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Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers

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Abstract

It is well known that UV radiation can cause deleterious effects to the physiological performance, growth and species assemblages of marine primary producers. In this review we describe the range of interactions observed between these impacts of ultraviolet radiation (UVR, 280–400 nm) with other environmental factors such as the availability of photosynthetically active radiation (PAR), nutrient status and levels of dissolved CO2, all of which can, in turn, be influenced by global climate change. Thus, increases in CO2 levels can affect the sensitivity of some species to UV-B radiation (UV-B), while others show no such impact on UV-B susceptibility. Both nitrogen- and phosphorus-limitation can have direct interactive effects on the susceptibility of algal cells and communities to UVR, though such effects are somewhat variable. Nutrient depletion can also potentially lead to a dominance of smaller celled species, which may be less able to screen out and are thus likely to be more susceptible to UVR-induced damage. The variability of responses to such interactions can lead to alterations in the species composition of algal assemblages.

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References

  1. J. A. Raven, P. G. Falkowski, Oceanic sinks for atmospheric CO2Plant, Cell Environ. 1999 22 741–755.

    Article  CAS  Google Scholar 

  2. M. J. Behrenfeld, R. T. O’Malley, D. A. Siegel, C. R. McClain, J. L. Sarmiento, G. C. Feldman, A. J. Milligan, P. G. Falkowski, R. M. Letelier, E. S. Boss, Climate-driven trends in contemporary ocean productivity Nature 2006 444 752–755.

    Article  CAS  PubMed  Google Scholar 

  3. S. Doney, The dangers of ocean acidification Sci. Am. 2006 294 58–65.

    Article  PubMed  Google Scholar 

  4. D.-P. Häder, H. D. Kumar, R. C. Smith, R. C. Worrest, Effects of solar UV radiation on aquatic ecosystems and interactions with climate change Photochem. Photobiol. Sci. 2007 6 267–285.

    Article  PubMed  Google Scholar 

  5. J. Beardall, J. A. Raven, The potential effects of global climate change on microalgal photosynthesis, growth and ecology Phycologia 2004 43 26–40.

    Article  Google Scholar 

  6. J. Beardall, S. Stojkovic, Microalgae under global environmental change: implications for growth and productivity, populations and trophic flow Science Asia 2006 32(s1) 1–10.

    Article  Google Scholar 

  7. J. W. Harrison, R. E. H. Smith, Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities Photochem. Photobiol. Sci. 2009 10.1039/b902604e.

    Google Scholar 

  8. S. Burkhardt, U. Riebesell, CO2 availability affects elemental composition (C:N:P) of the marine diatom Skeletonema costatum Mar. Ecol. Prog. Ser. 1997 155 67–76.

    Article  CAS  Google Scholar 

  9. S. Burkhardt, I. Zondervan I, U. Riebesell, Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: a species comparison Limnol. Oceanogr. 1999 44 683–90.

    Article  CAS  Google Scholar 

  10. U. Riebesell, U. A. T. Revill, D. G. Holfsworth, J. K. Volkman, The effect of varying CO2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi Geochim. Cosmochim. Acta 2000 64 4179–92.

    Article  CAS  Google Scholar 

  11. K. A. Hughen, J. T. Overpeck, L. C. Peterson, S. Trumbore, Rapid climate changes in the tropical Atlantic region during the last deglaciation Nature 1996 380 51–54.

    Article  CAS  Google Scholar 

  12. D. L. Hartmann, D.L.J. M. Wallace, J. M. V. Limpasuvan, V. D. W. J. Thompson, J. R. Holton, Can ozone depletion and global warming interact to produce rapid climate change? Proc. Natl. Acad. Sci. U. S. A. 2000 97 1412–1417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. W. F. Vincent, S. Roy, Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery Environ. Rev. 1993 1 1–12.

    Article  CAS  Google Scholar 

  14. M. J. Behrenfeld, D. R. S. Lean, H. Lee, Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic plankton J. Phycol. 1995 31 25–36.

    Article  CAS  Google Scholar 

  15. D. O. Hessen, E. Van Donk, T. Anderson, Growth responses, P-uptake and loss of flagella in Chlamydomonas reinhardtii exposed to UVB J. Plankton Res. 1995 17 17–27.

    Article  Google Scholar 

  16. D. Karentz, J. E. Cleaver, D. L. Mitchell, Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation J. Phycol. 1991 27 326–341.

    Article  CAS  Google Scholar 

  17. W. W. C. Gieskes, A. G. J. Buma, UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton Plant Ecol. 1997 128 17–25.

    Article  Google Scholar 

  18. A. G. J. Buma, T. van Oijen, W. van de Poll, M. J. W. Veldhuis, W. W. L. Gieskes, The sensitivity of Emiliania huxleyi (Prymnesiophyceae) to ultraviolet-B radiation J. Phycol. 2000 36 296–303.

    Article  CAS  Google Scholar 

  19. A. G. J. Buma, E. W. Helbling, M. K. de Boer, V. E. Villafane, Patterns of DNA damage and photoinhibition in temperate South-Atlantic picophytoplankton exposed to solar ultraviolet radiation J. Photochem. Photobiol., B 2001 62 9–18.

    Article  CAS  Google Scholar 

  20. E. W. Helbling, A. G. J. Buma, M. K. de Boer, V. E. Villafane, In situ impact of solar ultraviolet radiation on photosynthesis and DNA in temperate marine phytoplankton Mar. Ecol. Prog. Ser. 2001 211 43–49.

    Article  CAS  Google Scholar 

  21. UV Effects in Aquatic Organisms and Ecosystems, ed. H. Helbling and H. Zagarese, Royal Society of Chemistry, Cambridge2003.

    Google Scholar 

  22. W. F. Vincent and P. J. Neale, Mechanisms of UV damage to aquatic organisms, in The effects of UV radiation in the marine environment, ed. S. de Mora, S. Demers and M. Vernet, Cambridge University Press, Cambridge, 2000, pp. 149–176.

    Chapter  Google Scholar 

  23. M. P. Lesser, J. J. Cullen, J. J P. J. Neale, Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: Relative importance of damage and repair J. Phycol. 1994 30 183–192.

    Article  CAS  Google Scholar 

  24. P. J. Neale, Spectral weighting functions for quantifying the effects of ultraviolet radiation in marine ecosystems, in Effects of UV Radiation on the Marine Environment, ed. S. J. De Mora, S. Demers and M. Vernet, Cambridge University Press, Cambridge, 2000, pp. 73–100.

    Google Scholar 

  25. P. Heraud, P. J. Beardall, J. Changes, in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to ultraviolet radiation exposure indicate a dynamic interaction between damage and repair processes Photosynth. Res. 2000 63 123–134.

    Article  CAS  PubMed  Google Scholar 

  26. J. Rozema, L. O. Björn, J. F. Bornman, A. Gaberščik, D.-P. Häder, T. Trošt, M. Gšerm, M. Klish, A. Gröniger, R. P. Sinha, M. Lebert, Y. Y. He, R. Buffoni-Hall, N. V. J. de Bakker, J. van de Staaij, B. B. Meijkamp, The role of UVB radiation in aquatic and terrestrial ecosystems–an experimental and functional analysis of the evolution of UV-absorbing compounds J. Photochem. Photobiol., B 2002 66 2–12.

    Article  CAS  Google Scholar 

  27. W. H. Van de Poll, P. J. Janknegt, M. A. van Leeuwe, R. J. W. Visser, A. G. J. Buma, Excessive irradiance and antioxidant responses of an Antarctic marine diatom exposed to iron limitation and to dynamic irradiance J. Photochem. Photobiol., B 2009 94 32–37.

    Article  CAS  Google Scholar 

  28. J. Beardall, S. Roberts, E. Young, Approaches for determining phytoplankton nutrient limitation Aquat. Sci. 2001 63 44–69.

    Article  CAS  Google Scholar 

  29. J. Beardall, A. Allen, J. Bragg, Z. V. Finkel, K. J. Flynn, A. Quigg, T. A. V. Rees, A. J. Richardson, J. A. Raven, Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton New Phytol. 2009 181 295–309.

    Article  CAS  PubMed  Google Scholar 

  30. F. Garcia-Pichell, A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens Limnol. Oceanogr. 1994 39 1704–1717.

    Article  Google Scholar 

  31. J. A. Raven, Responses of aquatic photosynthetic organisms to increased solar UVB J. Photochem. Photobiol., B 1991 9 239–244.

    Article  Google Scholar 

  32. R. Sommaruga, Y. Chen, Z. Liu, Multiple strategies of bloom-forming Microcystis to minimize damage by solar ultraviolet radiation in surface waters Microb. Ecol. 2009 57 667–674.

    Article  PubMed  Google Scholar 

  33. J. A. Raven, Small is beautiful. The picophytoplankton Funct. Ecol. 1998 12 503–513.

    Article  Google Scholar 

  34. L. Bopp, O. Aumont, P. Cadule, S. Alvain, M. Gehlen, Response of diatoms distribution to global warming and potential implications: A global model study Geophys. Res. Lett. 2005 32 L19606.

    Article  CAS  Google Scholar 

  35. A. Bakun, Global climate change and intensification of coastal ocean upwelling Science 1990 247 198–201.

    Article  CAS  PubMed  Google Scholar 

  36. T. Takahashi, S. C. Sutherland, C. Sweeney, A. Poisson, N. Metzl, B. Tilbrook, N. Bates, R. Wanninkhof, R. A. Feely, C. Sabine, J. Olafsson, Y. C. Nojiri, Global sea-air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects Deep-Sea Res., Part II 2002 49 1601–1622.

    Article  CAS  Google Scholar 

  37. J. B. Reiskind, S. Beer, G. Bowes, Photosynthesis, photorespiration and ecophysiological interactions in marine macroalgae Aquat. Bot. 1989 34 131–152.

    Article  CAS  Google Scholar 

  38. R. G. Zepp, D. J. Erickson, III, N. D. Paul, B. Sulzberger, Interactive effects of solar UV radiation and climate change on biogeochemical cycling Photochem. Photobiol. Sci. 2007 6 286–300.

    Article  CAS  PubMed  Google Scholar 

  39. C. Sobrino, M. L. Ward, P. J. Neale, Acclimation to elevated CO2 and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis and spectral sensitivity of photoinhibition Limnol. Oceanogr. 2008 53 494–505.

    Article  CAS  Google Scholar 

  40. C. Sobrino, P. J. Neale, L. M. Lubián, Interaction of UV radiation and inorganic carbon supply in the inhibition of photosynthesis: Spectral and temporal responses of two marine picoplankters Photochem. Photobiol. 2005 81 384–393.

    Article  CAS  PubMed  Google Scholar 

  41. J. Beardall, P. Heraud, S. Roberts, K. Shelly, S. Stojkovic, Effects of UVB radiation on inorganic carbon acquisition by the marine microalga Dunaliella tertiolecta (Chlorophyceae) Phycologia 2002 41 268–272.

    Article  Google Scholar 

  42. M. Giordano, J. Beardall, J. A. Raven, CO2 concentrating mechanisms in algae: mechanisms, environmental modulation and evolution Annu. Rev. Plant Biol. 2005 56 99–131.

    Article  CAS  PubMed  Google Scholar 

  43. J. Beardall, M. Giordano, Ecological implications of microalgal and cyanobacterial CCMs and their regulation Funct. Plant Biol. 2002 29 335–347.

    Article  CAS  PubMed  Google Scholar 

  44. P. D. Tortell, G. H. Rau, F. M. M. Morel, Inorganic carbon acquisition in coastal Pacific phytoplankton communities Limnol. Oceanogr. 2000 45 1485–1500.

    Article  CAS  Google Scholar 

  45. P. D. Tortell, F. M. M. Morel, Sources of inorganic carbon for phytoplankton in the eastern Subtropical and Equatorial Pacific Ocean Limnol. Oceanogr 2002 47 1012–1022.

    Article  Google Scholar 

  46. J. Beardall, J. A. Raven, The potential effects of global climate change on microalgal photosynthesis, growth and ecology, Phycologia 204 26-40.

  47. J. A. Raven, Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: Relation to increased CO2 and temperature Plant, Cell Environ. 1991 14 779–794.

    Article  CAS  Google Scholar 

  48. J. E. Kübler, A. M. Johnston, J. A. Raven, The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata Plant, Cell Environ. 1999 22 1303–1310.

    Article  Google Scholar 

  49. J. M. Mercado, F. J. L. Gordillo, F. L. Figueroa, F. X. Niell, External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae J. Exp. Mar. Biol. Ecol. 1998 221 209–220.

    Article  CAS  Google Scholar 

  50. A. Israel, M. Hophy, Growth, photosynthetic properties and RUBISCO activies and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations Global Change Biol. 2002 8 831–840.

    Article  Google Scholar 

  51. S. Collins, D. Sultemeyer, G. Bell, Changes in C uptake in populations of Chlamydomonas reinhardtii selected at high CO2Plant, Cell Environ. 2006 29 1812–1819.

    Article  CAS  Google Scholar 

  52. P. J. Neale, R. F. Davis, J. J. Cullen, Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton Nature 1998 392 585–589.

    Article  CAS  Google Scholar 

  53. A. T. Banaszak, P. J. Neale, UV sensitivity of photosynthesis in phytoplankton from an estuarine environment Limnol. Oceanogr. 2001 46 592–600.

    Article  Google Scholar 

  54. P. J. Neale, E. Litchman, C. Sobrino, C. Callieri, G. Morabito, V. Montecino, Y. Huot, P. Bossard, C. Lehmann, D. Steiner, Quantifying the response of phytoplankton photosynthesis to ultraviolet radiation: biological weighting functions versus in situ measurements in two Swiss lakes Aquat. Sci. 2001 63 265–285.

    Article  Google Scholar 

  55. K. Gao, Y. Wu, G. Li, H. Wu, V. E. Villafañe, E. W. Helbling, Solar UV Radiation Drives CO2 Fixation in Marine Phytoplankton: A Double-Edged Sword Plant Physiol. 2007 144 54–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. J. A. Raven, Putting the C in Phycology Eur. J. Phycol. 1997 32 319–333.

    Article  Google Scholar 

  57. M. R. Badger, T. J. Andrews, S. M. Whitney, M. Ludwig, D. C. Yellowlees, W. Leggat, G. D. Price, The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae Can. J. Bot. 1998 76 1052–1071.

    CAS  Google Scholar 

  58. J. Beardall, A. M. Johnston, J. A. Raven, Environmental regulation of the CO2 concentrating mechanism in cyanobacteria and microalgae Can. J. Bot. 1998 76 1010–1017.

    CAS  Google Scholar 

  59. J. Beardall, J. A. Raven, Transport of inorganic carbon and the “CO2 concentrating mechanism” in Chlorella emersonii (Chlorophyceae) J. Phycol. 1981 17 134–141.

    Article  CAS  Google Scholar 

  60. K. Palmqvist, L.-G. Sundblad, G. Wingsle, G. Samuelsson, Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii Plant Physiol. 1990 94 357–366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. J. H. A. Nugent, S. Purton, M. C. W. Evans, Oxygenic photosynthesis in algae and cyanobacteria: electron transfer in photosystems I and II Adv. Photosynth. Respir. 2003 14 133–156.

    Article  CAS  Google Scholar 

  62. Y. Song, B. Qiu, The CO2-concentrating mechanism in the bloom-forming cyanobacterium Microcystis aeruginosa (Cyanophyceae) and effects of UVB radiation on its operation J. Phycol. 2007 43 957–964.

    Article  CAS  Google Scholar 

  63. H. Wu, K. Gao, Ultraviolet radiation stimulated activity of extracellular carbonic anhydrase in the marine diatom Skeletonema costatum Funct. Plant Biol. 2009 36 137–143.

    Article  CAS  PubMed  Google Scholar 

  64. C. Sobrino, P. J. Neale, J. D. Phillips-Kress, R. E. Moeller, J. A. Porter, Elevated CO2 increases sensitivity to ultraviolet radiation in lacustrine phytoplankton assemblages Limnol. Oceanogr. 2009, in press

    Google Scholar 

  65. P. D. Tortell, G. H. Rau, F. M. M. Morel, Inorganic carbon acquisition in coastal Pacific phytoplankton communities Limnol. Oceanogr. 2000 45 1485–1500.

    Article  CAS  Google Scholar 

  66. K. Aizawa, S. Miyachi, Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria FEMS Microbiol. Lett. 1986 39 215–233.

    Article  CAS  Google Scholar 

  67. I. Berman-Frank, J. Erez, A. Kaplan, Changes in inorganic carbon uptake during the progression of a dinoflagellate bloom in a lake ecosystem Can. J. Bot. 1998 76 1043–1051.

    CAS  Google Scholar 

  68. E. Litchman, P. J. Neale, A. T. Banaszak, Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair Limnol. Oceanogr. 2002 47 86–94.

    Article  CAS  Google Scholar 

  69. M. Surpin, R. M. Larkin, J. Chory, Signal Transduction between the chloroplast and the nucleus Plant Cell 2002 14 327–338.

    Article  CAS  Google Scholar 

  70. D. H. Zou, K. S. Gao, Z. X. Run, Daily, timing of emersion and elevated atmospheric CO2 concentration affect photosynthetic performance of the intertidal macroalga Ulva lactuca (Chorophyta) in sunlight Bot. Mar. 2007 50 275–279.

    Article  CAS  Google Scholar 

  71. K. Swanson, C. H. Fox, Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs Global Change Biol. 2007 13 1696–1709.

    Article  Google Scholar 

  72. V. E. Villafañe, K. Sundbäck, F. L. Figueroa and E. W. Helbling, Photosynthesis in the aquatic environment as affected by ultraviolet radiation, in UV effects in aquatic organisms and ecosystems, ed. E. W. Helbling and H. Zagarese, Royal Society of Chemistry, Cambridge, 2003, pp. 357–397.

    Google Scholar 

  73. M. J. Behrenfeld, H. Lee, L. F. Small, Interactions between nutritional status and long-term responses of ultraviolet-B radiation stress in a marine diatom Mar. Biol. 1994 118 523–530.

    Article  Google Scholar 

  74. A. Veen, M. Reuvers, P. Roncak, Effects of acute and chronic UVB exposure on a green alga: a continuous culture study using a computer-control dynamic light regime Plant Ecol. 1997 128 29–40.

    Article  Google Scholar 

  75. K. Shelly, P. Heraud, J. Beardall, Nitrogen limitation in Dunaliella tertiolecta Butcher (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity J. Phycol. 2002 38 713–720.

    Article  CAS  Google Scholar 

  76. K. Shelly, Interactions between UVB radiation and nutrient-limitation in a marine microalga, PhD thesis, Monash University, 2005.

    Google Scholar 

  77. Y. Zheng, K. Gao, Impacts of solar UV radiation on the photosynthesis, growth and UV-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations J. Phycol. 2009 45 314–323.

    Article  CAS  PubMed  Google Scholar 

  78. J. E. Tillberg, J. R. Rowley, Physiological and structural effects of phosphorus starvation on the unicellular alga Scenedesmus Physiol. Plant. 1989 75 315–332.

    Article  CAS  Google Scholar 

  79. G. P. Harris, B. B. Piccinin, Phosphorus limitation and carbon metabolism in a unicellular alga: interaction between growth rate and the measurement of net and gross photosynthesis J. Phycol. 1983 19 185–192.

    Article  CAS  Google Scholar 

  80. R. J. Geider, J. La Roche, R. M. Greene, M. Olaizola, Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate or iron starvation J. Phycol. 1993 29 755–766.

    Article  CAS  Google Scholar 

  81. J. La Roche, R. J. Geider, L. M. Graziano, H. Murray, K. Lewis, Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus- and nitrogen-deficient conditions J. Phycol. 1993 29 767–777.

    Article  Google Scholar 

  82. M. A. Xenopoulos, P. C. Frost, UV radiation, phosphorus, and their combined effects on the taxonomic composition of phytoplankton in boreal lake J. Phycol. 2003 39 291–302.

    Article  CAS  Google Scholar 

  83. M. L. Bothwell, D. Sherbot, A. C. Roberge, R. J. Daley, Influence of natural ultraviolet radiation on lotic periphytic diatom community growth, biomass accrual and species composition: short-term versus long-term effects J. Phycol. 1993 29 24–35.

    Article  Google Scholar 

  84. M. L. Bothwell, D. M. J. Sherbot, C. M. Pollock, Ecosystem responses to solar ultraviolet-B radiation: influence to trophic-level interactions Science 1994 265 97–100.

    Article  CAS  PubMed  Google Scholar 

  85. L. Aubriot, D. Conde, S. Bonilla, R. Sommaruga, Phosphate uptake behavior of natural phytoplankton during exposure to solar ultraviolet radiation in a shallow coastal lagoon Mar. Biol. 2004 144 623–631.

    Article  CAS  Google Scholar 

  86. C. D. Allen, R. E. H. Smith, The response of planktonic phosphate uptake and turnover to ultraviolet radiation in Lake Erie Can. J. Fish. Aquat. Sci. 2002 59 778–786.

    Article  Google Scholar 

  87. K. Garde, K. Gustavson, The impact of UVB radiation on alkaline phosphatase activity in phosphorus-depleted marine ecosystems J. Exp. Mar. Biol. Ecol. 1999 238 93–105.

    Article  CAS  Google Scholar 

  88. M. A. Xenopoulos, D. F. Bird, Effect of acute exposure to hydrogen peroxide on the production of phytoplankton and bacterioplankton in a mesohumic lake Photochem. Photobiol. 1997 66 471–478.

    Article  CAS  Google Scholar 

  89. R. G. Wetzel, P. G. Hatcher, T. S. Bianchi, Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism Limnol. Oceanogr. 1995 40 1369–1380.

    Article  CAS  Google Scholar 

  90. P. Heraud, S. Roberts, K. Shelly, J. Beardall, Interactions between UVB exposure and phosphorus nutrition. II. Effects, on rates of damage and repair J. Phycol. 2005 41 1212–1218.

    Article  CAS  Google Scholar 

  91. D. Pryputniewicz, L. Falkowska, D. Burska, Adenosine triphosphate in the marine boundary layer in the southern Baltic Sea. Oceanologia 2002 44 461–473.

    Google Scholar 

  92. S. Stojkovic, Studies on the effect of phosphorus loading of streams on the susceptibility of algal biofilms to UVB radiation, PhD Thesis, Monash University, 2005.

    Google Scholar 

  93. K. Shelly, S. Roberts, P. Heraud, J. Beardall, Interactions between UVB exposure and phosphorus nutrition. I. Effects, on growth, phosphorus uptake, and chlorophyll fluorescence J. Phycol. 2005 41 1204–1211.

    Article  CAS  Google Scholar 

  94. M. J. Behrenfeld, A. J. Bale, Z. S. Kolber, J. Aiken, P. G. Falkowski, Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean Nature 1996 383 508–511.

    Article  CAS  Google Scholar 

  95. W. H. van de Poll, M. A. van Leeuwe, J. Roggeveld, A. G. J. Buma, Nutrient limitation and high irradiance reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis J. Phycol. 2005 41 840–850.

    Article  Google Scholar 

  96. R. Sommaruga, J. S. Hofer, L. Alonso-Sáez, J. M. Gaso, Differential sunlight sensitivity of picophytoplankton from surface Mediterranean coastal waters Appl. Environ. Microbiol. 2005 71 2154–2157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. School of Biological Sciences, Monash University, Clayton, Victoria, 3800, Australia

    John Beardall (Professor) &  Slobodanka Stojkovic

  2. Departamento de Ecología y Biología Animal, Universidad de Vigo, 36310, Vigo, Spain

    Cristina Sobrino

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Beardall, J., Sobrino, C. & Stojkovic, S. Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochem Photobiol Sci 8, 1257–1265 (2009). https://doi.org/10.1039/b9pp00034h

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