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The interactive effects of stratospheric ozone depletion, UV radiation, and climate change on aquatic ecosystems

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Abstract

This assessment summarises the current state of knowledge on the interactive effects of ozone depletion and climate change on aquatic ecosystems, focusing on how these affect exposures to UV radiation in both inland and oceanic waters. The ways in which stratospheric ozone depletion is directly altering climate in the southern hemisphere and the consequent extensive effects on aquatic ecosystems are also addressed. The primary objective is to synthesise novel findings over the past four years in the context of the existing understanding of ecosystem response to UV radiation and the interactive effects of climate change. If it were not for the Montreal Protocol, stratospheric ozone depletion would have led to high levels of exposure to solar UV radiation with much stronger negative effects on all trophic levels in aquatic ecosystems than currently experienced in both inland and oceanic waters. This “world avoided” scenario that has curtailed ozone depletion, means that climate change and other environmental variables will play the primary role in regulating the exposure of aquatic organisms to solar UV radiation. Reductions in the thickness and duration of snow and ice cover are increasing the levels of exposure of aquatic organisms to UV radiation. Climate change was also expected to increase exposure by causing shallow mixed layers, but new data show deepening in some regions and shoaling in others. In contrast, climate-change related increases in heavy precipitation and melting of glaciers and permafrost are increasing the concentration and colour of UV-absorbing dissolved organic matter (DOM) and particulates. This is leading to the “browning” of many inland and coastal waters, with consequent loss of the valuable ecosystem service in which solar UV radiation disinfects surface waters of parasites and pathogens. Many organisms can reduce damage due to exposure to UV radiation through behavioural avoidance, photoprotection, and photoenzymatic repair, but meta-analyses continue to confirm negative effects of UV radiation across all trophic levels. Modeling studies estimating photoinhibition of primary production in parts of the Pacific Ocean have demonstrated that the UV radiation component of sunlight leads to a 20% decrease in estimates of primary productivity. Exposure to UV radiation can also lead to positive effects on some organisms by damaging less UV-tolerant predators, competitors, and pathogens. UV radiation also contributes to the formation of microplastic pollutants and interacts with artificial sunscreens and other pollutants with adverse effects on aquatic ecosystems. Exposure to UV-B radiation can decrease the toxicity of some pollutants such as methyl mercury (due to its role in demethylation) but increase the toxicity of other pollutants such as some pesticides and polycyclic aromatic hydrocarbons. Feeding on microplastics by zooplankton can lead to bioaccumulation in fish. Microplastics are found in up to 20% of fish marketed for human consumption, potentially threatening food security. Depletion of stratospheric ozone has altered climate in the southern hemisphere in ways that have increased oceanic productivity and consequently the growth, survival and reproduction of many sea birds and mammals. In contrast, warmer sea surface temperatures related to these climate shifts are also correlated with declines in both kelp beds in Tasmania and corals in Brazil. This assessment demonstrates that knowledge of the interactive effects of ozone depletion, UV radiation, and climate change factors on aquatic ecosystems has advanced considerably over the past four years and confirms the importance of considering synergies between environmental factors.

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References

  1. D.-P. Häder, C. E. Williamson, S.-Å. Wängberg, M. Rautio, K. C. Rose, K. Gao, E. W. Helbling, R. P. Sinha and R. Worrest, Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors, Photochem. Photobiol. Sci., 2015, 14 ,108–126.

    Article  Google Scholar 

  2. P. J. Neale, E. Helbling and H. Zagarese, Modulation of UV exposure and effects by vertical mixing and advection, in UV Effects in Aquatic Organisms and Ecosystems, ed. E. Helbling and H. Zagarese, Royal Society of Chemistry, 2003, pp. 107–134.

    Google Scholar 

  3. E. J. Fee, R. E. Hecky, S. E. M. Kasian and D. R. Cruikshank, Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes, Limnol. Oceanogr., 1996, 41, 912–920.

    Article  CAS  Google Scholar 

  4. J. Read and K. C. Rose, Physical responses of small temperate lakes to variation in dissolved organic carbon concentrations, Limnol. Oceanogr., 2013, 58, 921–931.

    Article  CAS  Google Scholar 

  5. K. C. Rose, L. A. Winslow, J. S. Read and G. J. A. Hansen, Climate-induced warming of lakes can be either amplified or suppressed by trends in water clarity, Limnol. Oceanogr. Lett., 2016, 1, 44–53.

    Article  Google Scholar 

  6. K. Zacher, R. Rautenberger, D. Hanelt, A. Wulff and C. Wiencke, The abiotic environment of polar marine benthic algae, Bot. Mar., 2009, 52, 483–490.

    Article  Google Scholar 

  7. A. F. Bais, G. Bernhard, R. L. McKenzie, P. J. Aucamp, P. J. Young, M. Ilyas, P. Jöckel and M. Deushi, Ozoneclimate interactions and effects on solar ultraviolet radiation, Photochem. Photobiol. Sci., 2019, 18, DOI: 10.1039/C8PP90059K.

  8. C. E. Williamson, E. P. Overholt, J. A. Brentrup, R. M. Pilla, T. H. Leach, S. G. Schladow, J. D. Warren, S. S. Urmy, S. Sadro, S. Chandra and P. J. Neale, Sentinel responses to droughts, wildfires, and floods: effects of UV radiation on lakes and their ecosystem services, Front. Ecol. Environ., 2016, 14, 102–109.

    Article  Google Scholar 

  9. B. Sulzberger, A. T Austin, R. M. Cory, R. G. Zepp and N. D. Paul, Solar UV radiation in a changing world: Roles of cryosphere-land-water-atmosphere interfaces in global biogeochemical cycles, Photochem. Photobiol. Sci., 2019, 18, DOI: 10.1039/C8PP90063A.

  10. S. R. Wilson, S. Madronich, J. D. Longstreth and K. R. Solomon, Interactive effects of changing stratospheric ozone and climate on tropospheric composition and air quality, and the consequences for human and ecosystem health, Photochem. Photobiol. Sci., 2019, 18, DOI:10.1039/C8PP90064G.

  11. J. M. Fischer, M. H. Olson, N. Theodore, C. E. Williamson, K. C. Rose and J. Hwang, Diel vertical migration of copepods in mountain lakes: the changing role of ultraviolet radiation across a transparency gradient, Limnol. Oceanogr., 2015, 60, 252–262.

    Article  Google Scholar 

  12. S. Urmy, C. E. Williamson, T. H. Leach, S. G. Schladow, E. Overholt and J. D. Warren, Vertical redistribution of zooplankton in an oligotrophic lake associated with reduction in ultraviolet radiation by wildfire smoke, Geophys. Res. Lett., 2016, 43, 3746–3753.

    Article  Google Scholar 

  13. B. Kirtman, S. B. Power, J. A. Adedoyin, G. J. Boer, R. Bojariu, I. Camilloni, F. J. Doblas-Reyes, A. M. Fiore, M. Kimoto, G. A. Meehl, M. Prather, A. Sarr, C. Schär, R. Sutton, G. J. van Oldenborgh, G. Vecchi and H. J. Wang, Near-term Climate Change: Projections and Predictability, in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P. M. Midgley, Cambridge University Press, Cambridge, United Kingdom, 2013.

    Google Scholar 

  14. J. J. Magnuson, D. M. Robertson, B. J. Benson, R. H. Whynne, D. M. Livingstone, T. Arai, R. A. Assel, R. G. Barry, V. Card, E. Kuusisto, N. G. Granin, K. M. Prowse, K. M. Steward and V. S. Vuglinski, Historical trends in lake and river ice cover in the Northern Hemisphere, Science, 2000, 289, 1743–1746.

    Article  CAS  PubMed  Google Scholar 

  15. C. J. Cox, R. S. Stone, D. C. Douglas, D. M. Stanitski, G. J. Divoky, G. S. Dutton, C. Sweeney, J. C. George and D. U. Longenecker, Drivers and environmental responses to the changing annual snow cycle of northern Alaska, Bull. Am. Meteorol. Soc., 2017, 98, 2559–2577.

    Article  Google Scholar 

  16. T. Smejkalova, M. E. Edwards and J. Dash, Arctic lakes show strong decadal trend in earlier spring ice-out, Sci. Rep., 2016, 6, 38449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. B. J. Benson, J. J. Magnuson, O. P. Jensen, V. M. Card, G. Hodgkins, J. Korhonen, D. M. Livingstone, K. M. Stewart, G. A. Weyhenmeyer and N. G. Granin, Extreme events, trends, and variability in Northern Hemisphere lake-ice phenology (1855–2005), Clim. Change, 2012, 112, 299–323.

    Article  Google Scholar 

  18. J. C. Comiso, W. N. Meier and R. A. Gersten, Variability and trends in the Arctic Sea ice cover: Results from different techniques, J. Geophys. Res.: Oceans, 2017, 122, 6883–6900.

    Article  Google Scholar 

  19. I. Fountoulakis, A. F. Bais, K. Tourpali, K. Fragkos and S. Misios, Projected changes in solar UV radiation in the Arctic and sub-Arctic Oceans: Effects from changes in reflectivity, ice transmittance, clouds, and ozone, J. Geophys. Res.: Atmos., 2014, 119, 8073–8090.

    Article  Google Scholar 

  20. S. Hylander, T. Kiørboe, P. Snoeijs, R. Sommaruga and T. G. Nielsen, Concentrations of sunscreens and antioxidant pigments in Arctic Calanus spp. in relation to ice cover, ultraviolet radiation, and the phytoplankton spring bloom, Limnol. Oceanogr., 2015, 60, 2197–2206.

    Google Scholar 

  21. R. M. Cory, K. H. Harrold, B. T. Neilson and G. W. Kling, Controls on dissolved organic matter (DOM) degradation in a headwater stream: the influence of photochemical and hydrological conditions in determining light-limitation or substrate-limitation of photo-degradation, Biogeosci. Discuss., 2015, 12, 9793–9838.

    Google Scholar 

  22. C. L. Osburn, H. E. Zagarese, D. P. Morris, B. R. Hargreaves and W. E. Cravero, Calculation of spectral weighting functions for the solar photobleaching of chromophoric dissolved organic matter in temperate lakes, Limnol. Oceanogr., 2001, 46, 1455–1467.

    Article  CAS  Google Scholar 

  23. J. R. Helms, A. Stubbins, J. D. Ritchie, E. C. Minor, D. J. Kieber and K. Mopper, Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter, Limnol. Oceanogr., 2008, 53, 955–969.

    Article  Google Scholar 

  24. M. E. Aullo-Maestro, P. Hunter, E. Spyrakos, P. Mercatoris, A. Kovacs, H. Horvath, T. Preston, M. Presing, J. T. Palenzuela and A. Tyler, Spatio-seasonal variability of chromophoric dissolved organic matter absorption and responses to photobleaching in a large shallow temperate lake, Biogeosciences, 2017, 14, 1215–1233.

    Article  CAS  Google Scholar 

  25. A. J. Constable, J. Melbourne-Thomas, S. P. Corney, K. R. Arrigo, C. Barbraud, D. K. A. Barnes, N. L. Bindoff, P. W. Boyd, A. Brandt, D. P. Costa, A. T. Davidson, H. W. Ducklow, L. Emmerson, M. Fukuchi, J. Gutt, M. A. Hindell, E. E. Hofmann, G. W. Hosie, T Iida, S. Jacob, N. M. Johnston, S. Kawaguchi, N. Kokubun, P. Koubbi, M. A. Lea, A. Makhado, R. A. Massom, K. Meiners, M. P. Meredith, E. J. Murphy, S. Nicol, K. Reid, K. Richerson, M. J. Riddle, S. R. Rintoul, W. O. Smith, C. Southwell, J. S. Stark, M. Sumner, K. M. Swadling, K. T. Takahashi, P. N. Trathan, D. C. Welsford, H. Weimerskirch, K. J. Westwood, B. C. Wienecke, D. Wolf-Gladrow, S. W. Wright, J. C. Xavier and P. Ziegler, Climate change and Southern Ocean ecosystems I: How changes in physical habitats directly affect marine biota, Glob. Change Biol., 2014, 20, 3004–3025.

    Article  Google Scholar 

  26. M. M. Holland, L. Landrum, Y. Kostov and J. Marshall, Sensitivity of Antarctic sea ice to the Southern Annular Mode in coupled climate models, Clim. Dyn., 2017, 49, 1813–1831.

    Article  Google Scholar 

  27. D. T. Monteith, J. L. Stoddard, C. D. Evans, H. A. de Wit, M. Forsius, T. Høgåsen, A. Wilander, B. L. Skjelkvåle, D. S. Jeffries, J. Vuorenmaa, B. Keller, J. Kopácek and J. Vesely, Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry, Nature, 2007, 450, 537–541.

    Article  CAS  PubMed  Google Scholar 

  28. C. E. Williamson, E. P. Overholt, R. M. Pilla, T. H. Leach, J. A. Brentrup, L. B. Knoll, E. M. Mette and R. E. Moeller, Ecological consequences of long-term browning in lakes, Sci. Rep., 2015, 5, 18666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. H. A. de Wit, S. Valinia, G. A. Weyhenmeyer, M. N. Futter, P. Kortelainen, K. Austnes, D. O. Hessen, A. Raike, H. Laudon and J. Vuorenmaa, Current browning of surface waters will be further promoted by wetter climate, Environ. Sci. Technol. Lett., 2016, 3, 430–435.

    Article  CAS  Google Scholar 

  30. E. S. Kritzberg, Centennial-long trends of lake browning show major effect of afforestation, Limnol. Oceanogr. Lett., 2017, 2, 105–112.

    Article  Google Scholar 

  31. C. G. Fichot, S. E. Lohrenz and R. Benner, Pulsed, cross-shelf export of terrigenous dissolved organic carbon to the Gulf of Mexico, J. Geophys. Res.: Oceans, 2014, 119, 1176–1194.

    Article  Google Scholar 

  32. A. Baum, T. Rixen and J. Samiaji, Relevance of peat draining rivers in central Sumatra for the riverine input of dissolved organic carbon into the ocean, Estuarine, Coastal Shelf Sci., 2007, 73, 563–570.

    Article  Google Scholar 

  33. S. Moore, V. Gauci, C. D. Evans and S. E. Page, Fluvial organic carbon losses from a Bornean blackwater river, Biogeosciences, 2011, 8, 901–909.

    Article  CAS  Google Scholar 

  34. G. A. Weyhenmeyer, R. A. Müller, M. Norman and L. J. Tranvik, Sensitivity of freshwaters to browning in response to future climate change, Clim.Change, 2016, 134, 225–239.

    Article  Google Scholar 

  35. R. M. Pilla, C. E. Williamson, J. Zhang, R. L. Smyth, J. D. Lenters, J. A. Brentrup, L. B. Knoll and T J. Fisher, Browning-related decreases in water transparency lead to long-term increases in surface water temperature and thermal stratification in two small lakes, J. Geophys. Res.: Biogeosci., 2018, 125, 1651–1665.

    Article  Google Scholar 

  36. C. Björnerås, G. A. Weyhenmeyer, C. D. Evans, M. O. Gessner, H. P. Grossart, K. Kangur, I. Kokorite, P. Kortelainen, H. Laudon, J. Lehtoranta, N. Lottig, D. T. Monteith, P. Nõges, T. Nõges, F. Oulehle, G. Riise, J. A. Rusak, A. Räike, J. Sire, S. Sterling and E. S. Kritzberg, Widespread increases in iron concentration in European and North American freshwaters, Global Biogeochem. Cycles, 2017, 31, 1488–1500.

    Article  CAS  Google Scholar 

  37. B. A. Poulin, J. N. Ryan and G. R. Aiken, Effects of iron on optical properties of dissolved organic matter, Environ. Sci. Technol., 2014, 48, 10098–10106.

    Article  CAS  PubMed  Google Scholar 

  38. C. G. Fichot, K. Kaiser, S. B. Hooker, R. M. W. Amon, M. Babin, S. Bélanger, S. A. Walker and R. Benner, Pan-Arctic distributions of continental runoff in the Arctic Ocean, Sci. Rep., 2013, 3, Article number: 1053.

  39. R. G. M. Spencer, P. J. Mann, T. Dittmar, T. I. Eglinton, C. McIntyre, R. M. Holmes, N. Zimov and A. Stubbins, Detecting the signature of permafrost thaw in Arctic rivers, Geophys. Res. Lett., 2015, 42, 2830–2835.

    Article  Google Scholar 

  40. J. E. Vonk, S. E. Tank, W. B. Bowden, I. Laurion, W. F. Vincent, P. Alekseychik, M. Amyot, M. F. Billet, J. Canário, R. M. Cory, B. N. Deshpande, M. Helbig, M. Jammet, J. Karlsson, J. Larouche, G. MacMillan, M. Rautio, K. M. Walter Anthony and K. P. Wickland, Reviews and syntheses: effects of permafrost thaw on Arctic aquatic ecosystems, Biogeosciences, 2015, 12, 7129–7167.

    Article  CAS  Google Scholar 

  41. P. J. Mann, T. I. Eglinton, C. P. McIntyre, N. Zimov, A. Davydova, J. E. Vonk, R. M. Holmes and R. G. M. Spencer, Utilization of ancient permafrost carbon in headwaters of Arctic fluvial networks, Nat. Commun., 2015, 6, 7856.

    Article  CAS  PubMed  Google Scholar 

  42. S. Hylander, T. Jephson, K. Lebret, J. von Einem, T. Fagerberg, E. Balseiro, B. Modenutti, M. S. Souza, C. Laspoumaderes, M. Jonsson, P. Ljungberg, A. Nicolle, P. A. Nilsson, L. Ranaker and L. A. Hansson, Climate-induced input of turbid glacial meltwater affects vertical distribution and community composition of phyto- and zooplankton, J. Plankton Res., 2011, 33, 1239–1248.

    Article  Google Scholar 

  43. K. C. Rose, D. P. Hamilton, C. E. Williamson, C. G. McBride, J. M. Fischer, M. H. Olson, J. E. Saros, M. G. Allan and N. Cabrol, Light attenuation characteristics of glacially-fed lakes, J. Geophys. Res.: Biogeosci., 2014, 119, 1446–1457.

    Article  Google Scholar 

  44. B. Tartarotti, N. Saul, S. Chakrabarti, F. Trattner, C. E. W. Steinberg and R. Sommaruga, UV-induced DNA damage in Cyclops abyssorum tatricus populations from clear and turbid alpine lakes, J. Plankton Res., 2014, 36, 557–566.

    CAS  Google Scholar 

  45. K. Havens, R. S. Fulton III, J. R. Beaver, E. E. Samples and J. Colee, Effects of climate variability on cladoceran zoo-plankton and cyanobacteria in a shallow subtropical lake, J. Plankton Res., 2016, 38, 418–430.

    Article  CAS  Google Scholar 

  46. K. Havens, H. Paerl, E. Phlips, M. Zhu, J. Beaver and A. Srifa, Extreme weather events and climate variability provide a lens to how shallow lakes may respond to climate change, Water, 2016, 8, 229.

    Article  CAS  Google Scholar 

  47. K. E. Strock, J. E. Saros, S. J. Nelson, S. D. Birkel, J. S. Kahl and W. H. McDowell, Extreme weather years drive episodic changes in lake chemistry: implications for recovery from sulfate deposition and long-term trends in dissolved organic carbon, Biogeochemistry, 2016, 127, 353–365.

    Article  CAS  Google Scholar 

  48. R. Somavilla, C. González-Pola and J. Fernández-Diaz, The warmer the ocean surface, the shallower the mixed layer. How much of this is true?, J. Geophys. Res.: Oceans, 2017, 122, 7698–7716.

    Article  CAS  Google Scholar 

  49. P. W. Boyd and S. C. Doney, Modelling regional responses by marine pelagic ecosystems to global climate change, Geophys. Res. Lett., 2002, 29, 53–1–53–4.

  50. 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 and E. S. Boss, Climate-driven trends in contemporary ocean productivity, Nature, 2006, 444, 752–755.

    Article  CAS  PubMed  Google Scholar 

  51. B. M. Kraemer, O. Anneville, S. Chandra, M. Dix, E. Kuusisto, D. M. Livingstone, A. Rimmer, G. Schladow, E. A. Silow, L. M. Sitoki, R. Tamatamah, Y. Vadeboncoeur and P. B. McIntyre, Morphometry and average temperature affect lake stratification responses to climate change, Geophys. Res. Lett., 2015, 42, 4981–4988.

    Article  Google Scholar 

  52. J. Russell, H. Benway, A. Bracco, C. Deutsch, T. Ito, I. Kamenkovich and M. Patterson, Ocean’s carbon and heat uptake: Uncertainties and metrics, U.S. CLIVAR Report 2015–3, 2015, p. 33. https://opensky.ucar.edu/islan-dora/object/usclivar%3A30.

  53. S. L. Deppeler and A. T. Davidson, Southern Ocean phytoplankton in a changing climate, Front. Mar. Sci., 2017, 4, 40.

    Article  Google Scholar 

  54. J. F. Bornman, P. W. Barnes, T. M. Robson, S. A. Robinson, M. A. K. Jansen, C. L. Ballaré and S. D. Flint, Linkages between stratospheric ozone, UV radiation, and climate change and their implications for terrestrial ecosystems, Photochem. Photobiol. Sci., 2019, 18, DOI: 10.1039/C8PP90061B.

  55. J. J. Heiskanen, I. Mammarella, A. Ojala, V. Stepanenko, K.-M. Erkkilä, H. Miettinen, H. Sandström, W. Eugster, M. Leppäranta, H. Järvinen, T. Vesala and A. Nordbo, Effects of water clarity on lake stratification and lakeatmosphere heat exchange, J. Geophys. Res., 2015, 120, 7412–7428.

    Article  Google Scholar 

  56. M. Llabrés, S. Agustí, M. Fernández, A. Canepa, F. Maurin, F. Vidal and C. M. Duarte, Impact of elevated UVB radiation on marine biota: a meta-analysis, Glob. Ecol. Biogeogr., 2013, 22, 131–144.

    Article  Google Scholar 

  57. B. A. Bancroft, N. J. Baker and A. R. Blaustein, Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta-analysis, Ecol. Lett., 2007, 10, 332–345.

    Article  PubMed  Google Scholar 

  58. S. Peng, H. Liao, T. Zhou and S. Peng, Effects of UVB radiation on freshwater biota: a meta-analysis, Glob. Ecol. Biogeogr., 2016, 26, 500–510.

    Article  Google Scholar 

  59. D. J. Kieber, G. W. Miller, P. J. Neale and K. Mopper, Wavelength and temperature-dependent apparent quantum yields for photochemical formation of hydrogen peroxide in seawater, Environ. Sci.: Processes Impacts, 2014, 16, 777–791.

    CAS  Google Scholar 

  60. P. J. Neale and B. C. Thomas, Inhibition by ultraviolet and photosynthetically available radiation lowers model estimates of depth-integrated picophytoplankton photosynthesis: global predictions for Prochlorococcus, and Synechococcus, Glob. Change Biol., 2017, 23, 293–306.

    Google Scholar 

  61. R. W. Sanders, S. L. Cooke, J. M. Fischer, S. B. Fey, A. W. Heinze, W. H. Jeffrey, A. L. Macaluso, R. E. Moeller, D. P. Morris, P. J. Neale, M. H. Olson, J. D. Pakulski, J. A. Porter, D. M. Schoener and C. E. Williamson, Shifts in microbial food web structure and productivity after additions of naturally occurring dissolved organic matter: Results from large-scale lacustrine mesocosms, Limnol. Oceanogr., 2015, 60, 2130–2144.

    Article  Google Scholar 

  62. S. Madronich and S. Flocke, The role of solar radiation in atmospheric chemistry, in Handbook of Environmental Chemistry, ed. P. Boule, Springer-Verlag, Heidelberg, 1999, pp. 1–26.

    Google Scholar 

  63. K. C. Rose, P. J. Neale, M. Tzortziou, C. L. Gallegos and T. E. Jordan, Patterns of spectral, spatial, and long-term variability in light attenuation in an optically complex sub-estuary, Limnol. Oceanogr., 2019, 64, S257–S272.

  64. P. J. Neale and D. J. Kieber, Assessing biological and chemical effects of UV in the marine environment: Spectral weighting functions, in Causes and Environmental Implications of Increased UV-B Radiation, ed. R. E. Hester and R. M. Harrison, Royal Society of Chemistry, 2000, pp. 61–83.

    Book  Google Scholar 

  65. J. W. Harrison and R. E. H. Smith, Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities, Photochem. Photobiol. Sci., 2009, 8, 1218–1232.

    Article  CAS  PubMed  Google Scholar 

  66. K. Gao and D.-P. Häder, Effects of ocean acidification and UV radiation on marine photosynthetic carbon fixation, in System Biology of Marine Ecosystems, ed. M. Kumar and P. Ralph, Springer, Cham, Switzerland, 2017, pp. 235–250.

    Book  Google Scholar 

  67. D.-P. Häder and K. Gao, Interactions of anthropogenic stress factors on marine phytoplankton, Front. Environ. Sci., 2015, 3, 14.

    Google Scholar 

  68. Y. P. Wu, F. R. Yue, J. T Xu and J. Beardall, Differential photosynthetic responses of marine planktonic and benthic diatoms to ultraviolet radiation under various temperature regimes, Biogeosciences, 2017, 14, 5029–5037.

    Article  CAS  Google Scholar 

  69. C.-Y. Wong, M.-L. Teoh, S.-M. Phang, P.-E. Lim and J. Beardall, Interactive effects of temperature and UV radiation on photosynthesis of Chlorella, strains from polar, temperate and tropical environments: Differential impacts on damage and repair, PLoS One, 2015, 10, e0139469.

  70. H. W. Paerl and T. G. Otten, Blooms bite the hand that feeds them, Science, 2013, 342, 433–434.

    Article  CAS  PubMed  Google Scholar 

  71. D. Häder and K. Gao, The impacts of climate change on marine phytoplankton, in Climate Change Impacts on Fisheries and Aquaculture, A Global Analysis, ed. B. F. Phillips and M. Perez-Ramirez, Wiley, Hoboken, NJ, 2017.

    Google Scholar 

  72. A. Fuentes-Lema, C. Sobrino, N. Gonzalez, M. Estrada and P. J. Neale, Effect of solar UVR on the production of particulate and dissolved organic carbon from phytoplankton assemblages in the Indian Ocean, Mar. Ecol.: Prog. Ser., 2015, 535, 47–61.

    Article  CAS  Google Scholar 

  73. S. D. Archer, J. Stefels, R. L. Airs, T. Lawson, T. J. Smyth, A. P. Rees and R. J. Geider, Limitation of dimethyl-sulfoniopropionate synthesis at high irradiance in natural phytoplankton communities of the Tropical Atlantic, Limnol. Oceanogr., 2018, 63, 227–242.

    Article  CAS  Google Scholar 

  74. P. J. Neale, A. L. Pritchard and R. Ihnacik, UV effects on the primary productivity of picophytoplankton: biological weighting functions and exposure response curves of Synechococcus, Biogeosciences, 2014, 11, 2883–2895.

    Article  Google Scholar 

  75. P. J. Neale and B. C. Thomas, Inhibition by ultraviolet and photosynthetically available radiation lowers model estimates of depth-integrated picophytoplankton photosynthesis: global predictions for Prochlorococcus and Synechococcus, Global Change Biol., 2017, 23, 293–306.

    Google Scholar 

  76. K. R. Arrigo, D. Lubin, G. L. van Dijken, O. Holm-Hansen and E. Morrow, Impact of a deep ozone hole on Southern Ocean primary production, J. Geophys. Res.: Oceans, 2003, 108.

  77. P. J. Neale, R. F. Davis and 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 

  78. S. Å. Wängberg, K. I. M. Andreasson, K. Garde, K. Gustavson, P. Henriksen and T. Reinthaler, Inhibition of primary production by UV-B radiation in an arctic bay - model calculations, Aquat. Sci., 2006, 68, 117–128.

    Article  Google Scholar 

  79. K. K. Newsham and S. A. Robinson, Responses of plants in polar regions to UVB exposure: a meta-analysis, Glob. Change Biol., 2009, 15, 2574–2589.

    Article  Google Scholar 

  80. V. S. Saba, M. A. M. Friedrichs, M. E. Carr, D. Antoine, R. A. Armstrong, I. Asanuma, O. Aumont, N. R. Bates, M. J. Behrenfeld, V. Bennington, L. Bopp, J. Bruggeman, E. T. Buitenhuis, M. J. Church, A. M. Ciotti, S. C. Doney, M. Dowell, J. Dunne, S. Dutkiewicz, W. Gregg, N. Hoepffner, K. J. W. Hyde, J. Ishizaka, T. Kameda, D. M. Karl, I. Lima, M. W. Lomas, J. Marra, G. A. McKinley, F. Melin, J. K. Moore, A. Morel, J. O’Reilly, B. Salihoglu, M. Scardi, T. J. Smyth, S. L. Tang, J. Tjiputra, J. Uitz, M. Vichi, K. Waters, T. K. Westberry and A. Yool, Challenges of modeling depth-integrated marine primary productivity over multiple decades: A case study at BATS and HOT, Global Biogeochem. Cycles, 2010, 24, GB3020.

  81. R. L. Smyth, C. Sobrino, J. Phillips-Kress, H. C. Kim and P. J. Neale, Phytoplankton photosynthetic response to solar ultraviolet irradiance in the Ross Sea Polynya: Development and evaluation of a time-dependent model with limited repair, Limnol. Oceanogr., 2012, 57, 1602–1618.

    Article  Google Scholar 

  82. R. L. Smyth, P. J. Neale, C. Akan and A. E. Tejada-Martinez, Quantifying phytoplankton productivity and photoinhibition in the Ross Sea Polynya with Large Eddy Simulation of Langmuir circulation, J. Geophys. Res.: Oceans, 2017, 122, 5545–5565.

    Article  CAS  Google Scholar 

  83. T. Li, Y. Bai, G. Li, X. He, C.-T. A. Chen, K. Gao and D. Liu, Effects of ultraviolet radiation on marine primary production with reference to satellite remote sensing, Front. Earth Sci., 2015, 9 ,237–247.

    Article  Google Scholar 

  84. J. Beardall, S. Stojkovic and K. Gao, Interactive effects of nutrient supply and other environmental factors on the sensitivity of marine primary producers to ultraviolet radiation: implications for the impacts of global change, Aquat. Biol., 2014, 22, 5–23.

    Article  Google Scholar 

  85. J. M. Gonzalez-Olalla, J. M. Medina-Sánchez, M. J. Cabrerizo, M. Villar-Argaiz, P. M. Sánchez-Castillo and P. Carrillo, Contrasting effect of Saharan dust and UVR on autotrophic picoplankton in nearshore versus offshore waters of Mediterranean Sea, J. Geophys. Res.: Biogeosci., 2017, 122, 2085–2103.

    Article  Google Scholar 

  86. P. Carrillo, J. M. Medina-Sánchez, M. Villar-Argaiz, F. J. Bullejos, C. Durán, M. Bastidas-Navarro, M. S. Souza, E. G. Balseiro and B. E. Modenutti, Vulnerability of mixotrophic algae to nutrient pulses and UVR in an oligotrophic Southern and Northern Hemisphere lake, Sci. Rep., 2017, 7, 6333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. P. Carrillo, J. M. Medina-Sánchez, G. Herrera, C. Durán, M. Segovia, D. Cortes, S. Salles, N. Korbee, F. L. Figueroa and J. M. Mercado, Interactive effect of UVR and phosphorus on the coastal phytoplankton community of the western Mediterranean Sea: Unravelling ecophysiological mechanisms, PLoS One, 2015, 10, e0142987.

  88. M. J. Cabrerizo, J. M. Medina-Sanchez, I. Dorado-Garcia, M. Villar-Argaiz and P. Carrillo, Rising nutrient-pulse frequency and high UVR strengthen microbial interactions, Sci. Rep., 2017, 7, DOI: 10.1038/Srep43615.

  89. Z. K. Li, G. Z. Dai, P. Juneau and B. S. Qiu, Different physiological responses of cyanobacteria to ultraviolet-B radiation under iron-replete and iron-deficient conditions: Implications for underestimating the negative effects of UV-B radiation, J. Phycol., 2017, 53, 425–436.

  90. M. J. A. Rijkenberg, A. C. Fischer, J. J. Kroon, L. J. A. Gerringa, K. R. Timmermans, H. T. Wolterbeek and H. J. W. de Baar, The influence of UV irradiation on the photoreduction of iron in the Southern Ocean, Mar. Chem., 2005, 93, 119–129.

    Article  CAS  Google Scholar 

  91. D. L. Shi, Y. Xu, B. M. Hopkinson and F. M. M. Morel, Effect of ocean acidification on iron availability to marine phytoplankton, Science, 2010, 327, 676–679.

    Article  CAS  PubMed  Google Scholar 

  92. X. N. Cai, D. A. Hutchins, F. X. Fu and K. S. Gao, Effects of ultraviolet radiation on photosynthetic performance and N-2 fixation in Trichodesmium erythraeum IMS 101, Biogeosciences, 2017, 14, 4455–4466.

    CAS  Google Scholar 

  93. A. B. Novak and F. T. Short, Transient and permanent leaf-reddening in the sea grass Thalassia testudinum, Bull. Mar. Sci., 2012, 88, 305–315.

    Article  Google Scholar 

  94. E. Cruces, P. Huovinen and I. Gomez, Interactive effects of UV radiation and enhanced temperature on photosynthesis, phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae, Mar. Biol., 2013, 160, 1–13.

    Article  CAS  Google Scholar 

  95. F. L. Figueroa, B. Dominguez-Gonzalez and N. Korbee, Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-functional groups, Mar. Environ. Res., 2014, 97, 30–38.

    Article  CAS  PubMed  Google Scholar 

  96. J. T. Hafting, J. S. Craigie, D. B. Stengel, R. R. Loureiro, A. H. Buschmann, C. Yarish, M. D. Edwards and A. T Critchley, Prospects and challenges for industrial production of seaweed bioactives, J. Phycol., 2015, 51, 821–837.

  97. N. Wada, T. Sakamoto and S. Matsugo, Mycosporine-like amino acids and their derivatives as natural antioxidants, Antioxidants, 2015, 4, 603–646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. K. P. Lawrence, P. F. Long and A. R. Young, Mycosporine-like amino acids for skin photoprotection, Curr. Med. Chem., 2017, 24, 1–16.

    Article  Google Scholar 

  99. N. Navarro, F. L. Figueroa, N. Korbee, F. Álvarez-Gómez and F. de la Coba, Mycosporine-like amino acids form red algae to develop natural UV sunscreen, in Sunscreens: Source, Formulations, Efficacy and Recommendations, ed. R. R. Rastogi, S. Patel and V. Vidyanagar, 2018.

    Google Scholar 

  100. Rajneesh, S. P. Singh, J. Pathak and R. P. Sinha, Cyanobacterial factories for the production of green energy and value-added products: An integrated approach for economic viability, Renewable Sustainable Energy Rev., 2017, 69, 578–595.

    Article  Google Scholar 

  101. Richa, J. Pathak, A. S. Sonker, V. Singh and R. P. Sinha, Nanobiotechnology of cyanobacterial UV-protective compounds: Innovations and prospects, in Food Preservation, ed. A. M. Grumezescu, Elsevier, New York, 2017, vol. 6, pp. 603–644.

  102. J. L. Shang, Z. C. Zhang, X. Y. Yin, M. Chen, F. H. Hao, K. Wang, J. L. Feng, H. F. Xu, Y. C. Yin, H. R. Tang and B. S. Qiu, UV-B induced biosynthesis of a novel sunscreen compound in solar radiation and desiccation tolerant cyanobacteria, Environ. Microbiol., 2018, 20, 200–213.

    Article  CAS  PubMed  Google Scholar 

  103. N. P. Navarro, F. L. Figueroa, N. Korbee, A. Mansilla, B. Matsuhiro, T. Barahona and E. M. Plastino, The effects of NO3 supply on Mazzaella laminarioides (Rhodophyta, Gigartinales) from southern Chile, Photochem. Photobiol., 2014, 90, 1299–1307.

    CAS  Google Scholar 

  104. N. P. Navarro, A. Mansilla, F. L. Figueroa, N. Korbee, J. Jofre and E. Plastino, Short-term effects of solar UV radiation and NO3– supply on the accumulation of mycosporine-like amino acids in Pyropia columbina (Bangiales, Rhodophyta) under spring ozone depletion in the sub-Antarctic region, Chile, Bot. Mar., 2014, 57, 9–20.

    CAS  Google Scholar 

  105. B. Briani, M. N. Sissini, L. A. Lucena, M. B. Batista, I. O. Costa, J. M. C. Nunes, C. Schmitz, F. Ramlov, M. Maraschin, N. Korbee, L. Rörig, P. A. Horta, F. L. Figueroa and J. B. Barufi, The influence of environmental features in the content of mycosporine-like amino acids in red marine algae along the Brazilian Coast, J. Phycol., 2018, 54, 380–390.

    Article  CAS  PubMed  Google Scholar 

  106. E. S. Fileman, D. A. White, R. A. Harmer, U. Aytan, G. A. Tarran, T. Smyth and A. Atkinson, Stress of life at the ocean’s surface: Latitudinal patterns of UV sunscreens in plankton across the Atlantic, Prog. Oceanogr., 2017, 158, 171–184.

    Article  Google Scholar 

  107. B. K. Tiwari and D. J. Troy, Seaweed Sustainability: Food and Non-food Applications, Academic Press, Cambridge, MA, 2015.

    Google Scholar 

  108. P. Cabral, H. Levrel, F. Viard, K. Frangoudes, S. Girard and P. Scemama, Ecosystem services assessment and compensation costs for installing seaweed farms, Mar. Policy, 2016, 71, 157–165.

    Article  Google Scholar 

  109. D. Krause-Jensen and C. M. Duarte, Substantial role of macroalgae in marine carbon sequestration, Nat. Geosci., 2016, 9, 737–742.

    Article  CAS  Google Scholar 

  110. S. Rosales-Mendoza, Algae-based biopharmaceutical, Springer, Switzerland, 2016.

    Book  Google Scholar 

  111. FAO, The State of Fisheries and Aquaculture 2016. Contributing to food security and nutrition for all, Rome, 2016, p. 200.

  112. C. S. Young and C. J. Gobler, Ocean acidification accelerates the growth of two bloom-forming macroalgae, PLoS One, 2016, 11, e0155152.

  113. A. H. Buschmann, C. Camus, J. Infante, A. Neori, Á. Israel, M. C. Hernández-González, S. V. Pereda, J. L. Gomez-Pinchetti, A. Golberg, N. Tadmor-Shalev and A. T. Critchley, Seaweed production: overview of the global state of exploitation, farming and emerging research activity, Eur. J. Phycol., 2017, 52, 391–406.

  114. I. K. Chung, C. F. A. Sondak and J. Beardall, The future of seaweed aquaculture in a rapidly changing world, Eur. J. Phycol., 2017, 52, 495–505.

  115. Richa, R. P. Sinha and D.-P. Häder, Effects of global change, including UV and UV screening compounds, in Physiology of Microalgae, 2016, vol. 6, pp. 373–409.

  116. F. Álvarez-Gómez, Z. L. Bouzon, N. Korbee, P. Celis-Pla, E. C. Schmidt and F. L. Figueroa, Combined effects of UVR and nutrients on cellultrastructure, photosynthesis and biochemistry in Gracilariopsis longissima (Gracilariales, Rhodophyta), Algal Res., 2017, 26, 190–202.

    Google Scholar 

  117. P. W. Boyd and C. J. Brown, Modes of interactions between environmental drivers and marine biota, Front. Mar. Sci., 2015, 2, DOI: 10.3389/fmars.2015.00009.

  118. C. M. Duarte, I. J. Losada, I. E. Hendriks, I. Mazarrasa and N. Marba, The role of coastal plant communities for climate change mitigation and adaptation, Nat. Clim. Change, 2013, 3, 961–968.

    Article  CAS  Google Scholar 

  119. Y. Gao, G. Yu, T. Yang, Y. Jia, N. He and J. Zhuang, New insight into global blue carbon estimation under human activity in land-sea interaction area: A case study of China, Earth-Sci. Rev., 2016, 159, 36–46.

    Article  CAS  Google Scholar 

  120. A. M. Al-Aidaroos, M. M. O. El-Sherbiny, S. Satheesh, G. Mantha, S. Agusti, B. Carreja and C. M. Duarte, Strong sensitivity of Red Sea zooplankton to UV-B radiation, Estuaries Coasts, 2015, 38, 846–853.

    Article  CAS  Google Scholar 

  121. C. Williamson, H. Zagarese, P. Schulze, B. Hargreaves and J. Seva, The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes, J. Plankton Res., 1994, 16, 205–218.

    Article  Google Scholar 

  122. S. C. Rhode, M. Pawlowski and R. Tollrian, The impact of ultraviolet radiation on the vertical distribution of zoo-plankton of the genus Daphnia, Nature, 2001, 412, 69–72.

    Article  CAS  PubMed  Google Scholar 

  123. S. Hylander, M. T. Ekvall, G. Bianco, X. Yang and L.-A. Hansson, Induced tolerance expressed as relaxed behavioural threat response in millimetre-sized aquatic organisms, Proc. R. Soc. B, 2014, 281, 20140364.

    Article  PubMed  PubMed Central  Google Scholar 

  124. S. J. Connelly, K. Walling, S. A. Wilbert, D. M. Catlin, C. E. Monaghan, S. Hlynchuk, P. G. Meehl, L. N. Resch, J. V. Carrera, S. M. Bowles, M. D. Clark, L. T. Tan and J. A. Cody, UV-stressed Daphnia pulex increase fitness through uptake of vitamin D3, PLoS One, 2015, 10, e0131847.

  125. E. P. Overholt, K. C. Rose, C. E. Williamson, J. Fischer and N. Cabrol, Behavioral responses of freshwater calanoid copepods to the presence of ultraviolet radiation: avoidance and attraction, J. Plankton Res., 2016, 38, 16–26.

    Article  Google Scholar 

  126. L. A. Hansson, G. Bianco, M. T. Ekvall, J. Heuschele, S. Hylander and X. Yang, Instantaneous threat escape and differentiated refuge demand among zooplankton taxa, Ecol., 2016, 97, 279–285.

    Article  Google Scholar 

  127. C. E. Fernández, M. Campero, C. Uvo and L.-A. Hansson, Disentangling population strategies of two cladocerans adapted to different ultraviolet regimes, Ecol. Evol., 2018, 8, 1995–2005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. E.-J. Won, J. Han, Y. Lee, K. S. Kumar, K.-H. Shin, S.-J. Lee, H. G. Park and J.-S. Lee, In vivo effects of UV radiation on multiple endpoints and expression profiles of DNA repair and heat shock protein (Hsp) genes in the cyclopoid copepod Paracyclopina nana, Aquat. Toxicol., 2015, 165, 1–8.

    CAS  Google Scholar 

  129. M. S. Valiñas and E. W. Helbling, Metabolic and behavioral responses of the reef fish Patagonotothen cornucola to ultraviolet radiation: Influence of the diet, J. Exp. Mar. Biol. Ecol., 2016, 474, 180–184.

  130. E. G. Kazerouni, C. E. Franklin and F. Seebacher, Parental exposure modulates the effects of UV-B on offspring in guppies, Funct. Ecol., 2017, 31, 1082–1090.

  131. L. Courtial, S. Roberty, J. M. Shick, F. Houlbreque and C. Ferrier-Pages, Interactive effects of ultraviolet radiation and thermal stress on two reef-building corals, Limnol. Oceanogr., 2017, 62, 1000–1013.

    Article  Google Scholar 

  132. M. J. Bok, N. W. Roberts and T. W. Cronin, Behavioural evidence for polychromatic ultraviolet sensitivity in mantis shrimp, Proc. R. Soc. B, 2018, 285, DOI: 10.1098/rspb.2018.1384.

  133. Z. Ma, W. Li and K. Gao, Horizontal migration of Acartia pacifica Steuer (copepoda) in response to UV-radiation, J. Photochem. Photobiol., B, 2010, 101, 233–237.

    CAS  Google Scholar 

  134. R. Wolf and J. Heuschele, Water browning influences the behavioral effects of ultraviolet radiation on zooplankton, Front. Ecol. Evol., 2018, 6, 26.

    Article  Google Scholar 

  135. C. E. Williamson, J. M. Fischer, S. M. Bollens, E. P. Overholt and J. K. Breckenridge, Toward a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm, Limnol. Oceanogr., 2011, 56, 1603–1623.

    Article  Google Scholar 

  136. M. T. Ekvall, S. Hylander, T. Walles, X. Yang and L.-A. Hansson, Diel vertical migration, size distribution and photoprotection in zooplankton as response to UV-A radiation, Limnol. Oceanogr., 2015, 60, 2048–2058.

    Article  Google Scholar 

  137. B. Tartarotti, F. Trattner, D. Remias, N. Saul, C. E. W. Steinberg and R. Sommaruga, Distribution and UV protection strategies of zooplankton in clear and glacier-fed alpine lakes, Sci. Rep., 2017, 7, 4487.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. T. H. Leach, C. E. Williamson, N. Theodore, J. M. Fischer and M. H. Olson, The role of ultraviolet radiation in the diel vertical migration of zooplankton: an experimental test of the transparency-regulator hypothesis, J. Plankton Res., 2015, 37, 886–896.

    Article  Google Scholar 

  139. K. Brander and P. C. F. Hurley, Distribution of early-stage Atlantic cod (Gadus morhua), haddock (Melanogrammus aeglefinus), and witch flounder (Glyptocephalus cynoglossus) eggs on the Scotian shelf - a reappraisal of evidence on the coupling of cod spawning and plankton production, Can. J. Fish. Aquat. Sci., 1992, 49, 238–251.

    Google Scholar 

  140. P. Wassmann, M. Reigstad, T. Haug, B. Rudels, M. L. Carroll, H. Hop, G. W. Gabrielsen, S. Falk-Petersen, S. G. Denisenko, E. Arashkevich, D. Slagstad and O. Pavlova, Food webs and carbon flux in the Barents Sea, Prog. Oceanogr., 2006, 71, 232–287.

    Article  Google Scholar 

  141. M. Brüsin, P. A. Svensson and S. Hylander, Individual changes in zooplankton pigmentation in relation to ultraviolet radiation and predator cues, Limnol. Oceanogr., 2016, 61, 1337–1344.

    Article  Google Scholar 

  142. T. Schneider, G. Grosbois, W. F. Vincent and M. Rautio, Carotenoid accumulation in copepods is related to lipid metabolism and reproduction rather than to UV-protection, Limnol. Oceanogr., 2016, 61, 1201–1213.

    Article  Google Scholar 

  143. B. Tartarotti, A. Alfreider, M. Egg, N. Saul, T. Schneider, R. Sommaruga, A. Tischler and J. Vetter, Seasonal plasticity in photoprotection modulates UV-induced hsp gene expression in copepods from a clear lake, Limnol. Oceanogr., 2018, 63, 1579–1592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. D. O. Hessen, Competitive trade-off strategies in Arctic Daphnia linked to melanism and UV-B stress, Polar Biol., 1996, 16, 573–579.

    Google Scholar 

  145. P. D. N. Hebert and C. J. Emery, The adaptive significance of cuticular pigmentation in Daphnia, Funct. Ecol., 1990, 4, 703–710.

    Article  Google Scholar 

  146. L. Nevalainen, T. P. Luoto, M. V. Rantala, A. Galkin and M. Rautio, Role of terrestrial carbon in aquatic UV exposure and photoprotective pigmentation of meiofauna in subarctic lakes, Freshwater Biol., 2015, 60, 2435–2444.

    Article  CAS  Google Scholar 

  147. L. Nevalainen, M. V. Rantala, T. P. Luoto, A. E. K. Ojala and M. Rautio, Long-term changes in pigmentation of arctic Daphnia provide potential for reconstructing aquatic UV exposure, Quat. Sci. Rev., 2016, 144, 44–50.

    Google Scholar 

  148. S. Debecker, R. Sommaruga, T. Maes and R. Stoks, Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin, Funct. Ecol., 2015, 29, 1292–1299.

    Article  Google Scholar 

  149. M. S. Valiñas and E. W. Helbling, Sex-dependent effects of ultraviolet radiation on the marine amphipod Ampithoe valida (Ampithoidae), J. Photochem. Photobiol., B, 2015, 147, 75–82.

    Google Scholar 

  150. R. Wolf, T. Andersen, D. O. Hessen, K. Hylland and M. Pfrender, The influence of dissolved organic carbon and ultraviolet radiation on the genomic integrity of Daphnia magna, Funct. Ecol., 2016, 31, 848–855.

    Article  Google Scholar 

  151. F. Baltar, T. Reinthaler, G. J. Herndl and J. Pinhassi, Major effect of hydrogen peroxide on bacterioplankton metabolism in the northeast Atlantic, PLoS One, 2013, 8, e61051.

  152. F. Leunert, W. Eckert, A. Paul, V. Gerhardt and H.-P. Grossart, Phytoplankton response to UV-generated hydrogen peroxide from natural organic matter, J. Plankton Res., 2014, 36, 185–197.

    Article  CAS  Google Scholar 

  153. L. Wolinski, B. Modenutti, M. S. Souza and E. Balseiro, Interactive effects of temperature, ultraviolet radiation and food quality on zooplankton alkaline phosphatase activity, Environ. Pollut, 2016, 213, 135–142.

    Article  CAS  PubMed  Google Scholar 

  154. R. Wolf, J.-E. Thrane, D. O. Hessen and T. Andersen, Modelling ROS formation in boreal lakes from interactions between dissolved organic matter and absorbed solar photon flux, Water Res., 2018, 132, 331–339.

    Article  CAS  PubMed  Google Scholar 

  155. M. Lindholm, R. Wolf, A. Finstad and D. O. Hessen, Water browning mediates predatory decimation of the Arctic fairy shrimp Branchinecta paludosa, Freshwater Biol., 2016, 61, 340–347.

    Article  Google Scholar 

  156. A. W. Vermilyea, S. Paul Hansard and B. M. Voelker, Dark production of hydrogen peroxide in the Gulf of Alaska, Limnol. Oceanogr., 2010, 55, 580–588.

    Article  CAS  Google Scholar 

  157. T. Zhang, C. M. Hansel, B. M. Voelker and C. H. Lamborg, Extensive dark biological production of reactive oxygen species in brackish and freshwater ponds, Environ. Sci. Technol., 2016, 50, 2983–2993.

    Article  CAS  PubMed  Google Scholar 

  158. R. M. Cory, T. W. Davis, G. J. Dick, T. Johengen, V. J. Denef, M. A. Berry, S. E. Page, S. B. Watson, K. Yuhas and G. W. Kling, Seasonal dynamics in dissolved organic matter, hydrogen peroxide, and cyanobacterial blooms in Lake Erie, Front. Mar. Sci., 2016, 3, 54.

  159. C. E. Williamson, O. G. Olson, S. E. Lott, N. D. Walker, D. R. Engstrom and B. R. Hargreaves, Ultraviolet radiation and zooplankton community structure following deglaciation in Glacier Bay, Alaska, Ecol., 2001, 82, 1748–1760.

    Article  Google Scholar 

  160. M. C. Marinone, S. M. Marque, D. A. Suárez, M. del Carmen Diéguez, P. Pérez, P. De Los Ríos, D. Soto and H. E. Zagarese, UV radiation as a potential driving force for zooplankton community structure in Patagonian lakes, Photochem. Photobiol., 2006, 82, 962–971.

    Article  CAS  PubMed  Google Scholar 

  161. S. Hylander and L. A. Hansson, Vertical migration mitigates UV effects on zooplankton community composition, J. Plankton Res., 2010, 32, 971–980.

    Article  CAS  Google Scholar 

  162. S. L. Cooke, J. M. Fischer, K. Kessler, C. E. Williamson, R. W. Sanders, D. P. Morris, J. A. Porter, W. H. Jeffrey, S. DeVaul Princiotta and J. D. Pakulski, Direct and indirect effects of additions of chromophoric dissolved organic matter on zooplankton during large-scale mesocosm experiments in an oligotrophic lake, Freshwater Biol., 2015, 60, 2362–2378.

    Article  CAS  Google Scholar 

  163. E. P. Overholt, S. H. Hall, C. E. Williamson, C. K. Meikle, M. A. Duffy and C. E. Cáceres, Solar radiation decreases parasitism in Daphnia, Ecol. Lett., 2012, 15, 47–54.

    Article  PubMed  Google Scholar 

  164. C. E. Williamson, S. Madronich, A. Lal, R. E. Zepp, R. M. Lucas, E. P. Overholt, K. C. Rose, G. Schladow and J. Lee-Taylor, Climate change-induced increases in precipitation are reducing the potential for solar ultraviolet radiation to inactivate pathogens in surface waters, Sci. Rep., 2017, 7, 13033.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Richa, R. P. Sinha and D.-P. Häder, Physiological aspects of UV-excitation of DNA, in Topics in Current Chemistry: Photoinduced Phenomena in Nucleic Acids II: DNA Fragments in Phenomenological Aspects, ed. M. Barbatto, A. C. Borin and S. Ullrich, Springer, Berlin, 2015, pp. 203–248.

    Google Scholar 

  166. D. M. Leech, W. J. Boeing, S. L. Cooke, C. E. Williamson and L. Torres, UV-enhanced fish predation and the differential migration of zooplankton in response to UV radiation and fish, Limnol. Oceanogr., 2009, 54, 1152–1161.

    Article  CAS  Google Scholar 

  167. I. N. Flamarique, Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones, Proc. R. Soc. B, 2016, 283, 20160058.

    Article  CAS  Google Scholar 

  168. D. M. Leech and S. Johnsen, Ultraviolet vision and foraging in juvenile bluegill (Lepomis macrochirus), Can. J. Fish. Aquat. Sci., 2006, 63, 2183–2190.

  169. R. M. Cory, C. P. Ward, B. C. Crump and G. W. Kling, Sunlight controls water column processing of carbon in arctic fresh waters, Science, 2014, 345, 925–928.

    Article  CAS  PubMed  Google Scholar 

  170. C. L. Sabine, R. A. Feely, N. Gruber, R. M. Key, K. Lee, J. L. Bullister, R. Wanninkhof, C. S. Wong, D. W. R. Wallace, B. Tilbrook, F. J. Millero, T. H. Peng, A. Kozyr, T. Ono and A. F. Rios, The oceanic sink for anthropogenic CO2, Science, 2004, 305, 367–371.

    Article  CAS  PubMed  Google Scholar 

  171. J. P. Gattuso, A. Magnan, R. Bille, W. W. L. Cheung, E. L. Howes, F. Joos, D. Allemand, L. Bopp, S. R. Cooley, C. M. Eakin, O. Hoegh-Guldberg, R. P. Kelly, H. O. Portner, A. D. Rogers, J. M. Baxter, D. Laffoley, D. Osborn, A. Rankovic, J. Rochette, U. R. Sumaila, S. Treyer and C. Turley, Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios, Science, 2015, 349, aac4722.

  172. J. Phillips, G. McKinley, V. Bennington, H. Bootsma, D. Pilcher, R. Sterner and N. Urban, The potential for CO2 -induced acidification in freshwater: A Great Lakes case study, Oceanography, 2015, 25, 136–145.

    Article  Google Scholar 

  173. L. C. Weiss, L. Pötter, A. Steiger, S. Kruppert, U. Frost and R. Tollrian, Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia, Curr. Biol., 2018, 28, 327–332.

    Article  CAS  PubMed  Google Scholar 

  174. U. Riebesell and J. P. Gattuso, Lessons learned from ocean acidification research, Nat. Clim. Change, 2015, 5, 12–14.

    Article  CAS  Google Scholar 

  175. D. Britton, C. E. Cornwall, A. T. Revill, C. L. Hurd and C. R. Johnson, Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata, Sci. Rep., 2016, 6, DOI: 10.1038/Srep26036.

  176. J. E. G. Raymont, Plankton and Productivity in the Oceans: Volume 1: Phytoplankton, Pergamon, 1980.

  177. G. Ou, H. Wang, R. Si and W. Guan, The dinoflagellate Akashiwo sanguinea will benefit from future climate change: The interactive effects of ocean acidification, warming and high irradiance on photophysiology and hemolytic activity, Harmful Algae, 2017, 68, 118–127.

    Google Scholar 

  178. T. K. Hattenrath-Lehmann, J. L. Smith, R. B. Wallace, L. R. Merlo, F. Koch, H. Mittelsdorf, J. A. Goleski, D. M. Anderson and C. J. Gobler, The effects of elevated CO2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, Alexandrium fundyense, Limnol. Oceanogr., 2015, 60, 198–214.

    Article  PubMed  Google Scholar 

  179. F. M. Monteiro, L. T. Bach, C. Brownlee, P. Bown, R. E. M. Rickaby, A. J. Poulton, T. Tyrrell, L. Beaufort, S. Dutkiewicz, S. Gibbs, M. A. Gutowska, R. Lee, U. Riebesell, J. Young and A. Ridgwell, Why marine phytoplankton calcify, Sci. Adv., 2016, 2, e1501822.

  180. J. S. Grear, T. A. Rynearson, A. L. Montalbano, B. Govenar and S. Menden-Deuer, pCO2 effects on species composition and growth of an estuarine phytoplankton community, Estuarine, Coastal Shelf Sci., 2017, 190, 40–49.

    Article  CAS  Google Scholar 

  181. G. Tilstone, B. Sediva, G. Tarran, R. Kana and O. Prasil, Effect of CO2 enrichment on phytoplankton photosynthesis in the North Atlantic sub-tropical gyre, Prog. Oceanogr., 2017, 158, 76–89.

    Article  Google Scholar 

  182. M. R. Gradoville, A. E. White, D. Bottjer, M. J. Church and R. M. Letelier, Diversity trumps acidification: Lack of evidence for carbon dioxide enhancement of Trichodesmium, community nitrogen or carbon fixation at Station ALOHA, Limnol. Oceanogr., 2014, 59, 645–659.

    CAS  Google Scholar 

  183. C. Girard, M. Leclerc and M. Amyot, Photodemethylation of methylmercury in eastern Canadian Arctic thaw pond and lake ecosystems, Environ. Sci. Technol., 2016, 50, 3511–3520.

    Article  CAS  PubMed  Google Scholar 

  184. A. E. Poste, H. F. V. Braaten, H. A. de Wit, K. Sørensen and T. Larssen, Effects of photodemethylation on the methylmercury budget of boreal Norwegian lakes, Environ. Toxicol. Chem., 2015, 34, 1213–1223.

    Article  CAS  PubMed  Google Scholar 

  185. A. R. Almeida, T. S. Andrade, V. Burkina, G. Fedorova and S. Loureiro, A. M. V. M. Soares and I. Domingues, Is UV radiation changing the toxicity of compounds to zebrafish embryos?, Ecotoxicol. Environ. Saf., 2015, 122, 145–152.

    Article  CAS  PubMed  Google Scholar 

  186. S. Yu, S. Tang, G. D. Mayer, G. P. Cobb and J. D. Maul, Interactive effects of ultraviolet-B radiation and pesticide exposure on DNA photo-adduct accumulation and expression of DNA damage and repair genes in Xenopus laevis embryos, Aquat. Toxicol., 2015, 159, 256–266.

    CAS  Google Scholar 

  187. M. Alloy, D. Baxter, J. Stieglitz, E. Mager, R. Hoenig, D. Benetti, M. Grosell, J. Oris and A. Roberts, Ultraviolet radiation enhances the toxicity of Deepwater Horizon Oil to Mahi-mahi (Coryphaena hippurus) embryos, Environ. Sci. Technol., 2016, 50, 2011–2017.

    Article  CAS  PubMed  Google Scholar 

  188. S. Yu, S. M. Weir, G. P. Cobb and J. D. Maul, The effects of pesticide exposure on ultraviolet-B radiation avoidance behavior in tadpoles, Sci. Total Environ., 2014, 481, 75–80.

    Article  CAS  PubMed  Google Scholar 

  189. C. A. Downs, E. Kramarsky-Winter, R. Segal, J. Fauth, S. Knutson, O. Bronstein, F. R. Ciner, R. Jeger, Y. Lichtenfeld, C. M. Woodley, P. Pennington, K. Cadenas, A. Kushmaro and Y. Loya, Toxicopathological effects of the sunscreen UV filter, Oxybenzone (Benzophenone-3), on coral planulae and cultured primary cells and its environmental contamination in Hawaii and the U.S. Virgin Islands, Arch. Environ. Contam. Toxicol., 2016, 70, 265–288.

    Article  CAS  Google Scholar 

  190. M. M. P. Tsui, J. C. W. Lam, T. Y. Ng, P. O. Ang, M. B. Murphy and P. K. S. Lam, Occurrence, distribution, and fate of organic UV filters in coral communities, Environ. Sci. Technol., 2017, 51, 4182–4190.

    Article  CAS  PubMed  Google Scholar 

  191. C. Corinaldesi, E. Damiani, F. Marcellini, C. Falugi, L. Tiano, F. Bruge and R. Danovaro, Sunscreen products impair the early developmental stages of the sea urchin Paracentrotus lividus, Sci. Rep., 2017, 7, 7815.

  192. H. C. H. Fong, J. C. H. Ho, A. H. Y. Cheung, K. P. Lai and W. K. F. Tse, Developmental toxicity of the common UV filter, benzophenone-2, in zebrafish embryos, Chemosphere, 2016, 164, 413–420.

    Article  CAS  PubMed  Google Scholar 

  193. I. Ozaez, M. Aquilino, G. Morcillo and J. L. Martinez-Guitarte, UV filters induce transcriptional changes of different hormonal receptors in Chironomus riparius embryos and larvae, Environ. Pollut., 2016, 214, 239–247.

    CAS  Google Scholar 

  194. D. Campos, C. Gravato, C. Quintaneiro, O. Golovko, V. Zlabek, A. Soares and J. L. T. Pestana, Toxicity of organic UV-filters to the aquatic midge Chironomus riparius, Ecotoxicol. Environ. Saf., 2017, 143, 210–216.

  195. R. M. Lucas, S. Yazar, A. R. Young, M. Norval, F. R. de Gruijl, Y. Takizawa, L. E. Rhodes, C. A. Sinclair and R. E. Neale, Human health in relation to exposure to solar ultraviolet radiation under changing stratospheric ozone and climate, Photochem. Photobiol Sci., 2019, 18, DOI:10.1039/C8PP90060D.

  196. Senate of Hawaii, Relating to Water Pollution, Bill number 2571, Honolulu, HI, 2018.

  197. T. J. Willenbrink, V. Barker and D. Diven, The effects of sunscreen on marine environments, Cutis, 2017, 100, 369–370.

    PubMed  Google Scholar 

  198. E. Chrapusta, A. Kaminski, K. Duchnik, B. Bober, M. Adamski and J. Bialczyk, Mycosporine-like amino acids: Potential health and beauty ingredients, Mar. Drugs, 2017, 15, 326.

    Article  PubMed Central  CAS  Google Scholar 

  199. M. E. Balmer, H. R. Buser, M. D. Muller and T. Poiger, Occurrence of some organic UV filters in wastewater, in surface waters, and in fish from Swiss lakes, Environ. Sci. Technol., 2005, 39, 953–962.

    Article  CAS  PubMed  Google Scholar 

  200. M. M. P. Tsui, H. W. Leung, T. C. Wai, N. Yamashita, S. Taniyasu, W. H. Liu, P. K. S. Lam and M. B. Murphy, Occurrence, distribution and ecological risk assessment of multiple classes of UV filters in surface waters from different countries, Water Res., 2014, 67, 55–65.

    Article  CAS  PubMed  Google Scholar 

  201. S. Ramos, V. Homem, A. Alves and L. Santos, A review of organic UV-filters in wastewater treatment plants, Environ. Int., 2016, 86, 24–44.

    Article  CAS  PubMed  Google Scholar 

  202. D. Sánchez-Quiles and A. Tovar-Sánchez, Are sunscreens a new environmental risk associated with coastal tourism?, Environ. Int., 2015, 83, 158–170.

    Article  PubMed  Google Scholar 

  203. C. Juliano and G. Magrini, Cosmetic ingredients as emerging pollutants of environmental and health concern. A mini-review, Cosmetics, 2017, 4, 11.

    Article  CAS  Google Scholar 

  204. M. H. Wu, D. G. Xie, G. Xu, R. Sun, X. Y. Xia, W. L. Liu and L. Tang, Benzophenone-type UV filters in surface waters: An assessment of profiles and ecological risks in Shanghai, China, Ecotoxicol Environ. Saf., 2017, 141, 235–241.

    Article  CAS  PubMed  Google Scholar 

  205. J. A. Ruszkiewicz, A. Pinkas, B. Ferrer, T. V. Peres, A. Tsatsakis and M. Aschner, Neurotoxic effect of active ingredients in sunscreen products,a contemporary review, Toxicol. Rep., 2017, 4, 245–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. R. Danovaro, L. Bongiorni, C. Corinaldesi, D. Giovannelli, E. Damiani, P. Astolfi, L. Greci and A. Pusceddu, Sunscreens cause coral bleaching by promoting viral infections, Environ. Health Perspect., 2008, 116, 441–447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. M. Sendra, D. Sanchez-Quiles, J. Blasco, I. Moreno-Garrido, L. M. Lubian, S. Perez-Garcia and A. Tovar-Sanchez, Effects of TiO2 nanoparticles and sunscreens on coastal marine microalgae: Ultraviolet radiation is key variable for toxicity assessment, Environ. Int., 2017, 98, 62–68.

    Article  CAS  PubMed  Google Scholar 

  208. P. Y. Kunz, H. F. Galicia and K. Fent, Comparison of in vitro and in vivo estrogenic activity of UV filters in fish, Toxicol. Sci., 2006, 90, 349–361.

    Article  CAS  PubMed  Google Scholar 

  209. S. Kim and K. Choi, Occurrences, toxicities, and ecological risks of benzophenone-3, a common component of organic sunscreen products: A mini-review, Environ. Int., 2014, 70, 143–157.

    Article  CAS  PubMed  Google Scholar 

  210. D. Kaiser, O. Wappelhorst, M. Oetken and J. Oehlmann, Occurrence of widely used organic UV filters in lake and river sediments, Environ. Chem., 2012, 9, 139–147.

    Article  CAS  Google Scholar 

  211. R. J. Miller, S. Bennett, A. A. Keller, S. Pease and H. S. Lenihan, TiO2 nanoparticles are phototoxic to marine phytoplankton, PLoS One, 2012, 7, e30321.

  212. E. Spisni, Toxicity assessment of industrial- and sunscreen-derived ZnO nanoparticles, University of Miami, (Coral Gables, FL), 2016.

    Google Scholar 

  213. T. A. Jarvis, R. J. Miller, H. S. Lenihan and G. K. Bielmyer, Toxicity of ZnO nanoparticles to the copepod Acartia tonsa, exposed through a phytoplankton diet, Environ. Toxicol. Chem., 2013, 32, 1264–1269.

    CAS  Google Scholar 

  214. B. Gewert, M. M. Plassmann and M. MacLeod, Pathways for degradation of plastic polymers floating in the marine environment, Environ. Sci.: Processes Impacts, 2015, 17, 1513–1521.

    CAS  Google Scholar 

  215. A. Andrady, P. J. Aucamp, A. Austin, A. F. Bais, C. L. Ballaré, P. W. Barnes, G. H. Bernhard, J. F. Bornman, M. M. Caldwell, F. R. De Gruijl, D. J. I. Erickson, S. D. Flint, K. Gao, P. Gies, D.-P. Häder, M. Ilyas, J. Longstreth, R. Lucas, S. Madronich, R. McKenzie, R. Neale, M. Norval, K. K. Pandy, N. D. Paul, M. Rautio, H. H. Redhwi, S. A. Robinson, K. Rose, M. Shao, R. P. Sinha, K. R. Solomon, B. Sulzberger, Y. Takizawa, X. Tang, A. Torikai, K. Tourpali, J. C. van der Leun, C. E. Williamson, S.-Å. Wängberg, S. R. Wilson, R. C. Worrest, A. R. Young and R. G. Zepp, Environmental effects of ozone depletion and its interactions with climate change: 2014 assessment : Executive summary, Photochem. Photobiol. Sci., 2015, 14, 14–18.

    Article  CAS  Google Scholar 

  216. A. L. Andrady, K. K. Pandey and A. M. Heikkilä, Interactive effects of solar UV radiation and climate change on material damage, Photochem. Photobiol. Sci., 2019, 18, DOI: 10.1039/C8PP90065E.

  217. UNEP, UNEP Frontiers 2016 Report: Emerging Issues of Environmental Concern, United Nations Environment Programme Report, Nairobi, 2016.

  218. J. R. Clark, M. Cole, P. K. Lindeque, E. Fileman, J. Blackford, C. Lewis, T. M. Lenton and T. S. Galloway, Marine microplastic debris: a targeted plan for understanding and quantifying interactions with marine life, Front. Ecol. Environ., 2016, 14, 317–324.

    Article  Google Scholar 

  219. A. Batel, F. Linti, M. Scherer, L. Erdinger and T. Braunbeck, Transfer of benzo[a]pyrene from microplastics to Artemia nauplii and further to zebrafish via a trophic food web experiment: CYP1A induction and visual tracking of persistent organic pollutants, Environ. Toxicol. Chem., 2016, 35, 1656–1666.

    CAS  Google Scholar 

  220. M. Cole, P. K. Lindeque, E. Fileman, J. Clark, C. Lewis, C. Halsband and T. S. Galloway, Microplastics alter the properties and sinking rates of zooplankton faecal pellets, Environ. Sci. Technol., 2016, 50, 3239–3246.

  221. A. M. Wieczorek, L. Morrison, P. L. Croot, A. L. Allcock, E. MacLoughlin, O. Savard, H. Brownlow and T. K. Doyle, Frequency of microplastics in mesopelagic fishes from the northwest Atlantic, Front. Mar. Sci., 2018, 5, 39.

    Article  Google Scholar 

  222. D. Eerkes-Medrano, R. C. Thompson and D. C. Aldridge, Microplastics in freshwater systems: A review of the emerging threats, identification of knowledge gaps and prioritisation of research needs, Water Res., 2015, 75, 63–82.

    Article  CAS  PubMed  Google Scholar 

  223. K. Mattsson, E. V. Johnson, A. Malmendal, S. Linse, L. A. Hansson and T. Cedervall, Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain, Sci. Rep., 2017, 7, 11452.

    Google Scholar 

  224. L. G. A. Barboza, A. Dick Vethaak, B. R. B. O. Lavorante, A.-K. Lundebye and L. Guilhermino, Marine microplastic debris: An emerging issue for food security, food safety and human health, Mar. Poll. Bull, 2018, 133, 336–348.

    Article  CAS  Google Scholar 

  225. S. L. Wright and F. J. Kelly, Plastic and human health: A micro issue?, Environ. Sci. Technol., 2017, 51, 6634–6647.

    Article  CAS  PubMed  Google Scholar 

  226. N. J. Abram, R. Mulvaney, F. Vimeux, S. J. Phipps, J. Turner and M. H. England, Evolution of the Southern Annular Mode during the past millennium, Nat. Clim. Change, 2014, 4, 564–569.

    Article  CAS  Google Scholar 

  227. S. A. Robinson and D. J. Erickson, Not just about sunburn - the ozone hole’s profound effect on climate has significant implications for Southern Hemisphere ecosystems, Glob. Change Biol., 2015, 21, 515–527.

    Article  Google Scholar 

  228. A. Solomon, L. M. Polvani, K. L. Smith and R. P. Abernathey, The impact of ozone depleting substances on the circulation, temperature, and salinity of the Southern Ocean: An attribution study with CESM1 (WACCM), Geophys. Res. Lett., 2015, 42, 5547–5555.

    Article  Google Scholar 

  229. WMO (World Meteorological Organization), Executive Summary: Scientific Assessment of Ozone Depletion: 2018, World Meteorological Organization, Global Ozone Research and Monitoring Project, Report no. 58, Geneva, Switzerland, 2018, p. 67.

  230. P. Landschützer, N. Gruber, F. A. Haumann, C. Rodenbeck, D. C. E. Bakker, S. van Heuven, M. Hoppema, N. Metzl, C. Sweeney, T. Takahashi, B. Tilbrook and R. Wanninkhof, The reinvigoration of the Southern Ocean carbon sink, Science, 2015, 349,1121–1124.

  231. D. J. Erickson III, B. Sulzberger, R. G. Zepp and A. T. Austin, Effects of stratospheric ozone depletion, solar UV radiation, and climate change on biogeochemical cycling: interactions and feedbacks, Photochem. Photobiol. Sci., 2015, 14, 127–148.

    Article  Google Scholar 

  232. V. H. L. Winton, A. R. Bowie, R. Edwards, M. Keywood, A. T. Townsend, P. van der Merwe and A. Bollhöfer, Fractional iron solubility of atmospheric iron inputs to the Southern Ocean, Mar. Chem., 2015, 177, 20–32.

    Article  CAS  Google Scholar 

  233. S. Leung, A. Cabre and I. Marinov, A latitudinally banded phytoplankton response to 21st century climate change in the Southern Ocean across the CMIP5 model suite, Biogeosciences, 2015, 12, 5715–5734.

    Article  Google Scholar 

  234. M. A. Hindell, C. J. Bradshaw, B. W. Brook, D. A. Fordham, K. Kerry, C. Hull and C. R. McMahon, Long-term breeding phenology shift in royal penguins, Ecol. Evol., 2012, 2, 1563–1571.

    Article  PubMed  PubMed Central  Google Scholar 

  235. N. Dehnhard, M. Eens, L. Demongin, P. Quillfeldt and M. Poisbleau, Individual consistency and phenotypic plasticity in Rockhopper penguins: Female but not male body mass links environmental conditions to reproductive investment, PLoS One, 2015, 10, e0128776.

  236. N. Dehnhard, M. Eens, L. Demongin, P. Quillfeldt, D. Suri and M. Poisbleau, Limited individual phenotypic plasticity in the timing of and investment into egg laying in southern rockhopper penguins under climate change, Mar. Ecol.: Prog. Ser., 2015, 524, 269–281.

    Article  Google Scholar 

  237. F. Abadi, C. Barbraud and O. Gimenez, Integrated population modeling reveals the impact of climate on the survival of juvenile Emperor penguins, Glob. Change Biol., 2017, 23, 1353–1359.

    Article  Google Scholar 

  238. L. Emmerson, R. Pike and C. Southwell, Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology, Mar. Ecol.: Prog. Ser., 2011, 440, 203–216.

    Article  Google Scholar 

  239. H. Weimerskirch, M. Lauzao, S. de Grissac and K. Delord, Changes in wind pattern alter albatross distribution and life-history traits, Science, 2012, 335, 211–214.

    Article  CAS  PubMed  Google Scholar 

  240. R. Fay, H. Weimerskirch, K. Delord and C. Barbraud, Population density and climate shape early-life survival and recruitment in a long-lived pelagic seabird, J. Anim. Ecol., 2015, 84, 1423–1433.

    Article  PubMed  Google Scholar 

  241. R. Fay, C. Barbraud, K. Delord and H. Weimerskirch, Contrasting effects of climate and population density over time and life stages in a long-lived seabird, Funct. Ecol., 2017, 31, 1275–1284.

    Article  PubMed  PubMed Central  Google Scholar 

  242. C. R. McMahon, R. G. Harcourt, H. R. Burton, O. Daniel and M. A. Hindell, Seal mothers expend more on offspring under favourable conditions and less when resources are limited, J. Anim. Ecol., 2017, 86, 359–370.

    Article  PubMed  Google Scholar 

  243. P. Cetina-Heredia, M. Roughan, E. van Sebille, M. Feng and M. A. Coleman, Strengthened currents override the effect of warming on lobster larval dispersal and survival, Glob. Change Biol., 2015, 21, 4377–4386.

    Article  Google Scholar 

  244. H. Evangelista, I. Wainer, A. Sifeddine, T. Correge, R. C. Cordeiro, S. Lamounier, D. Godiva, C. C. Shen, F. Le Cornec, B. Turcq, C. E. Lazareth and C. Y. Hu, Ideas and perspectives: Southwestern tropical Atlantic coral growth response to atmospheric circulation changes induced by ozone depletion in Antarctica, Biogeosciences, 2016, 13, 2379–2386.

    Article  Google Scholar 

  245. C. R. Johnson, S. C. Banks, N. S. Barrett, F. Cazassus, P. K. Dunstan, G. J. Edgar, S. D. Frusher, C. Gardner, M. Haddon, F. Helidoniotis, K. L. Hill, N. J. Holbrook, G. W. Hosie, P. R. Last, S. D. Ling, J. Melbourne-Thomas, K. Miller, G. T. Pecl, A. J. Richardson, K. R. Ridgway, S. R. Rintoul, D. A. Ritz, D. J. Ross, J. C. Sanderson, S. A. Shepherd, A. Slotvvinski, K. M. Swadling and N. Taw, Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania, J. Exp. Mar. Biol. Ecol., 2011, 400, 17–32.

    Article  Google Scholar 

  246. C. Coviaga, A. Rizzo, P. Perez, R. Daga, D. Poire, G. Cusminsky and S. R. Guevara, Reconstruction of the hydrologic history of a shallow Patagonian steppe lake during the past 700 years, using chemical, geologic, and biological proxies, Quat. Res., 2017, 87, 208–226.

    Article  CAS  Google Scholar 

  247. D. A. Hodgson, D. Roberts, A. McMinn, E. Verleyen, B. Terry, C. Corbett and W. Vyverman, Recent rapid salinity rise in three East Antarctic lakes, J. Paleolimnol., 2006, 36, 385–406.

    Article  Google Scholar 

  248. G. S. Blanco, J. P. Pisoni and F. Quintana, Characterization of the seascape used by juvenile and wintering adult Southern Giant Petrels from Patagonia Argentina, Estuarine, Coastal Shelf Sci., 2015, 153, 135–144.

    Article  Google Scholar 

  249. J. E. Ramos, G. T. Pecl, N. A. Moltschaniwskyj, J. M. Semmens, C. A. Souza and J. M. Strugnell, Population genetic signatures of a climate change driven marine range extension, Sci. Rep., 2018, 8, 9558.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  250. S. A. Robinson, D. H. King, J. Bramley-Alves, M. J. Waterman, M. B. Ashcroft, J. Wasley, J. D. Turnbull, R. E. Miller, E. Ryan-Colton, T. Benny, K. Mullany, L. J. Clarke, L. A. Barry and Q. Hua, Rapid change in East Antarctic terrestrial vegetation in response to regional drying, Nat. Clim. Change, 2018, 8, 879.

    Article  CAS  Google Scholar 

  251. G. T. Pecl, M. B. Araújo, J. D. Bell, J. Blanchard, T. C. Bonebrake, I.-C. Chen, T. D. Clark, R. K. Colwell, F. Danielsen, B. Evengård, L. Falconi, S. Ferrier, S. Frusher, R. A. Garcia, R. B. Griffis, A. J. Hobday, C. Janion-Scheepers, M. A. Jarzyna, S. Jennings, J. Lenoir, H. I. Linnetved, V. Y. Martin, P. C. McCormack, J. McDonald, N. J. Mitchell, T Mustonen, J. M. Pandolfi, N. Pettorelli, E. Popova, S. A. Robinson, B. R. Scheffers, J. D. Shaw, C. J. B. Sorte, J. M. Strugnell, J. M. Sunday, M.-N. Tuanmu, A. Vergés, C. Villanueva, T. Wernberg, E. Wapstra and S. E. Williams, Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being, Science, 2017, 355, eaai9214.

  252. C. E. Williamson, R. G. Zepp, R. M. Lucas, S. Madronich, A. T. Austin, C. L. Ballaré, M. Norval, B. Sulzberger, A. Bais, R. L. McKenzie, S. A. Robinson, D.-P. Häder, N. D. Paul and J. F. Bornman, Solar ultraviolet radiation in a changing climate, Nat. Clim. Change, 2014, 4, 434–441.

    Article  Google Scholar 

  253. K. Nakamura, M. Nashimoto, Y. Okuda, T. Ota and M. Yamamoto, Fish as a major source of vitamin D in the Japanese diet, Nutrition, 2002, 18, 415–416.

    Article  CAS  PubMed  Google Scholar 

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Williamson, C.E., Neale, P.J., Hylander, S. et al. The interactive effects of stratospheric ozone depletion, UV radiation, and climate change on aquatic ecosystems. Photochem Photobiol Sci 18, 717–746 (2019). https://doi.org/10.1039/c8pp90062k

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