Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Cruise track with larval krill sampling stations.
Fig. 2: Large-scale sea-ice thickness and degree of ice formation.
Fig. 3: Larval krill on a horizontal ice floe.
Fig. 4: Larval krill growth in relation to food supply in the water column and in sea ice, and diel vertical migration behaviour.
Fig. 5: Modelled distribution of Antarctic krill larvae and mean chl a concentration for two regions of the Scotia Sea.
Fig. 6: Winter krill habitat projections in the southwest Atlantic sector of the Southern Ocean.

Similar content being viewed by others

References

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

    Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Google Scholar 

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

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  Google Scholar 

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

    Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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. 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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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

Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Bettina Meyer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

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

Life Sciences Reporting Summary

Supplementary Video 1

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

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.

Supplementary Video 3

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

Supplementary Video 4

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

Supplementary Video 5

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meyer, B., Freier, U., Grimm, V. et al. The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill. Nat Ecol Evol 1, 1853–1861 (2017). https://doi.org/10.1038/s41559-017-0368-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0368-3

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing