Evidence for seasonal cycles in deep-sea fish abundances: A great migration in the deep SE Atlantic?

Animal migrations are of global ecological significance, providing mechanisms for the transport of nutrients and energy between distant locations. In much of the deep sea (>200 m water depth), the export of nutrients from the surface ocean provides a crucial but seasonally variable energy source to seafloor ecosystems. Seasonal faunal migrations have been hypothesized to occur on the deep seafloor as a result, but have not been documented. Here, we analyse a 7.5-year record of photographic data from the Deep-ocean Environmental Long-term Observatory Systems seafloor observatories to determine whether there was evidence of seasonal (intra-annual) migratory behaviours in a deep-sea fish assemblage on the West African margin and, if so, identify potential cues for the behaviour. Our findings demonstrate a correlation between intra-annual changes in demersal fish abundance at 1,400 m depth and satellite-derived estimates of primary production off the coast of Angola. Highest fish abundances were observed in late November with a smaller peak in June, occurring approximately 4 months after corresponding peaks in primary production. Observed changes in fish abundance occurred too rapidly to be explained by recruitment or mortality, and must therefore have a behavioural driver. Given the recurrent patterns observed, and the established importance of bottom-up trophic structuring in deep-sea ecosystems, we hypothesize that a large fraction of the fish assemblage may conduct seasonal migrations in this region, and propose seasonal variability in surface ocean primary production as a plausible cause. Such trophic control could lead to changes in the abundance of fishes across the seafloor by affecting secondary production of prey species and/or carrion availability for example. In summary, we present the first evidence for seasonally recurring patterns in deep-sea demersal fish abundances over a 7-year period, and demonstrate a previously unobserved level of dynamism in the deep sea, potentially mirroring the great migrations so well characterized in terrestrial systems.

As migrações dos animais são importantes para a ecologia global pois fornecem mecanismos para o transporte de nutrientes e energia entre diferentes locais. Em grande parte do oceano profundo (>200 m de profundidade), a exportação de nutrientes da superfície para os ecossistemas do fundo marinho é uma fonte de energia crucial, mas que varia entre estações. Consequentemente, calcula-se que ocorram migrações sazonais de animais no fundo marinho, mas tal nunca foi reportado. Neste estudo, nós analisamos dados fotográficos do observatório do fundo marinho DELOS colhidos ao longo de 7.5 anos, para determinar se existem indícios de comportamentos migratórios sazonais (intra-anuais) na comunidade de peixes de profundidade na costa oeste africana ao largo de Angola e, se se confirmar, tentar identificar o que desencadeia este comportamento. Os resultados obtidos mostram que há uma correlação entre as alterações intra-anuais da densidade de peixes demersais a 1,400 m de profundidade e as estimativas de produção primária obtidas por satélite. A densidade de peixes atinge o seu máximo no final de Novembro, com um pico menos acentuado em Junho, aproximadamente quatro meses após os respectivos picos de produção primária na superfície. As alterações na densidade de peixe ocorreram de uma forma tão rápida que não podem ser explicadas por recrutamento ou mortalidade, e como tal devem só podem ser geradas por uma alteração do comportamento. Dado a recorrência do padrão observado, e importância da estrutura trófica fundo-topo em ecossistemas do oceano profundo, nós colocamos a hipótese de que uma fracção grande da comunidade de peixes faz migrações sazonais nesta região, e propomos que a variação sazonal da produção primária na superfície esteja na sua origem. Este controlo trófico poderá levar a alterações na densidade de peixes no fundo marinho via, por exemplo, a produção secundária de presas e/ou disponibilidade de corpos em processo de decomposição. Resumindo, nós apresentamos aqui a primeira evidência de padrões sazonais recorrentes na densidade de peixes demersais de profundidade ao longo de um período de sete anos, e provamos existir um nível de dinamismo nunca dantes observado no oceano profundo, que poderá espelhar as grandes migrações comummente observadas em sistemas terrestres.

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.

Ecology of a polymetallic nodule occurrence gradient: Implications for deep-sea mining.

Abyssal polymetallic nodule fields constitute an unusual deep-sea habitat. The mix of soft sediment and the hard substratum provided by nodules increases the complexity of these environments. Hard substrata typically support a very distinct fauna to that of seabed sediments, and its presence can play a major role in the structuring of benthic assemblages. We assessed the influence of seafloor nodule cover on the megabenthos of a marine conservation area (area of particular environmental interest 6) in the Clarion Clipperton Zone (3950-4250 m water depth) using extensive photographic surveys from an autonomous underwater vehicle. Variations in nodule cover (1-20%) appeared to exert statistically significant differences in faunal standing stocks, some biological diversity attributes, faunal composition, functional group composition, and the distribution of individual species. The standing stock of both the metazoan fauna and the giant protists (xenophyophores) doubled with a very modest initial increase in nodule cover (from 1% to 3%). Perhaps contrary to expectation, we detected little if any substantive variation in biological diversity along the nodule cover gradient. Faunal composition varied continuously along the nodule cover gradient. We discuss these results in the context of potential seabed-mining operations and the associated sustainable management and conservation plans. We note in particular that successful conservation actions will likely require the preservation of areas comprising the full range of nodule cover and not just the low cover areas that are least attractive to mining.

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.

BioTIME: A database of biodiversity time series for the Anthropocene.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

Big in the benthos: Future change of seafloor community biomass in a global, body size-resolved model.

Deep-water benthic communities in the ocean are almost wholly dependent on near-surface pelagic ecosystems for their supply of energy and material resources. Primary production in sunlit surface waters is channelled through complex food webs that extensively recycle organic material, but lose a fraction as particulate organic carbon (POC) that sinks into the ocean interior. This exported production is further rarefied by microbial breakdown in the abyssal ocean, but a residual ultimately drives diverse assemblages of seafloor heterotrophs. Advances have led to an understanding of the importance of size (body mass) in structuring these communities. Here we force a size-resolved benthic biomass model, BORIS, using seafloor POC flux from a coupled ocean-biogeochemistry model, NEMO-MEDUSA, to investigate global patterns in benthic biomass. BORIS resolves 16 size classes of metazoans, successively doubling in mass from approximately 1 µg to 28 mg. Simulations find a wide range of seasonal responses to differing patterns of POC forcing, with both a decline in seasonal variability, and an increase in peak lag times with increasing body size. However, the dominant factor for modelled benthic communities is the integrated magnitude of POC reaching the seafloor rather than its seasonal pattern. Scenarios of POC forcing under climate change and ocean acidification are then applied to investigate how benthic communities may change under different future conditions. Against a backdrop of falling surface primary production (-6.1%), and driven by changes in pelagic remineralization with depth, results show that while benthic communities in shallow seas generally show higher biomass in a warmed world (+3.2%), deep-sea communities experience a substantial decline (-32%) under a high greenhouse gas emissions scenario. Our results underscore the importance for benthic ecology of reducing uncertainty in the magnitude and seasonality of seafloor POC fluxes, as well as the importance of studying a broader range of seafloor environments for future model development.

Links between deep-sea respiration and community dynamics.

It has been challenging to establish the mechanisms that link ecosystem functioning to environmental and resource variation, as well as community structure, composition, and compensatory dynamics. A compelling hypothesis of compensatory dynamics, known as "zero-sum" dynamics, is framed in terms of energy resource and demand units, where there is an inverse link between the number of individuals in a community and the mean individual metabolic rate. However, body size energy distributions that are nonuniform suggest a niche advantage at a particular size class, which suggests a limit to which metabolism can explain community structuring. Since 1989, the composition and structure of abyssal seafloor communities in the northeast Pacific and northeast Atlantic have varied interannually with links to climate and resource variation. Here, for the first time, class and mass-specific individual respiration rates were examined along with resource supply and time series of density and biomass data of the dominant abyssal megafauna, echinoderms. Both sites had inverse relationships between density and mean individual metabolic rate. We found fourfold variation in echinoderm respiration over interannual timescales at both sites, which were linked to shifts in species composition and structure. In the northeastern Pacific, the respiration of mobile surface deposit feeding echinoderms was positively linked to climate-driven particulate organic carbon fluxes with a temporal lag of about one year, respiring - 1-6% of the annual particulate organic carbon flux.

Autonomous marine environmental monitoring: Application in decommissioned oil fields.

Hundreds of Oil & Gas Industry structures in the marine environment are approaching decommissioning. In most areas decommissioning operations will need to be supported by environmental assessment and monitoring, potentially over the life of any structures left in place. This requirement will have a considerable cost for industry and the public. Here we review approaches for the assessment of the primary operating environments associated with decommissioning - namely structures, pipelines, cuttings piles, the general seabed environment and the water column - and show that already available marine autonomous systems (MAS) offer a wide range of solutions for this major monitoring challenge. Data of direct relevance to decommissioning can be collected using acoustic, visual, and oceanographic sensors deployed on MAS. We suggest that there is considerable potential for both cost savings and a substantial improvement in the temporal and spatial resolution of environmental monitoring. We summarise the trade-offs between MAS and current conventional approaches to marine environmental monitoring. MAS have the potential to successfully carry out much of the monitoring associated with decommissioning and to offer viable alternatives where a direct match for the conventional approach is not possible.

Biological effects 26 years after simulated deep-sea mining.

The potential for imminent abyssal polymetallic nodule exploitation has raised considerable scientific attention. The interface between the targeted nodule resource and sediment in this unusual mosaic habitat promotes the development of some of the most biologically diverse communities in the abyss. However, the ecology of these remote ecosystems is still poorly understood, so it is unclear to what extent and timescale these ecosystems will be affected by, and could recover from, mining disturbance. Using data inferred from seafloor photo-mosaics, we show that the effects of simulated mining impacts, induced during the "DISturbance and reCOLonization experiment" (DISCOL) conducted in 1989, were still evident in the megabenthos of the Peru Basin after 26 years. Suspension-feeder presence remained significantly reduced in disturbed areas, while deposit-feeders showed no diminished presence in disturbed areas, for the first time since the experiment began. Nevertheless, we found significantly lower heterogeneity diversity in disturbed areas and markedly distinct faunal compositions along different disturbance levels. If the results of this experiment at DISCOL can be extrapolated to the Clarion-Clipperton Zone, the impacts of polymetallic nodule mining there may be greater than expected, and could potentially lead to an irreversible loss of some ecosystem functions, especially in directly disturbed areas.

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.

Macrobenthic biomass relations in the Faroe-Shetland Channel: an Arctic-Atlantic boundary environment.

The Faroe-Shetland Channel, located in the NE Atlantic, ranges in depth from 0-1700 m and is an unusual deep-sea environment because of its complex and dynamic hydrographic regime, as well as having numerous different seafloor habitats. Macrofaunal samples have been collected on a 0.5 mm mesh sieve from over 300 stations in a wide area survey and on nested 0.5 and 0.25 mm mesh sieves along a specific depth transect. Contrary to general expectation, macrofauanl biomass in the Channel did not decline with increasing depth. When examined at phylum level, two main biomass patterns with depth were apparent: (a) polychaetes showed little change in biomass on the upper slope then increased markedly below 500 m to a depth of 1100 m before declining; and (b) other phyla showed enhanced biomass between 300-500 m. The polychaete response may be linked with a seafloor environment change to relatively quiescent hydrodynamic conditions and an increasing sediment mud content that occurs at c. 500 m. In contrast, the mid-slope enhancement of other phyla biomass may reflect the hydrodynamically active interface between the warm and cold water masses present in the Channel at c. 300-500 m. Again contrary to expectation, mean macrofaunal body size did not decline with depth, and the relative contribution of smaller (>0.25 mm<0.5 mm) to total (>0.25 mm) macrobenthos did not increase with depth. Overall our total biomass and average individual biomass estimates appear to be greater than those predicted from global analyses. It is clear that global models of benthic biomass distribution may mask significant variations at the local and regional scale.

The effects of natural iron fertilisation on deep-sea ecology: the Crozet Plateau, Southern Indian Ocean.

The addition of iron to high-nutrient low-chlorophyll (HNLC) oceanic waters stimulates phytoplankton, leading to greater primary production. Large-scale artificial ocean iron fertilization (OIF) has been proposed as a means of mitigating anthropogenic atmospheric CO(2), but its impacts on ocean ecosystems below the photic zone are unknown. Natural OIF, through the addition of iron leached from volcanic islands, has been shown to enhance primary productivity and carbon export and so can be used to study the effects of OIF on life in the ocean. We compared two closely-located deep-sea sites (∼400 km apart and both at ∼4200 m water depth) to the East (naturally iron fertilized; +Fe) and South (HNLC) of the Crozet Islands in the southern Indian Ocean. Our results suggest that long-term geo-engineering of surface oceanic waters via artificial OIF would lead to significant changes in deep-sea ecosystems. We found that the +Fe area had greater supplies of organic matter inputs to the seafloor, including polyunsaturated fatty acid and carotenoid nutrients. The +Fe site also had greater densities and biomasses of large deep-sea animals with lower levels of evenness in community structuring. The species composition was also very different, with the +Fe site showing similarities to eutrophic sites in other ocean basins. Moreover, major differences occurred in the taxa at the +Fe and HNLC sites revealing the crucial role that surface oceanic conditions play in changing and structuring deep-sea benthic communities.

Global patterns and predictions of seafloor biomass using random forests.

A comprehensive seafloor biomass and abundance database has been constructed from 24 oceanographic institutions worldwide within the Census of Marine Life (CoML) field projects. The machine-learning algorithm, Random Forests, was employed to model and predict seafloor standing stocks from surface primary production, water-column integrated and export particulate organic matter (POM), seafloor relief, and bottom water properties. The predictive models explain 63% to 88% of stock variance among the major size groups. Individual and composite maps of predicted global seafloor biomass and abundance are generated for bacteria, meiofauna, macrofauna, and megafauna (invertebrates and fishes). Patterns of benthic standing stocks were positive functions of surface primary production and delivery of the particulate organic carbon (POC) flux to the seafloor. At a regional scale, the census maps illustrate that integrated biomass is highest at the poles, on continental margins associated with coastal upwelling and with broad zones associated with equatorial divergence. Lowest values are consistently encountered on the central abyssal plains of major ocean basins The shift of biomass dominance groups with depth is shown to be affected by the decrease in average body size rather than abundance, presumably due to decrease in quantity and quality of food supply. This biomass census and associated maps are vital components of mechanistic deep-sea food web models and global carbon cycling, and as such provide fundamental information that can be incorporated into evidence-based management.