Small-scale turbulent mixing plays a pivotal role in shaping ocean circulation and a broad range of physical and biogeochemical processes. Despite advances in our understanding of the geophysical processes responsible for this mixing, the nature and importance of biomixing—turbulent mixing caused by marine biota—are still debated. A major source of uncertainty pertains to the efficiency of biomixing (the fraction of the turbulent energy produced through swimming that is spent in mixing the ocean vertically), which the few in situ observations available suggest to be much lower than that of geophysical turbulence. Here we shed light on this problem by analysing 14 days of continuous measurements of centimetre-scale turbulence in an area of coastal upwelling. We show that turbulent dissipation is elevated 10- to 100-fold (reaching 10−6–10−5 W kg−1) every night of the survey due to the swimming activity of large aggregations of anchovies that gather regularly over the spawning season. Turbulent mixing is invigorated concurrently with dissipation, and occurs with an efficiency comparable to that of geophysical turbulence. Our results demonstrate that biologically driven turbulence can be a highly effective mixing agent, and call for a re-examination of its impacts on productive upper ocean regions.
This is a preview of subscription content, access via your institution
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
The data that support the findings of this study are available via Zenodo at https://doi.org/10.5281/zenodo.5559023.
The scripts used for microstructure data processing are freely available via GitHub at https://github.com/bieitofernandez/MSS_processing.
Thorpe, S. A. The Turbulent Ocean (Cambridge Univ. Press, 2005).
Winters, K. B., Lombard, P. N., Riley, J. J. & D’Asaro, E. A. Available potential energy and mixing in density-stratified fluids. J. Fluid Mech. 289, 115–128 (1995).
Osborn, T. R. Estimates of the local rate of vertical diffusion from dissipation measurements. J. Phys. Oceanogr. 10, 83–89 (1980).
Oakey, N. S. Determination of the rate of dissipation of turbulent energy from simultaneous temperature and velocity shear microstructure measurements. J. Phys. Ocean. 12, 256–271 (1982).
Smyth, W. D. & Moum, J. N. Marginal instability and deep cycle turbulence in the eastern equatorial Pacific Ocean. Geophys. Res. Lett. 40, 6181–6185 (2013).
Gregg, M., D’Asaro, E., Riley, J. & Kunze, E. Mixing efficiency in the ocean. Ann. Rev. Mar. Sci. 10, 443–473 (2017).
Monismith, S. G., Koseff, J. R. & White, B. L. Mixing efficiency in the presence of stratification: when is it constant? Geophys. Res. Lett. 45, 5627–5634 (2018).
Visser, A. W. Biomixing of the oceans? Science 316, 838–839 (2007).
Wunsch, C. & Ferrari, R. Vertical mixing, energy, and the general circulation of the oceans. Annu. Rev. Fluid Mech. 36, 281–314 (2004).
Munk, W. H. Abyssal recipes. Deep Sea Res. 13, 707–730 (1966).
Kunze, E. Biologically generated mixing in the ocean. Ann. Rev. Mar. Sci. 11, 215–226 (2019).
Katija, K. Biogenic inputs to ocean mixing. J. Exp. Biol. 215, 1040–1049 (2012).
Huntley, M. E. & Zhou, M. Influence of animals on turbulence in the sea. Mar. Ecol. Prog. Ser. 273, 65–79 (2004).
Dewar, W. K. et al. Does the marine biosphere mix the ocean? J. Mar. Res. 64, 541–561 (2006).
Houghton, I. A., Koseff, J. R., Monismith, S. G. & Dabiri, J. O. Vertically migrating swimmers generate aggregation-scale eddies in a stratified column. Nature 556, 497–500 (2018).
Farmer, D. D., Crawford, G. B. & Osborn, T. R. Temperature and velocity microstructure caused by swimming fish. Limnol. Oceanogr. 32, 978–983 (1987).
Kunze, E., Dower, J. F., Bevaridge, I., Bawey, R. & Bartlett, K. P. Observations of biologically generated turbulence in a coastal inlet. Science 313, 1768–1770 (2006).
Rousseau, S., Kunze, E., Dewey, R., Bartlett, K. & Dower, J. On turbulence production by swimming marine organisms in the open ocean and coastal waters. J. Phys. Oceanogr. 40, 2107–2121 (2010).
Lorke, A. & Probst, W. N. In situ measurements of turbulence in fish shoals. Limnol. Oceanogr. 55, 354–364 (2010).
Sato, M., Klymak, J. M., Kunze, E., Dewey, R. & Dower, J. F. Turbulence and internal waves in Patricia Bay, Saanich Inlet, British Columbia. Cont. Shelf Res. 85, 153–167 (2014).
Simoncelli, S., Thackeray, S. J. & Wain, D. J. On biogenic turbulence production and mixing from vertically migrating zooplankton in lakes. Aquat. Sci. 80, 35 (2018).
Gregg, M. C. & Horne, J. K. Turbulence, acoustic backscatter, and pelagic nekton in Monterey Bay. J. Phys. Oceanogr. 39, 1097–1114 (2009).
Pujiana, K., Moum, J. N., Smyth, W. D. & Warner, S. J. Distinguishing ichthyogenic turbulence from geophysical turbulence. J. Geophys. Res. Oceans 120, 3792–3804 (2015).
Álvarez-Salgado, X., Gago, J., Míguez, B., Gilcoto, M. & Pérez, F. Surface waters of the NW Iberian Margin: upwelling on the shelf versus outwelling of upwelled waters from the Rías Baixas. Estuar. Coast. Shelf Sci. 51, 821–837 (2000).
Pardo, P. C., Gilcoto, M. & Pérez, F. F. Short-time scale coupling between thermohaline and meteorological forcing in the Ría de Pontevedra. Sci. Mar. 65, 229240 (2001).
Miles, J. Richardson’s criterion for the stability of stratified shear flow. Phys. Fluids 29, 3470 (1986).
Park, J. et al. Frequency responses of anchovy schools in the South Sea of South Korea in spring and winter. J. Korean Soc. Fish. Technol. 52, 111–120 (2016).
Ferreiro, M. J. El Ictioplancton de la Ría de Vigo. PhD thesis, Univ. Santiago de Compostela (1985).
Motos, L., Uriarte, A. & Valencia, V. The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Sci. Mar. 60, 117–140 (1996).
Motos, L. Reproductive biology and fecundity of the Bay of Biscay anchovy population (Engraulis encrasicolus L.). Sci. Mar. 60, 195–207 (1996).
Sola, A., Motos, L., Franco, C. & Lago de Lanzos, A. Seasonal occurrence of pelagic fish eggs and larvae in the Cantabrian Sea (VIIIc) and Galicia (IXa) from 1987 to 1989. In: ICES Conference and Meeting Documents 1990 H:25 (1990).
Simpson, J. H. et al. The annual cycle of energy input, modal excitation and physical plus biogenic turbulent dissipation in a temperate lake. Water Resour. Res. 57, e2020WR029441 (2021).
Hooper, J. A., Baringer, M. O., St. Laurent, L. C., Dewar, W. K. & Nowacek, D. Dissipation processes in the Tongue of the Ocean. J. Geophys. Res. Oceans 121, 3159–3170 (2016).
Claramunt, G., Cubillos, L., Herrera, G. & Díaz, E. Spawning marker patterns of Engraulis ringens of northern Chile. Fish. Res. 219, 105306 (2019).
Caulfield, C. Layering, instabilities, and mixing in turbulent stratified flows. Annu. Rev. Fluid Mech. 53, 113–145 (2021).
Ivey, G. N. & Imberger, J. On the nature of turbulence in a stratified fluid. Part I: the energetics of mixing. J. Phys. Oceanogr. 21, 650–658 (1991).
Mater, B. D., Schaad, S. M. & Venayagamoorthy, S. K. Relevance of the Thorpe length scale in stably stratified turbulence. Phys. Fluids 25, 076604 (2013).
Mashayek, A. et al. Efficiency of turbulent mixing in the abyssal ocean circulation. Geophys. Res. Lett. 44, 6296–6306 (2017).
Gargett, A. E., Osborn, T. R. & Nasmyth, P. W. Local isotropy and the decay of turbulence in a stratified fluid. J. Fluid Mech. 144, 231–280 (1984).
Massé, J., Uriarte, A., Angélico, M. M. & Carrera, P. Pelagic Survey Series for Sardine and Anchovy in ICES Subareas 8 and 9 (WGACEGG)—Towards an Ecosystem Approach Cooperative Research Report No. 332 (ICES, 2018).
Tanaka, M., Nagai, T., Okada, T. & Yamazaki, H. Measurement of sardine-generated turbulence in a large tank. Mar. Ecol. Prog. Ser. 571, 207–220 (2017).
Largier, J. L. Upwelling bays: how coastal upwelling controls circulation, habitat, and productivity in bays. Ann. Rev. Mar. Sci. 12, 415–447 (2020).
Cury, P. et al. Small pelagics in upwelling systems: patterns of interaction and structural changes in ‘wasp-waist’ ecosystems. ICES J. Mar. Sci. 57, 603–618 (2000).
Huse, G. A spatial approach to understanding herring population dynamics. Can. J. Fish. Aquat. Sci. 73, 177–188 (2016).
Sharples, J. et al. Phytoplankton distribution and survival in the thermocline. Limnol. Oceanogr. 46, 486–496 (2001).
Diaz, R. J. Overview of hypoxia around the world. J. Environ. Qual. 30, 275–281 (2001).
Ibaibarriaga, L. et al. Characterization of stage-classified biological processes using multinomial models: a case study of anchovy (Engraulis encrasicolus) eggs in the Bay of Biscay. Can. J. Fish. Aquat. Sci. 64, 539–553 (2007).
Prandke, H. & Stips, A. Test measurements with an operational microstructure-turbulence profiler: detection limit of dissipation rates. Aquat. Sci. 60, 191–209 (1998).
Levine, E. R. & Lueck, R. G. Turbulence measurement from an autonomous underwater vehicle. J. Atmos. Ocean. Technol. 16, 1533–1544 (1999).
Gregg, M. C. Uncertainties and limitations in measuring ϵ and χ(T). J. Atmos. Ocean. Technol. 16, 1483–1490 (1999).
Batchelor, G. K., Howells, I. D. & Townsend, A. A. Small-scale variation of convected quantities like temperature in turbulent fluid: part 1. General discussion and the case of small conductivity. J. Fluid Mech. 5, 113–133 (1959).
Piccolroaz, S., Fernández-Castro, B., Toffolon, M. & Dijkstra, H. A. A multi-site, year-round turbulence microstructure atlas for the deep perialpine Lake Garda. Sci. Data 8, 188 (2021).
Osborn, T. R. & Cox, C. S. Oceanic fine structure. Geophys. Fluid Dynam. 3, 321–345 (1972).
Thorpe, S. A. Turbulence and mixing in a Scottish Loch. Phil. Trans. R. Soc. Lond. A 286, 125–181 (1977).
Demer, D. A. et al. Calibration of Acoustic Instruments Cooperative Research Report No. 326 (ICES, 2015).
Moser, M. H. & Ahlstrom, E. H. in An Egg Production Method for Estimating Spawning Biomass of Pelagic Fish: Application to the Northern Anchovy, Engraulis mordax. NOAA Technical Report No. NMFS 36, 37–42 (US Department of Commerce, 1985).
Deines, K. L. Backscatter estimation using broadband acoustic Doppler current profilers. In Proc. IEEE Sixth Working Conference on Current Measurement 249–253 (IEEE, 1999); https://doi.org/10.1109/CCM.1999.755249
Mullison, J. Backscatter Estimation Using Broadband Acoustic Doppler Current Profilers–Updated Application Note FSA-031 (Teledyne RD Instruments, 2017).
Peraltilla, S. & Bertrand, S. In situ measurements of the speed of Peruvian anchovy schools. Fish. Res. 149, 92–94 (2014).
Funding for this work was provided by the Spanish Ministry of Economy and Innovation under the research project REMEDIOS (grant number CTM2016-75451-C2-1-R) to B.M.-C. B.F.C. was supported by the Spanish Ministry of Economy and Innovation through a Juan de La Cierva-Formación postdoctoral fellowship (grant number FJCI-641 2015-25712) and by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement number 834330 (SO-CUP). E.B. was supported by a postgraduate fellowship (grant number ED481A-2019/288) from Xunta de Galicia, co-funded by FSE Galicia. A.C. was supported by a postgraduate fellowship FPI (grant number BES-2017-080935) from the Spanish Ministry of Economy and Competitiveness. A.C.N.G. acknowledges the support of the Royal Society and the Wolfson Foundation. We thank all the participants in the REMEDIOS cruise, particularly the crew of the RV Ramón Margalef for their support, and P. Rial, I. Ramilo and M. Villamaña for their contribution to data collection. We are also thankful to G. Casas for his assistance in counting and staging anchovy eggs. We are especially grateful to P. Chouciño for her logistical support during the cruise and assistance with microstructure data processing. S. Piccoloraz and Ó. Sepúlveda Steiner contributed to the development of the microstructure processing functions. C. Ofelio designed the illustration in Fig. 4.
The authors declare no competing interests.
Peer review information
Nature Geoscience thanks Jonathan Nash, Hidekatsu Yamazaki and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Simon Harold, Kyle Frischkorn and James Super, in collaboration with the Nature Geoscience team.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Map of the location of the REMEDIOS sampling station P2-Bueu (red star, 42.357°N, 8.773°W, mean depth 30 m) in the Ría de Pontevedra (off the Galician coast, NW Iberian Peninsula). The location of the closest Meteogalicia (www.meteogalicia.gal) meteorological station (yellow dot, Cape Udra, 42.340°N, -8.884°E) is also shown.
Hourly mean time series of a salinity, b de-tided eastward velocity (u), c squared buoyancy frequency (N2), and d squared vertical shear of horizontal velocity (sh2) during the three sampling periods (I01, I02 and I03). Gray shading indicates night-time periods of enhanced biophysical turbulence. These periods were determined by inspection of the turbulent dissipation rate and volume backscattering strength records. De-tided residual velocity was calculated with a 24/25/24 h Godin filter. Positive eastward velocity imports offshore waters into the Ría, and negative westward velocity exports onshore waters out of the Ría. Note the use of logarithmic color scale in panels c and d.
Depth-averaged (10–25 m) ε vs. a depth-averaged Rig and b 38 KHz volume backscattering strength (Sv). ε median values in bins of Rig and Sv38kHz are indicated as larger circles. Linear fits in logarithmic scale and Spearman correlation coefficients are shown. The dot color scale represents Sv38kHz and Rig in panels a and b, respectively.
Three examples of night-time echograms at 18 KHz, recorded during sampling periods I01 (a, 4 July), I02 (b, 8 July) and I03 (c, 12 July). Panels d-f show the mean frequency response (Sv at each frequency minus Sv at 38 kHz) for the region enclosed by the orange rectangles in panels a-c.
Randomly selected wavenumber (kz, units: cycles per meter, cpm) spectra of vertical shear (a-d) and temperature gradient (e, f) microstructure between 10 and 25 m depth, during the third sampling period (I03). Periods dominated by geophysical turbulence are shown in the left column, and those dominated by biophysical turbulence (gray shading in Figure 1), in the right column. The corresponding universal spectra are indicated by dotted colored lines, and the computed dissipation rates of turbulent kinetic energy (ε) and thermal variance (χ) are reported. Spectra recorded with the two shear sensors over the same portion of the water column are shown a, b and c, d, respectively. Empirical spectra of thermistor noise are represented by the gray dotted line e,f.
Time series of hourly mean a rate of dissipation of thermal variance (χ), b Thorpe scale (LT), c buoyancy Reynolds number (Reb), d turbulent Reynolds number (ReT), d turbulent Froude number (FrT), and f flux Richardson number (Rf, a proxi for mixing efficiency) during the three sampling periods (I01, I02 and I03). Gray shading indicates night-time periods of enhanced biophysical turbulence. Note the use of a logarithmic color scale in all panels.
Time series of volume backscattering strength (Sv, dB) measured with a 300 KHz bottom-moored ADCP. Nights and biomixing events during the sampling periods (I01, I02 and I03) are indicated with black and gray shading, respectively. The y-axis coordinate is meters above bottom (mab).
About this article
Cite this article
Fernández Castro, B., Peña, M., Nogueira, E. et al. Intense upper ocean mixing due to large aggregations of spawning fish. Nat. Geosci. 15, 287–292 (2022). https://doi.org/10.1038/s41561-022-00916-3