Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Ubiquitous abundance distribution of non-dominant plankton across the global ocean

Abstract

Marine plankton populate 70% of Earth’s surface, providing the energy that fuels ocean food webs and contributing to global biogeochemical cycles. Plankton communities are extremely diverse and geographically variable, and are overwhelmingly composed of low-abundance species. The role of this rare biosphere and its ecological underpinnings are however still unclear. Here, we analyse the extensive dataset generated by the Tara Oceans expedition for marine microbial eukaryotes (protists) and use an adaptive algorithm to explore how metabarcoding-based abundance distributions vary across plankton communities in the global ocean. We show that the decay in abundance of non-dominant operational taxonomic units, which comprise over 99% of local richness, is commonly governed by a power-law. Despite the high spatial turnover in species composition, the power-law exponent varies by less than 10% across locations and shows no biogeographical signature, but is weakly modulated by cell size. Such striking regularity suggests that the assembly of plankton communities in the dynamic and highly variable ocean environment is governed by large-scale ubiquitous processes. Understanding their origin and impact on plankton ecology will be important for evaluating the resilience of marine biodiversity in a changing ocean.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Abundance distributions of protist swarms.
Fig. 2: Relationship between fitted nonlinear parameters.
Fig. 3: Sample locations and their associated average power-law exponent.

Similar content being viewed by others

References

  1. Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).

    Article  PubMed  CAS  Google Scholar 

  2. De Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).

  3. Fuhrman, J. A. Microbial community structure and its functional implications. Nature 459, 193–199 (2009).

    Article  CAS  PubMed  Google Scholar 

  4. Hutchinson, G. E. The paradox of the plankton. Am. Nat. 95, 137–145 (1961).

    Article  Google Scholar 

  5. d’Ovidio, F., Monte, S. D., Alvain, S., Dandonneau, Y. & Lévy, M. Fluid dynamical niches of phytoplankton types. Proc. Natl Acad. Sci. USA 107, 18366–18370 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).

    Article  CAS  PubMed  Google Scholar 

  7. McGillicuddy, D. J. Mechanisms of physical–biological–biogeochemical interaction at the oceanic mesoscale. Annu. Rev. Mar. Sci. 8, 125–159 (2016).

    Article  Google Scholar 

  8. Galand, P. E., Casamayor, E. O., Kirchman, D. L. & Lovejoy, C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl Acad. Sci. USA 106, 22427–22432 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Pedrós-Alió, C. The rare bacterial biosphere. Annu. Rev. Mar. Sci. 4, 449–466 (2012).

    Article  Google Scholar 

  10. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Lynch, M. D. J. & Neufeld, J. D. Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229 (2015).

    Article  CAS  PubMed  Google Scholar 

  12. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).

    Article  CAS  Google Scholar 

  13. Logares, R. et al. Patterns of rare and abundant marine microbial eukaryotes. Curr. Biol. 24, 813–821 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Barberán, A., Casamayor, E. O. & Fierer, N.The microbial contribution to macroecology. Front. Microbiol. 5, 203 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chust, G., Irigoien, X., Chave, J. & Harris, R. P. Latitudinal phytoplankton distribution and the neutral theory of biodiversity. Glob. Ecol. Biogeogr. 22, 531–543 (2013).

    Article  Google Scholar 

  16. Locey, K. J. & Lennon, J. T. Scaling laws predict global microbial diversity. Proc. Natl Acad. Sci. USA 113, 5970–5975 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Magurran, A. E. Measuring Biological Diversity (Blackwell, Oxford, 2004).

  18. McGill, B. J. et al. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett. 10, 995–1015 (2007).

    Article  PubMed  Google Scholar 

  19. Magurran, A. E. & McGill, B. J. Biological Diversity: Frontiers in Measurement and Assessment (Oxford Univ. Press, Oxford, 2011).

  20. Volkov, I., Banavar, J. R., Hubbell, S. P. & Maritan, A. Neutral theory and relative species abundance in ecology. Nature 424, 1035–1037 (2003).

    Article  CAS  PubMed  Google Scholar 

  21. Pueyo, S. Diversity: between neutrality and structure. Oikos 112, 392–405 (2006).

    Article  Google Scholar 

  22. Connolly, S. R. et al. Commonness and rarity in the marine biosphere. Proc. Natl Acad. Sci. USA 111, 8524–8529 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ulrich, W., Ollik, M. & Ugland, K. I. A meta-analysis of species-abundance distributions. Oikos 119, 1149–1155 (2009).

    Article  Google Scholar 

  24. Shoemaker, W. R., Locey, K. J. & Lennon, J. T. A macroecological theory of microbial biodiversity. Nat. Ecol. Evol. 1, 0107 (2017).

    Article  Google Scholar 

  25. Matthews, T. J. & Whittaker, R. J. Neutral theory and the species abundance distribution: recent developments and prospects for unifying niche and neutral perspectives. Ecol. Evol. 4, 2263–2277 (2014).

    PubMed  PubMed Central  Google Scholar 

  26. Baldridge, E. et al. An extensive comparison of species-abundance distribution models. PeerJ 4, e2823 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Xiao, X., O’Dwyer, J. P. & White, E. P. Comparing process‐based and constraint‐based approaches for modeling macroecological patterns. Ecology 97, 1228–1238 (2016).

    Article  PubMed  Google Scholar 

  28. Azaele, S., Pigolotti, S., Banavar, J. R. & Maritan, A. Dynamical evolution of ecosystems. Nature 444, 926–928 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. Magurran, A. E. & Henderson, P. A. Explaining the excess of rare species in natural species abundance distributions. Nature 422, 714–716 (2003).

  30. Ulrich, W. & Ollik, M. Frequent and occasional species and the shape of relative‐abundance distributions. Divers. Distrib. 10, 263–269 (2004).

    Article  Google Scholar 

  31. Mahé, F., Rognes, T., Quince, C., De Vargas, C. & Dunthorn, M. Swarmv2: highly-scalable and high-resolution amplicon clustering. PeerJ 3, e1420 (2015).

  32. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  33. Woodward, G. et al. Body size in ecological networks. Trends Ecol. Evol. 20, 402–409 (2005).

    Article  PubMed  Google Scholar 

  34. White, E. P., Ernest, S. K. M., Kerkhoff, A. J. & Enquist, B. J. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323–330 (2007).

    Article  PubMed  Google Scholar 

  35. Matthews, T. J., Borges, P. A., Azevedo, E. B. & Whittaker, R. J. A biogeographical perspective on species abundance distributions: recent advances and opportunities for future research. J. Biogeogr. 44, 1705–1710 (2017).

    Article  Google Scholar 

  36. Clauset, A., Shalizi, C. & Newman, M. Power-law distributions in empirical data. SIAM Rev. 51, 661–703 (2009).

    Article  Google Scholar 

  37. Jeraldo, P. et al. Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc. Natl Acad. Sci. USA 109, 9692–9698 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. He, F. Deriving a neutral model of species abundance from fundamental mechanisms of population dynamics. Funct. Ecol. 19, 187–193 (2005).

    Article  Google Scholar 

  39. Azaele, S. et al. Statistical mechanics of ecological systems: neutral theory and beyond. Rev. Mod. Phys. 88, 035003 (2016).

    Article  Google Scholar 

  40. Volkov, I., Banavar, J. R., He, F., Hubbell, S. P. & Maritan, A. Density dependence explains tree species abundance and diversity in tropical forests. Nature 438, 658–661 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Chaffron, S. et al. Environmental Context of Selected Samples from the Tara Oceans Expedition (2009–2013) (PANGAEA, 2014); https://doi.org/10.1594/PANGAEA.840718

  42. Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).

    Article  CAS  PubMed  Google Scholar 

  43. Gravel, D., Canham, C. D., Beaudet, M. & Messier, C. Reconciling niche and neutrality: the continuum hypothesis. Ecol. Lett. 9, 399–409 (2006).

    Article  PubMed  Google Scholar 

  44. Wilkins, D., Van Sebille, E., Rintoul, S. R., Lauro, F. M. & Cavicchioli, R. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 4, 2457 (2013).

    Article  PubMed  CAS  Google Scholar 

  45. Ferriere, R. & Cazelles, B. Universal power laws govern intermittent rarity in communities of interacting species. Ecology 80, 1505–1521 (1999).

    Article  Google Scholar 

  46. Lehahn, Y., d’Ovidio, F. & Koren, I.A satellite-based Lagrangian view on phytoplankton dynamics. Annu. Rev. Mar. Sci. 10, 99–119 (2018).

  47. Cram, J. A. et al. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 9, 563–580 (2015).

    Article  PubMed  Google Scholar 

  48. Martin-Platero, A. M. et al. High resolution time series reveals cohesive but short-lived communities in coastal plankton. Nat. Commun. 9, 266 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W. & Huse, S. M. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4, e6372 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).

    Article  CAS  PubMed  Google Scholar 

  51. Guillou, L. et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604 (2013).

    Article  CAS  PubMed  Google Scholar 

  52. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    Article  CAS  PubMed  Google Scholar 

  53. McKane, A., Alonso, D. & Solé, R. V. Mean-field stochastic theory for species-rich assembled communities. Phys. Rev. E 62, 8466–8484 (2000).

    Article  CAS  Google Scholar 

  54. Dennis, B. & Patil, G. P. The gamma distribution and weighted multimodal gamma distributions as models of population abundance. Math. Biosci. 68, 187–212 (1984).

    Article  Google Scholar 

  55. Pueyo, S., He, F. & Zillio, T. The maximum entropy formalism and the idiosyncratic theory of biodiversity. Ecol. Lett. 10, 1017–1028 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Green, J. L. & Plotkin, J. B. A statistical theory for sampling species abundances. Ecol. Lett. 10, 1037–1045 (2007).

    Article  PubMed  Google Scholar 

  57. Goldstein, M. L., Morris, S. A. & Yen, G. G. Problems with fitting to the power-law distribution. Eur. Phys. J. B 41, 255–258 (2004).

    Article  CAS  Google Scholar 

  58. Bauke, H. Parameter estimation for power-law distributions by maximum likelihood methods. Eur. Phys. J. B 58, 167–173 (2007).

    Article  CAS  Google Scholar 

  59. Tsallis, C. & Stariolo, D. A. Generalized simulated annealing. Phys. A 233, 395–406 (1996).

    Article  Google Scholar 

  60. Anderson, T. W. & Darling, D. A. Asymptotic theory of certain “goodness of fit” criteria based on stochastic processes. Ann. Math. Stat. 23, 193–212 (1952).

    Article  Google Scholar 

Download references

Acknowledgements

The authors are very grateful to F. d’Ovidio, V. Anjou and S. Audic, who participated in the early stages of this work, O. Missa, G. Sommeria-Klein and E. van Nimwegen for discussions on neutral models and model fitting, and the Tara Oceans consortium. The support of the informatics platform of IBENS has been essential for the computational part of this study. This work has received support under the programmes ‘Investissements d’Avenir’, launched by the French Government and implemented by ANR with the references ANR-10-LABX-54 MEMOLIFE, ANR-10-IDEX-0001-02 PSL* Research University and OCEANOMICS, as well as from the EU project MicroB3. C.B. additionally acknowledges funding from the ERC Advanced Award ‘Diatomite’, the Louis D Foundation of the Institut de France and the Radcliffe Institute of Advanced Study at Harvard University for a scholars fellowship during the 2016/17 academic year. This research was supported in part by National Science Foundation grant NSF PHY-1125915, NIH grant R25GM067110 and Gordon and Betty Moore Foundation grant 2919.01. This article is contribution number 76 of Tara Oceans.

Author information

Authors and Affiliations

Authors

Contributions

S.D.M. conceived and directed the study. E.S.-G. obtained the analytical results, designed the adaptive algorithm and produced the fits. S.M. carried out the preliminary analysis on the protist abundance distributions. L.Z. performed statistical analysis on the fitted parameters. S.D.M., E.S.-G., L.Z. and C.B. interpreted the results and wrote the manuscript. C.D.V. and E.K. provided access to the Tara Oceans dataset and commented on early versions of the manuscript.

Corresponding authors

Correspondence to Enrico Ser-Giacomi or Silvia De Monte.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods and Results, Supplementary Figures 1–4, Supplementary Tables 1–3, Supplementary References

Reporting Summary

Supplementary Data

This supplementary information provides all SADs, RADs and associated fits considered in this study

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ser-Giacomi, E., Zinger, L., Malviya, S. et al. Ubiquitous abundance distribution of non-dominant plankton across the global ocean. Nat Ecol Evol 2, 1243–1249 (2018). https://doi.org/10.1038/s41559-018-0587-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0587-2

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing