PlanktonID – Combining deep learning, in situ imaging and citizen science to resolve the distribution of zooplanktonin major upwelling regions

Recent publications revealed the global importance of single-celled zooplankton, belonging to the super group Rhizaria and highlighted the need of in-situ imaging to study these fragile organisms. The advance of in situ plankton imaging techniques leads to increasing amounts of image data sets that require identification to different taxonomic levels. Automatic classification by computer algorithms provides the means for fast data availability, however the accuracy of those algorithms still requires manual identification by humans. We combined state of the art automatic image classification by convolutional neural networks (deep learning) with a citizen science project to classify a large dataset of ~ 3 million images from an Underwater Vision Profiler 5 (UVP5). On our website https://planktonid.geomar.de, citizen scientists can confirm or reject the automatic assignment of UVP5 images to different plankton categories in a memory-like game. Inbuilt quality controls and multiple validations per image enable scientific analysis of the citizen science data. In total more than 500 users have validated more than 300.000 images until now. We will present further data on citizen scientist engagement, data quality assessment and the distribution analysis of large protists (Rhizaria) in the Mauretanian, Benguela and Humboldt Current upwelling systems

In situ imaging reveals the biomass of giant protists in the global ocean

International audiencePlanktonic organisms play crucial roles in oceanic food webs and global biogeochemical cycles1, 2. Most of our knowledge about the ecological impact of large zooplankton stems from research on abundant and robust crustaceans, and in particular copepods3, 4. A number of the other organisms that comprise planktonic communities are fragile, and therefore hard to sample and quantify, meaning that their abundances and effects on oceanic ecosystems are poorly understood. Here, using data from a worldwide in situ imaging survey of plankton larger than 600 μm, we show that a substantial part of the biomass of this size fraction consists of giant protists belonging to the Rhizaria, a super-group of mostly fragile unicellular marine organisms that includes the taxa Phaeodaria and Radiolaria (for example, orders Collodaria and Acantharia). Globally, we estimate that rhizarians in the top 200 m of world oceans represent a standing stock of 0.089 Pg carbon, equivalent to 5.2% of the total oceanic biota carbon reservoir5. In the vast oligotrophic intertropical open oceans, rhizarian biomass is estimated to be equivalent to that of all other mesozooplankton (plankton in the size range 0.2–20 mm). The photosymbiotic association of many rhizarians with microalgae may be an important factor in explaining their distribution. The previously overlooked importance of these giant protists across the widest ecosystem on the planet6 changes our understanding of marine planktonic ecosystems

Optical techniques for remote and in-situ characterization of particles pertinent to GEOTRACES

Field and laboratory characterization of marine particles is laborious and expensive. Proxies of particle properties have been developed that allow researchers to obtain high frequency distributions of such properties in space or time. We focus on optical techniques used to characterize marine particles in-situ, with a focus on GEOTRACES-relevant properties, such as bulk properties including particle mass, cross-sectional area, particle size distribution, particle shape information, and also single particle optical properties, such as individual particle type and size. We also address the use of optical properties of particles to infer particulate organic or inorganic carbon. In addition to optical sensors we review advances in imaging technology and its use to study marine particles in situ. This review addresses commercially available technology and techniques that can be used as a proxy for particle properties and the associated uncertainties with particular focus to open ocean environments, the focus of GEOTRACES

The wineglass effect shapes particle export to the deep ocean in mesoscale eddies

Mesoscale eddies in the ocean strongly impact the distribution of planktonic particles, mediating carbon fluxes over ~1/3 of the world ocean. However, mechanisms controlling particle transport through eddies are complex and challenging to measure in situ. Here we show the subsurface distribution of eddy particles funneled into a wineglass shape down to 1000 m, leading to a sevenfold increase of vertical carbon flux in the eddy center versus the eddy flanks, the “wineglass effect”. We show that the slope of the wineglass (R) is the ratio of particle sinking velocity to the radially inward velocity, such that R represents a tool to predict radial particle movement (here 0.05 m s−1). A simple model of eddy spindown predicts such an ageostrophic flow concentrating particles in the eddy center. We explore how size-specific particle flux toward the eddy center impacts eddies' biogeochemistry and export fluxes

The Seasonal and Inter-Annual Fluctuations of Plankton Abundance and Community Structure in a North Atlantic Marine Protected Area

Marine Protected Areas have become a major tool for the conservation of marine biodiversity and resources. Yet our understanding of their efficacy is often limited because it is measured for a few biological components, typically top predators or species of commercial interest. To achieve conservation targets, marine protected areas can benefit from ecosystem-based approaches. Within such an approach, documenting the variation of plankton indicators and their covariation with climate is crucial as plankton represent the base of the food webs. With this perspective, we sought to document the variations in the emerging properties of the plankton to better understand the dynamics of the pelagic fishes, mammals and seabirds that inhabit the region. For the first time, we analyze the temporal variations of the entire plankton community of one of the widest European protected areas, the Parc Naturel Marin de la Mer d’Iroise. We used data from several sampling transects carried out in the Iroise Sea from 2011 to 2015 to explore the seasonal and inter-annual variations of phytoplankton and mesozooplankton abundance, composition and size, as well as their covariation with abiotic variables, through multiple multivariate analyses. Overall, our observations are coherent with the plankton dynamics that have been observed in other regions of the North-East Atlantic. We found that both phytoplankton and zooplankton show consistent seasonal patterns in taxonomic composition and size structure but also display inter-annual variations. The spring bloom was associated with a higher contribution of large chain-forming diatoms compared to nanoflagellates, the latter dominating in fall and summer. Dinoflagellates show marked inter-annual variations in their relative contribution. The community composition of phytoplankton has a large impact on the mesozooplankton together with the distance to the coast. The size structure of the mesozooplankton community, examined through the ratio of small to large copepods, also displays marked seasonal patterns. We found that larger copepods (members of the Calanidae) are more abundant in spring than in summer and fall. We propose several hypotheses to explain the observed temporal patterns and we underline their importance for understanding the dynamics of other components of the food-web (such as sardines). Our study is a first step toward the inclusion of the planktonic compartment into the planning of the resources and diversity conservation within the Marine Protected Area

Particulate matter flux interception in oceanic mesoscale eddies by the polychaete Poeobius sp.

Gelatinous zooplankton hold key functions in the ocean and have been shown to significantly influence the transport of organic carbon to the deep sea. We discovered a gelatinous, flux‐feeding polychaete of the genus Poeobius in very high abundances in a mesoscale eddy in the tropical Atlantic Ocean, where it co‐occurred with extremely low particle concentrations. Subsequent analysis of an extensive in situ imaging dataset revealed that Poeobius sp. occurred sporadically between 5°S–20°N and 16°W–46°W in the upper 1000 m. Abundances were significantly elevated and the depth distribution compressed in anticyclonic modewater eddies (ACMEs). In two ACMEs, high Poeobius sp. abundances were associated with strongly reduced particle concentrations and fluxes in the layers directly below the polychaete. We discuss possible reasons for the elevated abundances of Poeobius sp. in ACMEs and provide estimations showing that a single zooplankton species can completely intercept the downward particle flux by feeding with their mucous nets, thereby substantially altering the biogeochemical setting within the eddy

Plankton networks driving carbon export in the oligotrophic ocean

The biological carbon pump is the process by which CO 2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterized. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria and alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of a few bacterial and viral genes can predict a significant fraction of the variability in carbon export in these regions

Global Distribution of Zooplankton Biomass Estimated by In Situ Imaging and Machine Learning

Zooplankton plays a major role in ocean food webs and biogeochemical cycles, and provides major ecosystem services as a main driver of the biological carbon pump and in sustaining fish communities. Zooplankton is also sensitive to its environment and reacts to its changes. To better understand the importance of zooplankton, and to inform prognostic models that try to represent them, spatially-resolved biomass estimates of key plankton taxa are desirable. In this study we predict, for the first time, the global biomass distribution of 19 zooplankton taxa (1-50 mm Equivalent Spherical Diameter) using observations with the Underwater Vision Profiler 5, a quantitative in situ imaging instrument. After classification of 466,872 organisms from more than 3,549 profiles (0-500 m) obtained between 2008 and 2019 throughout the globe, we estimated their individual biovolumes and converted them to biomass using taxa-specific conversion factors. We then associated these biomass estimates with climatologies of environmental variables (temperature, salinity, oxygen, etc.), to build habitat models using boosted regression trees. The results reveal maximal zooplankton biomass values around 60 degrees N and 55 degrees S as well as minimal values around the oceanic gyres. An increased zooplankton biomass is also predicted for the equator. Global integrated biomass (0-500 m) was estimated at 0.403 PgC. It was largely dominated by Copepoda (35.7%, mostly in polar regions), followed by Eumalacostraca (26.6%) Rhizaria (16.4%, mostly in the intertropical convergence zone). The machine learning approach used here is sensitive to the size of the training set and generates reliable predictions for abundant groups such as Copepoda (R2 approximate to 20-66%) but not for rare ones (Ctenophora, Cnidaria, R2 < 5%). Still, this study offers a first protocol to estimate global, spatially resolved zooplankton biomass and community composition from in situ imaging observations of individual organisms. The underlying dataset covers a period of 10 years while approaches that rely on net samples utilized datasets gathered since the 1960s. Increased use of digital imaging approaches should enable us to obtain zooplankton biomass distribution estimates at basin to global scales in shorter time frames in the future

Global Trends in Marine Plankton Diversity across Kingdoms of Life

35 pages, 18 figures, 1 table, supplementary information https://doi.org/10.1016/j.cell.2019.10.008.-- Raw reads of Tara Oceans are deposited at the European Nucleotide Archive (ENA). In particular, newly released 18S rRNA gene metabarcoding reads are available under the number ENA: PRJEB9737. ENA references for the metagenomics reads corresponding to the size fraction < 0.22 μm (for prokaryotic viruses) analyzed in this study are included in Gregory et al. (2019); see their Table S3. ENA references for the metagenomics reads corresponding to the size fraction 0.22-1.6/3 μm (for prokaryotes and giruses) correspond to Salazar et al. (2019) (see https://zenodo.org/record/3473199). Imaging datasets from the nets are available through the collaborative web application and repository EcoTaxa (Picheral et al., 2017) under the address https://ecotaxa.obs-vlfr.fr/prj/412 for regent data, within the 3 projects https://ecotaxa.obs-vlfr.fr/prj/397, https://ecotaxa.obs-vlfr.fr/prj/398, https://ecotaxa.obs-vlfr.fr/prj/395 for bongo data, and within the 2 projects https://ecotaxa.obs-vlfr.fr/prj/377 and https://ecotaxa.obs-vlfr.fr/prj/378 for WP2 data. A table with Shannon values and multiple samples identifiers, plus a table with flow cytometry data split in six groups are available (https://doi.org/10.17632/p9r9wttjkm.1). Contextual data from the Tara Oceans expedition, including those that are newly released from the Arctic Ocean, are available at https://doi.org/10.1594/PANGAEA.875582The ocean is home to myriad small planktonic organisms that underpin the functioning of marine ecosystems. However, their spatial patterns of diversity and the underlying drivers remain poorly known, precluding projections of their responses to global changes. Here we investigate the latitudinal gradients and global predictors of plankton diversity across archaea, bacteria, eukaryotes, and major virus clades using both molecular and imaging data from Tara Oceans. We show a decline of diversity for most planktonic groups toward the poles, mainly driven by decreasing ocean temperatures. Projections into the future suggest that severe warming of the surface ocean by the end of the 21st century could lead to tropicalization of the diversity of most planktonic groups in temperate and polar regions. These changes may have multiple consequences for marine ecosystem functioning and services and are expected to be particularly significant in key areas for carbon sequestration, fisheries, and marine conservationTara Oceans (which includes both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Ocean Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org/). We further thank the commitment of the following sponsors: CNRS (in particular Groupement de Recherche GDR3280 and the Research Federation for the Study of Global Ocean Systems Ecology and Evolution FR2022/Tara Oceans-GOSEE), the European Molecular Biology Laboratory (EMBL), Genoscope/CEA, the French Ministry of Research, and the French Government “Investissements d’Avenir” programs OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), the PSL∗ Research University (ANR-11-IDEX-0001-02), as well as EMBRC-France (ANR-10-INBS-02). Funding for the collection and processing of the Tara Oceans data set was provided by NASA Ocean Biology and Biogeochemistry Program under grants NNX11AQ14G, NNX09AU43G, NNX13AE58G, and NNX15AC08G (to the University of Maine); the Canada Excellence research chair on remote sensing of Canada’s new Arctic frontier; and the Canada Foundation for Innovation. We also thank agnès b. and Etienne Bourgois, the Prince Albert II de Monaco Foundation, the Veolia Foundation, Region Bretagne, Lorient Agglomeration, Serge Ferrari, Worldcourier, and KAUST for support and commitment. The global sampling effort was enabled by countless scientists and crew who sampled aboard the Tara from 2009–2013, and we thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expeditions. We are also grateful to the countries who graciously granted sampling permission. We thank Stephanie Henson for providing ocean carbon export data and are also grateful to the other researchers who kindly made their data available. We thank Juan J. Pierella-Karlusich for advice regarding single-copy genes. C.d.V. and N.H. thank the Roscoff Bioinformatics platform ABiMS (http://abims.sb-roscoff.fr) for providing computational resources. C.B. acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation Program (grant agreement 835067) as well as the Radcliffe Institute of Advanced Study at Harvard University for a scholar’s fellowship during the 2016-2017 academic year. M.B.S. thanks the Gordon and Betty Moore Foundation (award 3790) and the National Science Foundation (awards OCE#1536989 and OCE#1829831) as well as the Ohio Supercomputer for computational support. S.G.A. thanks the Spanish Ministry of Economy and Competitiveness (CTM2017-87736-R), and J.M.G. is grateful for project RT2018-101025-B-100. F.L. thanks the Institut Universitaire de France (IUF) as well as the EMBRC platform PIQv for image analysis. M.C.B., D.S., and J.R. received financial support from the French Facility for Global Environment (FFEM) as part of the “Ocean Plankton, Climate and Development” project. M.C.B. also received financial support from the Coordination for the Improvement of Higher Education Personnel of Brazil (CAPES 99999.000487/2016-03)Peer Reviewe