Carbonate compensation depth drives abyssal biogeography in the northeast Pacific.

Abyssal seafloor communities cover more than 60% of Earth's surface. Despite their great size, abyssal plains extend across modest environmental gradients compared to other marine ecosystems. However, little is known about the patterns and processes regulating biodiversity or potentially delimiting biogeographical boundaries at regional scales in the abyss. Improved macroecological understanding of remote abyssal environments is urgent as threats of widespread anthropogenic disturbance grow in the deep ocean. Here, we use a new, basin-scale dataset to show the existence of clear regional zonation in abyssal communities across the 5,000 km span of the Clarion-Clipperton Zone (northeast Pacific), an area targeted for deep-sea mining. We found two pronounced biogeographic provinces, deep and shallow-abyssal, separated by a transition zone between 4,300 and 4,800 m depth. Surprisingly, species richness was maintained across this boundary by phylum-level taxonomic replacements. These regional transitions are probably related to calcium carbonate saturation boundaries as taxa dependent on calcium carbonate structures, such as shelled molluscs, appear restricted to the shallower province. Our results suggest geochemical and climatic forcing on distributions of abyssal populations over large spatial scales and provide a potential paradigm for deep-sea macroecology, opening a new basis for regional-scale biodiversity research and conservation strategies in Earth's largest biome.

First in-situ monitoring of sponge response and recovery to an industrial sedimentation event.

Assessment of risks to seabed habitats from industrial activities is based on the resilience and potential for recovery. Increased sedimentation, a key impact of many offshore industries, results in burial and smothering of benthic organisms. Sponges are particularly vulnerable to increases in suspended and deposited sediment, but response and recovery have not been observed in-situ. We quantified the impact of sedimentation from offshore hydrocarbon drilling over ∼5 days on a lamellate demosponge, and its recovery in-situ over ∼40 days using hourly time-lapse photographs with measurements of backscatter (a proxy of suspended sediment) and current speed. Sediment accumulated on the sponge then cleared largely gradually but occasionally sharply, though it did not return to the initial state. This partial recovery likely involved a combination of active and passive removal. We discuss the use of in-situ observing, which is critical to monitoring impacts in remote habitats, and need for calibration to laboratory conditions.

Making marine image data FAIR.

Underwater images are used to explore and monitor ocean habitats, generating huge datasets with unusual data characteristics that preclude traditional data management strategies. Due to the lack of universally adopted data standards, image data collected from the marine environment are increasing in heterogeneity, preventing objective comparison. The extraction of actionable information thus remains challenging, particularly for researchers not directly involved with the image data collection. Standardized formats and procedures are needed to enable sustainable image analysis and processing tools, as are solutions for image publication in long-term repositories to ascertain reuse of data. The FAIR principles (Findable, Accessible, Interoperable, Reusable) provide a framework for such data management goals. We propose the use of image FAIR Digital Objects (iFDOs) and present an infrastructure environment to create and exploit such FAIR digital objects. We show how these iFDOs can be created, validated, managed and stored, and which data associated with imagery should be curated. The goal is to reduce image management overheads while simultaneously creating visibility for image acquisition and publication efforts.

Benthic megafauna of the western Clarion-Clipperton Zone, Pacific Ocean.

There is a growing interest in the exploitation of deep-sea mineral deposits, particularly on the abyssal seafloor of the central Pacific Clarion-Clipperton Zone (CCZ), which is rich in polymetallic nodules. In order to effectively manage potential exploitation activities, a thorough understanding of the biodiversity, community structure, species ranges, connectivity, and ecosystem functions across a range of scales is needed. The benthic megafauna plays an important role in the functioning of deep-sea ecosystems and represents an important component of the biodiversity. While megafaunal surveys using video and still images have provided insight into CCZ biodiversity, the collection of faunal samples is needed to confirm species identifications to accurately estimate species richness and species ranges, but faunal collections are very rarely carried out. Using a Remotely Operated Vehicle, 55 specimens of benthic megafauna were collected from seamounts and abyssal plains in three Areas of Particular Environmental Interest (APEI 1, APEI 4, and APEI 7) at 3100-5100 m depth in the western CCZ. Using both morphological and molecular evidence, 48 different morphotypes belonging to five phyla were found, only nine referrable to known species, and 39 species potentially new to science. This work highlights the need for detailed taxonomic studies incorporating genetic data, not only within the CCZ, but in other bathyal, abyssal, and hadal regions, as representative genetic reference libraries that could facilitate the generation of species inventories.

Giant, highly diverse protists in the abyssal Pacific: vulnerability to impacts from seabed mining and potential for recovery.

Xenophyophores, giant deep-sea agglutinated foraminifera, dominate the benthic megafauna in the eastern equatorial Pacific Clarion-Clipperton Zone. This abyssal (>4000 m depth) region hosts major deposits of polymetallic nodules targeted for future seabed mining, an activity that would destroy these highly diverse and delicate protists, particularly those living on the nodules themselves. Since the cell occupies only a small proportion of their test volume, xenophyophores may make a fairly modest contribution to benthic biomass and carbon cycling. Nevertheless, xenophyophore tests can passively enhance particle deposition, concentrate food, and provide habitat structure utilized by diverse organisms. Their destruction could therefore influence the recovery of benthic communities. Species requiring nodule substrates will likely not recover, since nodules take millions of years to form. However, xenophyophores can grow quickly and colonize extensive volcanic ash deposits within years, suggesting that sediment-dwelling species could be among the first large immobile organisms to reappear in mining-impacted areas.

Xenophyophores (Rhizaria, Foraminifera), including four new species and two new genera, from the western Clarion-Clipperton Zone (abyssal equatorial Pacific).

The Clarion-Clipperton Zone (CCZ) occupies a vast swathe of the Pacific with extensive polymetallic nodule deposits. Eastern and central parts host diverse assemblages of xenophyophores (megafaunal agglutinated foraminifera). Here we describe xenophyophores obtained using a Remotely Operated Vehicle from the western CCZ. Eleven distinct forms include two known species, Stannophyllum zonarium Haeckel, 1888 and Aschemonella monile Gooday and Holzmann in Gooday et al., 2017b. Another four are described as new species based on morphological and genetic data. In Abyssalia foliformis gen. nov., sp. nov. and Abyssalia sphaerica sp. nov. the flattened or spherical test comprises a homogeneous framework of sponge spicules. Psammina tenuis sp. nov. has a delicate, thin, plate-like test. Moanammina semicircularis gen. nov., sp. nov. has a stalked, fan-shaped test and is genetically identical to 'Galatheammina sp. 6' of Gooday and co-workers from the eastern CCZ. Sequence data revealed a spherical 'mudball', which disintegrated and cannot be formally described, to be a novel xenophyophore. Finally, four morphospecies are represented by dead tests: Psammina spp., Reticulammina sp., and an unknown genus with a unique test structure. This collection enhances our knowledge of Pacific xenophyophore diversity and provides the first genetic confirmation of wide geographic ranges for abyssal species.

Monitoring mosaic biotopes in a marine conservation zone by autonomous underwater vehicle.

The number of marine protected areas (MPAs) has increased dramatically in the last decade and poses a major logistic challenge for conservation practitioners in terms of spatial extent and the multiplicity of habitats and biotopes that now require assessment. Photographic assessment by autonomous underwater vehicle (AUV) enables the consistent description of multiple habitats, in our case including mosaics of rock and sediment. As a case study, we used this method to survey the Greater Haig Fras marine conservation zone (Celtic Sea, northeast Atlantic). We distinguished 7 biotopes, detected statistically significant variations in standing stocks, species density, species diversity, and faunal composition, and identified significant indicator species for each habitat. Our results demonstrate that AUV-based photography can produce robust data for ecological research and practical marine conservation. Standardizing to a minimum number of individuals per sampling unit, rather than to a fixed seafloor area, may be a valuable means of defining an ecologically appropriate sampling unit. Although composite sampling represents a change in standard practice, other users should consider the potential benefits of this approach in conservation studies. It is broadly applicable in the marine environment and has been successfully implemented in deep-sea conservation and environmental impact studies. Without a cost-effective method, applicable across habitats, it will be difficult to further a coherent classification of biotopes or to routinely assess their conservation status in the rapidly expanding global extent of MPAs.

Monitoreo de Mosaicos de Biotopos en una Zona Marina de Conservación por medio de un Vehículo Submarino Autónomo Resumen El número de áreas marinas protegidas (AMP) ha incrementado dramáticamente en la última década y ahora presenta un gran reto logístico para quienes practican la conservación en términos de extensión espacial y la multitud de hábitats y biotopos que ahora requieren ser evaluados. La evaluación fotográfica por medio de vehículos submarinos autónomos (VSA) habilita la descripción constante de múltiples hábitats, y en nuestro caso incluso mosaicos de rocas y sedimento. Como estudio de caso usamos este método para censar la zona marina de conservación de Greater Haig Fras (Mar Celta, noreste del Atlántico). En él distinguimos siete biotopos; detectamos variaciones estadísticamente significativas en el stock permanente, la densidad de especies, la diversidad de especies y la composición faunística; e identificamos especies indicadoras significativas para cada hábitat. Nuestros resultados demuestran que la fotografía basada en VSA puede producir datos sólidos para la investigación ecológica y la conservación marina práctica. La estandarización a un número mínimo de individuos por unidad de muestreo, en lugar de a un área fija del fondo marino, puede ser un recurso valioso para definir una unidad de muestreo ecológicamente adecuada. Aunque el muestreo compuesto representa un cambio en la práctica habitual, otros usuarios deberían considerar los beneficios potenciales de esta estrategia en los estudios de conservación. Este método puede aplicarse de manera generalizada en el ambiente marino y ha sido implementado exitosamente en la conservación y en estudios de impacto ambiental en mares profundos. Si no existe un método rentable, aplicable en todos los hábitats, será difícil avanzar hacia una clasificación coherente de los biotopos o hacia una evaluación rutinaria de su estado de conservación en la extensión mundial de rápida expansión de las AMP.

Megafaunal variation in the abyssal landscape of the Clarion Clipperton Zone.

The potential for imminent polymetallic nodule mining in the Clarion Clipperton Fracture Zone (CCZ) has attracted considerable scientific and public attention. This concern stems from both the extremely large seafloor areas that may be impacted by mining, and the very limited knowledge of the fauna and ecology of this region. The environmental factors regulating seafloor ecology are still very poorly understood. In this study, we focus on megafaunal ecology in the proposed conservation zone 'Area of Particular Environmental Interest 6' (study area centred 17°16'N, 122°55'W). We employ bathymetric data to objectively define three landscape types in the area (a level bottom Flat, an elevated Ridge, a depressed Trough; water depth 3950-4250 m) that are characteristic of the wider CCZ. We use direct seabed sampling to characterise the sedimentary environment in each landscape, detecting no statistically significant differences in particle size distributions or organic matter content. Additional seafloor characteristics and data on both the metazoan and xenophyophore components of the megafauna were derived by extensive photographic survey from an autonomous underwater vehicle. Image data revealed that there were statistically significant differences in seafloor cover by nodules and in the occurrence of other hard substrata habitat between landscapes. Statistically significant differences in megafauna standing stock, functional structuring, diversity, and faunal composition were detected between landscapes. The Flat and Ridge areas exhibited a significantly higher standing stock and a distinct assemblage composition compared to the Trough. Geomorphological variations, presumably regulating local bottom water flows and the occurrence of nodule and xenophyophore test substrata, between study areas may be the mechanism driving these assemblage differences. We also used these data to assess the influence of sampling unit size on the estimation of ecological parameters. We discuss these results in the contexts of regional benthic ecology and the appropriate management of potential mining activities in the CCZ and elsewhere in the deep ocean.

Abyssal deposit-feeding rates consistent with the metabolic theory of ecology.

The Metabolic Theory of Ecology (MTE) posits that metabolic rate controls ecological processes, such as the rate of resource uptake, from the individual- to the ecosystem-scale. Metabolic rate has been found empirically to be an exponential function of whole organism body mass. We test a fundamental assumption of MTE, whether resource uptake scales to metabolism, by examining detritivores accessing a single common resource pool, an ideal study case. We used an existing empirical model of ingestion for aquatic deposit feeders adjusted for temperature to test whether ingestion by abyssal deposit feeders conforms to MTE-predicted feeding rates. We estimated the sediment deposit-feeding rates of large invertebrates from two abyssal study sites using time-lapse photography, and related those rates to body mass, environmental temperature, and sediment organic matter content using this framework. Ingestion was significantly related to individual wet mass, with a mass-scaling coefficient of 0.81, with 95% confidence intervals that encompass the MTE-predicted value of 0.75, and the same pattern determined in other aquatic systems. Our results also provide insight into the potential mechanism through which this fundamental assumption operates. After temperature correction, both deep- and shallow-water taxa might be summarized into a single mass-scaled ingestion rate.

A framework for the development of a global standardised marine taxon reference image database (SMarTaR-ID) to support image-based analyses.

Video and image data are regularly used in the field of benthic ecology to document biodiversity. However, their use is subject to a number of challenges, principally the identification of taxa within the images without associated physical specimens. The challenge of applying traditional taxonomic keys to the identification of fauna from images has led to the development of personal, group, or institution level reference image catalogues of operational taxonomic units (OTUs) or morphospecies. Lack of standardisation among these reference catalogues has led to problems with observer bias and the inability to combine datasets across studies. In addition, lack of a common reference standard is stifling efforts in the application of artificial intelligence to taxon identification. Using the North Atlantic deep sea as a case study, we propose a database structure to facilitate standardisation of morphospecies image catalogues between research groups and support future use in multiple front-end applications. We also propose a framework for coordination of international efforts to develop reference guides for the identification of marine species from images. The proposed structure maps to the Darwin Core standard to allow integration with existing databases. We suggest a management framework where high-level taxonomic groups are curated by a regional team, consisting of both end users and taxonomic experts. We identify a mechanism by which overall quality of data within a common reference guide could be raised over the next decade. Finally, we discuss the role of a common reference standard in advancing marine ecology and supporting sustainable use of this ecosystem.

Resilience of benthic deep-sea fauna to mining activities.

With increasing demand for mineral resources, extraction of polymetallic sulphides at hydrothermal vents, cobalt-rich ferromanganese crusts at seamounts, and polymetallic nodules on abyssal plains may be imminent. Here, we shortly introduce ecosystem characteristics of mining areas, report on recent mining developments, and identify potential stress and disturbances created by mining. We analyze species' potential resistance to future mining and perform meta-analyses on population density and diversity recovery after disturbances most similar to mining: volcanic eruptions at vents, fisheries on seamounts, and experiments that mimic nodule mining on abyssal plains. We report wide variation in recovery rates among taxa, size, and mobility of fauna. While densities and diversities of some taxa can recover to or even exceed pre-disturbance levels, community composition remains affected after decades. The loss of hard substrata or alteration of substrata composition may cause substantial community shifts that persist over geological timescales at mined sites.

Biological responses to disturbance from simulated deep-sea polymetallic nodule mining.

Commercial-scale mining for polymetallic nodules could have a major impact on the deep-sea environment, but the effects of these mining activities on deep-sea ecosystems are very poorly known. The first commercial test mining for polymetallic nodules was carried out in 1970. Since then a number of small-scale commercial test mining or scientific disturbance studies have been carried out. Here we evaluate changes in faunal densities and diversity of benthic communities measured in response to these 11 simulated or test nodule mining disturbances using meta-analysis techniques. We find that impacts are often severe immediately after mining, with major negative changes in density and diversity of most groups occurring. However, in some cases, the mobile fauna and small-sized fauna experienced less negative impacts over the longer term. At seven sites in the Pacific, multiple surveys assessed recovery in fauna over periods of up to 26 years. Almost all studies show some recovery in faunal density and diversity for meiofauna and mobile megafauna, often within one year. However, very few faunal groups return to baseline or control conditions after two decades. The effects of polymetallic nodule mining are likely to be long term. Our analyses show considerable negative biological effects of seafloor nodule mining, even at the small scale of test mining experiments, although there is variation in sensitivity amongst organisms of different sizes and functional groups, which have important implications for ecosystem responses. Unfortunately, many past studies have limitations that reduce their effectiveness in determining responses. We provide recommendations to improve future mining impact test studies. Further research to assess the effects of test-mining activities will inform ways to improve mining practices and guide effective environmental management of mining activities.

Abundance and morphology of Paleodictyon nodosum, observed at the Clarion-Clipperton Zone.

Paleodictyon is an important trace fossil characterised by a regular hexagonal structure and typical of ancient deep-ocean habitats as far back as the Ordovician. It is represented in modern deep-sea settings by Paleodictyon nodosum, known from the Mid-Atlantic Ridge, the South Atlantic, and off eastern Australia. Here we report the occurrence of P. nodosum in the Clarion Clipperton Zone (CCZ), abyssal equatorial Pacific, an area characterised by polymetallic nodule fields. At the study site within the International Seabed Authority northeastern Area of Particular Environmental Interest (APEI-6), P. nodosum appeared as a compact, regular pattern of small circular openings on the seafloor, each pattern interpreted as reflecting the activity of an individual organism. The patterns had a mean size (maximum dimension) of 45 mm ± 16 mm SD (n = 841) and occurred at a density of 0.33 individuals m-2. Most (82%) were interrupted by nodules, but those that were not displayed both regular (59%) and irregular (41%) forms, the former having equal numbers of rows along the three axes (6 x 6 x 6 and 8 x 8 x 8). In both size and morphology, our Paleodictyon traces were more similar to the Australian examples than to those from the Mid-Atlantic Ridge.

Landscape-scale spatial heterogeneity in phytodetrital cover and megafauna biomass in the abyss links to modest topographic variation.

Sinking particulate organic matter (POM, phytodetritus) is the principal limiting resource for deep-sea life. However, little is known about spatial variation in POM supply to the abyssal seafloor, which is frequently assumed to be homogenous. In reality, the abyss has a highly complex landscape with millions of hills and mountains. Here, we show a significant increase in seabed POM % cover (by ~1.05 times), and a large significant increase in megafauna biomass (by ~2.5 times), on abyssal hill terrain in comparison to the surrounding plain. These differences are substantially greater than predicted by current models linking water depth to POM supply or benthic biomass. Our observed variations in POM % cover (phytodetritus), megafauna biomass, sediment total organic carbon and total nitrogen, sedimentology, and benthic boundary layer turbidity, all appear to be consistent with topographically enhanced current speeds driving these enhancements. The effects are detectable with bathymetric elevations of only 10 s of metres above the surrounding plain. These results imply considerable unquantified heterogeneity in global ecology.