Under-ice distribution of polar cod Boreogadus saida in the central Arctic Ocean and their association with sea-ice habitat properties

Abstract

In the Arctic Ocean, sea-ice habitats are undergoing rapid environmental change. Polar cod (Boreogadus saida) is the most abundant fish known to reside under the pack-ice. The under-ice distribution, association with sea-ice habitat properties and origins of polar cod in the central Arctic Ocean, however, are largely unknown. During the RV Polarstern expedition ARK XXVII/3 in the Eurasian Basin in 2012, we used for the first time in Arctic waters a Surface and Under Ice Trawl with an integrated bio-environmental sensor array. Polar cod was ubiquitous throughout the Eurasian Basin with a median abundance of 5000 ind. km−2. The under-ice population consisted of young specimens with a total length between 52 and 140 mm, dominated by 1-year-old fish. Higher fish abundance was associated with thicker ice, higher ice coverage and lower surface salinity, or with higher densities of the ice-amphipod Apherusa glacialis. The fish were in good condition and well fed according to various indices. Back-tracking of the sea-ice indicated that sea-ice sampled in the Amundsen Basin originated from the Laptev Sea coast, while sea-ice sampled in the Nansen Basin originated from the Kara Sea. Assuming that fish were following the ice drift, this suggests that under-ice polar cod distribution in the Eurasian Basin is dependent on the coastal populations where the sea-ice originates. The omnipresence of polar cod in the Eurasian Basin, in a good body condition, suggests that the central Arctic under-ice habitats may constitute a favourable environment for this species survival, a potential vector of genetic exchange and a recruitment source for coastal populations around the Arctic Ocean.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Anthony JA, Roby DD, Turco KR (2000) Lipid content and energy density of forage fishes from the northern Gulf of Alaska. J Exp Mar Biol Ecol 248:53–78. doi:10.1016/S0022-0981(00)00159-3

    CAS  Article  PubMed  Google Scholar 

  2. Barbosa AM, Brown JA, Jimenez-Valverde A, Real R (2015) modEvA: model evaluation and analysis. http://R-Forge.R-project.org/projects/modeva/

  3. Benoit D, Simard Y, Fortier L (2008) Hydroacoustic detection of large winter aggregations of Arctic cod (Boreogadus saida) at depth in ice-covered Franklin Bay (Beaufort Sea). J Geophys Res Oceans. doi:10.1029/2007JC004276

    Google Scholar 

  4. Benoit D, Simard Y, Fortier L (2014) Pre-winter distribution and habitat characteristics of polar cod (Boreogadus saida) in southeastern Beaufort Sea. Polar Biol 37:149–163. doi:10.1007/s00300-013-1419-0

    Article  Google Scholar 

  5. Boetius A et al (2013) Export of algal biomass from the melting Arctic sea-ice. Science 339:1430–1432. doi:10.1126/science.1231346

    CAS  Article  PubMed  Google Scholar 

  6. Bouchard C, Fortier L (2008) Effects of polynyas on the hatching season, early growth and survival of polar cod Boreogadus saida in the Laptev Sea. Mar Ecol Prog Ser 355:247–256. doi:10.3354/Meps07335

    Article  Google Scholar 

  7. Bouchard C, Fortier L (2011) Circum-arctic comparison of the hatching season of polar cod Boreogadus saida: a test of the freshwater winter refuge hypothesis. Prog Oceanogr 90:105–116. doi:10.1016/j.pocean.2011.02.008

    Article  Google Scholar 

  8. Bradstreet MSW, Cross WE (1982) Trophic relationships at high Arctic ice edges. Arctic 35:1–12

    Google Scholar 

  9. Brekke B, Gabrielsen G (1994) Assimilation efficiency of adult Kittiwakes and Brünnich’s Guillemots fed Capelin and Arctic Cod. Polar Biol 14:279–284. doi:10.1007/bf00239177

    Article  Google Scholar 

  10. Cairns D (1987) Diet and foraging ecology of Black guillemots in Northeastern Hudson Bay. Can J Zool 65:1257–1263

    Article  Google Scholar 

  11. Craig PC, Griffiths WB, Haldorson L, McElderry H (1982) Ecological studies of Arctic Cod (Boreogadus saida) in Beaufort Sea coastal waters, Alaska. Can J Fish Aquat Sci 39:395–406. doi:10.1139/f82-057

    Article  Google Scholar 

  12. Crawford R, Jorgenson J (1996) Quantitative studies of Arctic cod (Boreogadus saida) schools: important energy stores in the Arctic food web. Arctic 49:181–193

    Article  Google Scholar 

  13. David C, Lange B, Rabe B, Flores H (2015) Community structure of under-ice fauna in the Eurasian central Arctic Ocean in relation to environmental properties of sea-ice habitats. Mar Ecol Prog Ser 522:15–32. doi:10.3354/meps11156

    Article  Google Scholar 

  14. Elliott KH, Gaston AJ (2008) Mass–length relationships and energy content of fishes and invertebrates delivered to nestling thick-billed murres Uria lomvia in the Canadian Arctic, 1981–2007. Mar Ornithol 36:25–34

    Google Scholar 

  15. Falk-Petersen I-B, Frivoll V, Gulliksen B, Haug T (1986) Occurrence and size/age relations of polar cod, Boreogadus Saida (Lepechin), in Spitsbergen coastal waters. Sarsia 71:235–245. doi:10.1080/00364827.1986.10419693

    Article  Google Scholar 

  16. Fernández-Méndez M, Rabe B, Katlein C, Nicolaus M, Peeken I, Flores H, Boetius A (2015) Photosynthetic production in the Central Arctic during the record sea-ice minimum in 2012. Biogeosci Discuss 12:2897–2945. doi:10.5194/bgd-12-2897-2015

    Article  Google Scholar 

  17. Fetterer F, Knowles K, Meier W, Savoie M (2002) Sea-ice index. monthly mean sea-ice extent. Boulder, Colorado USA: National Snow and Ice Data Center. http://dx.doi.org/10.7265/N5QJ7F7W

  18. Flores H et al (2012) The Association of Antarctic Krill Euphausia superba with the under-ice habitat. PLoS One. doi:10.1371/journal.pone.0031775

    Google Scholar 

  19. Fortier L, Sirois P, Michaud J, Barber D (2006) Survival of Arctic cod larvae (Boreogadus saida) in relation to sea-ice and temperature in the Northeast Water Polynya (Greenland Sea). Can J Fish Aquat Sci 63:1608–1616. doi:10.1139/f06-064

    Article  Google Scholar 

  20. Fowler C, Emery W, Tschudi M (2013) Polar pathfinder daily 25 km EASE-grid sea-ice motion vectors. Version 2. (daily and mean gridded field). Boulder, Colorado USA: NASA National Snow and Ice Data Center Distributed Active Archive Center. http://dx.doi.org/10.5067/LHAKY495NL2T

  21. Geoffroy M, Robert D, Darnis G, Fortier L (2011) The aggregation of polar cod (Boreogadus saida) in the deep Atlantic layer of ice-covered Amundsen Gulf (Beaufort Sea) in winter. Polar Biol 34:1959–1971. doi:10.1007/s00300-011-1019-9

    Article  Google Scholar 

  22. Geoffroy M, Majewski A, LeBlanc M, Gauthier S, Walkusz W, Reist JD, Fortier L (in press) Vertical segregation of age-0 and age-1 + polar cod (Boreogadus saida) over the annual cycle in the Canadian Beaufort Sea. Polar Biol Special ‘Arctic Gadids’ issue

  23. Gjøsæter H, Prozorkevich D (2012) In: Eriksen E (Ed.) Survey report from the joint Norwegian/Russian ecosystem survey in the Barents Sea August–October 2012. IMR/PINRO Joint Report Series, no. 2/2012, pp 50–56, ISSN:1502-8828

  24. Gradinger RR, Bluhm BA (2004) In-situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea-ice of the High Arctic Canada Basin. Polar Biol 27:595–603. doi:10.1007/s00300-004-0630-4

    Article  Google Scholar 

  25. Graham M, Hop H (1995) Aspects of reproduction and larval biology of Arctic cod (Boreogadus saida). Arctic 48:130–135

    Article  Google Scholar 

  26. Harter BB, Elliott KH, Divoky GJ, Davoren GK (2013) Arctic cod (Boreogadus saida) as prey: fish length-energetics relationships in the Beaufort Sea and Hudson Bay. Arctic 66:191–196

    Article  Google Scholar 

  27. Haug T, Tormod Nilssen K, Lindblom L, Lindstrøm U (2007) Diets of hooded seals (Cystophora cristata) in coastal waters and drift ice waters along the east coast of Greenland. Mar Biol Res 3:123–133. doi:10.1080/17451000701358531

    Article  Google Scholar 

  28. Hop H, Gjøsæter H (2013) Polar cod (Boreogadus saida) and capelin (Mallotus villosus) as key species in marine food webs of the Arctic and the Barents Sea. Mar Biol Res 9:878–894. doi:10.1080/17451000.2013.775458

    Article  Google Scholar 

  29. Hop H, Pavlova O (2008) Distribution and biomass transport of ice amphipods in drifting sea-ice around Svalbard. Deep Sea Res Part II Top Stud Oceanogr 55:2292–2307. doi:10.1016/j.dsr2.2008.05.023

    Article  Google Scholar 

  30. Hop H, Trudeau VL, Graham M (1995) Spawning energetics of Arctic cod (Boreogadus saida) in relation to seasonal development of the ovary and plasma sex steroid levels. Can J Fish Aquat Sci 52:541–550. doi:10.1139/f95-055

    CAS  Article  Google Scholar 

  31. Hop H, Tonn WM, Welch HE (1997a) Bioenergetics of Arctic cod (Boreogadus saida) at low temperatures. Can J Fish Aquat Sci 54:1772–1784

    Article  Google Scholar 

  32. Hop H, Welch HE, Crawford RE (1997b) Population structure and feeding ecology of Arctic cod schools in the Canadian High Arctic. In: Reynolds J (ed) Fish Ecology in Arctic North America, Fairbanks, Alaska, 19–21 May 1992. Am Fish Soc Symp 19, Bethesda, Maryland, pp 68–80

  33. Hop H, Mundy C, Gosselin M, Rossnagel A, Barber D (2011) Zooplankton boom and ice amphipod bust below melting sea-ice in the Amundsen Gulf, Arctic Canada. Polar Biol 34:1947–1958. doi:10.1007/s00300-011-0991-4

    Article  Google Scholar 

  34. IPPC (2014) Part A: global and sectoral aspects-working group II contribution to the fifth assesment report of the intergovernmental panel of climate change. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation and vulnerability. Cambridge University Press, Cambridge, 1132 pp

  35. Krumpen T, Janout M, Hodges KI, Gerdes R, Girard-Ardhuin F, Holemann JA, Willmes S (2013) Variability and trends in Laptev Sea-ice outflow between 1992–2011. Cryosphere 7:349–363. doi:10.5194/tc-7-349-2013

    Article  Google Scholar 

  36. Kwok R, Rothrock DA (2009) Decline in Arctic sea-ice thickness from submarine and ICESat records: 1958–2008. Geophys Res Lett 36:L15501. doi:10.1029/2009gl039035

    Article  Google Scholar 

  37. Lønne O, Gabrielsen G (1992) Summer diet of seabirds feeding in sea-ice-covered waters near Svalbard. Polar Biol 12:685–692

    Article  Google Scholar 

  38. Lønne O, Gulliksen B (1989) Size, age and diet of polar cod, Boreogadus saida (Lepechin 1773), in ice covered waters. Polar Biol 9:187–191

    Article  Google Scholar 

  39. Markus T, Stroeve JC, Miller J (2009) Recent changes in Arctic sea-ice melt onset, freezeup, and melt season length. J Geophys Res Oceans 114:C12024. doi:10.1029/2009jc005436

    Article  Google Scholar 

  40. Matley JK, Crawford RE, Dick TA (2012) Summer foraging behaviour of shallow-diving seabirds and distribution of their prey, Arctic cod (Boreogadus saida), in the Canadian Arctic. Polar Res. doi:10.3402/polar.v31i0.15894

    Google Scholar 

  41. Matley J, Fisk A, Dick T (2013) The foraging ecology of Arctic cod (Boreogadus saida) during open water (July–August) in Allen Bay, Arctic Canada. Mar Biol 160:2993–3004. doi:10.1007/s00227-013-2289-2

    CAS  Article  Google Scholar 

  42. McCullagh P, Nelder JA (1989) Generalized linear models, vol 2. Chapman and Hall London, United Kingdom

    Google Scholar 

  43. Melnikov IA, Chernova NV (2013) Characteristics of under-ice swarming of polar cod Boreogadus saida (Gadidae) in the Central Arctic Ocean. J Ichthyol 53:7–15. doi:10.1134/s0032945213010086

    Article  Google Scholar 

  44. Nahrgang J, Camus L, Broms F, Christiansen JS, Hop H (2010) Seasonal baseline levels of physiological and biochemical parameters in polar cod (Boreogadus saida): implications for environmental monitoring. Mar Pollut Bull 60:1336–1345. doi:10.1016/j.marpolbul.2010.03.004

    CAS  Article  PubMed  Google Scholar 

  45. Nahrgang J, Varpe Ø, Korshunova E, Murzina S, Hallanger IG, Vieweg I, Berge J (2014) Gender specific reproductive strategies of an arctic key species (Boreogadus saida) and implications of climate change. PLoS One 9:e98452. doi:10.1371/journal.pone.0098452

    Article  PubMed  PubMed Central  Google Scholar 

  46. Ponomarenko V (2000) Eggs, larvae, and juveniles of polar cod Boreogadus saida in the Barents, Kara, and White Seas. J Ichthyol 40:165–173

    Google Scholar 

  47. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  48. Rabe B, Wisotzki A, Rettig S, Somavilla Cabrillo R, Sander H (2012) Physical oceanography during POLARSTERN cruise ARK-XXVII/3 (IceArc). Alfred Wegener Inst Helmholtz Cent Polar Mar Res Bremerhav. doi:10.1594/PANGAEA.802904

    Google Scholar 

  49. Renaud P, Berge J, Varpe Ø, Nahrgang J, Ottesen C, Hallanger I (2012) Is the poleward expansion by Atlantic cod and haddock threatening native polar cod, Boreogadus saida? Polar Biol 35:401–412. doi:10.1007/s00300-011-1085-z

    Article  Google Scholar 

  50. Rigor IG, Wallace JM (2004) Variations in the age of Arctic sea-ice and summer sea-ice extent. Geophys Res Lett. doi:10.1029/2004gl019492

    Google Scholar 

  51. Rozman P et al (2011) Validating satellite derived and modelled sea-ice drift in the Laptev Sea with in situ measurements from the winter of 2007/08. Polar Res. doi:10.3402/Polar.V30i0.7218

    Google Scholar 

  52. Rudels B, Schauer U, Björk G, Korhonen M, Pisarev S, Rabe B, Wisotzki A (2013) Observations of water masses and circulation in the Eurasian Basin of the Arctic Ocean from the 1990s to the late 2000s. Ocean Sci Discuss 9:147–169. doi:10.5194/os-9-147-2013

    Article  Google Scholar 

  53. Scott CL, Falk-Petersen S, Sargent JR, Hop H, Lønne OJ, Poltermann M (1999) Lipids and trophic interactions of ice fauna and pelagic zooplankton in the marginal ice zone of the Barents Sea. Polar Biol 21:65–70. doi:10.1007/s003000050335

    Article  Google Scholar 

  54. Shaw W, Stanton T, McPhee M, Morison J, Martinson D (2009) Role of the upper ocean in the energy budget of Arctic sea-ice during SHEBA. J Geophys Res Oceans. doi:10.1029/2008JC004991

    Google Scholar 

  55. Shimada K et al (2006) Pacific Ocean inflow: influence on catastrophic reduction of sea-ice cover in the Arctic Ocean. Geophys Res Lett. doi:10.1029/2005gl025624

    Google Scholar 

  56. Snyder JP (1992) An Equal-Area Map Projection For Polyhedral Globes. Cartographica. Int J Geogr Inf Geovis 29:10–21. doi:10.3138/27h7-8k88-4882-1752

    Google Scholar 

  57. Søreide JE, Hop H, Carroll ML, Falk-Petersen S, Hegseth EN (2006) Seasonal food web structures and sympagic–pelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Prog Oceanogr 71:59–87. doi:10.1016/j.pocean.2006.06.001

    Article  Google Scholar 

  58. Stroeve J, Serreze M, Holland M, Kay J, Malanik J, Barrett A (2012) The Arctic’s rapidly shrinking sea-ice cover: a research synthesis. Clim Change 110:1005–1027. doi:10.1007/s10584-011-0101-1

    Article  Google Scholar 

  59. Sumata H et al (2014) An intercomparison of Arctic ice drift products to deduce uncertainty estimates. J Geophys Res Oceans 119:4887–4921. doi:10.1002/2013jc009724

    Article  Google Scholar 

  60. Van de Putte A, Flores H, Volckaert F, van Franeker J (2006) Energy content of Antarctic mesopelagic fishes: implications for the marine food web. Polar Biol 29:1045–1051. doi:10.1007/s00300-006-0148-z

    Article  Google Scholar 

  61. Van de Putte AP, Jackson GD, Pakhomov E, Flores H, Volckaert FAM (2010) Distribution of squid and fish in the pelagic zone of the Cosmonaut Sea and Prydz Bay region during the BROKE-West campaign. Deep Sea Res Part II Top Stud Oceanogr 57:956–967

    Article  Google Scholar 

  62. van Franeker JA, Flores H, Van Dorssen M (2009) Surface and Under Ice Trawl (SUIT). In: Flores H (ed) Frozen Desert alive—the role of sea-ice for pelagic macrofauna and its predators: implications for the Antarctic pack-ice food web. Dissertation, University of Groningen, Groningen, Netherlands

  63. Vaz S, Martin CS, Eastwood PD, Ernande B, Carpentier A, Meaden GJ, Coppin F (2008) Modelling species distributions using regression quantiles. J Appl Ecol 45:204–217. doi:10.1111/j.1365-2664.2007.01392.x

    Article  Google Scholar 

  64. Welch HE et al (1992) Energy flow through the marine ecosystem of the Lancaster sound region, Arctic Canada. Arctic 45:343–357

    Article  Google Scholar 

  65. Welch HE, Crawford RE, Hop H (1993) Occurrence of Arctic cod (Boreogadus saida) schools and their vulnerability to predation in the Canadian High Arctic. Arctic 46:331–339

    Google Scholar 

  66. Weslawski JM, Ryg M, Smith TG, Oritsland NA (1994) Diet of ringed seals (Phoca hispida) in a fjord of West Svalbard. Arctic 47:109–114

    Article  Google Scholar 

  67. Wilcoxon F (1945) Individual comparisons by ranking methods. Biometrics Bulletin 1:80–83

    Article  Google Scholar 

Download references

Acknowledgments

We thank Captain Uwe Pahl and the crew of RV Polarstern expedition IceArc (ARK XXVII/3) for their excellent support with work at sea. We thank Michiel van Dorssen for operational and technical support with the Surface and Under Ice Trawl (SUIT). SUIT was developed by IMARES with support from the Netherlands Ministry of EZ (project WOT-04-009-036) and the Netherlands Polar Program (projects ALW 851.20.011 and 866.13.009). We thank Felipe Oliveira Ribas and Sander Holthuijsen from the Royal Netherlands Institute for Sea Research (NIOZ) for their support in energy content measurements in fish samples. This study is part of the Helmholtz Association Young Investigators Group Iceflux: Ice-ecosystem carbon flux in polar oceans (VH-NG-800). We thank the three anonymous reviewers for their helpful suggestions and comments that contributed significantly to the improvement of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Carmen David.

Ethics declarations

This article does not contain any studies with human participants performed by any of the authors or any experimental studies with animals performed by any of the authors. All works were performed according to and within the regulations enforced by the German Animal Welfare Organisation, and no specific permissions were required. The R/V Polarstern is operated by Alfred Wegener Institute and has all necessary authorisation to use trawls to collect animals for scientific purposes. The organisms collected are neither protected nor endangered in the central Arctic waters.

Additional information

This article belongs to the special issue on the “Ecology of Arctic Gadids”, coordinated by Franz Mueter, Jasmine Nahrgang, John Nelson and Jørgen Berge.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 227 kb)

Supplementary material 2 (PDF 247 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

David, C., Lange, B., Krumpen, T. et al. Under-ice distribution of polar cod Boreogadus saida in the central Arctic Ocean and their association with sea-ice habitat properties. Polar Biol 39, 981–994 (2016). https://doi.org/10.1007/s00300-015-1774-0

Download citation

Keywords

  • Polar cod
  • Under-ice habitats
  • Ice drift
  • Sea-ice properties
  • Apherusa glacialis
  • GLM