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Phytoplankton dynamics in a changing Arctic Ocean

Abstract

Changes in the Arctic atmosphere, cryosphere and Ocean are drastically altering the dynamics of phytoplankton, the base of marine ecosystems. This Review addresses four major complementary questions of ongoing Arctic Ocean changes and associated impacts on phytoplankton productivity, phenology and assemblage composition. We highlight trends in primary production over the last two decades while considering how multiple environmental drivers shape Arctic biogeography. Further, we consider changes to Arctic phenology by borealization and hidden under-ice blooms, and how the diversity of phytoplankton assemblages might evolve in a novel Arctic ‘biogeochemical landscape’. It is critical to understand these aspects of changing Arctic phytoplankton dynamics as they exert pressure on marine Arctic ecosystems in addition to direct effects from rapid environmental changes.

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Fig. 1: Changing sea-ice extent and age.
Fig. 2: Global trends in Arctic primary production over the two last decades.
Fig. 3: Environmental drivers shaping Arctic phytoplankton dynamics.
Fig. 4: Synthesis of selected observed regional environmental changes in the Arctic Ocean.
Fig. 5: Changing Arctic sea-ice algae and phytoplankton phenology with the receding sea-ice cover.
Fig. 6: Major phytoplankton taxa and its environmental drivers in the Arctic Ocean.

References

  1. 1.

    AMAP. Snow, Water, Ice and Permafrost in the Arctic (SWIPA) 2017 (AMAP, 2017).

  2. 2.

    Notz, D. & Stroeve, J. Observed Arctic sea-ice loss directly follows anthropogenic CO2 emission. Science 354, 747–750 (2016).

    CAS  Google Scholar 

  3. 3.

    Haine, T. W. N. et al. Arctic freshwater export: status, mechanisms, and prospects. Glob. Planet. Change 125, 13–35 (2015).

    Google Scholar 

  4. 4.

    Aagaard, K. & Carmack, E. C. The role of sea ice and other fresh water in the Arctic circulation. J. Geophys. Res. 94, 14485–14498 (1989).

    Google Scholar 

  5. 5.

    Aagaard, K., Coachman, L. K. & Carmack, E. On the halocline of the Arctic Ocean. Deep Sea Res. Pt A 28, 529–545 (1981).

    Google Scholar 

  6. 6.

    Polyakov, I. V. et al. Greater role for Atlantic inflows on sea-ice loss in the Eurasian Basin of the Arctic Ocean. Science 356, 285–291 (2017).

    CAS  Google Scholar 

  7. 7.

    Aagaard, K. & Coachman, L. K. Toward an ice-free Arctic ocean. Eos Trans. Amer. Geophys. Union 56, 484–486 (1975).

    Google Scholar 

  8. 8.

    Kwok, R. Arctic sea ice thickness, volume, and multiyear ice coverage: losses and coupled variability (1958–2018). Environ. Res. Lett. 13, 105005 (2018).

    Google Scholar 

  9. 9.

    Post, E. et al. Ecological consequences of sea-ice decline. Science 341, 519–524 (2013).

    CAS  Google Scholar 

  10. 10.

    Post, E. et al. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358 (2009).

    CAS  Google Scholar 

  11. 11.

    Gregory, A. C. et al. Marine viral macro- and micro-diversity from pole to pole. Cell 177, 1109–1123 (2019).

    CAS  Google Scholar 

  12. 12.

    Arrigo, K. R., van Dijken, G. & Pabi, S. Impact of a shrinking Arctic ice cover on marine primary production. Geophys. Res. Lett. 35, L19603 (2008).

    Google Scholar 

  13. 13.

    Kahru, M., Lee, Z.-P., Mitchell, B. G. & Nevison, C. D. Effects of sea ice cover on satellite-detected primary production in the Arctic ocean. Biol. Lett. 12, 20160223 (2016).

    Google Scholar 

  14. 14.

    Bélanger, S., Babin, M. & Tremblay, J.-É. Increasing cloudiness in Arctic damps the increase in phytoplankton primary production due to sea ice receding. Biogeosciences 10, 4087–4101 (2013).

    Google Scholar 

  15. 15.

    Kahru, M., Brotas, V., Manzano-Sarabio, M. & Mitchell, B. G. Are phytoplankton blooms occurring earlier in the Arctic? Glob. Change Biol. 17, 1733–1739 (2010).

    Google Scholar 

  16. 16.

    Ardyna, M. et al. Recent Arctic Ocean sea-ice loss triggers novel fall phytoplankton blooms. Geophys. Res. Lett. 41, 6207–6212 (2014).

    Google Scholar 

  17. 17.

    Arrigo, K. R. & van Dijken, G. L. Continued increases in Arctic Ocean primary production. Prog. Oceanogr. 136, 60–70 (2015).

    Google Scholar 

  18. 18.

    Lewis, K. M., van Dijken, G. & Arrigo, K. R. Changes in phytoplankton concentration, not sea ice, now drive increased Arctic Ocean primary production. Science 369, 198–202 (2020).

    CAS  Google Scholar 

  19. 19.

    Olson, M. B. & Strom, S. L. Phytoplankton growth, microzooplankton herbivory and community structure in the southeast Bering Sea: insight into the formation and temporal persistence of an Emiliania huxleyi bloom. Deep Sea Res. Pt. 2 49, 5969–5990 (2002).

    CAS  Google Scholar 

  20. 20.

    Sherr, E. B., Sherr, B. F. & Ross, C. Microzooplankton grazing impact in the Bering Sea during spring sea ice conditions. Deep Sea Res. Pt. 2 94, 57–67 (2013).

    CAS  Google Scholar 

  21. 21.

    Forest, A. et al. Biogenic carbon flows through the planktonic food web of the Amundsen Gulf (Arctic Ocean): a synthesis of field measurements and inverse modeling analyses. Prog. Oceanogr. 91, 410–436 (2011).

    Google Scholar 

  22. 22.

    Franzè, G. & Lavrentyev, P. J. Microbial food web structure and dynamics across a natural temperature gradient in a productive polar shelf system. Mar. Ecol. Prog. Ser. 569, 89–102 (2017).

    Google Scholar 

  23. 23.

    Menden-Deuer, S., Lawrence, C. & Franzè, G. Herbivorous protist growth and grazing rates at in situ and artificially elevated temperatures during an Arctic phytoplankton spring bloom. PeerJ 6, e5264 (2018).

    Google Scholar 

  24. 24.

    Carmack, E. C. & Wassmann, P. Food webs and physical-biological coupling on pan-Arctic shelves: unifying concepts and comprehensive perspectives. Prog. Oceanogr. 71, 446–477 (2006).

    Google Scholar 

  25. 25.

    Harrison, W. G. & Cota, G. F. Primary production in polar waters: relation to nutrient availability. Polar Res. 10, 87–104 (1991).

    Google Scholar 

  26. 26.

    Sakshaug, E. in The Organic Carbon Cycle in the Arctic Ocean (eds Stein, R. & MacDonald, R. W.) 57–81 (Springer, 2004).

  27. 27.

    Michel, C., Nielsen, T. G., Nozais, C. & Gosselin, M. Significance of sedimentation and grazing by ice micro- and meiofauna for carbon cycling in annual sea ice (northern Baffin Bay). Aquat. Microb. Ecol. 30, 57–68 (2002).

    Google Scholar 

  28. 28.

    Krause, J. W. et al. Biogenic silica production and diatom dynamics in the Svalbard region during spring. Biogeosciences 15, 6503–6517 (2018).

    CAS  Google Scholar 

  29. 29.

    Ardyna, M., Gosselin, M., Michel, C., Poulin, M. & Tremblay, J.-É. Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Mar. Ecol. Prog. Ser. 442, 37–57 (2011).

    CAS  Google Scholar 

  30. 30.

    Taylor, R. L. et al. Colimitation by light, nitrate, and iron in the Beaufort Sea in late summer. J. Geophys. Res. 118, 3260–3277 (2013).

    Google Scholar 

  31. 31.

    Tremblay, J.-É. et al. Global and regional drivers of nutrient supply, primary production and CO2 drawdown in the changing Arctic Ocean. Prog. Oceanogr. 139, 171–196 (2015).

    Google Scholar 

  32. 32.

    Tremblay, J.-É. & Gagnon, J. in Influence of Climate Change on the Changing Arctic and Sub-Arctic Conditions (eds J. C. J. Nihoul & A. G. Kostianoy) 73–93 (Springer, 2009).

  33. 33.

    Michel, C. et al. Arctic Ocean outflow shelves in the changing Arctic: a review and perspectives. Prog. Oceanogr. 139, 66–88 (2015).

    Google Scholar 

  34. 34.

    Bourgault, D. et al. Turbulent nitrate fluxes in the Amundsen Gulf during ice-covered conditions. Geophys. Res. Lett. 38, L15602 (2011).

    Google Scholar 

  35. 35.

    Randelhoff, A., Fer, I., Sundfjord, A., Tremblay, J.-É. & Reigstad, M. Vertical fluxes of nitrate in the seasonal nitracline of the Atlantic sector of the Arctic Ocean. J. Geophys. Res. Oceans 121, 5282–5295 (2016).

    CAS  Google Scholar 

  36. 36.

    Toole, J. M. et al. Influences of the ocean surface mixed layer and thermohaline stratification on Arctic Sea ice in the central Canada Basin. J. Geophys. Res. Oceans 115, C10018 (2010).

    Google Scholar 

  37. 37.

    Lind, S., Ingvaldsen, R. B. & Furevik, T. Arctic warming hotspot in the northern Barents Sea linked to declining sea-ice import. Nat. Clim. Change 8, 634–639 (2018).

    Google Scholar 

  38. 38.

    Mioduszewski, J., Vavrus, S. & Wang, M. Diminishing Arctic sea ice promotes stronger surface winds. J. Climate 31, 8101–8119 (2018).

    Google Scholar 

  39. 39.

    Bendif, E. M. et al. Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa. Nat. Commun. 10, 4234 (2019).

    Google Scholar 

  40. 40.

    Oziel, L. et al. Faster Atlantic currents drive poleward expansion of temperate marine species in the Arctic Ocean. Nat. Commun. 11, 1705 (2020).

    CAS  Google Scholar 

  41. 41.

    Neukermans, G., Oziel, L. & Babin, M. Increased intrusion of warming Atlantic water leads to rapid expansion of temperate phytoplankton in the Arctic. Glob. Change Biol. 24, 2545–2553 (2018).

    Google Scholar 

  42. 42.

    Oziel, L. et al. Role for Atlantic inflows and sea ice loss on shifting phytoplankton blooms in the Barents Sea. J. Geophys. Res. 122, 5121–5139 (2017).

    Google Scholar 

  43. 43.

    Paulsen, M. L. et al. Synechococcus in the Atlantic gateway to the Arctic Ocean. Front. Mar. Sci. 3, 191 (2016).

    Google Scholar 

  44. 44.

    Winter, A., Henderiks, J., Beaufort, L., Rickaby, R. E. M. & Brown, C. W. Poleward expansion of the coccolithophore Emiliania huxleyi. J. Plankton Res. 36, 316–325 (2014).

    CAS  Google Scholar 

  45. 45.

    Wassmann, P. et al. The contiguous domains of Arctic Ocean advection: trails of life and death. Prog. Oceanogr. 139, 42–65 (2015).

    Google Scholar 

  46. 46.

    Kortsch, S., Primicerio, R., Fossheim, M., Dolgov, A. V. & Aschan, M. Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proc. Royal Soc. B 282, 20151546 (2015).

    Google Scholar 

  47. 47.

    Frainer, A. et al. Climate-driven changes in functional biogeography of Arctic marine fish communities. Proc. Natl Acad. Sci. USA 114, 12202–12207 (2017).

    CAS  Google Scholar 

  48. 48.

    Fossheim, M. et al. Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat. Clim. Change 5, 673–677 (2015).

    Google Scholar 

  49. 49.

    Beaugrand, G. et al. Prediction of unprecedented biological shifts in the global ocean. Nat. Clim. Change 9, 237–243 (2019).

    Google Scholar 

  50. 50.

    Carmack, E. C. et al. Freshwater and its role in the Arctic marine system: sources, disposition, storage, export, and physical and biogeochemical consequences in the Arctic and global oceans. J. Geophys. Res. Biogeosci. 121, 675–717 (2016).

    CAS  Google Scholar 

  51. 51.

    Marchese, C. et al. Changes in phytoplankton bloom phenology over the North Water (NOW) polynya: a response to changing environmental conditions. Polar Biol. 40, 1721–1737 (2017).

    Google Scholar 

  52. 52.

    Mayot, N. et al. Springtime export of Arctic sea ice influences phytoplankton production in the Greenland Sea. J. Geophys. Res. Oceans 125, e2019JC015799 (2020).

    Google Scholar 

  53. 53.

    Carmack, E. C. The alpha/beta ocean distinction: a perspective on freshwater fluxes, convection, nutrients and productivity in high-latitude seas. Deep Sea Res. Pt. 2 54, 2578–2598 (2007).

    Google Scholar 

  54. 54.

    Blais, M. et al. Contrasting interannual changes in phytoplankton productivity and community structure in the coastal Canadian Arctic Ocean. Limnol. Oceanogr. 62, 2480–2497 (2017).

    Google Scholar 

  55. 55.

    Meire, L. et al. High export of dissolved silica from the Greenland Ice Sheet. Geophys. Res. Lett. 43, 9173–9182 (2016).

    CAS  Google Scholar 

  56. 56.

    Hawkings, J. R. et al. Ice sheets as a significant source of highly reactive nanoparticulate iron to the oceans. Nat. Commun. 5, 3929 (2014).

    CAS  Google Scholar 

  57. 57.

    Hawkings, J. et al. The Greenland Ice Sheet as a hot spot of phosphorus weathering and export in the Arctic. Glob. Biogeochem. Cycle 30, 191–210 (2016).

    CAS  Google Scholar 

  58. 58.

    Arrigo, K. R. et al. Melting glaciers stimulate large summer phytoplankton blooms in southwest Greenland waters. Geophys. Res. Lett. 44, 6278–6285 (2017).

    Google Scholar 

  59. 59.

    Meire, L. et al. Marine-terminating glaciers sustain high productivity in Greenland fjords. Glob. Change Biol. 23, 5344–5357 (2017).

    Google Scholar 

  60. 60.

    Boone, W. et al. Coastal freshening prevents fjord bottom water renewal in northeast Greenland: a mooring study from 2003 to 2015. Geophys. Res. Lett. 45, 2726–2733 (2018).

    Google Scholar 

  61. 61.

    Le Fouest, V. et al. Modeling plankton ecosystem functioning and nitrogen fluxes in the oligotrophic waters of the Beaufort Sea, Arctic Ocean: a focus on light-driven processes. Biogeosciences 10, 4785–4800 (2013).

    Google Scholar 

  62. 62.

    Le Fouest, V., Manizza, M., Tremblay, B. & Babin, M. Modelling the impact of riverine DON removal by marine bacterioplankton on primary production in the Arctic Ocean. Biogeosciences 12, 3385–3402 (2015).

    Google Scholar 

  63. 63.

    Tremblay, J.-É. et al. Impact of river discharge, upwelling and vertical mixing on the nutrient loading and productivity of the Canadian Beaufort Shelf. Biogeosciences 11, 4853–4868 (2014).

    Google Scholar 

  64. 64.

    Ardyna, M. et al. Shelf-basin gradients shape ecological phytoplankton niches and community composition in the coastal Arctic Ocean (Beaufort Sea). Limnol. Oceanogr. 62, 2113–2132 (2017).

    Google Scholar 

  65. 65.

    Fichot, C. G. et al. Pan-Arctic distributions of continental runoff in the Arctic Ocean. Sci. Rep. 3, 1053 (2013).

    Google Scholar 

  66. 66.

    Matsuoka, A. et al. Pan-Arctic optical characteristics of colored dissolved organic matter: tracing dissolved organic carbon in changing Arctic waters using satellite ocean color data. Remote Sens. Environ. 200, 89–101 (2017).

    Google Scholar 

  67. 67.

    Arrigo, K. R. et al. Phytoplankton blooms beneath the sea ice in the Chukchi Sea. Deep Sea Res. Pt. 2 105, 1–16 (2014).

    Google Scholar 

  68. 68.

    Arrigo, K. R. et al. Massive phytoplankton blooms under Arctic sea ice. Science 336, 1408 (2012).

    CAS  Google Scholar 

  69. 69.

    Kelly, R. et al. Recent burning of boreal forests exceeds fire regime limits of the past 10,000 years. Proc. Natl Acad. Sci. USA 110, 13055–13060 (2013).

    CAS  Google Scholar 

  70. 70.

    French, N. H. F. et al. Fire in Arctic tundra of Alaska: past fire activity, future fire potential, and significance for land management and ecology. Int. J. Wildland Fire 24, 1045–1061 (2015).

    Google Scholar 

  71. 71.

    Masrur, A., Petrov, A. N. & DeGroote, J. Circumpolar spatio-temporal patterns and contributing climatic factors of wildfire activity in the Arctic tundra from 2001–2015. Environ. Res. Lett. 13, 014019 (2018).

    Google Scholar 

  72. 72.

    Evangeliou, N. et al. Open fires in Greenland in summer 2017: transport, deposition and radiative effects of BC, OC and BrC emissions. Atmos. Chem. Phys. 19, 1393–1411 (2019).

    CAS  Google Scholar 

  73. 73.

    Lutsch, E. et al. Unprecedented atmospheric ammonia concentrations detected in the high Arctic from the 2017 Canadian wildfires. J. Geophys. Res. Atmos. 124, 8178–8202 (2019).

    CAS  Google Scholar 

  74. 74.

    Skiles, S. M., Flanner, M., Cook, J. M., Dumont, M. & Painter, T. H. Radiative forcing by light-absorbing particles in snow. Nat. Clim. Change 8, 964–971 (2018).

    Google Scholar 

  75. 75.

    Light, B., Eicken, H., Maykut, G. A. & Grenfell, T. C. The effect of included participates on the spectral albedo of sea ice. J. Geophys. Res. Oceans 103, 27739–27752 (1998).

    Google Scholar 

  76. 76.

    Holland, M. M., Bailey, D. A., Briegleb, B. P., Light, B. & Hunke, E. Improved sea ice shortwave radiation physics in CCSM4: the impact of melt ponds and aerosols on Arctic sea ice. J. Climate 25, 1413–1430 (2011).

    Google Scholar 

  77. 77.

    Marks, A. A., Lamare, M. L. & King, M. D. Optical properties of sea ice doped with black carbon – an experimental and radiative-transfer modelling comparison. Cryosphere 11, 2867–2881 (2017).

    Google Scholar 

  78. 78.

    Dentener, F. et al. Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob. Biogeochem. Cycle 20, GB4003 (2006).

    Google Scholar 

  79. 79.

    Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycle 22, GB4026 (2008).

    Google Scholar 

  80. 80.

    Torres-Valdés, S., Tsubouchi, T., Davey, E., Yashayaev, I. & Bacon, S. Relevance of dissolved organic nutrients for the Arctic Ocean nutrient budget. Geophys. Res. Lett. 43, 6418–6426 (2016).

    Google Scholar 

  81. 81.

    AMAP Assessment 2018: Arctic Ocean Acidification (AMAP, 2018).

  82. 82.

    Yamamoto-Kawai, M., McLaughlin, F. A., Carmack, E. C., Nishino, S. & Shimada, K. Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326, 1098–1100 (2009).

    CAS  Google Scholar 

  83. 83.

    Qi, D. et al. Increase in acidifying water in the western Arctic Ocean. Nat. Clim. Change 7, 195–199 (2017).

    CAS  Google Scholar 

  84. 84.

    Terhaar, J., Kwiatkowski, L. & Bopp, L. Emergent constraint on Arctic Ocean acidification in the twenty-first century. Nature 582, 379–383 (2020).

    CAS  Google Scholar 

  85. 85.

    Hoppe, C. J. M. et al. Resistance of Arctic phytoplankton to ocean acidification and enhanced irradiance. Polar Biol. 41, 399–413 (2018).

    CAS  Google Scholar 

  86. 86.

    Hoppe, C. J. M., Schuback, N., Semeniuk, D. M., Maldonado, M. T. & Rost, B. Functional redundancy facilitates resilience of subarctic phytoplankton assemblages toward ocean acidification and high irradiance. Front. Mar. Sci. 4, 229 (2017).

    Google Scholar 

  87. 87.

    Hoppe, C. J. M., Wolf, K. K. E., Schuback, N., Tortell, P. D. & Rost, B. Compensation of ocean acidification effects in Arctic phytoplankton assemblages. Nat. Clim. Change 8, 529–533 (2018).

    CAS  Google Scholar 

  88. 88.

    Hussherr, R. et al. Impact of ocean acidification on Arctic phytoplankton blooms and dimethyl sulfide concentration under simulated ice-free and under-ice conditions. Biogeosciences 14, 2407–2427 (2017).

    CAS  Google Scholar 

  89. 89.

    White, E., Hoppe, C. J. M. & Rost, B. The Arctic picoeukaryote Micromonas pusilla benefits from ocean acidification under constant and dynamic light. Biogeosciences 17, 635–647 (2020).

    CAS  Google Scholar 

  90. 90.

    Yoshimura, T. et al. Impacts of elevated CO2 on particulate and dissolved organic matter production: microcosm experiments using iron-deficient plankton communities in open subarctic waters. J. Oceanogr. 69, 601–618 (2013).

    CAS  Google Scholar 

  91. 91.

    Thoisen, C., Riisgaard, K., Lundholm, N., Nielsen, T. G. & Hansen, P. J. Effect of acidification on an Arctic phytoplankton community from Disko Bay, West Greenland. Mar. Ecol. Prog. Ser. 520, 21–34 (2015).

    CAS  Google Scholar 

  92. 92.

    Coello-Camba, A., Agustí, S., Holding, J., Arrieta, J. M. & Duarte, C. M. Interactive effect of temperature and CO2 increase in Arctic phytoplankton. Front. Mar. Sci. 1, 49 (2014).

    Google Scholar 

  93. 93.

    Perovich, D. K. & Polashenski, C. Albedo evolution of seasonal Arctic sea ice. Geophys. Res. Lett. 39, L08501 (2012).

    Google Scholar 

  94. 94.

    Perovich, D. K. The Optical Properties of Sea Ice (Office of Naval Research, 1996).

  95. 95.

    Hill, V. J., Cota, G. & Stockwell, D. Spring and summer phytoplankton communities in the Chukchi and Eastern Beaufort Seas. Deep Sea Res. Pt 2 52, 3369–3385 (2005).

    Google Scholar 

  96. 96.

    Perrette, M., Yool, A., Quartly, G. D. & Popova, E. E. Near-ubiquity of ice-edge blooms in the Arctic. Biogeosciences 7, 515–524 (2011).

    Google Scholar 

  97. 97.

    Janout, M. A. et al. Sea-ice retreat controls timing of summer plankton blooms in the Eastern Arctic Ocean. Geophys. Res. Lett. 12, 12493–12501 (2016).

    Google Scholar 

  98. 98.

    Sakshaug, E. Biomass and productivity distributions and their variability in the Barents Sea. ICES J. Mar. Sci. 54, 341–350 (1997).

    Google Scholar 

  99. 99.

    Subba Rao, D. V. & Platt, T. Primary production of arctic waters. Polar Biol. 3, 191–201 (1984).

    Google Scholar 

  100. 100.

    Pabi, S., van Dijken, G. L. & Arrigo, K. R. Primary production in the Arctic Ocean, 1998–2006. J. Geophys. Res. 113, C08005 (2008).

    Google Scholar 

  101. 101.

    Arrigo, K. R. & van Dijken, G. L. Secular trends in Arctic Ocean net primary production. J. Geophys. Res. 116, C09011 (2011).

    Google Scholar 

  102. 102.

    Fortier, M., Fortier, L., Michel, C. & Legendre, L. Climatic and biological forcing of the vertical flux of biogenic particles under seasonal Arctic sea ice. Mar. Ecol. Prog. Ser. 225, 1–16 (2002).

    Google Scholar 

  103. 103.

    Mundy, C. J. et al. Role of environmental factors on phytoplankton bloom initiation under landfast sea ice in Resolute Passage, Canada. Mar. Ecol. Prog. Ser. 497, 39–49 (2014).

    Google Scholar 

  104. 104.

    Duerksen, S. W. et al. Large, omega-3 rich, pelagic diatoms under Arctic Sea ice: sources and Implications for food webs. PLoS ONE 9, e114070 (2014).

    Google Scholar 

  105. 105.

    Galindo, V. et al. Contrasted sensitivity of DMSP production to high light exposure in two Arctic under-ice blooms. J. Exp. Mar. Biol. Ecol. 475, 38–48 (2016).

    CAS  Google Scholar 

  106. 106.

    Galindo, V. et al. Under-ice microbial dimethylsulfoniopropionate metabolism during the melt period in the Canadian Arctic Archipelago. Mar. Ecol. Prog. Ser. 524, 39–53 (2015).

    CAS  Google Scholar 

  107. 107.

    Galindo, V. et al. Biological and physical processes influencing sea ice, under-ice algae, and dimethylsulfoniopropionate during spring in the Canadian Arctic Archipelago. J. Geophys. Res. Oceans 119, 3746–3766 (2014).

    CAS  Google Scholar 

  108. 108.

    Ardyna, M. et al. Ecological drivers controlling spring phytoplankton blooms in the Arctic Ocean. Elem. Sci. Anth. 8, 30 (2020).

    Google Scholar 

  109. 109.

    Assmy, P. et al. Leads in Arctic pack ice enable early phytoplankton blooms below snow-covered sea ice. Sci. Rep. 7, 40850 (2017).

    CAS  Google Scholar 

  110. 110.

    Mayot, N. et al. Assessing phytoplankton activities in the seasonal ice zone of the Greenland Sea over an annual cycle. J. Geophys. Res. Oceans 123, 8004–8025 (2018).

    Google Scholar 

  111. 111.

    Strass, V. H. & Nöthig, E.-M. Seasonal shifts in ice edge phytoplankton blooms in the Barents Sea related to the water column stability. Polar Biol. 16, 409–422 (1996).

    Google Scholar 

  112. 112.

    Pavlov, A. K. et al. Altered inherent optical properties and estimates of the underwater light field during an Arctic under-ice bloom of Phaeocystis pouchetii. J. Geophys. Res. Oceans 122, 4939–4961 (2017).

    Google Scholar 

  113. 113.

    Lalande, C. et al. Variability in under-ice export fluxes of biogenic matter in the Arctic Ocean. Glob. Biogeochem. Cycle 28, 571–583 (2014).

    CAS  Google Scholar 

  114. 114.

    Yager, P. L. et al. Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol. Oceanogr. 46, 790–801 (2001).

    CAS  Google Scholar 

  115. 115.

    Hill, V. J., Light, B., Steele, M. & Zimmerman, R. C. Light availability and phytoplankton growth beneath Arctic sea ice: integrating observations and modeling. J. Geophys. Res. Oceans 123, 3651–3667 (2018).

    Google Scholar 

  116. 116.

    Lewis, K. M. et al. Photoacclimation of Arctic Ocean phytoplankton to shifting light and nutrient limitation. Limnol. Oceanogr. 64, 284–301 (2019).

    CAS  Google Scholar 

  117. 117.

    Grebmeier, J. M. Shifting patterns of life in the Pacific Arctic and sub-Arctic seas. Annu. Rev. Mar. Sci. 4, 63–78 (2012).

    Google Scholar 

  118. 118.

    Grebmeier, J. M., Moore, S. E., Overland, J. E., Frey, K. E. & Gradinger, R. Biological response to recent Pacific Arctic sea ice retreats. Eos Trans. Amer. Geophys. Union 91, 161–162 (2010).

    Google Scholar 

  119. 119.

    Tamelander, T., Kivimäe, C., Bellerby, R. G. J., Renaud, P. E. & Kristiansen, S. Base-line variations in stable isotope values in an Arctic marine ecosystem: effects of carbon and nitrogen uptake by phytoplankton. Hydrobiologia 630, 63–73 (2009).

    CAS  Google Scholar 

  120. 120.

    Degen, R. et al. Patterns and drivers of megabenthic secondary production on the Barents Sea shelf. Mar. Ecol. Prog. Ser. 546, 1–16 (2016).

    Google Scholar 

  121. 121.

    Wassmann, P. & Reigstad, M. Future Arctic Ocean seasonal ice zones and implications for pelagic-benthic coupling. Oceanography 24, 220–231 (2011).

    Google Scholar 

  122. 122.

    Fujiwara, A. et al. Changes in phytoplankton community structure during wind-induced fall bloom on the central Chukchi shelf. Polar Biol. 41, 1279–1295 (2018).

    Google Scholar 

  123. 123.

    Uchimiya, M. et al. Coupled response of bacterial production to a wind-induced fall phytoplankton bloom and sediment resuspension in the Chukchi Sea Shelf, Western Arctic Ocean. Front. Mar. Sci. 3, 231 (2016).

    Google Scholar 

  124. 124.

    Goñi, M. A. et al. Particulate organic matter distributions in surface waters of the Pacific Arctic shelf during the late summer and fall season. Mar. Chem. 211, 75–93 (2019).

    Google Scholar 

  125. 125.

    Juranek, L., Takahashi, T., Mathis, J. & Pickart, R. Significant biologically mediated CO2 uptake in the Pacific Arctic during the late open water season. J. Geophys. Res. Oceans 124, 821–843 (2019).

    CAS  Google Scholar 

  126. 126.

    Not, F. et al. Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnol. Oceanogr. 50, 1677–1686 (2005).

    CAS  Google Scholar 

  127. 127.

    Ardyna, M. et al. Parameterization of vertical chlorophyll a in the Arctic Ocean: impact of the subsurface chlorophyll maximum on regional, seasonal, and annual primary production estimates. Biogeosciences 10, 4383–4404 (2013).

    Google Scholar 

  128. 128.

    Wassmann, P., Peinert, R. & Smetacek, V. Patterns of production and sedimentation in the boreal and polar Northeast Atlantic. Polar Res. 10, 209–228 (1991).

    Google Scholar 

  129. 129.

    Martin, J. et al. Prevalence, structure and properties of subsurface chlorophyll maxima in Canadian Arctic waters. Mar. Ecol. Prog. Ser. 412, 69–84 (2010).

    CAS  Google Scholar 

  130. 130.

    Coupel, P. et al. The impact of freshening on phytoplankton production in the Pacific Arctic Ocean. Prog. Oceanogr. 131, 113–125 (2015).

    Google Scholar 

  131. 131.

    Huot, Y., Babin, M. & Bruyant, F. Photosynthetic parameters in the Beaufort Sea in relation to the phytoplankton community structure. Biogeosciences 10, 3445–3454 (2013).

    Google Scholar 

  132. 132.

    Monier, A. et al. Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J. 9, 990–1002 (2014).

    Google Scholar 

  133. 133.

    McLaughlin, F. A. & Carmack, E. C. Deepening of the nutricline and chlorophyll maximum in the Canada Basin interior. Geophys. Res. Lett. 37, L24602 (2010).

    Google Scholar 

  134. 134.

    Gran, H. H. Das Plankton des norwegischen Nordmeeres (Fiskeridirektoratets havforskningsinstitutt, 1902).

  135. 135.

    Poulin, M. et al. The pan-Arctic biodiversity of marine pelagic and sea-ice unicellular eukaryotes: a first-attempt assessment. Mar. Biodiv. 41, 13–28 (2011).

    Google Scholar 

  136. 136.

    Lovejoy, C., von Quillfeldt, C., Hopcroft, R. R., Poulin, M. & Thaler, M. in State of the Arctic Marine Biodiversity Report (eds T Barry. et al.) 62–83 (Conservation of Arctic Flora and Fauna International Secretariat, 2017).

  137. 137.

    Tremblay, G. et al. Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: strong numerical dominance by picoeukaryotes. Aquat. Microb. Ecol. 54, 55–70 (2009).

    Google Scholar 

  138. 138.

    Berge, J. et al. Diel vertical migration of Arctic zooplankton during the polar night. Biol. Lett. 5, 69–72 (2009).

    Google Scholar 

  139. 139.

    Lovejoy, C. et al. Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J. Phycol. 43, 78–89 (2007).

    CAS  Google Scholar 

  140. 140.

    Stoecker, D. K. & Lavrentyev, P. J. Mixotrophic plankton in the polar seas: a pan-Arctic review. Front. Mar. Sci. 5, 292 (2018).

    Google Scholar 

  141. 141.

    Balzano, S. et al. Diversity of cultured photosynthetic flagellates in the northeast Pacific and Arctic Oceans in summer. Biogeosciences 9, 4553–4571 (2012).

    CAS  Google Scholar 

  142. 142.

    Joli, N. et al. Need for focus on microbial species following ice melt and changing freshwater regimes in a Janus Arctic Gateway. Sci. Rep. 8, 9405 (2018).

    Google Scholar 

  143. 143.

    Okolodkov, Y. B. The global distributional patterns of toxic, bloom dinoflagellates recorded from the Eurasian Arctic. Harmful Algae 4, 351–369 (2005).

    Google Scholar 

  144. 144.

    Brosnahan, M. L., Fischer, A. D., Lopez, C. B., Moore, S. K. & Anderson, D. M. Cyst-forming dinoflagellates in a warming climate. Harmful Algae 91, 101728 (2020).

    Google Scholar 

  145. 145.

    Lefebvre, K. A. et al. Prevalence of algal toxins in Alaskan marine mammals foraging in a changing arctic and subarctic environment. Harmful Algae 55, 13–24 (2016).

    CAS  Google Scholar 

  146. 146.

    Lovejoy, C., Legendre, L., Martineau, M. J., Bacle, J. & von Quillfeldt, C. H. Distribution of phytoplankton and other protists in the North Water. Deep Sea Res. Pt 2 49, 5027–5047 (2002).

    Google Scholar 

  147. 147.

    Booth, B. C. et al. Dynamics of Chaetoceros socialis blooms in the North Water. Deep Sea Res. Pt 2 49, 5003–5025 (2002).

    CAS  Google Scholar 

  148. 148.

    Schoemann, V., Becquevort, S., Stefels, J., Rousseau, V. & Lancelot, C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea. Res. 53, 43–66 (2005).

    CAS  Google Scholar 

  149. 149.

    Smith, W. O. et al. Importance of Phaeocystis blooms in the high-latitude ocean carbon cycle. Nature 352, 514–516 (1991).

    Google Scholar 

  150. 150.

    Simo-Matchim, A. G., Gosselin, M., Poulin, M., Ardyna, M. & Lessard, S. Summer and fall distribution of phytoplankton in relation to environmental variables in Labrador fjords, with special emphasis on Phaeocystis pouchetii. Mar. Ecol. Prog. Ser. 572, 19–42 (2017).

    CAS  Google Scholar 

  151. 151.

    Crawford, D. W., Cefarelli, A. O., Wrohan, I. A., Wyatt, S. N. & Varela, D. E. Spatial patterns in abundance, taxonomic composition and carbon biomass of nano- and microphytoplankton in Subarctic and Arctic Seas. Prog. Oceanogr. 162, 132–159 (2018).

    Google Scholar 

  152. 152.

    Nöthig, E.-M. et al. Summertime plankton ecology in Fram Strait—a compilation of long- and short-term observations. Polar Res. 34, 23349 (2015).

    Google Scholar 

  153. 153.

    Hodal, H., Falk-Petersen, S., Hop, H., Kristiansen, S. & Reigstad, M. Spring bloom dynamics in Kongsfjorden, Svalbard: nutrients, phytoplankton, protozoans and primary production. Polar Biol. 35, 191–203 (2012).

    Google Scholar 

  154. 154.

    Hátún, H. et al. The subpolar gyre regulates silicate concentrations in the North Atlantic. Sci. Rep. 7, 14576 (2017).

    Google Scholar 

  155. 155.

    Slagstad, D., Wassmann, P. F. J. & Ellingsen, I. Physical constrains and productivity in the future Arctic Ocean. Front. Mar. Sci. 2, 85 (2015).

    Google Scholar 

  156. 156.

    Hegseth, E. N. et al. in The Ecosystem of Kongsfjorden, Svalbard (eds Hop, H. & Wiencke, C.) 173–227 (Springer International Publishing, 2019).

  157. 157.

    Lacour, T. et al. Decoupling light harvesting, electron transport and carbon fixation during prolonged darkness supports rapid recovery upon re-illumination in the Arctic diatom Chaetoceros neogracilis. Polar Biol. http://doi.org/d6rs (2019).

  158. 158.

    Kvernvik, A. C. et al. Fast reactivation of photosynthesis in arctic phytoplankton during the polar night. J. Phycol. 54, 461–470 (2018).

    CAS  Google Scholar 

  159. 159.

    McMinn, A. & Martin, A. Dark survival in a warming world. Proc. Biol. Sci. 280, 20122909 (2013).

    CAS  Google Scholar 

  160. 160.

    Joli, N., Monier, A., Logares, R. & Lovejoy, C. Seasonal patterns in Arctic prasinophytes and inferred ecology of Bathycoccus unveiled in an Arctic winter metagenome. ISME J. 11, 13727 (2017).

    Google Scholar 

  161. 161.

    Vader, A., Marquardt, M., Meshram, A. R. & Gabrielsen, T. M. Key Arctic phototrophs are widespread in the polar night. Polar Biol. 38, 13–21 (2015).

    Google Scholar 

  162. 162.

    McMinn, A. & Martin, A. Dark survival in a warming world. Proc. Biol. Sci. 280, 20122909 (2013).

    CAS  Google Scholar 

  163. 163.

    van de Poll, W., Abdullah, E., Visser, R., Fischer, P. & Buma, A. Taxon-specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring. Limnol. Oceanogr. 65, 903–914 (2019).

    Google Scholar 

  164. 164.

    Boyd, P. W., Lennartz, S. T., Glover, D. M. & Doney, S. C. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5, 71–79 (2014).

    Google Scholar 

  165. 165.

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

    Google Scholar 

  166. 166.

    Vancoppenolle, M. et al. Future Arctic Ocean primary productivity from CMIP5 simulations: uncertain outcome, but consistent mechanisms. Glob. Biogeochem. Cycle 27, 605–619 (2013).

    CAS  Google Scholar 

  167. 167.

    Tedesco, L., Vichi, M. & Scoccimarro, E. Sea-ice algal phenology in a warmer Arctic. Sci. Adv. 5, eaav4830 (2019).

    CAS  Google Scholar 

  168. 168.

    Babin, M. et al. Estimation of primary production in the Arctic Ocean using ocean colour remote sensing and coupled physical-biological models: strengths, limitations and how they compare. Prog. Oceanogr. 139, 197–220 (2015).

    Google Scholar 

  169. 169.

    Lacour, T., Larivière, J. & Babin, M. Growth, Chl a content, photosynthesis, and elemental composition in polar and temperate microalgae. Limnol. Oceanogr. 201, 43–58 (2016).

    Google Scholar 

  170. 170.

    Lacour, T. et al. The role of sustained photoprotective non-photochemical quenching in low temperature and high light acclimation in the bloom-forming Arctic diatom Thalassiosira gravida. Front. Mar. Sci. 5, 354 (2018).

    Google Scholar 

  171. 171.

    Graham, R. M. et al. Winter storms accelerate the demise of sea ice in the Atlantic sector of the Arctic Ocean. Sci. Rep. 9, 9222 (2019).

    Google Scholar 

  172. 172.

    Berge, J. et al. Unexpected levels of biological activity during the polar night offer new perspectives on a warming Arctic. Curr. Biol. 25, 2555–2561 (2015).

    CAS  Google Scholar 

  173. 173.

    Berge, J. et al. In the dark: a review of ecosystem processes during the Arctic polar night. Prog. Oceanogr. 139, 258–271 (2015).

    Google Scholar 

  174. 174.

    Kipp, L. E., Charette, M. A., Moore, W. S., Henderson, P. B. & Rigor, I. G. Increased fluxes of shelf-derived materials to the central Arctic Ocean. Sci. Adv. 4, eaao1302 (2018).

    Google Scholar 

  175. 175.

    Abram, N. J. et al. Early onset of industrial-era warming across the oceans and continents. Nature 536, 411 (2016).

    CAS  Google Scholar 

  176. 176.

    Osman, M. B. et al. Industrial-era decline in subarctic Atlantic productivity. Nature 569, 551–555 (2019).

    CAS  Google Scholar 

  177. 177.

    Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).

    CAS  Google Scholar 

  178. 178.

    Rahmstorf, S. et al. Exceptional twentieth-century slowdown in Atlantic Ocean overturning circulation. Nat. Clim. Change 5, 475–480 (2015).

    Google Scholar 

  179. 179.

    Caesar, L., Rahmstorf, S., Robinson, A., Feulner, G. & Saba, V. Observed fingerprint of a weakening Atlantic Ocean overturning circulation. Nature 556, 191–196 (2018).

    CAS  Google Scholar 

  180. 180.

    Thornalley, D. J. R. et al. Anomalously weak Labrador Sea convection and Atlantic overturning during the past 150 years. Nature 556, 227–230 (2018).

    CAS  Google Scholar 

  181. 181.

    Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).

    CAS  Google Scholar 

  182. 182.

    Bakker, P. et al. Fate of the Atlantic Meridional Overturning Circulation: strong decline under continued warming and Greenland melting. Geophys. Res. Lett. 43, 12,252–12,260 (2016).

    Google Scholar 

  183. 183.

    Takahashi, T. et al. Climatological mean and decadal change in surface ocean pCO2, and net sea-air CO2 flux over the global oceans. Deep Sea Res. Pt 2 56, 554–577 (2009).

    CAS  Google Scholar 

  184. 184.

    Stock, C. A. et al. Reconciling fisheries catch and ocean productivity. Proc. Natl Acad. Sci. USA 114, E1441–E1449 (2017).

    CAS  Google Scholar 

  185. 185.

    Cavalieri, D. J., Parkinson, C., Gloersen, P. & Zwally, H. J. Sea Ice Concentrations From Nimbus-7 SMMR and DMSP SSM/I Passive Microwave Data Version 1 (NASA National Snow and Ice Data Center Distributed Active Archive Center, 1996); https://nsidc.org/data/NSIDC-0051/versions/1

  186. 186.

    Tschudi, M., Meier, W. N., Stewart, J. S., Fowler, C. & Maslanik, J. EASE-Grid Sea Ice Age Version 4 (NASA National Snow and Ice Data Center Distributed Active Archive Center, 2019); https://doi.org/10.5067/UTAV7490FEPB

  187. 187.

    Anderson, L. G. & Macdonald, R. W. Observing the Arctic Ocean carbon cycle in a changing environment. Polar Res. 34, 26891 (2015).

    Google Scholar 

  188. 188.

    Horner, R. & Schrader, G. C. Contributions of ice Algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. Arctic 35, 485–503 (1982).

    Google Scholar 

  189. 189.

    Mundy, C. J. et al. Contribution of under-ice primary production to an ice-edge upwelling phytoplankton bloom in the Canadian Beaufort Sea. Geophys. Res. Lett. 36, L17601 (2009).

    Google Scholar 

  190. 190.

    Oziel, L. et al. Environmental factors influencing the seasonal dynamics of under-ice spring blooms in Baffin Bay. Elem. Sci. Anth. 7, 34 (2019).

    Google Scholar 

  191. 191.

    Ferland, J., Gosselin, M. & Starr, M. Environmental control of summer primary production in the Hudson Bay system: the role of stratification. J. Mar. Syst. 88, 385–400 (2011).

    Google Scholar 

  192. 192.

    Lalande, C., Nöthig, E. M. & Fortier, L. Algal export in the Arctic Ocean in times of global warming. Geophys. Res. Lett. 46, 5959–5967 (2019).

    Google Scholar 

  193. 193.

    Lalande, C., Grebmeier, J. M., Hopcroft, R. R. & Danielson, S. L. Annual cycle of export fluxes of biogenic matter near Hanna Shoal in the northeast Chukchi Sea. Deep Sea Res. Pt 2 177, 104730 (2020).

    CAS  Google Scholar 

  194. 194.

    Silkin, V., Pautova, L., Giordano, M., Kravchishina, M. & Artemiev, V. Interannual variability of Emiliania huxleyi blooms in the Barents Sea: in situ data 2014–2018. Mar. Pollut. Bull. 158, 111392 (2020).

    CAS  Google Scholar 

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Acknowledgements

M.A. was supported by a European Union’s Horizon 2020 Marie Sklodowska-Curie grant (no. 746748). This work represents a contribution to the Sorbonne Université and Stanford University. We thank M. Gosselin, M. Poulin and E. Leu for sharing their expertize on phytoplankton ecology and taxonomy; M. Nicolaus and W. Meier for sharing their expertize on sea-ice; and L. Oziel and the whole Arrigo’s laboratory for insightful comments on the Review.

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Ardyna, M., Arrigo, K.R. Phytoplankton dynamics in a changing Arctic Ocean. Nat. Clim. Chang. 10, 892–903 (2020). https://doi.org/10.1038/s41558-020-0905-y

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