Microbes as marine habitat formers and ecosystem engineers.

Despite their small individual size, marine prokaryotic and eukaryotic microbes can form large 3D structures and complex habitats. These habitats contribute to seafloor heterogeneity, facilitating colonization by animals and protists. They also provide food and refuge for a variety of species and promote novel ecological interactions. Here we illustrate the role of microbes as ecosystem engineers and propose a classification based on five types of habitat: microbial mats, microbial forests, microbial-mineralized habitats, microbial outcrops and microbial nodules. We also describe the metabolic processes of microbial habitat formers and their ecological roles, highlighting current gaps in knowledge. Their biogeography indicates that these habitats are widespread in all oceans and are continuously being discovered across latitudes and depths. These habitats are also expected to expand under future global change owing to their ability to exploit extreme environmental conditions. Given their high ecological relevance and their role in supporting endemic species and high biodiversity levels, microbial habitats should be included in future spatial planning, conservation and management measures.

Waste barrel contamination and macrobenthic communities in the San Pedro Basin DDT dumpsite.

Industrial waste barrels were discarded from 1947 to 1961 at a DDT dumpsite in the San Pedro Basin (SPB) in southern California, USA at ~890 m. The barrels were studied for effects on sediment concentrations of DDX, PCBs, PAHs and sediment properties, and on benthic macrofaunal assemblages, including metazoan meiofaunal taxa >0.3 mm. DDX concentration was highest in the 2-6 cm fraction of the 10-cm deep cores studied but exhibited no correlation with macrofaunal density, composition or diversity. Macrofaunal diversity was lowest and distinct in sediments within discolored halos surrounding the barrels. Low macrobenthos density and diversity, high dominance by Entoprocta, and numerical prevalence of large nematodes may result from the very low oxygen concentrations in bottom waters (< 4.4 µM). There is potential for macrofauna to remobilize DDX into the water column and ultimately the food web in the SPB.

Towards a scientific community consensus on designating Vulnerable Marine Ecosystems from imagery.

Management of deep-sea fisheries in areas beyond national jurisdiction by Regional Fisheries Management Organizations/Arrangements (RFMO/As) requires identification of areas with Vulnerable Marine Ecosystems (VMEs). Currently, fisheries data, including trawl and longline bycatch data, are used by many RFMO/As to inform the identification of VMEs. However, the collection of such data creates impacts and there is a need to collect non-invasive data for VME identification and monitoring purposes. Imagery data from scientific surveys satisfies this requirement, but there currently is no established framework for identifying VMEs from images. Thus, the goal of this study was to bring together a large international team to determine current VME assessment protocols and establish preliminary global consensus guidelines for identifying VMEs from images. An initial assessment showed a lack of consistency among RFMO/A regions regarding what is considered a VME indicator taxon, and hence variability in how VMEs might be defined. In certain cases, experts agreed that a VME could be identified from a single image, most often in areas of scleractinian reefs, dense octocoral gardens, multiple VME species' co-occurrence, and chemosynthetic ecosystems. A decision flow chart is presented that gives practical interpretation of the FAO criteria for single images. To further evaluate steps of the flow chart related to density, data were compiled to assess whether scientists perceived similar density thresholds across regions. The range of observed densities and the density values considered to be VMEs varied considerably by taxon, but in many cases, there was a statistical difference in what experts considered to be a VME compared to images not considered a VME. Further work is required to develop an areal extent index, to include a measure of confidence, and to increase our understanding of what levels of density and diversity correspond to key ecosystem functions for VME indicator taxa. Based on our results, the following recommendations are made: 1. There is a need to establish a global consensus on which taxa are VME indicators. 2. RFMO/As should consider adopting guidelines that use imagery surveys as an alternative (or complement) to using bycatch and trawl surveys for designating VMEs. 3. Imagery surveys should also be included in Impact Assessments. And 4. All industries that impact the seafloor, not just fisheries, should use imagery surveys to detect and identify VMEs.

Wide-Area Debris Field and Seabed Characterization of a Deep Ocean Dump Site Surveyed by Autonomous Underwater Vehicles.

Disposal of industrial and hazardous waste in the ocean was a pervasive global practice in the 20th century. Uncertainty in the quantity, location, and contents of dumped materials underscores ongoing risks to marine ecosystems and human health. This study presents an analysis of a wide-area side-scan sonar survey conducted with autonomous underwater vehicles (AUVs) at a dump site in the San Pedro Basin, California. Previous camera surveys located 60 barrels and other debris. Sediment analysis in the region showed varying concentrations of the insecticidal chemical dichlorodiphenyltrichloroethane (DDT), of which an estimated 350-700 t were discarded in the San Pedro Basin between 1947 and 1961. A lack of primary historical documents specifying DDT acid waste disposal methods has contributed to the ambiguity surrounding whether dumping occurred via bulk discharge or containerized units. Barrels and debris observed during previous surveys were used for ground truth classification algorithms based on size and acoustic intensity characteristics. Image and signal processing techniques identified over 74,000 debris targets within the survey region. Statistical, spectral, and machine learning methods characterize seabed variability and classify bottom-type. These analytical techniques combined with AUV capabilities provide a framework for efficient mapping and characterization of uncharted deep-water disposal sites.

Deep-sea impacts of climate interventions.

Ocean manipulation to mitigate climate change may harm deep-sea ecosystems.

Reduced Oxygen Impairs Photobehavior in Marine Invertebrate Larvae.

AbstractOrganisms in coastal waters experience naturally high oxygen variability and steep oxygen gradients with depth, in addition to ocean deoxygenation. They often undergo diel vertical migration involving a change in irradiance that initiates a visual behavior. Retinal function has been shown to be highly sensitive to oxygen loss; here we assess whether visual behavior (photobehavior) in paralarvae of the squid Doryteuthis opalescens and the octopus Octopus bimaculatus is affected by low oxygen conditions, using a novel behavioral paradigm. Larvae showed an irradiance-dependent, descending photobehavior after extinction of the light stimulus, measured through the change in vertical position of larvae in the chamber. The magnitude of photobehavior was decreased as oxygen was reduced, and the response was entirely gone at <6.4 kPa partial pressure of oxygen (<74.7 µmol kg-1 at 15.3 °C) in D. opalescens paralarvae. Oxygen also affected photobehavior in O. bimaculatus paralarvae. The mean vertical velocity of paralarvae was unaffected by exposure to reduced oxygen, indicating that oxygen deficits selectively affect vision prior to locomotion. These findings suggest that variable and declining oxygen conditions in coastal upwelling areas and elsewhere will impair photobehavior and likely affect the distribution, migration behavior, and survival of highly visual marine species.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

Using deep-sea images to examine ecosystem services associated with methane seeps.

Deep-sea images are routinely collected during at-sea expeditions and represent a repository of under-utilized knowledge. We leveraged dive videos collected by the remotely-operated vehicle Hercules (deployed from E/V Nautilus, operated by the Ocean Exploration Trust), and adapted biological trait analysis, to develop an approach that characterizes ecosystem services. Specifically, fisheries and climate-regulating services related to carbon are assessed for three southern California methane seeps: Point Dume (∼725 m), Palos Verdes (∼506 m), and Del Mar (∼1023 m). Our results enable qualitative intra-site comparisons that suggest seep activity influences ecosystem services differentially among sites, and site-to-site comparisons that suggest the Del Mar site provides the highest relative contributions to fisheries and carbon services. This study represents a first step towards ecosystem services characterization and quantification using deep-sea images. The results presented herein are foundational, and continued development should help guide research and management priorities by identifying potential sources of ecosystem services.

Does substrate matter in the deep sea? A comparison of bone, wood, and carbonate rock colonizers.

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.

Actions to halt biodiversity loss generally benefit the climate.

The two most urgent and interlinked environmental challenges humanity faces are climate change and biodiversity loss. We are entering a pivotal decade for both the international biodiversity and climate change agendas with the sharpening of ambitious strategies and targets by the Convention on Biological Diversity and the United Nations Framework Convention on Climate Change. Within their respective Conventions, the biodiversity and climate interlinked challenges have largely been addressed separately. There is evidence that conservation actions that halt, slow or reverse biodiversity loss can simultaneously slow anthropogenic mediated climate change significantly. This review highlights conservation actions which have the largest potential for mitigation of climate change. We note that conservation actions have mainly synergistic benefits and few antagonistic trade-offs with climate change mitigation. Specifically, we identify direct co-benefits in 14 out of the 21 action targets of the draft post-2020 global biodiversity framework of the Convention on Biological Diversity, notwithstanding the many indirect links that can also support both biodiversity conservation and climate change mitigation. These relationships are context and scale-dependent; therefore, we showcase examples of local biodiversity conservation actions that can be incentivized, guided and prioritized by global objectives and targets. The close interlinkages between biodiversity, climate change mitigation, other nature's contributions to people and good quality of life are seldom as integrated as they should be in management and policy. This review aims to re-emphasize the vital relationships between biodiversity conservation actions and climate change mitigation in a timely manner, in support to major Conferences of Parties that are about to negotiate strategic frameworks and international goals for the decades to come.

Scientific and budgetary trade-offs between morphological and molecular methods for deep-sea biodiversity assessment.

Deep-sea biodiversity, a source of critical ecological functions and ecosystem services, is increasingly subject to the threat of disturbance from existing practices (e.g., fishing, waste disposal, oil and gas extraction) as well as emerging industries such as deep-seabed mining. Current scientific tools may not be adequate for monitoring and assessing subsequent changes to biodiversity. In this paper, we evaluate the scientific and budgetary trade-offs associated with morphology-based taxonomy and metabarcoding approaches to biodiversity surveys in the context of nascent deep-seabed mining for polymetallic nodules in the Clarion-Clipperton Zone, the area of most intense interest. For the dominant taxa of benthic meiofauna, we discuss the types of information produced by these methods and use cost-effectiveness analysis to compare their abilities to yield biological and ecological data for use in environmental assessment and management. On the basis of our evaluation, morphology-based taxonomy is less cost-effective than metabarcoding but offers scientific advantages, such as the generation of density, biomass, and size structure data. Approaches that combine the two methods during the environmental assessment phase of commercial activities may facilitate future biodiversity monitoring and assessment for deep-seabed mining and for other activities in remote deep-sea habitats, for which taxonomic data and expertise are limited. Integr Environ Assess Manag 2022;18:655-663. © 2021 SETAC.

Bright spots as climate-smart marine spatial planning tools for conservation and blue growth.

Marine spatial planning that addresses ocean climate-driven change ('climate-smart MSP') is a global aspiration to support economic growth, food security and ecosystem sustainability. Ocean climate change ('CC') modelling may become a key decision-support tool for MSP, but traditional modelling analysis and communication challenges prevent their broad uptake. We employed MSP-specific ocean climate modelling analyses to inform a real-life MSP process; addressing how nature conservation and fisheries could be adapted to CC. We found that the currently planned distribution of these activities may become unsustainable during the policy's implementation due to CC, leading to a shortfall in its sustainability and blue growth targets. Significant, climate-driven ecosystem-level shifts in ocean components underpinning designated sites and fishing activity were estimated, reflecting different magnitudes of shifts in benthic versus pelagic, and inshore versus offshore habitats. Supporting adaptation, we then identified: CC refugia (areas where the ecosystem remains within the boundaries of its present state); CC hotspots (where climate drives the ecosystem towards a new state, inconsistent with each sectors' present use distribution); and for the first time, identified bright spots (areas where oceanographic processes drive range expansion opportunities that may support sustainable growth in the medium term). We thus create the means to: identify where sector-relevant ecosystem change is attributable to CC; incorporate resilient delivery of conservation and sustainable ecosystem management aims into MSP; and to harness opportunities for blue growth where they exist. Capturing CC bright spots alongside refugia within protected areas may present important opportunities to meet sustainability targets while helping support the fishing sector in a changing climate. By capitalizing on the natural distribution of climate resilience within ocean ecosystems, such climate-adaptive spatial management strategies could be seen as nature-based solutions to limit the impact of CC on ocean ecosystems and dependent blue economy sectors, paving the way for climate-smart MSP.

Relationships between biodiversity and ecosystem functioning proxies strengthen when approaching chemosynthetic deep-sea methane seeps.

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.

Impacts of hypoxic events surpass those of future ocean warming and acidification.

Over the past decades, three major challenges to marine life have emerged as a consequence of anthropogenic emissions: ocean warming, acidification and oxygen loss. While most experimental research has targeted the first two stressors, the last remains comparatively neglected. Here, we implemented sequential hierarchical mixed-model meta-analyses (721 control-treatment comparisons) to compare the impacts of oxygen conditions associated with the current and continuously intensifying hypoxic events (1-3.5 O2 mg l-1) with those experimentally yielded by ocean warming (+4 °C) and acidification (-0.4 units) conditions on the basis of IPCC projections (RCP 8.5) for 2100. In contrast to warming and acidification, hypoxic events elicited consistent negative effects relative to control biological performance-survival (-33%), abundance (-65%), development (-51%), metabolism (-33%), growth (-24%) and reproduction (-39%)-across the taxonomic groups (mollusks, crustaceans and fish), ontogenetic stages and climate regions studied. Our findings call for a refocus of global change experimental studies, integrating oxygen concentration drivers as a key factor of ocean change. Given potential combined effects, multistressor designs including gradual and extreme changes are further warranted to fully disclose the future impacts of ocean oxygen loss, warming and acidification.

Deep-Sea Misconceptions Cause Underestimation of Seabed-Mining Impacts.

Scientific misconceptions are likely leading to miscalculations of the environmental impacts of deep-seabed mining. These result from underestimating mining footprints relative to habitats targeted and poor understanding of the sensitivity, biodiversity, and dynamics of deep-sea ecosystems. Addressing these misconceptions and knowledge gaps is needed for effective management of deep-seabed mining.

Climate change considerations are fundamental to management of deep-sea resource extraction.

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.

Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage.

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.