Abstract

A dominant Antarctic ecological paradigm suggests that winter sea ice is generally the main feeding ground for krill larvae. Observations from our winter cruise to the southwest Atlantic sector of the Southern Ocean contradict this view and present the first evidence that the pack-ice zone is a food-poor habitat for larval development. In contrast, the more open marginal ice zone provides a more favourable food environment for high larval krill growth rates. We found that complex under-ice habitats are, however, vital for larval krill when water column productivity is limited by light, by providing structures that offer protection from predators and to collect organic material released from the ice. The larvae feed on this sparse ice-associated food during the day. After sunset, they migrate into the water below the ice (upper 20 m) and drift away from the ice areas where they have previously fed. Model analyses indicate that this behaviour increases both food uptake in a patchy food environment and the likelihood of overwinter transport to areas where feeding conditions are more favourable in spring.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Marr, J. W. S. The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Rep. 32, 33–464 (1962).

  2. 2.

    Croxall, J. P., Reid, K. & Prince, P. A. Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar. Ecol. Prog. Ser. 177, 115–131 (1999).

  3. 3.

    Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432, 100–103 (2004).

  4. 4.

    Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).

  5. 5.

    Siegel, V. Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biol. 29, 1–22 (2005).

  6. 6.

    Quetin, L. B. et al. Growth of larval krill, Euphausia superba, in fall and winter west of the Antarctic Peninsula. Mar. Biol. 143, 833–843 (2003).

  7. 7.

    Quetin, L. B., Ross, R. M., Fritsen, C. H. & Vernet, M. Ecological responses of Antarctic krill to environmental variability: can we predict the future? Antarct. Sci. 19, 253–266 (2007).

  8. 8.

    Ross, R. M., Quetin, L. B., Newberger, T. & Oakes, S. A. Growth and behaviour of larval krill (Euphausia superba) under the ice in late winter 2001 west of the Antarctic Peninsula. Deep-Sea Res. Pt II 51, 2169–2184 (2004).

  9. 9.

    Ross, R. M. et al. Trends, cycles, interannual variability for three pelagic species west of the Antarctic Peninsula 1993−2008. Mar. Ecol. Prog. Ser. 515, 11–32 (2014).

  10. 10.

    Reiss, C. S. et al. Overwinter habitat selection by Antarctic krill under varying sea-ice conditions: implications for top predators and fishery management. Mar. Ecol. Prog. Ser. 568, 1–16 (2017).

  11. 11.

    Lowe, A. T., Ross, R. M., Quetin, L. B., Vernet, M. & Fritsen, C. H. Simulating larval Antarctic krill growth and condition factor during fall and winter in response to environmental variability. Mar. Ecol. Prog. Ser. 452, 27–43 (2012).

  12. 12.

    Ryabov, A. B., de Roos, A. M., Meyer, B., Kawaguchi, S. & Blasius, B. Competition-induced starvation drives large-scale population cycles in Antarctic krill. Nat. Ecol. Evol. 1, 0177 (2017).

  13. 13.

    Fritsen, C. H., Memmott, J. & Stewart, F. J. Inter-annual sea-ice dynamics and micro-algal biomass in winter pack ice of Marguerite Bay, Antarctica. Deep-Sea Res. Pt II 55, 2059–2067 (2008).

  14. 14.

    Meyer, B. et al. Physiology, growth and development of larval krill Euphausia superba in autumn and winter in the Lazarev Sea, Antarctica. Limnol. Oceanogr. 54, 1595–1614 (2009).

  15. 15.

    Daly, K. L. Overwintering growth and development of larval Euphausia superba: an interannual comparison under varying environmental conditions west of the Antarctic Peninsula. Deep-Sea Res. Pt II 51, 2139–2168 (2004).

  16. 16.

    Murphy, E. J. et al. Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centered food web. Phil. Trans. R. Soc. B 362, 113–148 (2007).

  17. 17.

    Thorpe, S. E., Murphy, E. J. & Watkins, J. L. Circumpolar connections between Antarctic krill (Euphausia superba Dana) populations: investigating the roles of ocean and sea ice transport. Deep-Sea Res. Pt I 54, 792–810 (2007).

  18. 18.

    Melbourne-Thomas, J. et al. Under-ice habitats for Antarctic krill larvae: could less mean more under climate warming? Geophys. Res. Lett. 43, 10322–10327 (2016).

  19. 19.

    Meehl G. et al. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) Ch. 10 (Cambridge Univ. Press, Cambridge, 2007).

  20. 20.

    Meyer, B. The overwintering of Antarctic krill, Euphausia superba, from an ecophysiological perspective. A Review. Polar Biol. 35, 15–37 (2012).

  21. 21.

    Frazer, T. K., Quetin, L. B. & Ross, R. M. Abundance, size and developmental stages of larval krill, Euphausia superba, during winter in ice-covered seas west of the Antarctic Peninsula. J. Plank. Res. 24, 1067–1077 (2002).

  22. 22.

    Quetin, L. B., Ross, R. M., Frazer, T. K. & Haberman, K. I. Factors affecting distribution and abundance of zooplankton, with an emphasis on Antarctic krill Euphausia superba. Antarct. Res. Ser. 70, 357–371 (1996).

  23. 23.

    Heywood, R. B., Everson, I. & Priddle, J. The absence of krill from the South Georgia zone, winter 1983. Deep-Sea Res. 32, 369–378 (1985).

  24. 24.

    Morris, D. J. & Priddle, J. Observation on the feeding and moulting of the Antarctic krill, Euphausia superba Dana, in winter. Brit. Antarct. Surv. Bull. 65, 57–63 (1984).

  25. 25.

    Marra, J. & Boardman, C. Late winter chlorophyll a distribution in the Weddell Sea. Mar. Ecol. Prog. Ser. 19, 197–208 (1984).

  26. 26.

    Meiners, K. M. et al. Chlorophyll a in Antarctic sea ice from historical ice core data. Geophys. Res. Lett. 39, L21602 (2012).

  27. 27.

    Atkinson, A. et al. Oceanic circumpolar habitats of Antarctic krill. Mar. Ecol. Prog. Ser. 362, 1–23 (2008).

  28. 28.

    Hewitt, R. P. et al. Variation in the biomass density and demography of Antarctic krill in the vicinity of the South Shetland Islands during the 1999/2000 austral summer. Deep-Sea Res. Pt II 51, 1411–1419 (2004).

  29. 29.

    Siegel, V. et al. Krill demography and large-scale distribution in the southwest Atlantic during January/February 2000. Deep-Sea Res. Pt II 51, 1253–1273 (2004).

  30. 30.

    Nicol, S. et al. Ocean circulation off east Antarctica affects structure and sea-ice extent. Nature 406, 204–507 (2000).

  31. 31.

    Piñones, A., Hoffmann, E. E., Daly, K. L. & Dinniman, S. Modeling environmental controls on the transport and fate of early life stages of Antarctic krill (Euphausia superba) on the western Antarctic Peninsula continental shelf. Deep-Sea Res. Pt I 82, 17–31 (2013).

  32. 32.

    Montes-Hugo, M. et al. Recent changes in phytoplankton communities associated with rapid regional climate change along the western Antarctic Peninsula. Science 323, 1470–1473 (2009).

  33. 33.

    Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).

  34. 34.

    Rose, J. M. et al. Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages. Biogeosciences 6, 3131–3147 (2009).

  35. 35.

    Hoppema, M. et al. Whole season net community production in the Weddell Sea. Polar Biol. 31, 101–111 (2007).

  36. 36.

    Arrigo, K. R., van Dijken, G. L. & Bushinsky, S. Primary production in the Southern Ocean, 1997–2006. J. Geophys. Res. 113, C08004 (2008).

  37. 37.

    de Jong, J. et al. Natural iron fertilization of the Atlantic sector of the Southern Ocean by continental shelf sources of the Antarctic Peninsula. J. Geophys. Res. 117, G01029 (2012).

  38. 38.

    Wiedenmann, J., Cresswell, K. A. & Mangel, M. Connecting recruitment of Antarctic krill and sea ice. Limnol. Oceanogr. 54, 799–811 (2009).

  39. 39.

    Knap, A., Michaels, A., Close, A., Ducklow, H. & Dickson, A. Measurement of chlorophyll a and phaeopigments by fluorometric analysis. JGOFS Rep. 19, 118–122 (1996).

  40. 40.

    Haas, C., Lobach, J., Hendricks, S., Rabenstein, L. & Pfaffling, A. Helicopter-borne measurements of sea ice thickness, using a small and lightweight, digital EM system. J. Appl. Geophys. 67, 234–241 (2009).

  41. 41.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2014); http://www.R-project.org/

  42. 42.

    Meyer, B., Atkinson, A., Blume, B. & Bathmann, U. V. Feeding and energy budgets of larval Antarctic krill Euphausia superba in summer. Mar. Ecol. Prog. Ser. 257, 167–178 (2003).

  43. 43.

    Pakhomov, E. A., Atkinson, A., Meyer, B., Oettl, B. & Bathmann, U. Daily rations and growth of larval Euphausia superba in the Eastern Bellingshausen Sea during austral autumn. Deep-Sea Res. Pt II 51, 2185–2198 (2004).

  44. 44.

    Fraser, F. C. On the development and distribution of young stages of krill (Euphausia superba). Discovery Rep. 24, 1–192 (1936).

  45. 45.

    Meyer, B. et al. Seasonal variation in body composition, metabolic activity, feeding, and growth of adult krill Euphausia superba in the Lazarev Sea. Mar. Ecol. Prog. Ser. 398, 1–18 (2010).

  46. 46.

    Nicol, S. et al. Condition of Euphausia crystallorophias off East Antarctica in winter in comparison to other seasons. Deep-Sea Res. Pt II 51, 2215–2224 (2004).

  47. 47.

    O’Brien, C., Virtue, P., Kawaguchi, S. & Nichols, P. D. Aspects of krill growth and condition during late winter–early spring of East Antarctica (110–130°E). Deep-Sea Res. Pt II 58, 1211–1221 (2010).

  48. 48.

    Quetin, L. B. & Ross, R. M. Behavioural and physiological characteristics of the Antarctic krill Euphausia superba. Am. Zool. 31, 49–63 (1991).

  49. 49.

    Gradinger, R. & Bluhm, B. Timing of ice algal grazing by the Arctic nearshore benthic amphipod Onisimus litoralis. Arctic 63, 355–358 (2010).

  50. 50.

    Scott, F. J. & Marchant, H. Antarctic Marine Protists (Australian Antarctic Division, Hobart Australian Biological Resources Study, Canberra, 2005).

  51. 51.

    Thresher, R. E. & Gunn, J. S. Comparative analysis of visual census techniques for highly mobile, reef-associated piscivores (Carangidae). Environ. Biol. Fish. 17, 93–116 (1986).

  52. 52.

    Efron, B. & Tibshirani, R. Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statist. Sci. 1, 54–77 (1986).

  53. 53.

    Buckland, S. T. Monte-Carlo confidence intervals. Biometrics 40, 811–817 (1984).

  54. 54.

    Grimm, V. et al. The ODD protocol: a review and first update. Ecol. Model. 221, 2760–2768 (2010).

  55. 55.

    Renner, A. H. H., Heywood, K. J. & Thorpe, S. E. Validation of three global ocean models in the Weddell Sea. Ocean Model. 30, 1–15 (2009).

  56. 56.

    Tschudi, M., Fowler, C., Maslanik, J., Stewart, J. S. & Meier, W. Polar Pathfinder Daily 25 km EASE-Grid Sea Ice Motion Vectors, Version 3 (National Snow and Ice Data Center, Boulder, CO, 2013); https://doi.org/10.5067/O57VAIT2AYYY

  57. 57.

    Schwegmann, S., Haas, C., Fowler, C. & Gerdes, R. A. Comparison of satellite-derived sea-ice motion with drifting-buoy data in the Weddell Sea, Antarctica. Ann. Glaciol. 52, 103–110 (2011).

  58. 58.

    McPhee, M. G. & Martinson, D. G. Turbulent mixing under drifting pack ice in the Weddell Sea. Science 263, 218–221 (1994).

  59. 59.

    Cole, S. T., Timmermans, M. L., Toole, J. M., Krishfield, R. A. & Thwaites, F. T. Ekman veering, internal waves, and turbulence observed under Arctic sea ice. J. Phys. Oceanogr. 44, 1306–1328 (2014).

  60. 60.

    Bailey, D. et al. Community Ice CodE (CICE) User’s Guide Version 4.0 (National Center for Atmospheric Research, 2010).

Download references

Acknowledgements

We thank the captain and crew of RV Polarstern expedition WISKY (ANTXXIX-7) as well as our helicopter teams for their excellent support with work at sea, R. Schlicht for statistical consultation and B. Raymond for technical contribution to present results. This work was funded by the PACES (Polar Regions and Coasts in a changing Earth System) programme (Topic 1, WP 5) of the Helmholtz Association. Additional funds were made available via the Helmholtz Virtual Institute ‘PolarTime’ (VH-VI-500: Biological timing in a changing marine environment—clocks and rhythms in polar pelagic organisms) and the Australian Government through Antarctic Science grant #4073 and the Antarctic Climate and Ecosystem Cooperative Research Centre. S.E.T. and E.J.M. were funded by the Natural Environment Research Council under British Antarctic Survey National Capability-Ecosystems. The surface velocity data were produced by Ssalto/Duacs and distributed by Aviso, with support from Cnes (http://www.aviso.altimetry.fr/duacs/). TerraSAR-X images used to identify sampling sites were provided by German Space Agency (DLR) via the proposal “Investigation of the role of sea ice and snow properties on Antarctic krill distribution and condition in winter/spring”. We thank T. Busche (DLR) and E. Schwarz (DLR) for organizing near-real time image delivery on board of Polarstern.

Author information

Affiliations

  1. Department of Biosiences, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Section Polar Biological Oceanography, Bremerhaven, Germany

    • Bettina Meyer
    • , Ulrich Freier
    • , Christine Klaas
    • , Laura Halbach
    •  & Mathias Teschke
  2. Institute for Chemistry and Biology of the Marine Environment, Carl von Ossietzky University Oldenburg, Oldenburg, Germany

    • Bettina Meyer
  3. Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg, Oldenburg, Germany

    • Bettina Meyer
  4. SC-Scientific Consulting, Neuss, Germany

    • Ulrich Freier
  5. Department of Ecological Modelling, Helmholtz Centre for Environmental Research—UFZ, Leipzig, Germany

    • Volker Grimm
  6. Institute of Forest Growth and Computer Science, Technische Universität Dresden, Tharandt, Germany

    • Jürgen Groeneveld
  7. Department of Earth and Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada

    • Brian P. V. Hunt
    •  & Evgeny Pakhomov
  8. Hakai Institute, Heriot Bay, British Columbia, Canada

    • Brian P. V. Hunt
  9. Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, British Columbia, Canada

    • Brian P. V. Hunt
    •  & Evgeny Pakhomov
  10. Department of Agriculture, Forestry and Fisheries, Fisheries Research and Development, Cape Town, South Africa

    • Sven Kerwath
    •  & Lutz Auerswald
  11. Department of Biological Sciences, University of Cape Town, Rondebosch, South Africa

    • Sven Kerwath
  12. Department of Animal Sciences, Stellenbosch University, Stellenbosch, South Africa

    • Sven Kerwath
    •  & Lutz Auerswald
  13. Department of the Environment and Energy, Australian Antarctic Division, Kingston, Tasmania, Australia

    • Rob King
    • , Klaus M. Meiners
    • , Jessica Melbourne-Thomas
    • , Simon Jarman
    • , So Kawaguchi
    •  & Michael Sumner
  14. Antarctic Climate and Ecosystems Cooperative Research Centre, University of Tasmania, Hobart, Tasmania, Australia

    • Klaus M. Meiners
    • , Jessica Melbourne-Thomas
    • , So Kawaguchi
    • , Michael Sumner
    •  & Rowan Trebilco
  15. British Antarctic Survey, Natural Environment Research Council, Cambridge, UK

    • Eugene J. Murphy
    •  & Sally E. Thorpe
  16. Institute of Arctic and Alpine Research, University of Colorado, Boulder, CO, USA

    • Sharon Stammerjohn
  17. Department of Biosiences, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Section Marine BioGeoScience, Bremerhaven, Germany

    • Dieter Wolf-Gladrow
    •  & Gernot Nehrke
  18. South African Environmental Observation Network, Elwandle Node, Grahamstown, South Africa

    • Albrecht Götz
  19. Department of Ichthyology and Fisheries Science, Rhodes University, Grahamstown, South Africa

    • Albrecht Götz
  20. Zoology Department, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa

    • Albrecht Götz
  21. Trace and Environmental DNA (TrEnD) Laboratory, Department of Environment and Agriculture, Curtin University, Bentley, Western Australia, Australia

    • Simon Jarman
  22. Department Climate Sciences, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Section Sea Ice Physics, Bremerhaven, Germany

    • Thomas Krumpen
    •  & Robert Ricker
  23. Institute of Marine Sciences and Management, Istanbul University, Istanbul, Turkey

    • Noyan I. Yilmaz

Authors

  1. Search for Bettina Meyer in:

  2. Search for Ulrich Freier in:

  3. Search for Volker Grimm in:

  4. Search for Jürgen Groeneveld in:

  5. Search for Brian P. V. Hunt in:

  6. Search for Sven Kerwath in:

  7. Search for Rob King in:

  8. Search for Christine Klaas in:

  9. Search for Evgeny Pakhomov in:

  10. Search for Klaus M. Meiners in:

  11. Search for Jessica Melbourne-Thomas in:

  12. Search for Eugene J. Murphy in:

  13. Search for Sally E. Thorpe in:

  14. Search for Sharon Stammerjohn in:

  15. Search for Dieter Wolf-Gladrow in:

  16. Search for Lutz Auerswald in:

  17. Search for Albrecht Götz in:

  18. Search for Laura Halbach in:

  19. Search for Simon Jarman in:

  20. Search for So Kawaguchi in:

  21. Search for Thomas Krumpen in:

  22. Search for Gernot Nehrke in:

  23. Search for Robert Ricker in:

  24. Search for Michael Sumner in:

  25. Search for Mathias Teschke in:

  26. Search for Rowan Trebilco in:

  27. Search for Noyan I. Yilmaz in:

Contributions

B.M. and U.F. designed the research and B.M. wrote the paper with support from the co-authors. U.F., S.K. and A.G. designed the scientific dive operations with support from I.N.Y., G.N., M.T. and L.A. Ice physical investigations were performed by T.K., R.R., K.M.M. and S.S. The foraging model was designed by J.G. with support from V.G. S.E.T. and E.J.M. worked on the advection model, whereas J.M.-T., R.T., M.S., S.K. and K.M.M. performed the sea-ice model. Larval krill morphology, physiology and abundance data were collected and processed by R.K., L.H., E.P., B.P.V.H., M.T., S.J. and B.M. Sea-ice biology data were collected and analysed by L.H., B.M. and K.M.M. The climatology and water column data were collected and processed by C.K. and D.W.-G.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Bettina Meyer.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–11, Supplementary Tables 1–2, Supplementary Methods.

  2. Life Sciences Reporting Summary

  3. Supplementary Video 1

    Patchiness and behaviour of larvae under sea ice during the day in the pack-ice zone.

  4. Supplementary Video 2

    Patchiness and behaviour of larvae in the marginal ice zone during sunset, larvae starting to leave the ice to be dispersed in the water column.

  5. Supplementary Video 3

    Larval krill feeding on a horizontal ice floe (“terrace”).

  6. Supplementary Video 4

    Larval krill feeding on the under-side of sea ice, frozen overnight at the diving hole.

  7. Supplementary Video 5

    Larval krill dispersed in the water column during night in the pack-ice zone.