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
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Marr, J. W. S. The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Rep. 32, 33–464 (1962).
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).
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).
Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).
Siegel, V. Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biol. 29, 1–22 (2005).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Meehl G. et al. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) Ch. 10 (Cambridge Univ. Press, Cambridge, 2007).
Meyer, B. The overwintering of Antarctic krill, Euphausia superba, from an ecophysiological perspective. A Review. Polar Biol. 35, 15–37 (2012).
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).
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).
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).
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).
Marra, J. & Boardman, C. Late winter chlorophyll a distribution in the Weddell Sea. Mar. Ecol. Prog. Ser. 19, 197–208 (1984).
Meiners, K. M. et al. Chlorophyll a in Antarctic sea ice from historical ice core data. Geophys. Res. Lett. 39, L21602 (2012).
Atkinson, A. et al. Oceanic circumpolar habitats of Antarctic krill. Mar. Ecol. Prog. Ser. 362, 1–23 (2008).
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).
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).
Nicol, S. et al. Ocean circulation off east Antarctica affects structure and sea-ice extent. Nature 406, 204–507 (2000).
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).
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).
Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).
Rose, J. M. et al. Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages. Biogeosciences 6, 3131–3147 (2009).
Hoppema, M. et al. Whole season net community production in the Weddell Sea. Polar Biol. 31, 101–111 (2007).
Arrigo, K. R., van Dijken, G. L. & Bushinsky, S. Primary production in the Southern Ocean, 1997–2006. J. Geophys. Res. 113, C08004 (2008).
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).
Wiedenmann, J., Cresswell, K. A. & Mangel, M. Connecting recruitment of Antarctic krill and sea ice. Limnol. Oceanogr. 54, 799–811 (2009).
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).
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).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2014); http://www.R-project.org/
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).
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).
Fraser, F. C. On the development and distribution of young stages of krill (Euphausia superba). Discovery Rep. 24, 1–192 (1936).
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).
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).
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).
Quetin, L. B. & Ross, R. M. Behavioural and physiological characteristics of the Antarctic krill Euphausia superba. Am. Zool. 31, 49–63 (1991).
Gradinger, R. & Bluhm, B. Timing of ice algal grazing by the Arctic nearshore benthic amphipod Onisimus litoralis. Arctic 63, 355–358 (2010).
Scott, F. J. & Marchant, H. Antarctic Marine Protists (Australian Antarctic Division, Hobart Australian Biological Resources Study, Canberra, 2005).
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).
Efron, B. & Tibshirani, R. Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statist. Sci. 1, 54–77 (1986).
Buckland, S. T. Monte-Carlo confidence intervals. Biometrics 40, 811–817 (1984).
Grimm, V. et al. The ODD protocol: a review and first update. Ecol. Model. 221, 2760–2768 (2010).
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).
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
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).
McPhee, M. G. & Martinson, D. G. Turbulent mixing under drifting pack ice in the Weddell Sea. Science 263, 218–221 (1994).
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).
Bailey, D. et al. Community Ice CodE (CICE) User’s Guide Version 4.0 (National Center for Atmospheric Research, 2010).
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.
The authors declare no competing financial interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Figures 1–11, Supplementary Tables 1–2, Supplementary Methods.
Patchiness and behaviour of larvae under sea ice during the day in the pack-ice zone.
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.
Larval krill feeding on a horizontal ice floe (“terrace”).
Larval krill feeding on the under-side of sea ice, frozen overnight at the diving hole.
Larval krill dispersed in the water column during night in the pack-ice zone.
About this article
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
Spatial and temporal diet variability of Adélie (Pygoscelis adeliae) and Emperor (Aptenodytes forsteri) Penguin: a multi tissue stable isotope analysis
Polar Biology (2021)
Polar Biology (2021)
Successful ecosystem-based management of Antarctic krill should address uncertainties in krill recruitment, behaviour and ecological adaptation
Communications Earth & Environment (2020)
Antarctic Krill Lipid and Fatty acid Content Variability is Associated to Satellite Derived Chlorophyll a and Sea Surface Temperatures
Scientific Reports (2020)
Nature Climate Change (2020)