variability of the species, which would have repercussions for the maintenance of existing populations and the ecosystem as a whole.

While ocean acidification is a global issue, the severity of ecosystem effects is likely to vary considerably at regional scales. The lack of understanding of how biogeographically separated populations will respond to acidification hampers our ability to predict the future of vital ecosystems. Cold-water corals are important drivers of biodiversity in ocean basins across the world and are considered one of the most vulnerable ecosystems to ocean acidification. We tested the short-term physiological response of the cold-water coral Lophelia pertusa to three pH treatments (pH = 7.9, 7.75 and 7.6) for Gulf of Mexico (USA) and Tisler Reef (Norway) populations, and found that reductions in seawater pH elicited contrasting responses. Gulf of Mexico corals exhibited reductions in net calcification, respiration and prey capture rates with decreasing pH. In contrast, Tisler Reef corals showed only slight reductions in net calcification rates under decreased pH conditions while significantly elevating respiration and capture rates. These differences are likely the result of environmental differences (depth, pH, food supply) between the two regions, invoking the potential for local adaptation or acclimatization to alter their response to global change. However, it is also possible that variations in the methodology used in the experiments contributed to the observed differences. Regardless, these results provide insights into the resilience of L. pertusa to ocean acidification as well as the potential influence of regional differences on the viability of species in future oceans.

Cold-water corals serve as important foundation species by building complex habitat within deep-sea benthic communities. Little is known about the stress response of these foundation species yet they are increasingly exposed to anthropogenic disturbance as human industrial presence expands further into the deep sea. A recent prominent example is the Deepwater Horizon oil-spill disaster and ensuing clean-up efforts that employed chemical dispersants. This study examined the effects of bulk oil–water mixtures, water-accommodated oil fractions, the dispersant Corexit 9500A ® , and the combination of hydrocarbons and dispersants on three species of corals living near the spill site in the Gulf of Mexico between 500 and 1100 m depths: Paramuricea type B3, Callogorgia delta and Leiopathes glaberrima . Following short-term toxicological assays (0–96 h), all three coral species examined showed more severe health declines in response to dispersant alone (2.3–3.4 fold) and the oil–dispersant mixtures (1.1–4.4 fold) than in the oil-only treatments. Higher concentrations of dispersant alone and the oil–dispersant mixtures resulted in more severe health declines. C. delta exhibited somewhat less severe health declines than the other two species in response to oil and oil/dispersant mixture treatments, likely related to its increased abundance near natural hydrocarbon seeps. These experiments provide direct evidence for the toxicity of both oil and dispersant on deep-water corals, which should be taken into consideration in the development of strategies for intervention in future oil spills.

The global decrease in seawater pH known as ocean acidification has important ecological consequences and is an imminent threat for numerous marine organisms. Even though the deep sea is generally considered to be a stable environment, it can be dynamic and vulnerable to anthropogenic disturbances including increasing temperature, deoxygenation, ocean acidification and pollution. Lophelia pertusa is among the better-studied cold-water corals but was only recently documented along the US West Coast, growing in acidified conditions. In the present study, coral fragments were collected at ∼300 m depth along the southern California margin and kept in recirculating tanks simulating conditions normally found in the natural environment for this species. At the collection site, waters exhibited persistently low pH and aragonite saturation states (Ωarag) with average values for pH of 7.66 ± 0.01 and Ωarag of 0.81 ± 0.07. In the laboratory, fragments were grown for three weeks in “favorable” pH/Ωarag of 7.9/1.47 (aragonite saturated) and “unfavorable” pH/Ωarag of 7.6/0.84 (aragonite undersaturated) conditions. There was a highly significant treatment effect (P −1 and net dissolution of −0.010 ± 0.014% d-1 for unfavorable conditions. We did not find any treatment effect on feeding rates, which suggests that corals did not depress feeding in low pH/ Ωarag in an attempt to conserve energy. However, these results suggest that the suboptimal conditions for L. pertusa from the California margin could potentially threaten the persistence of this cold-water coral with negative consequences for the future stability of this already fragile ecosystem.

The deep sea is home to many species that have longer life spans than their shallow-water counterparts. This trend is primarily related to the decline in metabolic rates with temperature as depth increases. However, at bathyal depths, the cold-seep vestimentiferan tubeworm species Lamellibrachia luymesi and Seepiophila jonesi reach extremely old ages beyond what is predicted by the simple scaling of life span with body size and temperature. Here, we use individual-based models based on in situ growth rates to show that another species of cold-seep tubeworm found in the Gulf of Mexico, Escarpia laminata, also has an extraordinarily long life span, regularly achieving ages of 100-200 years with some individuals older than 300 years. The distribution of results from individual simulations as well as whole population simulations involving mortality and recruitment rates support these age estimates. The low 0.67% mortality rate measurements from collected populations of E. laminata are similar to mortality rates in L. luymesi and S. jonesi and play a role in evolution of the long life span of cold-seep tubeworms. These results support longevity theory, which states that in the absence of extrinsic mortality threats, natural selection will select for individuals that senesce slower and reproduce continually into their old age.

Ocean acidification, the decrease in seawater pH due to the absorption of atmospheric CO2, profoundly threatens the survival of a large number of marine species. Cold-water corals are considered to be among the most vulnerable organisms to ocean acidification because they are already exposed to relatively low pH and corresponding low calcium carbonate saturation states (Ω). Lophelia pertusa is a globally distributed cold-water scleractinian coral that provides critical three-dimensional habitat for many ecologically and economically significant species. In this study, four different genotypes of L. pertusa were exposed to three pH treatments (pH=7.60, 7.75, and 7.90) over a short (two-week) experimental period, and six genotypes were exposed to two pH treatments (pH=7.60, and 7.90) over a long (six-month) experimental period. Their physiological response was measured as net calcification rate and the activity of carbonic anhydrase, a key enzyme in the calcification pathway. In the short-term experiment, net calcification rates did not significantly change with pH, although they were highly variable in the low pH treatment, including some genotypes that maintained positive net calcification in undersaturated conditions. In the six-month experiment, average net calcification was significantly reduced at low pH, with corals exhibiting net dissolution of skeleton. However, one of the same genotypes that maintained positive net calcification (+0.04% day-1) under the low pH treatment in the short-term experiment also maintained positive net calcification longer than the other genotypes in the long-term experiment, although none of the corals maintained positive calcification for the entire 6 months. Average carbonic anhydrase activity was not affected by pH, although some genotypes exhibited small, insignificant, increases in activity after the sixth month. Our results suggest that while net calcification in L. pertusa is adversely affected by ocean acidification in the long term, it is possible that some genotypes may prove to be more resilient than others, particularly to short perturbations of the carbonate system. These results provide evidence that populations of L. pertusa in the Gulf of Mexico may contain the genetic variability necessary to support an adaptive response to future ocean acidification.

Here, the development and construction of recirculating aquaria for the long-term maintenance and study of deep-water corals in the laboratory is described. This system may be applied to the maintenance and experimentation on marine organisms in the absence of a natural seawater supply. Since 2009, numerous colonies of Lophelia pertusa as well as several species of associated invertebrates from the Gulf of Mexico have been maintained in the described systems. The behavior of some of these species, including L. pertusa, the corallivorous snail Coralliophila sp., the polychaete Eunice sp., and the galetheoid crab Eumunida picta in the laboratory is described. Additionally, these systems were used for the manipulation of pH and dissolved oxygen for short-term experiments using L. pertusa. The detailed manipulation of carbonate chemistry in artificial seawater is described for use in ocean acidification experiments.

Species in the genus Paramuricea are among the most common corals in deep waters (>200 m) of the Gulf of Mexico. Paramuricea spp. increase habitat heterogeneity and provide substrate for numerous faunal associates, including ophiuroids that occur on the majority of coral colonies. In light of the Deepwater Horizon oil spill in the Gulf of Mexico, it has become apparent that there is a critical need for data on population dynamics within this genus. To date, at least one species of Paramuricea (P. biscaya) is known to be negatively impacted by the spill. Using remotely operated vehicles from 2009 to 2011, we documented the density and size frequency distributions of Paramuricea across 21 sites at depths of 250–2500 m. Molecular barcoding (mtCOI+igr+MutS) was used to delineate species boundaries among the specimens collected. Results suggested that seven haplotypes are present in the Gulf, and appear to be partially segregated by depth [(type H

Deep-sea communities are becoming increasingly vulnerable to anthropogenic disturbances, as fishing, hydrocarbon exploration and extraction, and mining activities extend into deeper water. Negative impacts from such activities were recently documented in the Gulf of Mexico (GoM), where the Deepwater Horizon oil spill caused substantial damage to a deep-water octocoral community. Although a faunal checklist and numerous museum records are currently available for the entire GoM, local-scale diversity and assemblage structure of octocoral communities remains unknown, particularly in deep water. On a series of recent cruises (2008–2011) using remotely operated vehicles, 435 octocorals were collected from 33 deep-water sites (250–2500 m) in the northern GoM. To elucidate species boundaries, the extended mitochondrial barcode (COI+igr1+msh) was successfully amplified and sequenced for 422 of these specimens, yielding a total of 64 haplotypes representing at least 52 species. Further, at least 29% of the species collected were either previously not known to occur in the GoM (12 species) or represent new species (at least three species). Overall, species richness at each site was fairly low (1–12 spp.). The greatest species richness occurred at the shallowest (

The industrialization of the deep sea is expanding world wide. Increasing oil and gas exploration activities in the absence of sufficient baseline data in deep-sea ecosystems has made environmental management challenging. Here, we review the types of activities that are associated with global offshore oil and gas development in water depths over 200 m, the typical impacts of these activities, some of the more extreme impacts of accidental oil and gas releases, and the current state of management in the major regions of offshore industrial activity including 18 exclusive economic zones. Direct impacts of infrastructure installation, including sediment resuspension and burial by seafloor anchors and pipelines, are typically restricted to a radius of ∼100 m on from the installation on the seafloor. Discharges of water-based and low toxicity oil based drilling muds and produced water can extend over 2 km, while the ecological impacts at the population and community levels on the sea floor are most commonly on the order of 200–300 m from their source. These impacts may persist in the deep sea for many years and likely longer for its more fragile ecosystems, such as cold-water corals. This synthesis of information provides the basis for a series of recommendations for the management of offshore oil and gas development. An effective management strategy, aimed at minimizing risk of significant environmental harm, will typically encompass regulations of the activity itself (e.g., discharge practices, materials used), combined with spatial (e.g., avoidance rules and marine protected areas), and temporal measures (e.g., restricted activities during peak reproductive periods). Spatial management measures that encompass representatives of all of the regional deep-sea community types is important in this context. Implementation of these management strategies should consider minimum buffer zones to displace industrial activity beyond the range of typical impacts: at least 2 km from any discharge points and surface infrastructure and 200 m from seafloor infrastructure with no expected discharges. Although managing natural resources is, arguably, more challenging in deep-water environments, inclusion of these proven conservation tools contributes to robust environmental management strategies for oil and gas extraction in the deep sea.

The ecological and evolutionary processes that interact to shape community structure are poorly studied in the largest environment on earth, the deep sea. Phylogenetic data and morphological traits of octocorals were coupled with environmental factors to test hypotheses of community assembly in the deep (250-2500 m) Gulf of Mexico. We found lineage turnover at a depth of 800-1200 m, with isidids and chrysogorgiids at deeper depths and a diversity of species from across the phylogeny occupying shallower depths. Traits, including axis type, polyp shape, and polyp retraction, differed among species occupying the shallowest (250-800 m) and deepest (1200-2500 m) depths. Results also indicated that octocoral species sort along an environmental gradient of depth. Closely related octocoral species sorted into different depth strata on the upper to middle slope, likely due to barriers imposed by water masses followed by adaptive divergence. Within any given depth zone down to 2000 m, the phylogenetic relatedness of co-existing octocorals was random, indicating that stochastic processes, such as recruitment, also shape community structure. At depths >2000 m, octocorals were more closely related than expected by chance due to the diversification of chrysogorgiids and isidids, which retain conserved traits that impart survival at deeper and/or colder depths. Polyp density, size, and inter-polyp distance were significantly correlated with depth, particularly in plexaurids and isidids, highlighting trait lability across depth and supporting that environmental gradients influence octocoral morphology. Our community phylogenetics approach indicates that both environmental filtering and neutral processes shape community assembly in the deep sea.

Lamellibrachia luymesi is a long-lived vestimentiferan polychaete that produces biogenic habitat at hydrocarbon seeps on the upper Louisiana slope of the Gulf of Mexico. Lamellibrachia luymesi relies on endosymbiotic, chemoautotrophic bacteria for nutrition which are supplied with hydrogen sulphide acquired from seep sediments by the tube worms. In this study, an individual-based model is developed for L. luymesi aggregations. The results show that aggregations can persist for centuries because of extremely low mortality rates. Recruitment patterns reflect intraspecific competition for settlement space, with the recruitment period estimated between 11 and 68 years. Substantial hydrogen sulphide requirements are estimated for large aggregations of L. luymesi, exceeding 30 mmol h−1. In addition to modifying habitat through physical structure, L. luymesi may be considered to be an ecosystem engineer because of its profound effect on the chemical environment at hydrocarbon seep sites.

On April 20, 2010, the Deepwater Horizon (DWH) blowout occurred, releasing more oil than any accidental spill in history. Oil release continued for 87 d and much of the oil and gas remained in, or returned to, the deep sea. A coral community significantly impacted by the spill was discovered in late 2010 at 1,370 m depth. Here we describe the discovery of five previously unknown coral communities near the Macondo wellhead and show that at least two additional coral communities were impacted by the spill. Although the oil-containing flocullent material that was present on corals when the first impacted community was discovered was largely gone, a characteristic patchy covering of hydrozoans on dead portions of the skeleton allowed recognition of impacted colonies at the more recently discovered sites. One of these communities was 6 km south of the Macondo wellhead and over 90% of the corals present showed the characteristic signs of recent impact. The other community, 22 km southeast of the wellhead between 1,850 and 1,950 m depth, was more lightly impacted. However, the discovery of this site considerably extends the distance from Macondo and depth range of significant impact to benthic macrofaunal communities. We also show that most known deep-water coral communities in the Gulf of Mexico do not appear to have been acutely impacted by the spill, although two of the newly discovered communities near the wellhead apparently not impacted by the spill have been impacted by deep-sea fishing operations.

Environmental variables that are correlated with depth have been suggested to be among the major forces underlying speciation in the deep sea. This study incorporated phylogenetics and ecological niche models (ENM) to examine whether congeneric species of Callogorgia (Octocorallia: Primnoidae) occupy different ecological niches across the continental slope of the Gulf of Mexico (GoM) and whether this niche divergence could be important in the evolution of these closely related species. Callogorgia americana americana, Callogorgia americana delta and Callogorgia gracilis were documented at 13 sites in the GoM (250-1000 m) from specimen collections and extensive video observations. On a first order, these species were separated by depth, with C. gracilis occurring at the shallowest sites, C. a. americana at mid-depths and C. a. delta at the deepest sites. Callogorgia a. delta was associated with areas of increased seep activity, whereas C. gracilis and C. a. americana were associated with narrow, yet warmer, temperature ranges and did not occur near cold seeps. ENM background and identity tests revealed little to no overlap in ecological niches between species. Temporal calibration of the phylogeny revealed the formation of the Isthmus of Panama was a vicariance event that may explain some of the patterns of speciation within this genus. These results elucidate the potential mechanisms for speciation in the deep sea, emphasizing both bathymetric speciation and vicariance events in the evolution of a genus across multiple regions.

Baker, Maria C. ... et al.

The United Nations Decade of Ocean Science for Sustainable Development presents an exceptional opportunity to effect positive change in ocean use. We outline what is required of the deep-sea research community to achieve these ambitious objectives. The health of the global ocean, on which society depends, is in decline. The importance of sustainable use to ocean health has long been recognized1, yet the United Nations (UN) First World Ocean Assessment2 from 2017 highlighted increasing ocean pressures from accelerated expansion of human activities, including climate change. These pressures affect all ocean regions, from the coast to the deep sea3. In response to this concern, and to align with several international policy commitments, the UN General Assembly proclaimed 2021–2030 the Decade of Ocean Science for Sustainable Development4. The roadmap for this Ocean Decade recognizes the deep sea as a frontier of science and discovery, and calls for research to advance understanding of deep-sea ecosystems, their functions, vulnerabilities and services to society. Published in March 2020, the draft implementation plan for the Ocean Decade guides the design and implementation of ‘Actions’ that underpin the desired move from ‘the ocean we have’ to ‘the ocean we want’ (Fig. 1). The draft plan calls on the scientific community to develop Actions, at programme, project, activity or contribution levels, to help deliver on four key objectives: (1) increase capacity to generate, understand, manage and use ocean knowledge; (2) identify and generate required ocean data, information and knowledge; (3) build comprehensive understanding of the ocean and its governance systems; and (4) increase the use of ocean knowledge.