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Methane seeps harbor uncharacterized animal–microbe symbioses with unique nutritional strategies. Three undescribed sea spider species (family Ammotheidae; genusSericosura) endemic to methane seeps were found along the eastern Pacific margin, from California to Alaska, hosting diverse methane- and methanol-oxidizing bacteria on their exoskeleton. δ¹³C tissue isotope values of in situ specimens corroborated methane assimilation (−45‰, on average). Live animal incubations with¹³C-labeled methane and methanol, followed by nanoscale secondary ion mass spectrometry, confirmed that carbon derived from both compounds was actively incorporated into the tissues within five days. Methano- and methylotrophs of the bacterial families Methylomonadaceae, Methylophagaceae and Methylophilaceae were abundant, based on environmental metagenomics and 16S rRNA sequencing, and fluorescence and electron microscopy confirmed dense epibiont aggregations on the sea spider exoskeleton. Egg sacs carried by the males hosted identical microbes suggesting vertical transmission. We propose that these sea spiders farm and feed on methanotrophic and methylotrophic bacteria, expanding the realm of animals known to harness C1 compounds as a carbon source. These findings advance our understanding of the biology of an understudied animal lineage, unlocking some of the unique nutritional links between the microbial and faunal food webs in the oceans. 

Methane seeps are highly productive ecosystems that provide carbon sequestration services, host diverse communities including endemic species, and serve as habitats for commercial fisheries. Little is known about the economic value the public places on them. Discrete Choice Experiments (DCEs) are administered to a sample of Costa Rican taxpayers to evaluate their willingness to pay (WTP) in monetary terms using tradeoffs made in a survey context involving three of the main attributes of methane seep ecosystems to provide insights for future conservation and management efforts. Extensive effort is devoted to understanding how Costa Ricans view different aspects of the deep sea. We find that they associate it with strange animals, natural resources, the unknown, and being far from reach. Perhaps surprisingly, they underestimate how much they know about the deep sea. We find that WTP for methane seep protection is the highest for programs that protect seeps with endemic species, followed by seeps with high climate change mitigation potential and commercial fishing habitat. Higher-income groups and women are more likely to prefer options that increase the current level of protection. We discuss how science communication and community engagement contribute to care expressed toward the deep sea. 

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 mtypes 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. 

The methane seeps on the Pacific margin of Costa Rica support extensive animal diversity and offer insights into deep-sea biogeography. During five expeditions between 2009 and 2019, we conducted intensive faunal sampling via 63 submersible dives to 11 localities at depths of 300–3600 m. Based on these expeditions and published literature, we compiled voucher specimens, images, and 274 newly published DNA sequences to present a taxonomic inventory of macrofaunal and megafaunal diversity with a focus on invertebrates. In total 488 morphospecies were identified, representing the highest number of distinct morphospecies published from a single seep or vent region to date. Of these, 131 are described species, at least 58 are undescribed species, and the remainder include some degree of taxonomic uncertainty, likely representing additional undescribed species. Of the described species, 38 are known only from the Costa Rica seeps and their vicinity. Fifteen range extensions are also reported for species known from Mexico, the Galápagos seamounts, Chile, and the western Pacific; as well as 16 new depth records and three new seep records for species known to occur at vents or organic falls. No single evolutionary narrative explains the patterns of biodiversity at these seeps, as even morphologically indistinguishable species can show different biogeographic affinities, biogeographic ranges, or depth ranges. The value of careful molecular taxonomy and comprehensive specimen-based regional inventories is emphasized for biodiversity research and monitoring. 

Abstract. Anthropogenic warming and nutrient over-enrichment of our oceans have resulted in significant, and often catastrophic, reductions in dissolved oxygen (deoxygenation). Stress on water-breathing animals from this deoxygenation has been shown to occur at all levels of biological organization: cellular, organ, individual, species, population, community, and ecosystem. Most climate forecasts predict increases in ocean deoxygenation; thus, it is essential to develop reliable biological indicators of low-oxygen stress that can be used by regional and global oxygen monitoring efforts to detect and assess the impacts of deoxygenation on ocean life. This review focuses on responses to low-oxygen stress that are manifest at different levels of biological organization and at a variety of spatial and temporal scales. We compare particular attributes of these biological indicators to the dissolved oxygen threshold of response, timescales of response, sensitive life stages and taxa, and the ability to scale the response to oxygen stress across levels of organization. Where there is available evidence, we discuss the interactions of other biological and abiotic stressors on the biological indicators of low-oxygen stress. We address the utility, confounding effects, and implementation of the biological indicators of oxygen stress for research and societal applications. Our hope is that further refinement and dissemination of these oxygen stress indicators will provide more direct support for environmental managers, fisheries and mariculture scientists, conservation professionals, and policymakers to confront the challenges of ocean deoxygenation. An improved understanding of the sensitivity of different ocean species, communities, and ecosystems to low-oxygen stress will empower efforts to design monitoring programs, assess ecosystem health, develop management guidelines, track conditions, and detect low-oxygen events. 

IntroductionA defining aspect of the Intergovernmental Panel on Climate Change (IPCC) assessment reports (AR) is a formal uncertainty language framework that emphasizes higher certainty issues across the reports, especially in the executive summaries and short summaries for policymakers. As a result, potentially significant risks involving understudied components of the climate system are shielded from view. MethodsHere we seek to address this in the latest, sixth assessment report (AR6) for one such component—the deep ocean—by summarizing major uncertainties (based on discussions of low confidence issues or gaps) regarding its role in our changing climate system. The goal is to identify key research priorities to improve IPCC confidence levels in deep ocean systems and facilitate the dissemination of IPCC results regarding potentially high impact deep ocean processes to decision-makers. This will accelerate improvement of global climate projections and aid in informing efforts to mitigate climate change impacts. An analysis of 3,000 pages across the six selected AR6 reports revealed 219 major science gaps related to the deep ocean. These were categorized by climate stressor and nature of impacts. ResultsHalf of these are biological science gaps, primarily surrounding our understanding of changes in ocean ecosystems, fisheries, and primary productivity. The remaining science gaps are related to uncertainties in the physical (32%) and biogeochemical (15%) ocean states and processes. Model deficiencies are the leading cited cause of low certainty in the physical ocean and ice states, whereas causes of biological uncertainties are most often attributed to limited studies and observations or conflicting results. DiscussionKey areas for coordinated effort within the deep ocean observing and modeling community have emerged, which will improve confidence in the deep ocean state and its ongoing changes for the next assessment report. This list of key “known unknowns” includes meridional overturning circulation, ocean deoxygenation and acidification, primary production, food supply and the ocean carbon cycle, climate change impacts on ocean ecosystems and fisheries, and ocean-based climate interventions. From these findings, we offer recommendations for AR7 to avoid omitting low confidence-high risk changes in the climate system. 

The deep sea (below 200 m depth) is the largest carbon sink on Earth. It hosts abundant biodiversity that underpins the carbon cycle and provides provisioning, supporting, regulating and cultural ecosystem services. There is growing attention to climate-regulating ocean ecosystem services from the scientific, business and political sectors. In this essay we synthesize the unique biophysical, socioeconomic and governance characteristics of the deep sea to critically assess opportunities for deep-sea blue carbon to mitigate climate change. Deep-sea blue carbon consists of carbon fluxes and storage including carbon transferred from the atmosphere by the inorganic and organic carbon pumps to deep water, carbon sequestered in the skeletons and bodies of deep-sea organisms, carbon buried within sediments or captured in carbonate rock. However, mitigating climate change through deep-sea blue carbon enhancement suffers from lack of scientific knowledge and verification, technological limitations, potential environmental impacts, a lack of cooperation and collaboration, and underdeveloped governance. Together, these issues suggest that deep-sea climate change mitigation is limited. Thus, we suggest that a strong focus on blue carbon is too limited a framework for managing the deep sea to contribute to international goals, including the Sustainable Development Goals (SDGs), the Paris Agreement and the post-2020 Biodiversity Goals. Instead, the deep sea can be viewed as a more holistic nature-based solution, including many ecosystem services and biodiversity in addition to climate. Environmental impact assessments (EIAs), area-based management, pollution reduction, moratoria, carbon accounting and fisheries management are tools in international treaties that could help realize benefits from deep-sea, nature-based solutions. 

Organisms 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 umol kg-1 at 15.3 7C) 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.