Recent observations of biologically generated turbulence in the ocean have led to conflicting conclusions regarding the significance of the contribution of animal swimming to ocean mixing. Measurements indicate elevated turbulent dissipation—comparable with levels caused by winds and tides—in the vicinity of large populations of planktonic animals swimming together1. However, it has also been noted that elevated turbulent dissipation is by itself insufficient proof of substantial biogenic mixing, because much of the turbulent kinetic energy of small animals is injected below the Ozmidov buoyancy length scale, where it is primarily dissipated as heat by the fluid viscosity before it can affect ocean mixing2. Ongoing debate regarding biogenic mixing has focused on comparisons between animal wake turbulence and ocean turbulence3,4. Here, we show that a second, previously neglected mechanism of fluid mixing—first described over 50 years ago by Charles Darwin5— is the dominant mechanism of mixing by swimming animals. The efficiency of mixing by Darwin’s mechanism is dependent on animal shape rather than fluid length scale and, unlike turbulent wake mixing, is enhanced by fluid viscosity. Therefore, it provides a means of biogenic mixing that can be equally effective in small zooplankton and large mammals. A theoretical model for the relative contributions of Darwinian mixing and turbulent wake mixing is created and validated by in situ field measurements of swimming jellyfish using a newly developed scuba-based laser velocimetry device6. Extrapolation of these results to other animals is straightforward given knowledge of the animal shape and orientation during vertical migration. On the basis of calculations of a broad range of aquatic animal species, we conclude that biogenic mixing via Darwin’s mechanism can be a significant contributor to ocean mixing and nutrient transport.
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We acknowledge W. M. Graham, J. H. Costello and H. Swift for assistance in field measurements and M. Schaadt for preparatory dive assistance. Additional logistical support was provided by the Coral Reef Research Foundation. Field work in Palau was supported by the National Science Foundation Biological Oceanography Program (to M. N. Dawson and J.O.D.). Additional support (to J.O.D.) from NSF Biological Oceanography, Ocean Technology, Fluid Dynamics, and Energy for Sustainability and from the Office of Naval Research (K.-H. Kim) is acknowledged, as are NSF and NDSEG fellowships (to K.K.) and the Charles Lee Powell Foundation.
Author Contributions K.K. and J.O.D. designed the study, analysed the data and wrote the manuscript. K.K. performed the experiments and viscous flow simulations. J.O.D. performed the inviscid flow simulations and derivation of equation (1).
This file contains Supplementary Figure S1 with Legend. (PDF 65 kb)
This animated movie file shows the computed fluid drift induced by the vertical passage of a sphere. Trajectories of individual fluid particles are indicated. (MPG 2057 kb)
This animated movie file shows the computed fluid drift induced by the vertical passage of a sphere. Vertical (only) drift of the horizontal layer defined by the fluid particles is indicated. (MPG 2077 kb)
This movie file shows a 5-cm Mastigias sp. jellyfish swimming through a patch of dye injected upstream. Region of forward-drifting dye induced by jellyfish motion is apparent immediately behind the animal. (MPG 1831 kb)
This movie file shows a 8-cm Mastigias sp. jellyfish swimming through a patch of dye injected upstream. Region of forward-drifting dye induced by jellyfish motion is apparent immediately behind the animal. (MPG 1565 kb)
This movie file shows a Mastigias sp. jellyfish swimming through a dye-labelled density stratification. (MPG 1544 kb)
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Katija, K., Dabiri, J. A viscosity-enhanced mechanism for biogenic ocean mixing. Nature 460, 624–626 (2009). https://doi.org/10.1038/nature08207
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