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

Nature volume 532, pages 504–507 (2016)Cite this article

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Abstract

Planktonic 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.

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Figure 1: Worldwide contribution of giant Rhizaria to zooplankton communities (>600 μm) in the top 500 m of the water column.
Figure 2: Latitudinal distribution of depth-integrated biomass (0–200 m depth) of Rhizaria (blue, in situ optical assessment, this study; 848 sampling stations) and mesozooplankton (orange, plankton net-based assessments31; 26,918 samples).
Figure 3: Latitudinal distribution of depth integrated biomass (mg carbon (mg C) m−2) for the different rhizarian taxa identified.

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Acknowledgements

Thanks to J.-O. Irisson for help with the R language and statistical analysis and I. Probert and J. Dolan for comments and English proofreading. The following people were involved in cruise organization: T. Moutin (BOUM), M. Landry and M. Ohman (CCE LTER), S. Blain (KEOPS II), V. Smetacek and W. Naqvi (LOHAFEX), J. Karstensen (M96), M. Babin (Malina), L. Coppola (Moose GE), P. Brandt (MSM22) and M. Visbeck (MSM23). The following people were involved in plankton image sorting: L. Burdorf (CNRS LOV), C. Desnos (CNRS LOV), A. Forest (Tackuvit), G. IdAoud (CNRS LOV), M. P. Jouandet (MIO Pytheas), J. Poulain (CEA), J. Baptiste Romagnan (CNRS LOV), F. Roullier (CNRS LOV), S. Searson (CNRS LOV), B. Serranito (EBMA-PROTEE) and N. Vasset (CNRS LOV). This study is a contribution from the CCE-LTER program, supported by the U.S. National Science Foundation. For the Tara Oceans expedition we thank the CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, Fund for Scientific Research – Flanders, Rega Institute, KU Leuven and the French Ministry of Research. We also thank A. Bourgois and E. Bourgois, the Veolia Environment Foundation, Région Bretagne, Lorient Agglomération, World Courier, Illumina, the EDF Foundation, FRB, the Prince Albert II de Monaco Foundation, the Tara schooner and its captains and crew. We are also grateful to the French Ministry of Foreign Affairs for supporting the expedition and to the countries who granted sampling permission. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans.taraexpeditions.org). The authors further declare that all data reported herein are fully and freely available from the date of publication, with no restrictions, and that all of the samples, analyses, publications, and ownership of data are free from legal entanglement or restriction of any sort by the various nations in whose waters the Tara Oceans expedition sampled. Data described herein are available at PANGAEA (http://doi.pangaea.de/10.1594/PANGAEA.842227), and the data release policy regarding future public release of Tara Oceans data is described in ref. 29. Funding was from DESIR project Emergence-UPMC from Université Pierre et Marie Curie, JST-CNRS exchange program, CHAIRE CNRS/UPMC Vision, Investissements d’Avenir’ programmes OCEANOMICS (ANR-11-BTBR-0008), DFG through SFB754 (GEOMAR and Kiel University) and Future Ocean (Kiel University and GEOMAR). This article is contribution number 38 from Tara Oceans.

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Authors and Affiliations

  1. Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire Adaptation et Diversité en Milieu Marin UMR7144, Station Biologique de Roscoff, Roscoff, 29688, France

    Tristan Biard & Fabrice Not

  2. Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire d’Océanographie de Villefranche (LOV) UMR7093, Observatoire Océanologique, 06230, Villefranche-sur-Mer, France

    Tristan Biard, Lars Stemmann, Marc Picheral, Nicolas Mayot, Gabriel Gorsky & Lionel Guidi

  3. GEOMAR Helmholtz Centre for Ocean Research Kiel, Wischhofstrasse 1–3, Kiel, 24148, Germany

    Pieter Vandromme, Helena Hauss & Rainer Kiko

Authors
  1. Tristan Biard
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Contributions

F.N. and L.S. designed the study. M.P., T.B., R.K., P.V., H.H., N.M. and G.G. acquired and extracted raw data. T.B. produced the morphological classification of the rhizarian UVP images. T.B., L.S. and L.G. performed statistical analyses. R.K. and T.B. calculated the primary production contributions. F.N. and T.B. wrote the manuscript and produced display items. L.S., R.K., L.G., M.P., H.H. and G.G. discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Lars Stemmann or Fabrice Not.

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Extended data figures and tables

Extended Data Figure 1 Sampling effort of the Underwater Vision Profiler surveys used in our study, represented across latitudes and months of the year.

Rectangles identify latitude intervals of 5° affiliated to a given month. Numbers inside rectangles indicate the number of stations sampled. a, Sampling effort for the full dataset. b, Sampling stations identified as belonging to one of Longhurst’s gyral biogeochemical provinces. c, Sampling stations identified as belonging to oligotrophic waters (Chlasat < 0.1 mg m−3; ref. 44). White rectangles with dashed edges highlight sampling stations not belonging to a gyre nor oligotrophic waters.

Extended Data Figure 2 Images of the different rhizarian categories obtained with the UVP5.

a–c, Phaeodaria: (a) phaeodarian spheres (PhaSe), (b) phaeodarian spheres with thorn edges (PhaSt) and (c) phaeodarians with long extensions (PhaL). d, Unidentified rhizarians (Rhiz). e, Acantharia (Acn). f–j, Collodaria: (f) solitary collodarians with a dark central capsule (SolB), (g) solitary collodarians with a fuzzy central capsule (SolF), (h) solitary collodarians with a grey central capsule (SolG), (i) solitary collodarians with a globule-like appearance (SolGlob) and (j) colonial collodarians (Col). Detailed descriptions of the different categories are provided in the Methods. Scale bars, 2 mm.

Extended Data Figure 3 Calibration of rhizarian categories through comparison of single specimen images acquired by UVP5 and optical microscopy.

Optical microscopy images and UVP5 images were obtained from the same specimens. a, Thalassicolla caerulea (SolB). b, c, Unidentified solitary collodarian species with dark central capsules (SolB). d, Small collodarian colonies (Col). e, Procyttarium primordialis (two solitary collodarians with a white central capsule; SolG). f, Physematium muelleri (a solitary collodarian with a granular and opaque surface, similar to SolG). g, The Phaeosphaeridae family of Phaeodaria (PhaSe). Scale bars, 2 mm.

Extended Data Figure 4 Size distribution of rhizarian categories in the UVP5 dataset.

The dashed line represents the 600-μm size threshold of the camera. The overall mean equivalent spherical diameter (ESD) is 2.06 mm (red line). Dark horizontal lines represent the mean, boxes represent the first and third quartiles for data distribution around the mean and the whiskers denote the lowest and highest values within 1.5 IQR from the first and third quartiles. Outlier values are represented by dots.

Extended Data Figure 5 Latitudinal biomass distribution (mg C m−2) of the different rhizarian taxa identified (Acantharia, Collodaria, Phaeodaria and other Rhizaria) integrated over the top 500 m of the oceans (694 sampling stations).

Loess regressions with polynomial fitting were computed to illustrate the latitudinal trends. Shaded areas represent 95% confidence intervals.

Extended Data Figure 6 Variation in UVP5 depth-integrated abundances (0–100 m depth) as a function of the MODIS surface chlorophyll a extracted from satellite data (Oregon University Database).

Solid and dashed red lines indicate significant and non-significant linear regressions, respectively. The shaded areas represent the standard error. a, The integrated abundance of photosymbiotic Rhizaria (n = 521) was not significantly linearly dependent on chlorophyll a concentrations (F = 0.622, R2adj = −0.0007, P = 0.431). We assume that all collodarian species are photosymbiotic13,14 and that the majority of large acantharian cells found in the photic layer are known to harbour symbionts24,25. b, The integrated abundance of other zooplankton (including asymbiotic Rhizaria; n = 793) decreased linearly along a trophic gradient (F = 94.51, R2adj = 0.106, P < 10−16).

Extended Data Table 1 Sampling cruise information, number of stations sampled, and number of UVP5 deployments (for example, profiles) used to generate the dataset analysed in this study
Full size table
Extended Data Table 2 Respective contributions of Rhizaria and other zooplankton abundances to the zooplankton community (>600 μm) integrated for the top 0–500 m of the water column
Full size table
Extended Data Table 3 Carbon conversion factors used to assess biomass for the rhizarian categories discriminated
Full size table
Extended Data Table 4 Net primary production of photosymbiotic giant rhizarians (Collodaria and Acantharia) and their contribution to total and >2-μm net primary production in the global ocean and oligotrophic regions
Full size table

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Biard, T., Stemmann, L., Picheral, M. et al. In situ imaging reveals the biomass of giant protists in the global ocean. Nature 532, 504–507 (2016). https://doi.org/10.1038/nature17652

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