, Volume 761, Issue 1, pp 261–275 | Cite as

Aspects of resilience of polar sea ice algae to changes in their environment

  • Meghana A. Rajanahally
  • Phil J. Lester
  • Peter Convey
Biology of the Ross Sea


Sea ice algae are primary producers of the ice-covered oceans in both polar regions. Changes in sea ice distribution are potentially altering exposure to photosynthetically active radiation (PAR) and ultraviolet-B (UV-B) wavelengths of light. Incubations using monospecific cultures of common species from the Ross Sea, Antarctic Peninsula and Arctic Ocean were carried out at ecologically relevant light levels during periods of 7 days to examine tolerance to conditions likely to be faced during sea ice thinning and melt. Algal responses were assessed using chlorophyll fluorescence techniques and superoxide dismutase (SOD) activity. Quantum yields of cultures incubated in the dark and at ambient light did not differ. At higher light levels, the Ross Sea and Arctic cultures showed no significant change in photosynthetic health. Cultures from the Antarctic Peninsula showed a significant decrease. Antarctic cultures showed no detectable changes in SOD activity. Arctic culture showed dynamic changes, initially increasing, then decreasing to the end of the study. The general lack of significant changes signals the need for further parameters to be assessed during such experiments. The coupling between measured parameters appeared to protect photosynthetic health, even though significant effects have been detected in other studies when subjected to PAR or UV-B alone.


Sea ice algae Photoprotection Stress Ultraviolet-B Ross Sea Antarctic Peninsula Arctic Ocean 



The authors acknowledge support from VUW Grant 100241, and FRST Grant VICX0706. MAF permits 2009037596 and 2010040450 were used to transport cultures and samples from Antarctica to New Zealand. The authors thank Antarctica New Zealand for logistic support in the field. Dr. Claire Hughes and Associate Professor Else Hegspeth are thanked for the provision of cultures originally obtained from the Antarctic Peninsula and Arctic Ocean. Two anonymous reviewers are thanked for constructive comments. PC is supported by NERC core funding to the BAS Biodiversity, Evolution and Adaptation Programme. This paper also contributes to the SCAR AnT-ERA International Science Programme.


  1. Arrigo, K. R., 2014. Sea ice ecosystems. Annual Review of Marine Science 6: 439–467.CrossRefPubMedGoogle Scholar
  2. Arrigo, K. R. & D. N. Thomas, 2004. Large scale importance of sea ice biology in the Southern Ocean. Antarctic Science 16: 471–486.CrossRefGoogle Scholar
  3. Arrigo, K. R., C. W. Sullivan & J. N. Kremer, 1991. A bio-optical model of Antarctic sea ice. Journal of Geophysical Research: Oceans 96: 10581–10592.CrossRefGoogle Scholar
  4. Arrigo, K. R., T. Mock & M. P. Lizotte, 2010. Primary producers and sea ice. In Thomas, D. N. & G. S. Dieckmann (eds), Sea Ice, 2nd ed. Blackwell Publishing Ltd., Oxford: 283–325.Google Scholar
  5. Arrigo, K. R., D. K. Perovich, R. S. Pickart, Z. W. Brown, G. L. van Dijken, K. E. Lowry, et al., 2012. Massive phytoplankton blooms under Arctic Sea ice. Science 336: 1408.CrossRefPubMedGoogle Scholar
  6. Beauchamp, C. & I. Fridovich, 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44: 276–287.CrossRefPubMedGoogle Scholar
  7. Beyer, W. F. & I. Fridovich, 1987. Assaying for superoxide dismutase activity: some large consequences for minor changes in conditions. Analytical Biochemistry 161: 559–566.CrossRefPubMedGoogle Scholar
  8. Cunningham, W. L. & A. Leventer, 1998. Diatom assemblages in surface sediments of the Ross Sea: relationship to present oceanographic conditions. Antarctic Science 10: 134–146.CrossRefGoogle Scholar
  9. Davidson, A. T., D. Bramich, H. J. Marchant & A. McMinn, 1994. Effects of UV-B irradiation on growth and survival of Antarctic marine diatoms. Marine Biology 119: 507–515.CrossRefGoogle Scholar
  10. Eicken, H., 1992. The role of sea ice in structuring Antarctic ecosystems. Polar Biology 12: 3–13.CrossRefGoogle Scholar
  11. Evans, C. A., J. E. O’Reilly & J. P. Thomas, 1987. A Handbook for the Measurement of Chlorophyll a and Primary Production. Texas A&M University, College Station.Google Scholar
  12. Folt, C. L., C. Y. Chen, M. V. Moore & J. Burnaford, 1999. Synergism and antagonism among multiple stressors. Limnology and Oceanography 44: 864–877.CrossRefGoogle Scholar
  13. Fryer, M. J., J. R. Andrews, K. Oxborough, D. A. Blowers & R. Baker, 1998. Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116: 571–580.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Gao, K., J. Xu, G. Gao, Y. Li, D. A. Hutchins, B. Huang, L. Wang, Y. Zheng, P. Jin, X. Cai, D.-P. Hader, W. Li, K. Xu, N. Liu & U. Riebesell, 2012. Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Climate Change 2: 519–523.Google Scholar
  15. Garibotti, I. A., M. Vernet & M. E. Ferrario, 2005. Annually recurrent phytoplanktonic assemblages during summer in the seasonal ice zone west of the Antarctic Peninsula (Southern Ocean). Deep Sea Research Part I: Oceanographic Research Papers 52: 1823–1841.CrossRefGoogle Scholar
  16. Greenhouse, S. W. & S. Geisser, 1959. On methods in the analysis of profile data. Psychometrika 24: 95–112.CrossRefGoogle Scholar
  17. Gregory, E. M. & I. Fridovich, 1973. Induction of superoxide dismutase by molecular oxygen. Journal of Bacteriology 114: 543–548.PubMedCentralPubMedGoogle Scholar
  18. Halac, S., E. Garcia-Mendoza & A. T. Banaszak, 2009. Ultraviolet radiation reduces the photoprotective capacity of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae, Heterokontophyta). Photochemistry and Photobiology 85: 807–815.CrossRefPubMedGoogle Scholar
  19. Halac, S. R., V. E. Villafañe & E. W. Helbling, 2010. Temperature benefits the photosynthetic performance of the diatoms Chaetoceros gracilis and Thalassiosira weissflogii when exposed to UVR. Journal of Photochemistry and Photobiology B: Biology 101: 196–205.CrossRefGoogle Scholar
  20. Hancke, K., T. B. Hancke, L. M. Olsen, G. Johnsen & R. N. Glud, 2008. Temperature effects on microalgal photosynthesis-light responses measured by O2 production, pulse-amplitude-modulated fluorescence, and 14C assimilation. Journal of Phycology 44: 501–514.CrossRefGoogle Scholar
  21. Hannach, G. & A. C. Sigleo, 1998. Photoinduction of UV-absorbing compounds in six species of marine phytoplankton. Marine Ecology Progress Series 174: 207–222.CrossRefGoogle Scholar
  22. Harrison, W. G. & G. F. Cota, 1991. Primary production in polar waters: relation to nutrient availability. Polar Research 10: 87–104.CrossRefGoogle Scholar
  23. Janknegt, P. J., J. W. Rijstenbil, W. H. van de Poll, T. S. Gechev & A. G. J. Buma, 2007. A comparison of quantitative and qualitative superoxide dismutase assays for application to low temperature microalgae. Journal of Photochemistry and Photobiology B: Biology 87: 218–226.CrossRefGoogle Scholar
  24. Janknegt, P. J., C. M. de Graaff, W. H. van de Poll, R. J. W. Visser, J. W. Rijstenbil & A. G. J. Buma, 2009. Short-term antioxidative responses of 15 microalgae exposed to excessive irradiance including ultraviolet radiation. European Journal of Phycology 44: 525–539.CrossRefGoogle Scholar
  25. Katayama, T. & S. Taguchi, 2013. Photoprotective responses of an ice algal community in Saroma-Ko Lagoon, Hokkaido, Japan. Polar Biology 36: 1431–1439.CrossRefGoogle Scholar
  26. Leu, E., S.-Å. Wängberg, A. Wulff, S. Falk-Petersen, J. Børre Ørbæk & D. O. Hessen, 2006. Effects of changes in ambient PAR and UV radiation on the nutritional quality of an Arctic diatom (Thalassiosira antarctica var. borealis). Journal of Experimental Marine Biology and Ecology 337: 65–81.CrossRefGoogle Scholar
  27. Leu, E., J. Wiktor, J. E. Søreide, J. Berge & S. Falk-Petersen, 2010. Increased irradiance reduces food quality of sea ice algae. Marine Ecology Progress Series 411: 49–60.CrossRefGoogle Scholar
  28. Lund-Hansen, L. C., I. Hawes, B. K. Sorrell & M. H. Nielsen, 2013. Removal of snow cover inhibits spring growth of Arctic ice algae through physiological and behavioral effects. Polar Biology 37: 471–481.CrossRefGoogle Scholar
  29. Majewska, R., M. C. Gambi, C. M. Totti & M. De Stefano, 2013. Epiphytic diatom communities of Terra Nova Bay (Ross Sea, Antarctica): structural analysis and relations to algal host. Antarctic Science 25: 501–513.CrossRefGoogle Scholar
  30. Maksym, T., S. E. Stammerjohn, S. Ackley & R. Massom, 2012. Antarctic sea ice – a polar opposite? Oceanography 25: 140–151.CrossRefGoogle Scholar
  31. Mangoni, O., M. Saggiomo, M. Modigh, G. Catalano, A. Zingone & V. Saggiomo, 2009. The role of platelet ice microalgae in seeding phytoplankton blooms in Terra Nova Bay (Ross Sea, Antarctica): a mesocosm experiment. Polar Biology 32: 311–323.CrossRefGoogle Scholar
  32. Martin, A., A. McMinn, M. Heath, E. N. Hegseth & K. G. Ryan, 2012. The physiological response to increased temperature in over-wintering sea ice algae and phytoplankton in McMurdo Sound, Antarctica and Tromso Sound, Norway. Journal of Experimental Marine Biology and Ecology 428: 57–66.CrossRefGoogle Scholar
  33. McMinn, A. & E. N. Hegseth, 2004. Quantum yield and photosynthetic parameters of marine microalgae from the southern Arctic Ocean, Svalbard. Journal of the Marine Biological Association of the United Kingdom 84: 865–871.CrossRefGoogle Scholar
  34. Mundy, C., M. Gosselin, J. Ehn, C. Belzile, M. Poulin, E. Alou, et al., 2011. Characteristics of two distinct high-light acclimated algal communities during advanced stages of sea ice melt. Polar Biology 34: 1869–1886.CrossRefGoogle Scholar
  35. Nicol, S., J. Clarke, S. J. Romaine, S. Kawaguchi, G. Williams & G. W. Hosie, 2008. Krill (Euphausia superba) abundance and Adélie penguin (Pygoscelis adeliae) breeding performance in the waters off the Béchervaise Island colony, East Antarctica in 2 years with contrasting ecological conditions. Deep Sea Research Part II: Topical Studies in Oceanography 55: 540–557.CrossRefGoogle Scholar
  36. Parkhill, J.-P., G. Maillet & J. J. Cullen, 2001. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. Journal of Phycology 37: 517–529.CrossRefGoogle Scholar
  37. Petrou, K. & P. Ralph, 2011. Photosynthesis and net primary productivity in three Antarctic diatoms: possible significance for their distribution in the Antarctic marine ecosystem. Marine Ecology Progress Series 437: 27–40.CrossRefGoogle Scholar
  38. Petrou, K., S. A. Kranz, M. A. Doblin & P. J. Ralph, 2011. Photophysiological responses of Fragilariopsis cylindrus (Bacillariophyceae) to nitrogen depletion at two temperatures. Journal of Phycology 48: 127–136.CrossRefGoogle Scholar
  39. Rajanahally, M. A. 2014. Antarctic microalgae: physiological acclimation to environmental change. MSc Thesis, Victoria University of Wellington, Wellington.Google Scholar
  40. Rajanahally, M. A., D. Sim, K. G. Ryan & P. Convey, 2014. Can bottom ice algae tolerate irradiance and temperature changes? Journal of Experimental Marine Biology and Ecology 461: 516–527.CrossRefGoogle Scholar
  41. Ralph, P. J. & R. Gademann, 2005. Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82: 222–237.CrossRefGoogle Scholar
  42. Ratkova, T. N., A. F. Sazhin & K. N. Kosobokova, 2004. Unicellular inhabitants of the White Sea under ice pelagic zone during the early spring period. Oceanology 44: 240–246.Google Scholar
  43. Riebesell, U., I. Schloss & V. Smetacek, 1991. Aggregation of algae released from melting sea ice: implications for seeding and sedimentation. Polar Biology 11: 239–248.CrossRefGoogle Scholar
  44. Ritchie, R., 2008. Fitting light saturation curves measured using modulated fluorometry. Photosynthesis Research 96: 201–215.CrossRefPubMedGoogle Scholar
  45. Rost, B., U. Riebesell & D. Sultemeyer, 2006. Carbon acquisition of marine phytoplankton: effect of photoperiod length. Limnology and Oceanography 51: 12–20.CrossRefGoogle Scholar
  46. Ryan, K. G., A. McMinn, K. A. Mitchell & L. Trenerry, 2002. Mycosporine-like amino acids in Antarctic Sea ice algae, and their response to UVB radiation. Zeitschrift fur Naturforschung 57: 471–477.PubMedGoogle Scholar
  47. Ryan, K. G., R. O. M. Cowie, E. Liggins, D. McNaughtan, A. Martin & S. K. Davy, 2009. The short-term effect of irradiance on the photosynthetic properties of antarctic fast-ice microalgal communities. Journal of Phycology 45: 1290–1298.CrossRefGoogle Scholar
  48. Ryan, K. G., M. L. Tay, A. Martin, A. McMinn & S. K. Davy, 2011. Chlorophyll fluorescence imaging analysis of the responses of Antarctic bottom-ice algae to light and salinity during melting. Journal of Experimental Marine Biology and Ecology 399: 156–161.CrossRefGoogle Scholar
  49. Ryan, K. G., A. McMinn, E. N. Hegseth & S. K. Davy, 2012. The effects of ultraviolet-B radiation on Antarctic Sea-ice algae. Journal of Phycology 48: 74–84.CrossRefGoogle Scholar
  50. Rysgaard, S., M. Kuhl, R. N. Glud & J. W. Hansen, 2001. Biomass, production and horizontal patchiness of sea ice algae in a high-Arctic fjord (Young Sound, NE Greenland). Marine Ecology Progress Series 223: 15–26.CrossRefGoogle Scholar
  51. Salleh, S. & A. McMinn, 2011. Photosynthetic response and recovery of Antarctic marine benthic microalgae exposed to elevated irradiances and temperatures. Polar Biology 34: 855–869.CrossRefGoogle Scholar
  52. SooHoo, J. B., A. C. Palmisano, S. T. Kottmeier, M. P. Lizotte, S. L. SooHoo & C. W. Sullivan, 1987. Spectral light absorption and quantum yield of photosynthesis in sea ice microalgae and a bloom of Phaeocystis pouchetii from McMurdo Sound, Antarctica. Marine Ecology Progress Series 39: 175–189.CrossRefGoogle Scholar
  53. Stammerjohn, S., R. Massom, D. Rind & D. Martinson, 2012. Regions of rapid sea ice change: an inter-hemispheric seasonal comparison. Geophysical Research Letters 39: L06501.CrossRefGoogle Scholar
  54. Thomas, D. N. & G. S. Dieckmann, 2003. Sea Ice: An Introduction to its Physics, Chemistry, Biology and Geology. Wiley-Blackwell, Oxford.CrossRefGoogle Scholar
  55. Turner, J., N. E. Barrand, T. J. Bracegirdle, P. Convey, D. A. Hodgson, M. Jarvis, et al., 2013. Antarctic climate change and the environment: an update. Polar Record 50: 237–259.CrossRefGoogle Scholar
  56. van de Poll, W. H. & A. G. J. Buma, 2009. Does ultraviolet radiation affect the xanthophyll cycle in marine phytoplankton? Photochemical and Photobiological Sciences 8: 1295–1301.CrossRefPubMedGoogle Scholar
  57. van de Poll, W. H., M. A. van Leeuwe, J. Roggeveld & A. G. J. Buma, 2005. Nutrient limitation and high irradiance acclimation reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). Journal of Phycology 41: 840–850.CrossRefGoogle Scholar
  58. van de Poll, W. H., P. J. Janknegt, M. A. van Leeuwe, R. J. W. Visser & A. G. J. Buma, 2009. Excessive irradiance and antioxidant responses of an Antarctic marine diatom exposed to iron limitation and to dynamic irradiance. Journal of Photochemistry and Photobiology B: Biology 94: 32–37.CrossRefGoogle Scholar
  59. Vernet, M., D. Martinson, R. Iannuzzi, S. Stammerjohn, W. Kozlowski, K. Sines, et al., 2008. Primary production within the sea-ice zone west of the Antarctic Peninsula: sea ice, summer mixed layer, and irradiance. Deep Sea Research Part II: Topical Studies in Oceanography 55: 2068–2085.CrossRefGoogle Scholar
  60. Zor, T. & Z. Selinger, 1996. Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Analytical Biochemistry 236: 302–308.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Meghana A. Rajanahally
    • 1
  • Phil J. Lester
    • 1
  • Peter Convey
    • 1
    • 2
  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.British Antarctic SurveyNERCCambridgeUK

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