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Protist assemblages in winter sea ice: setting the stage for the spring ice algal bloom

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Abstract

This study documents, for the first time, the abundance and species composition of protist assemblages in Arctic sea ice during the dark winter period. Lack of knowledge of sea-ice assemblages during the dark period has left questions about the retention and survival of protist species that initiate the ice algal bloom. Sea-ice and surface water samples were collected between December 27, 2007 and January 31, 2008 within the Cape Bathurst flaw lead, Canadian Beaufort Sea. Samples were analyzed for protist identification and counts, chlorophyll (chl) a, and total particulate carbon and nitrogen concentrations. Sea-ice chl a concentrations (max. 0.27 μg l−1) and total protist abundances (max. 4 × 103 cells l−1) were very low, indicating minimal retention of protists in the ice during winter. The diversity of winter ice protists (134 taxa) was comparable to spring ice assemblages. Pennate diatoms dominated the winter protist assemblage numerically (averaging 77% of total protist abundances), with Nitzschia frigida being the most abundant species. Only 56 taxa were identified in surface waters, where dinoflagellates were the dominant group. Our results indicate that differences in the timing of ice formation may have a greater impact on the abundance than structure of protist assemblages present in winter sea ice and at the onset of the spring ice algal bloom.

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References

  • Ardyna M (in press) Influence des facteurs du milieu sur la structure et le fonctionnement des communautés phytoplanctoniques de haut-Arctique Canadien: Distinction des régions oligotrophes et eutrophes. Dissertation, Université du Québec à Rimouski

  • Arrigo KR, van Dijken GL (2004) Annual cycles of sea ice and phytoplankton in Cape Bathurst polynya, southeastern Beaufort Sea, Canadian Arctic. Geophys Res Lett 31:L08304. doi:10.1029/2003GL018978

    Article  Google Scholar 

  • Arrigo KR, van Dijken GL, Pabi S (2008) Impact of a shrinking Arctic ice cover on marine primary production. Geophys Res Lett 35:L19603. doi:10.1029/2008GL035028

    Article  Google Scholar 

  • Baldisserotto C, Ferroni L, Andreoli C, Fasulo MP, Bonora A, Pancaldi S (2005) Dark-acclimation of the chloroplast in Koliella antarctica exposed to a simulated austral night condition. Arct Antarct Alp Res 37:146–156

    Article  Google Scholar 

  • Barber DG, Hanesiak JM (2004) Meteorological forcing of sea ice concentrations in the southern Beaufort Sea over the period 1979 to 2000. J Geophys Res 109:C06014. doi:10.1029/2003JC002027

    Article  Google Scholar 

  • Barber DG, Asplin MG, Gratton Y, Lukovich JV, Galley RJ, Raddatz RL, Leitch D (2010) The International polar year (IPY) circumpolar flaw lead (CFL) system study: overview and the physical system. Atmos Ocean 48:225–243

    Google Scholar 

  • Brugel S, Nozais C, Poulin M, Tremblay J-É, Miller LA, Simpson KG, Gratton Y, Demers S (2009) Phytoplankton biomass and production in the southeastern Beaufort Sea in autumn 2002 and 2003. Mar Ecol Prog Ser 377:63–77

    Article  CAS  Google Scholar 

  • Canadian Ice Services (2005) Manual of standard procedures for observing and reporting ice conditions (MANICE), 9th edn. Environment Canada, Ottawa

    Google Scholar 

  • Carmack EC, Macdonald RW, Jasper S (2004) Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar Ecol Prog Ser 277:37–50

    Article  Google Scholar 

  • Carmack E, Barber DG, Christensen JR, Macdonald RW, Rudels B, Sakshaug E (2006) Climate variability and physical forcing of the food webs and the carbon budget on panarctic shelves. Prog Oceanogr 71:145–181

    Article  Google Scholar 

  • Cota GF, Smith REH (1991) Ecology of bottom ice algae: III. Comparative physiology. J Mar Syst 2:297–315

    Article  Google Scholar 

  • Dieckmann GS, Nehrke G, Uhlig C, Göttlicher J, Gerland S, Granskog MA, Thomas DN (2010) Ikaite (CaCO3*6H2O) discovered in Arctic sea ice. Cryosphere Discuss 4:153–161

    Article  Google Scholar 

  • Doucette GJ, Fryxell GA (1983) Thalassiosira antarctica: vegetative and resting stage chemical composition of an ice-related marine diatom. Mar Biol 78:1–6

    Article  CAS  Google Scholar 

  • Eicken H, Gradinger R, Gaylord A, Mahoney A, Rigor I, Melling H (2005) Sediment transport by sea ice in the Chukchi and Beaufort Seas: increasing importance due to changing ice conditions? Deep-Sea Res II 52:3281–3302

    Article  Google Scholar 

  • Ferroni L, Baldisserotto C, Zennaro V, Soldani C, Fasulo MP, Pancaldi S (2007) Acclimation to darkness in the marine chlorophyte Koliella antarctica cultured under low salinity: hypotheses on its origin in the polar environment. Eur J Phycol 42:91–104

    Article  CAS  Google Scholar 

  • Forest A, Sampei M, Makabe R, Sasaki H, Barber DG, Gratton Y, Wassmann P, Fortier L (2008) The annual cycle of particulate organic carbon export in Franklin Bay (Canadian Arctic): environmental control and food web implications. J Geophys Res 113:C03S05. doi:10.1029/2007JC004262

  • Garrison DL, Buck KR (1986) Organism losses during ice melting: a serious bias in sea ice community studies. Polar Biol 6:237–239

    Article  Google Scholar 

  • Gosselin M, Legendre L, Demers S, Ingram RG (1985) Responses of sea-ice microalgae to climatic and fortnightly tidal energy inputs (Manitounuk Sound, Hudson Bay). Can J Fish Aquat Sci 42:999–1006

    Article  Google Scholar 

  • Gosselin M, Legendre L, Therriault J-C, Demers S, Rochet M (1986) Physical control of the horizontal patchiness of sea-ice microalgae. Mar Ecol Prog Ser 29:289–298

    Article  Google Scholar 

  • Gradinger R, Ikävalko J (1998) Organism incorporation into newly forming Arctic sea ice in the Greenland Sea. J Plankton Res 20:871–886

    Article  Google Scholar 

  • Hegseth EN (1992) Sub-ice algal assemblages of the Barents Sea: species composition, chemical composition and growth rates. Polar Biol 12:485–496

    Article  Google Scholar 

  • Horner R, Alexander V (1972) Algal populations in Arctic sea ice: an investigation of heterotrophy. Limnol Oceanogr 17:454–458

    Article  Google Scholar 

  • Horner R, Schrader GC (1982) Relative contributions of ice algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. Arctic 4:485–503

    Google Scholar 

  • Juul-Pedersen T, Michel C, Gosselin M, Seuthe L (2008) Seasonal changes in the sinking export of particulate material under first-year sea ice on the Mackenzie Shelf (western Canadian Arctic). Mar Ecol Prog Ser 353:13–25

    Article  Google Scholar 

  • Juul-Pedersen T, Michel C, Gosselin C (2010) Sinking export of particulate organic material from the euphotic zone in the eastern Beaufort Sea. Mar Ecol Prog Ser 410:55–70

    Article  CAS  Google Scholar 

  • Krembs C, Deming JW (2008) The role of exopolymers in microbial adaptation to sea ice. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 247–264

    Chapter  Google Scholar 

  • Krembs C, Eicken H, Junge K, Deming JW (2002) High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep-Sea Res 49:2163–2181

    CAS  Google Scholar 

  • Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implication for ice habitability and biogeochemistry in a warmer arctic. US Proc Natl Acad Sci 108:3653–3658

    Article  CAS  Google Scholar 

  • Lavoie D, Denman K, Michel C (2005) Modelling ice algae growth and decline in a seasonally ice-covered region of the Arctic Ocean (Resolute Passage, Canadian Archipelago). J Geophys Res 110. doi:10.1029/2005JC002922

  • Lewin J, Hellebust JA (1975) Heterotrophic nutrition of the marine pennate diatom Navicula pavillardi Hustedt. Can J Microbiol 21:1335–1342

    Article  PubMed  CAS  Google Scholar 

  • Li WK, McLaughlin FA, Lovejoy C, Carmack E (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539

    Article  PubMed  CAS  Google Scholar 

  • Logan BE, Grossart H-P, Simon M (1994) Direct observation of phytoplankton, TEP and aggregates on polycarbonate filters using brightfield microscopy. J Plankton Res 16:1811–1815

    Article  Google Scholar 

  • Lüder UH, Wiencke C, Knoetzel J (2002) Acclimation of photosynthesis and pigments during and after six months of darkness in Palmaria decipiens (Rhodophyta): a study to simulate Antarctic winter sea ice cover. J Phycol 38:904–913

    Article  Google Scholar 

  • Lukovich JV, Barber DG (2005) On sea ice concentration anomaly coherence in the southern Beaufort Sea. Geophys Res Lett 32:L10705. doi:10.1029/2005GL022737

    Article  Google Scholar 

  • Lund JWG, Kipling C, Le Cren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiol 11:143–170

    Article  Google Scholar 

  • Maykut GA (1986) The surface heat and mass balance. In: Untersteiner N (ed) Geophysics of the sea ice. Series B: physics. Plenum Press, vol 146, pp 395–463

  • Michel C, Legendre L, Ingram RG, Gosselin M, Levasseur M (1996) Carbon budget of sea-ice algae in spring: evidence of a significant transfer to zooplankton grazers. J Geophys Res 101:18345–18360

    Article  CAS  Google Scholar 

  • Mock T, Gradinger R (2000) Changes in photosynthetic carbon allocations in algal assemblages of Arctic sea ice with decreasing nutrient concentrations and irradiance. Mar Ecol Prog Ser 202:1–11

    Article  CAS  Google Scholar 

  • Mundy CJ, Gosselin M, Ehn J, Gratton Y, Rossnagel A, Barber DG, Martin J, Tremblay J-É, Palmer M et al (2009) Contribution of under-ice primary production to an ice-edge upwelling phytoplankton bloom in the Canadian Beaufort Sea. Geophys Res Lett 36:L17601. doi:10.1029/2009GL038837

    Article  Google Scholar 

  • Palmisano AC, Sullivan CW (1982) Physiology of sea ice diatoms. I. Response of three polar diatoms to a simulated summer-winter transition. J Phycol 18:489–498

    Article  Google Scholar 

  • Palmisano AC, Sullivan CW (1985) Growth, metabolism and, dark survival in sea ice microalgae. In: Horner RA (ed) Sea ice biota. CRC Press, Boca Raton, pp 131–146

    Google Scholar 

  • Papadimitriou S, Thomas DN, Kennedy H, Haas C, Kuosa H, Krell A, Dieckmann GS (2007) Biogeochemical composition of natural sea ice brines from the Weddell Sea during early austral summer. Limnol Oceanogr 52:1809–1823

    Article  CAS  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Toronto

    Google Scholar 

  • Peters E, Thomas DN (1996) Prolonged darkness and diatom mortality I: marine Antarctic species. J Exp Mar Biol Ecol 207:25–41

    Article  Google Scholar 

  • Qing Z, Gradinger R, Qingsong Z (2003) Competition within the marine microalgae over the polar dark period in the Greenland Sea of high Arctic. Acta Oceanol Sinica 22:233–242

    Google Scholar 

  • Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of sea-water. In: Hill MN (ed) The sea. Interscience, New York, vol 2, pp 26–77

  • Reeves S, McMinn A, Martin A (2011) The effect of prolonged darkness on the growth, recovery and survival of Antarctic sea ice diatoms. Polar Biol. doi:10.1007/s00300-011-0961-x

  • Reimnitz E, Marincovich L Jr, McCormick M, Briggs WM (1992) Suspension freezing of bottom sediment and biota in the Northwest Passage and implications for Arctic Ocean sedimentation. Can J Earth Sci 29:693–703

    Article  Google Scholar 

  • Reimnitz E, Clayton JR, Kempema EW, Payne JR, Weber WS (1993) Interaction of rising frazil with suspended particles: tank experiments with applications to nature. Cold Reg Sci Technol 21:117–135

    Article  Google Scholar 

  • Riedel A, Michel C, Poulin M, Lessard S (2003) Taxonomy and abundance of microalgae and protists at a first-year sea ice station near Resolute Bay, Nunavut, spring to early summer 2001. Can Data Rep Hydrogr Ocean Sci 159:1–53

    Google Scholar 

  • Riedel A, Michel C, Gosselin M (2006) Seasonal study of sea-ice exopolymeric substances (EPS) on the Mackenzie shelf: implications for the transport of sea-ice bacteria and algae. Aquat Microb Ecol 45:195–206

    Article  Google Scholar 

  • Riedel A, Michel C, Gosselin M, LeBlanc B (2007) Enrichment of nutrients and organisms in newly formed sea ice on the Mackenzie shelf: significance of heterotrophic regeneration and exopolymeric substances. Mar Ecol Prog Ser 342:55–67

    Article  CAS  Google Scholar 

  • Riedel A, Michel C, Gosselin M, LeBlanc B (2008) Winter-spring dynamics in sea ice carbon cycling in the coastal Arctic Ocean. J Mar Syst 74:918–932

    Article  Google Scholar 

  • Rivkin RB, Putt M (1987) Heterotrophy and photoheterotrophy by Antarctic microalgae: light-dependent incorporation of amino acids and glucose. J Phycol 23:442–452

    Article  CAS  Google Scholar 

  • Różańska M, Poulin M, Gosselin M (2008) Protist entrapment in newly formed sea ice in the coastal Arctic Ocean. J Mar Syst 74:887–901

    Article  Google Scholar 

  • Różańska M, Gosselin M, Poulin M, Wiktor JM, Michel C (2009) Influence of environmental factors on the development of bottom ice protist communities during the winter–spring transition. Mar Ecol Prog Ser 386:43–59

    Article  Google Scholar 

  • Sallon A, Michel C, Gosselin M (2011) Summertime primary production and carbon export in the coastal Arctic Ocean during the low ice year of 2008. Polar Biol. doi:10.1007/s00300-011-1055-5

  • Smith REH, Herman AW (1992) In situ patterns of intracellular photosynthate allocation by sea ice algae in the Canadian high Arctic. Polar Biol 12:545–551

    Google Scholar 

  • Smith REH, Clement P, Head EJ (1990) Night metabolism of recent photosynthate by sea ice algae in the high Arctic. Mar Biol 107:255–261

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman, New York

    Google Scholar 

  • Søreide JE, Leu E, Berge J, Graeve M, Falk-Petersen S (2010) Effects of omega-3 fatty acid production on Calanus glacialis reproduction and growth in a changing marine Arctic. Global Change Biol (in press)

  • Syvertsen EE (1991) Ice algae in the Barents Sea: types of assemblages, origin, fate and role in the ice-edge phytoplankton bloom. Polar Res 10:277–288

    Article  Google Scholar 

  • Tang KW, Smith WO Jr, Shields AR, Elliott DT (2009) Survival and recovery of Phaeocystis antarctica (Prymnesiophyceae) from prolonged darkness and freezing. Proc R Soc B 276:81–90

    Article  PubMed  Google Scholar 

  • Tuchman NC, Schollett MA, Rier ST, Geddes P (2006) Differential heterotrophic utilization of organic compounds by diatoms and bacteria under light and dark conditions. Hydrobiol 561:167–177

    Article  CAS  Google Scholar 

  • Tuschling K, Juterzenka K, Okolodkov YB, Anoshkin A (2000) Composition and distribution of the pelagic and sympagic algal assemblages in the Laptev Sea during autumnal freeze-up. J Plankton Res 22:843–864

    Article  Google Scholar 

  • Underwood GJC, Fietz S, Papadimitriou S, Thomas DN, Dieckmann GS (2010) Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar Ecol Prog Ser 404:1–19

    Article  CAS  Google Scholar 

  • von Quillfeldt CH, Ambrose WG, Clough LM (2003) High number of diatom species in first year-ice from the Chukchi Sea. Polar Biol 26:806–818

    Article  Google Scholar 

  • Weissenberger J, Grossmann S (1998) Experimental formation of sea ice: importance of water circulation and wave action for incorporation of phytoplankton and bacteria. Polar Biol 20:178–188

    Article  Google Scholar 

  • Werner I, Ikävalko J, Schünemann H (2007) Sea-ice algae in Arctic pack ice during late winter. Polar Biol 30:1493–1504

    Article  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE (2001) Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science 292:2073–2075

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Gradinger R, Spindler M (1998) Dark survival of marine microalgae in the high Arctic (Greenland Sea). Polarforsch 65:111–116

    Google Scholar 

  • Zhang X, Ikeda M, Walsh JE (2003) Coordinated changes of sea ice over the Beaufort and Chukchi seas: regional and seasonal perspectives. Polar Res 22:83–90

    Article  Google Scholar 

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Acknowledgments

We sincerely thank the officers and crew of the CCGS Amundsen for their support of this research and G. Niemi for assistance in the field and laboratory during the expedition. The support of the chief scientists and other participants of CFL leg 5 is greatly appreciated. We also thank H. Kuosa, R. Horner and one anonymous reviewer for constructive comments that helped improve the manuscript. Yves Gagnon, Institut Maurice-Lamontagne, conducted the PC and PN analyses and Tim Papakyriakou and Bruce Johnson provided the PAR data. This research was made possible by grants from the Canadian International Polar Year Federal Program, Natural Sciences and Engineering Research Council (NSERC) of Canada IPY Funds and Discovery Grant to C.M., Canadian Museum of Nature and Fisheries and Oceans Canada. This is a contribution to the research programs of the Circumpolar Flaw Lead (CFL) system study and the Freshwater Institute (Fisheries and Oceans Canada).

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Correspondence to Andrea Niemi.

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This article belongs to the special issue “Circumpolar Flaw Lead Study (CFL)”, coordinated by J. Deming and L. Fortier.

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Niemi, A., Michel, C., Hille, K. et al. Protist assemblages in winter sea ice: setting the stage for the spring ice algal bloom. Polar Biol 34, 1803–1817 (2011). https://doi.org/10.1007/s00300-011-1059-1

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