Article

Turbulence drives microscale patches of motile phytoplankton

  • Nature Communications 4, Article number: 2148 (2013)
  • doi:10.1038/ncomms3148
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Abstract

Patchiness plays a fundamental role in phytoplankton ecology by dictating the rate at which individual cells encounter each other and their predators. The distribution of motile phytoplankton species is often considerably more patchy than that of non-motile species at submetre length scales, yet the mechanism generating this patchiness has remained unknown. Here we show that strong patchiness at small scales occurs when motile phytoplankton are exposed to turbulent flow. We demonstrate experimentally that Heterosigma akashiwo forms striking patches within individual vortices and prove with a mathematical model that this patchiness results from the coupling between motility and shear. When implemented within a direct numerical simulation of turbulence, the model reveals that cell motility can prevail over turbulent dispersion to create strong fractal patchiness, where local phytoplankton concentrations are increased more than 10-fold. This ‘unmixing’ mechanism likely enhances ecological interactions in the plankton and offers mechanistic insights into how turbulence intensity impacts ecosystem productivity.

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Acknowledgements

We thank David Kulis and Donald Anderson for supplying H. akashiwo, Calcul en Midi-Pyrénées and Cineca Supercomputing Center for use of high-performance computational facilities, and Katharine Coyte, Kevin Foster, Nuno Oliveira and Jonas Schluter for comments on the manuscript. We acknowledge the support of the Human Frontier Science Program (to W.M.D.), MIUR PRIN-2009PYYZM5 and EU COST Action MP0806 (to G.B., M.C. and F.D.), MIT MISTI-France program (to E.C. and R.S.), and NSF grants OCE-0744641-CAREER and CBET-1066566 (to R.S.).

Author information

Affiliations

  1. Ralph M. Parsons Laboratory, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, USA

    • William M. Durham
    • , Michael Barry
    •  & Roman Stocker
  2. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • William M. Durham
  3. Institut de Mécanique des Fluides, Université de Toulouse, INPT–UPS–CNRS, Allée du Pr. Camille Soula, F-31400 Toulouse, France

    • Eric Climent
  4. DICCA, Università di Genova, via Montallegro 1, Genova 16145, Italy

    • Filippo De Lillo
  5. Dipartimento di Fisica and INFN, Università di Torino, via P. Giuria 1, Torino 10125, Italy

    • Filippo De Lillo
    •  & Guido Boffetta
  6. Istituto dei Sistemi Complessi, Consiglio Nazionale delle Ricerche, via dei Taurini 19, Rome 00185, Italy

    • Massimo Cencini

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Contributions

W.M.D., M.B. and R.S. were responsible for vortex experiments and simulations thereof, W.M.D., E.C., F.D.L., G.B., M.C. and R.S. performed and analysed DNS simulations, F.D.L., G.B. and M.C. developed analytical tools to interpret DNS simulations, W.M.D. and R.S. wrote the paper with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to William M. Durham or Roman Stocker.

Supplementary information

PDF files

  1. 1.

    Supplementary Figures, Table, Methods and References.

    Supplementary Figures S1-S9, Supplementary Table S1, Supplementary Methods and Supplementary References.

Videos

  1. 1.

    Supplementary Movie 1

    Phytoplankton motility in a steady vortex pair drives aggregations of cells. The toxic phytoplankton species Heterosigma akashiwo swimming within the central plane of the experimental device forms patches within the central downwelling region and within the vortex cores. The first still image shows cell trajectories collected over 1.5 s of the experiment. Non-motile, killed cells did not form aggregations. The arrow denotes the direction of gravity.

  2. 2.

    Supplementary Movie 2

    A model of gyrotactic cell motility accurately captures the patterns of cell patchiness observed in experiments. An individual-based model of gyrotaxis embedded within a simulation of the experimental flow field shows agreement with patterns of cell patchiness observed in experiments (Supplementary Movie 1). The model was parameterized with measured motility parameters of H. akashiwo. The simulation was developed using the experimental device's exact geometry and imposed flow rates. The arrow denotes the direction of gravity.

  3. 3.

    Supplementary Movie 3

    Gyrotactic motility in turbulence unmixes the distribution of cells, forming intense patches. An isotropic, homogenous turbulent flow (Re? = 36) seeded with 104 cells whose trajectories are governed by the equations of gyrotaxis (with ?=0.6 and F=3), shows that an initially random distribution of motile cells rapidly forms patches, increasing the local cell concentrations by more than tenfold. Non-motile cells remain randomly distributed. Time t is non-dimensionalized by the Kolmogorov timescale 1/?K. The cells' preferred swimming direction, k, is vertically upwards.

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