Throughout the ocean, countless small animals swim to depth in the daytime, presumably to seek refuge from large predators1,2. These animals return to the surface at night to feed1,2. This substantial diel vertical migration can result in the transfer of significant amounts of carbon and nutrients from the surface to depth3,4,5,6,7. However, its consequences on ocean chemistry at the global scale have remained uncertain8,9. Here, we determine the depths of these diel migrations in the global ocean using a global array of backscatter data from acoustic Doppler current profilers, collected between 1990 and 2011. We show that the depth of diel migration follows coherent large-scale patterns. We find that migration depth is greater where subsurface oxygen concentrations are high, such that seawater oxygen concentration is the best single predictor of migration depth at the global scale. In oxygen minimum zone areas, migratory animals generally descend as far as the upper margins of the low-oxygen waters. Using an ocean biogeochemical model coupled to a general circulation model, we show that by focusing oxygen consumption in poorly ventilated regions of the upper ocean, diel vertical migration intensifies oxygen depletion in the upper margin of oxygen minimum zones. We suggest that future changes in the extent of oxygen minimum zones could alter the migratory depths of marine organisms, with consequences for marine biogeochemistry, food webs and fisheries.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Vinogradov, M. E. Vertical Distribution of the Oceanic Zooplankton (Nauka, 1968).
Longhurst, A. R. The Ecology of the Seas 116–137 (Blackwell Science, 1976).
Longhurst, A. R. & Harrison, W. G. Vertical nitrogen flux from the oceanic photic zone by diel migrant zooplankton and nekton. Deep-Sea Res. I 35, 881–889 (1988).
Zhang, X. S. & Dam, H. G. Downward export of carbon by diel migrant mesozooplankton in the central equatorial Pacific. Deep-Sea Res. II 44, 2191–2202 (1997).
Steinberg, D. K., Cope, J. S., Wilson, S. E. & Kobari, T. A comparison of mesopelagic mesozooplankton community structure in the subtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 55, 1615–1635 (2008).
Hernandez-Leon, S. & Ikeda, T. Respiration in Aquatic Environment 57–82 (Oxford Univ. Press, 2005).
Hidaka, K., Kawaguchi, K., Murakami, M. & Takahashi, M. Downward transport of organic carbon by diel migratory micronekton in the western equatorial Pacific: Its quantitative and qualitative importance. Deep-Sea Res. I 48, 1923–1939 (2001).
Robinson, C. et al. Mesopelagic zone ecology and biogeochemistry—a synthesis. Deep-Sea Res. II 57, 1504–1518 (2010).
Buesseler, K. O. & Boyd, P. W. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54, 1210–1232 (2009).
Jennings, S. et al. Global-scale predictions of community and ecosystem properties from simple ecological theory. Proc. R. Soc. B 275, 1375–1383 (2008).
Murray, J. & Hjort, J. The Depths of the Ocean (Macmillan, 1912).
Eyring, C. F., Christensen, R. J. & Raitt, R. W. Reverberation in the Sea. J. Acoust. Soc. Am. 20, 462–475 (1948).
Barham, E. G. Deep scattering layer migration and composition—observations from a diving saucer. Science 151, 1399 (1966).
Roe, H. S. J. et al. The diel migrations and distributions within a mesopelagic community in the Northeast Atlantic. 1. Introduction and sampling procedures. Prog. Oceanogr. 13, 245–268 (1984).
Luo, J. G., Ortner, P. B., Forcucci, D. & Cummings, S. R. Diel vertical migration of zooplankton and mesopelagic fish in the Arabian Sea. Deep-Sea Res. II 47, 1451–1473 (2000).
Ashjian, C. J., Smith, S. L., Flagg, C. N. & Idrisi, N. Distribution, annual cycle, and vertical migration of acoustically derived biomass in the Arabian Sea during 1994–1995. Deep-Sea Res. II 49, 2377–2402 (2002).
Lampert, W. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3, 21–27 (1989).
Wishner, K. F., Gowing, M. M. & Gelfman, C. Mesozooplankton biomass in the upper 1000 m in the Arabian Sea: Overall seasonal and geographic patterns, and relationship to oxygen gradients. Deep-Sea Res. II 45, 2405–2432 (1998).
Cohen, J. H. & Forward, R. B. Zooplankton diel vertical migration—a review of proximate control. Oceanogr. Mar. Biol. 47, 77–109 (2009).
Seibel, B. A. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J. Exp. Biol. 214, 326–336 (2011).
Stramma, L. et al. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nature Clim. Change 2, 33–37 (2012).
Galbraith, E. D., Gnanadesikan, A., Dunne, J. P. & Hiscock, M. R. Regional impacts of iron-light colimitation in a global biogeochemical model. Biogeosciences 7, 1043–1064 (2010).
Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. Vertex—carbon cycling in the northeast pacific. Deep-Sea Res. 34, 267–285 (1987).
Bianchi, D., Dunne, J. P., Sarmiento, J. L. & Galbraith, E. D. Data-based estimates of suboxia, denitrification, and N2O production in the ocean and their sensitivities to dissolved O2 . Glob. Biogeochem. Cycles 26 http://dx.doi.org/10.1029/2011GB004209 (2012).
Childress, J. J. & Seibel, B. A. Life at stable low oxygen levels: Adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201, 1223–1232 (1998).
Wyrtki, K. The oxygen minima in relation to ocean circulation. Deep-Sea Res. 9, 11–23 (1962).
Keeling, R. F., Kortzinger, A. & Gruber, N. Ocean deoxygenation in a warming world. Annu. Rev. Mar. Sci. 2, 199–229 (2010).
Steinberg, D. K., Lomas, M. W. & Cope, J. S. Long-term increase in mesozooplankton biomass in the Sargasso Sea: Linkage to climate and implications for food web dynamics and biogeochemical cycling. Glob. Biogeochem. Cycles 26 http://dx.doi.org/10.1029/2010GB004026 (2012).
Flagg, C. N. & Smith, S. L. On the use of the acoustic doppler current profiler to measure zooplankton abundance. Deep-Sea Res. I 36, 455–474 (1989).
Heywood, K. J., Scropehowe, S. & Barton, E. D. Estimation of zooplankton abundance from ship-borne adcp backscatter. Deep-Sea Res. I 38, 677–691 (1991).
The authors thank J. L. Sarmiento and J. P. Dunne for insightful comments on the project, P. Caldwell for kindly providing the JASADCP data and D. Balachandran for preliminary analysis. D.B. and E.D.G. were financially supported by the Canadian Institute for Advanced Research (CIFAR) Earth System Evolution Program. K.A.S. was financially supported by the Carbon Mitigation Initiative with support from BP and the NOAA Cooperative Institute for Climate Science. D.A.C. acknowledges the support of SSHRC of Canada. Computation resources were provided by the SciNet HPC consortium, the Canada Foundation for Innovation and Compute Canada.
The authors declare no competing financial interests.
About this article
Cite this article
Bianchi, D., Galbraith, E., Carozza, D. et al. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nature Geosci 6, 545–548 (2013). https://doi.org/10.1038/ngeo1837
Distribution, associations and role in the biological carbon pump of Pyrosoma atlanticum (Tunicata, Thaliacea) off Cabo Verde, NE Atlantic
Scientific Reports (2021)
Scientific Data (2021)
Phylogenetic positions of “pico-sized” radiolarians from middle layer waters of the tropical Pacific
Progress in Earth and Planetary Science (2020)
Nature Geoscience (2020)
In situ observations show vertical community structure of pelagic fauna in the eastern tropical North Atlantic off Cape Verde
Scientific Reports (2020)