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Fossil pollen and spores as a tool for reconstructing ancient solar-ultraviolet irradiance received by plants: an assessment of prospects and challenges using proxy-system modelling

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Abstract

Ultraviolet-B radiation (UV-B, 280–315 nm) constitutes less than 1% of the total solar radiation that reaches the Earth’s surface but has a disproportional impact on biological and ecological processes from the individual to the ecosystem level. Absorption of UV-B by ozone is also one of the primary heat sources to the stratosphere, so variations in UV-B have important relationships to the Earth’s radiation budget. Yet despite its importance for understanding atmospheric and ecological processes, there is limited understanding about the changes in UV-B radiation in the geological past. This is because systematic measurements of total ozone and surface UV-B only exist since the 1970s, so biological or geochemical proxies from sediment archives are needed to reconstruct UV-B irradiance received at the Earth surface beyond the experimental record. Recent developments have shown that the quantification of UV-B-absorbing compounds in pollen and spores have the potential to provide a continuous record of the solar-ultraviolet radiation received by plants. There is increasing interest in developing this proxy in palaeoclimatic and palaeoecological research. However, differences in interpretation exist between palaeoecologists, who are beginning to apply the proxy under various geological settings, and UV-B ecologists, who question whether a causal dose–response relationship of pollen and spore chemistry to UV-B irradiance has really been established. Here, we use a proxy-system modelling approach to systematically assess components of the pollen- and spore-based UV-B-irradiance proxy to ask how these differences can be resolved. We identify key unknowns and uncertainties in making inferences about past UV-B irradiance, from the pollen sensor, the sedimentary archive, and through the laboratory and experimental procedures in order to target priority areas of future work. We argue that an interdisciplinary approach, modifying methods used by plant ecologists studying contemporary responses to solar-UV-B radiation specifically to suit the needs of palaeoecological analyses, provides a way forward in developing the most reliable reconstructions for the UV-B irradiance received by plants across a range of timescales.

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References

  1. IARC, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Lyon, France, 2012, vol. 100D.

  2. A. B. Britt, DNA damage and repair in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, 47, 75–100.

    Article  CAS  PubMed  Google Scholar 

  3. A. Sancar and G. B. Sancar, DNA-Repair Enzymes, Annu. Rev. Biochem., 1988, 57, 29–67.

    Article  CAS  PubMed  Google Scholar 

  4. J. Rozema, J. van de Staaij, L. O. Björn and M. Caldwell, UV-B as an environmental factor in plant life: Stress and regulation, Trends Ecol. Evolut., 1997, 12, 22–28.

  5. S. Weber, Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase, Biochim. Biophys. Acta, Bioenerg., 2005, 1707, 1–23.

  6. K. J. Willis, K. D. Bennett and H. J. B. Birks, Variability in thermal and UV-B energy fluxes through time and their influence on plant diversity and speciation, J. Biogeogr., 2009, 36, 1630–1644.

    Article  Google Scholar 

  7. J. F. Bornman, P. W. Barnes, S. A. Robinson, C. L. Bailaré, S. D. Flint and M. M. Caldwell, Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems, Photochem. Photobiol. Sci., 2015, 14, 88–107.

    Article  CAS  PubMed  Google Scholar 

  8. A. F. Bais, R. M. Lucas, J. F. Bornman, C. E. Williamson, B. Sulzberger, A. T. Austin, S. R. Wilson, A. L. Andrady, G. Bernhard, R. L. McKenzie, P. J. Aucamp, S. Madronich, R. E. Neale, S. Yazar, A. R. Young, F. R. de Gruijl, M. Norval, Y. Takizawa, P. W. Barnes, T. M. Robson, S. A. Robinson, C. L. Ballaré, S. D. Flint, P. J. Neale, S. Hylander, K. C. Rose, S. Å. Wängberg, D. P. Häder, R. C. Worrest, R. G. Zepp, N. D. Paul, R. M. Cory, K. R. Solomon, J. Longstreth, K. K. Pandey, H. H. Redhwi, A. Torikai and A. M. Heikkilä, Environmental effects of ozone depletion, UV radiation and interactions with climate change: UNEP Environmental Effects Assessment Panel, update 2017, Photochem. Photobiol. Sci., 2018, 17, 127–179.

  9. L. O. Björn, S. Widell and T. Wang, Evolution of UV-B regulation and protection in plants, Adv. Space Res., 2002, 30, 1557–1562.

    Article  PubMed  Google Scholar 

  10. P. E. Jardine, W. T. Fraser, B. H. Lomax, M. A. Sephton, T. M. Shanahan, C. S. Miller and W. D. Gosling, Pollen and spores as biological recorders of past ultraviolet irradiance, Sci. Rep., 2016, 6, 39269, DOI: 10.1038/srep39269.

  11. J. Rozema, B. van Geel, L. O. Björn, J. Lean and S. Madronich, Toward solving the UV puzzle, Science, 2002, 296, 1621–1622.

    Article  CAS  PubMed  Google Scholar 

  12. D. J. Beerling, M. Harfoot, B. Lomax and J. A. Pyle, The stability of the stratospheric ozone layer during the end-Permian eruption of the Siberian Traps, Philos. Trans. R. Soc., A, 2007, 365, 1843–1866.

    Article  CAS  Google Scholar 

  13. C. V. Looy, R. J. Twitchett, D. L. Dilcher, J. H. A. Van Konijnenbyrg-Van Cittert and H. Visscher, Life in the end-Permian dead zone, Proc. Natl. Acad. Sci. U. S. A., 2001, 98, 7879–7883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. H. Visscher, C. V. Looy, M. E. Collinson, H. Brinkhuis, J. H. A. Van Konijnenbyrg-Van Cittert, W. M. Kürschner and M. A. Sephton, Environmental mutagenesis during the end-Permian ecological crisis, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 12952–12956.

  15. C. B. Foster and S. A. Afonin, Abnormal pollen grains: an outcome of deteriorating atmospheric conditions around the Permian–Triassic boundary, J. Geol. Soc., 2005, 162, 653–659.

  16. J. R. Flenley, Why is pollen yellow? And why are there so many species in the tropical rain forest?, J. Biogeogr., 2011, 38, 809–816.

  17. B. H. Lomax, W. T. Fraser, G. Harrington, S. Blackmore, M. A. Sephton and N. B. W. Harris, A novel palaeoaltimetry proxy based on spore and pollen wall chemistry, Earth Planet. Sci. Lett., 2012, 353–354, 22–28.

  18. R. L. McKenzie, P. J. Aucamp, A. F. Bais, L. O. Björn, M. Ilyas and S. Madronich, Ozone depletion and climate change: impacts on UV radiation, Photochem. Photobiol. Sci., 2011, 10, 182–198.

  19. A. F. Bais, R. L. McKenzie, G. Bernhard, P. J. Aucamp, M. Ilyas, S. Madronich and K. Tourpali, Ozone depletion and climate change: impacts on UV radiation, Photochem. Photobiol. Sci., 2015, 14, 19–52.

    Article  CAS  PubMed  Google Scholar 

  20. C. E. Williamson, R. G. Zepp, R. M. Lucas, S. Madronich, A. T. Austin, C. L. Bailaré, M. Norval, B. Sulzberger, A. F. 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 

  21. J. R. McConnell, A. Burke, N. W. Dunbar, P. Köhler, J. L. Thomas, M. M. Arienzo, N. J. Chellman, O. J. Maselli, M. Sigl, J. F. Adkins, D. Baggenstos, J. F. Burkhart, E. J. Brook, C. Buizert, J. Cole-Dai, T. J. Fudge, G. Knorr, H.-F. Graf, M. M. Grieman, N. Iverson, K. C. McGwire, R. Mulvaney, G. Paris, R. H. Rhodes, E. S. Saltzman, J. P. Severinghaus, J. P. Steffensen, K. C. Taylor and G. Winckler, Synchronous volcanic eruptions and abrupt climate change ~17.7 ka plausibly linked by stratospheric ozone depletion. Proc. Natl. Acad. Sci. U. S. A., 2017, 114, 10035–10040.

  22. J. Beer and B. van Geel, in, Natural Climate Variability and Global Warming: A Holocene Perspective, ed. R. W. Battarbee and H. Binney, Blackwell, Chichester, UK, 2008, pp. 138–162.

  23. P. Moffa-Sánchez, A. Born, I. R. Hall, D. J. R. Thornalley and S. Barker, Solar forcing of North Atlantic surface temperature and salinity over the past millennium, Nat. Geosci., 2014, 7, 275–278.

    Article  CAS  Google Scholar 

  24. V. E. Fioletov, G. E. Bodeker, A. J. Miller, R. D. McPeters and R. Stolarski, Global and zonal total ozone variations estimated from ground-based and satellite measurements: 1964–2000, J. Geophys. Res.: Atmos., 2002, 107, 4647.

    Article  CAS  Google Scholar 

  25. D. A. Hodgson, W. Vyverman, E. Verleyen, P. R. Leavitt, K. Sabbe, A. H. Squier and B. J. Keely, Late Pleistocene record of elevated UV radiation in an Antarctic lake, Earth Planet. Sci. Lett., 2005, 236, 765–772.

    Article  CAS  Google Scholar 

  26. Q. Chen, Y. Nie, X. Liu, L. Xu and S. D. Emslie, An 800-year ultraviolet radiation record inferred from sedimentary pigments in the Ross Sea area, East Antarctica, Boreas, 2015, 44, 693–705.

  27. Beyond the visible: a handbook of best practice in plant UV photobiology. COST Action FA0906 UV4growth, ed. P. J. Aphalo, A. Albert, L. O. Björn, A. McLeod, T. M. Robson and E. Rosenqvist, University of Helsinki, Division of Plant Biology, Helsinki, 2012.

  28. J. Rozema, A. J. Noordijk, R. A. Broekman, A. van Beem, B. M. Meijkamp, N. V. J. de Bakker, J. W. M. van de Staaij, M. Stroetenga, S. J. P. Bohncke, M. Konert, S. Kars, H. Peat, R. I. L. Smith and P. Convey, (Poly)phenolic compounds in pollen and spores of Antarctic plants as indicators of solar UV-B – A new proxy for the reconstruction of past solar UV-B?, Plant Ecol., 2001, 154, 9–26.

    Article  Google Scholar 

  29. K. J. Willis, A. Feurdean, H. J. B. Birks, A. E. Bjune, E. Breman, R. Broekman, J.-A. Grytnes, M. New, J. S. Singarayer and J. Rozema, Quantification of UV-B flux through time using UV-B-absorbing compounds contained in fossil, Pinus sporopollenin, New Phytol., 2011, 192, 553–560.

    Article  CAS  PubMed  Google Scholar 

  30. W. T. Fraser, M. A. Sephton, J. S. Watson, S. Self, B. H. Lomax, D. I. James, C. H. Wellman, T. V. Callaghan and D. J. Beerling, UV-B absorbing pigments in spores: biochemical responses to shade in a high-latitude birch forest and implications for sporopollenin-based proxies of past environmental change, Polar Res., 2011, 30, 6026.

    Article  CAS  Google Scholar 

  31. B. H. Lomax, W. T. Fraser, M. A. Sephton, T. V. Callaghan, S. Self, M. Harfoot, J. A. Pyle, C. H. Wellman and D. J. Beerling, Plant spore walls as a record of long-term changes in ultraviolet-B radiation, Nat. Geosci., 2008, 1, 592–596.

    Article  CAS  Google Scholar 

  32. P. Blokker, P. Boelen, R. Broekman and J. Rozema, The occurrence of p-coumaric acid and ferulic acid in fossil plant materials and their use as UV-proxy, Plant Ecol., 2006, 182, 197–207.

    Google Scholar 

  33. P. Blokker, D. Yeloff, P. Boelen, R. A. Broekman and J. Rozema, Development of a Proxy for Past Surface UV-B Irradiation: A Thermally Assisted Hydrolysis and Methylation py-GC/MS Method for the Analysis of Pollen and Spores, Anal. Chem., 2005, 77, 6026–6031.

    Article  CAS  PubMed  Google Scholar 

  34. J. Rozema, P. Blokker, M. A. Mayoral Fuertes and R. Broekman, UV-B absorbing compounds in present-day and fossil pollen, spores, cuticles, seed coats and wood: evaluation of a proxy for solar UV radiation, Photochem. Photobiol. Sci., 2009, 8, 1233–1212.

    Article  CAS  PubMed  Google Scholar 

  35. J. S. Watson, M. A. Sephton, S. V. Sephton, S. Self, W. T. Fraser, B. H. Lomax, I. Gilmour, C. H. Wellman and D. J. Beerling, Rapid determination of spore chemistry using thermochemolysis gas chromatography-mass spectrometry and micro-Fourier transform infrared spectroscopy, Photochem. Photobiol. Sci., 2007, 6, 689.

    Article  CAS  PubMed  Google Scholar 

  36. W. T. Fraser, B. H. Lomax, P. E. Jardine, W. D. Gosling and M. A. Sephton, Pollen and spores as a passive monitor of ultraviolet radiation, Front. Ecol. Evol., 2014, 2, 437.

    Article  Google Scholar 

  37. J. W. de Leeuw, G. J. M. Versteegh and P. F. van Bergen, in, Plants and Climate Change, Springer Netherlands, Dordrecht, 2006, vol. 182, pp. 209–233.

  38. S. D. Flint and M. M. Caldwell, Partial inhibition of in vitro pollen germination by simulated solar ultraviolet-B radiation, Ecology, 1984, 65, 792–795.

    Article  Google Scholar 

  39. N. Tuteja, M. B. Singh, M. K. Misra, P. L. Bhalla and R. Tuteja, Molecular mechanisms of DNA damage and repair: progress in plants, Crit. Rev. Biochem. Mol. Biol., 2008, 36, 337–397.

    Article  Google Scholar 

  40. É. Hideg, M. A. K. Jansen and Å. Strid, UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates?, Trends Plant Sci., 2013, 18, 107–115.

    Article  CAS  PubMed  Google Scholar 

  41. W. T. Fraser, A. C. Scott, A. E. S. Forbes, I. J. Glasspool, R. E. Plotnick, F. Kenig and B. H. Lomax, Evolutionary stasis of sporopollenin biochemistry revealed by unaltered Pennsylvanian spores, New Phytol., 2012, 196, 397–401.

    Article  CAS  PubMed  Google Scholar 

  42. J. Rozema, R. A. Broekman, P. Blokker, B. B. Meijkamp, N. de Bakker, J. van de Staaij, A. van Beem, F. Ariese and S. M. Kars, UV-B absorbance and UV-B absorbing compounds (para-coumaric acid) in pollen and sporopollenin: the perspective to track historic UV-B levels, J. Photochem. Photobiol., B, 2001, 62, 108–117.

    Article  CAS  Google Scholar 

  43. M. Jokerud, Plastic response in Pinus spp., determining the temporal window of response and species-level variation of UV-B absorbing compounds to short-term variation in UV-B radiation. Advances in developing a pollen-based UV-B proxy using THM py-GC/MS, PhD Thesis, University of Bergen, Norway, 2017.

  44. A. W. R. Seddon, M. Jokerud, T. Barth, H. J. B. Birks, L. C. Krüger, V. Vandvik and K. J. Willis, Improved quantification of UV-B absorbing compounds in, Pinus sylvestris L. pollen grains using an internal standard methodology, Rev. Palaeobot. Palynol., 2017, 247, 97–104.

    Article  Google Scholar 

  45. B. A. Bell, W. J. Fletcher, P. Ryan, A. W. Seddon, R. A. Wogelius and R. Ilmen, UV-B-absorbing compounds in modern, Cedrus atlantica pollen: The potential for a summer UV-B proxy for Northwest Africa, Holocene, 2018, 49, 095968361877707–13.

    Google Scholar 

  46. B. C. Thomas, B. D. Goracke and S. M. Dalton, Atmospheric constituents and surface-level UVB: Implications for a paleoaltimetry proxy and attempts to reconstruct UV exposure during volcanic episodes, Earth Planet. Sci. Lett., 2016, 453, 141–151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. M. N. Evans, S. E. Tolwinski-Ward, D. M. Thompson and K. J. Anchukaitis, Applications of proxy system modeling in high resolution paleoclimatology, Quat. Sci. Rev., 2013, 76, 16–28.

    Article  Google Scholar 

  48. S. T. Jackson, Representation of flora and vegetation in Quaternary fossil assemblages: known and unknown knowns and unknowns, Quat. Sci. Rev., 2012, 49, 1–15.

  49. M. N. Evans, Toward forward modeling for paleoclimatic proxy signal calibration: A case study with oxygen isotopic composition of tropical woods, Geochem., Geophys., Geosyst., 2007, 8, Q07008.

  50. M. E. Mann, Z. Zhang, M. K. Hughes, R. S. Bradley, S. K. Miller, S. Rutherford and F. Ni, Proxy-based reconstructions of hemispheric and global surface temperature variations over the past two millennia, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 13252–13257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. D. M. Thompson, T. R. Ault, M. N. Evans, J. E. Cole and J. Emile-Geay, Comparison of observed and simulated tropical climate trends using a forward model of coral, δ18O, Geophys. Res. Lett., 2011, 38, L14706.

  52. J. Verdebout, A European satellite-derived UV climatology available for impact studies, Radiat. Prot. Dosim., 2004, 111, 407–411.

  53. J. Laskar, P. Robutel, F. Joutel, M. Gastineau, A. C. M. Correia and B. Levrard, A long-term numerical solution for the insolation quantities of the Earth, Astron. Astrophys., 2004, 428, 261–285.

    Article  Google Scholar 

  54. L. Rizzini, J.-J. Favory, C. Cloix, D. Faggionato, A. O’Hara, E. Kaiserli, R. Baumeister, E. Schaefer, F. Nagy, G. I. Jenkins and R. Ulm, Perception of UV-B by the Arabidopsis UVR8 protein, Science, 2011, 332, 103–106.

    Article  CAS  PubMed  Google Scholar 

  55. J. M. Christie, A. S. Arvai, K. J. Baxter, M. Heilmann, A. J. Pratt, A. O’Hara, S. M. Kelly, M. Hothorn, B. O. Smith, K. Hitomi, G. I. Jenkins and E. D. Getzoff, Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges, Science, 2012, 335, 1492–1496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. S. Wallace, C. C. Chater, Y. Kamisugi, A. C. Cuming, C. H. Wellman, D. J. Beerling and A. J. Fleming, Conservation of Male Sterility 2function during spore and pollen wall development supports an evolutionarily early recruitment of a core component in the sporopollenin bio-synthetic pathway, New Phytol., 2014, 205, 390–401.

    Article  PubMed  CAS  Google Scholar 

  57. B. H. Lomax and W. T. Fraser, Palaeoproxies: botanical monitors and recorders of atmospheric change, Palaeontology, 2015, 58, 759–768.

    Article  Google Scholar 

  58. M. Bağcıoğlu, B. Zimmermann and A. Kohler, A multi-scale vibrational spectroscopic approach for identification and biochemical characterization of pollen, PLoS One, 2015, 10, e0137899–e0137819.

  59. B. Zimmermann, M. Bağcıoğlu, C. Sandt and A. Kohler, Vibrational microspectroscopy enables chemical characterization of single pollen grains as well as comparative analysis of plant species based on pollen ultrastructure, Planta, 2015, 242, 1237–1250.

    Article  CAS  PubMed  Google Scholar 

  60. T. M. Robson and P. J. Aphalo, Species-specific effect of UV-B radiation on the temporal pattern of leaf growth, Physiol. Plant, 2012, 144, 146–160.

    Article  CAS  PubMed  Google Scholar 

  61. J. Torabinejad, M. M. Caldwell, S. D. Flint and S. Durham, Susceptibility of pollen to UV-B radiation: an assay of 34 taxa, Am. J. Bot., 1998, 85, 360–369.

    Article  CAS  PubMed  Google Scholar 

  62. K. Klem, P. Holub, M. Štroch, J. Nezval, V. Špunda, J. Tříska, M. A. K. Jansen, T. M. Robson and O. Urban, Ultraviolet and photosynthetically active radiation can both induce photoprotective capacity allowing barley to overcome high radiation stress, Plant Physiol. Biochem., 2015, 93, 74–83.

    Article  CAS  PubMed  Google Scholar 

  63. T. Kotilainen, R. Tegelberg, R. Julkunen-Tiitto, A. Lindfors and P. J. Aphalo, Metabolite specific effects of solar UV-A and UV-B on alder and birch leaf phenolics, Glob. Chang. Biol., 2008, 14, 1294–1304.

    Article  Google Scholar 

  64. M. Schreiner, M. Wiesner-Reinhold, S. Baldermann, F. S. Hanschen, S. Neugart, in, Plant UV Biology, ed. B. Jordan, CABI publishers, 2017, ch. 4, pp. 39–57.

  65. P. W. Barnes, T. M. Robson, M. A. Tobler, I. N. Bottger and S. D. Flint, Plant UV Biology, CABI publishers, 2017.

  66. S. T. Andersen, Influence of Climatic Variation on Pollen Season Severity in Wind-Pollinated Trees and Herbs, Grana, 1980, 19, 47–52.

  67. J. N. Owens, The reproductive biology of lodgepole pine, 2006, FGC extension note, 07, Prepared for Forest Genetics Council of British Columbia.

  68. B. Zimmermann and A. Kohler, Infrared spectroscopy of pollen identifies plant species and genus as well as environmental conditions, PLoS One, 2014, 9, e95417.

  69. D. Treutter, Managing phenol contents in crop plants by phytochemical farming and breeding—visions and constraints, Int. J. Mol. Sci., 2010, 11, 807–857.

  70. Q.-W. Wang, C. Kamiyama, J. Hidema and K. Hikosaka, Ultraviolet-B-induced DNA damage and ultraviolet-B tolerance mechanisms in species with different functional groups coexisting in subalpine moorlands, Oecologia, 2016, 181, 1069–1082.

    Article  PubMed  Google Scholar 

  71. Y. O. Kim and E. J. Lee, Comparison of phenolic compounds and the effects of invasive and native species in East Asia: support for the novel weapons hypothesis, Ecol. Res., 2011, 26, 87–94.

    Article  Google Scholar 

  72. H. Wang, X. Ma, L. Zhang, J. Zou and E. Siemann, UV-B has larger negative impacts on invasive populations of Triadica sebiferabut ozone impacts do not vary, J. Plant Ecol., 2016, 9, 61–68.

    Article  Google Scholar 

  73. M. Beckmann, M. Hock, H. Bruelheide and A. Erfmeier, The role of UV-B radiation in the invasion of, Hieracium pilosella-A comparison of German and New Zealand plants, Environ. Exp. Bot., 2012, 75, 173–180.

    Article  Google Scholar 

  74. M. Hock, M. Beckmann, R. R. Hofmann, H. Bruelheide and A. Erfmeier, Effects of UV-B radiation on germination characteristics in invasive plants in New Zealand, NeoBiota, 2015, 26, 21–37.

    Article  Google Scholar 

  75. T. Václavík, M. Beckmann, A. F. Cord and A. M. Bindewald, Effects of UV-B radiation on leaf hair traits of invasive plants—Combining historical herbarium records with novel remote sensing data, PLoS One, 2017, 12,e0175671–e0175618.

  76. F. Valladares, S. Matesanz, F. Guilhaumon, M. B. Araujo, L. Balaguer, M. Benito-Garzón, W. Cornwell, E. Gianoli, M. van Kleunen, D. E. Naya, A. B. Nicotra, H. Poorter and M. A. Zavala, The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change, Ecol. Lett., 2014, 17, 1351–1364.

    Article  PubMed  Google Scholar 

  77. M. Benito-Garzón, R. Alía, T. M. Robson and M. A. Zavala, Intra-specific variability and plasticity influence potential tree species distributions under climate change, Glob. Ecol. Biogeogr., 2011, 20, 766–778.

    Article  Google Scholar 

  78. S. M. Hartikainen, A. Jach, A. Grané and T. M. Robson, Assessing scale-wise similarity of curves with a thick pen: As illustrated through comparisons of spectral irradiance, Ecol. Evol., 2018, 1, 21–13.

    Google Scholar 

  79. S. D. Flint and M. M. Caldwell, A biological spectral weighting function for ozone depletion research with higher plants, Physiol. Plant., 2003, 117, 137–144.

    Article  CAS  Google Scholar 

  80. S. D. Flint and M. M. Caldwell, Field testing of UV biological spectral weighting functions for higher plants, Physiol. Plant., 2003, 117, 145–153.

    Article  CAS  Google Scholar 

  81. T. Kotilainen, T. Venäläinen, R. Tegelberg, A. Lindfors, R. Julkunen-Tiitto, S. Sutinen, R. B. O’Hara and P. J. Aphalo, Assessment of UV biological spectral weighting functions for phenolic metabolites and growth responses in silver birch seedlings, Photochem. Photobiol., 2009, 85, 1346–1355.

    Article  CAS  PubMed  Google Scholar 

  82. R. Julkunen-Tiitto, H. Häggman, P. J. Aphalo, A. Lavola, R. Tegelberg and T. Veteli, Growth and defense in deciduous trees and shrubs under UV-B, Environ. Pollut., 2005, 137, 404–414.

    Article  CAS  PubMed  Google Scholar 

  83. P. Krauss, C. Markstädter and M. Riederer, Attenuation of UV radiation by plant cuticles from woody species, Plant, Cell Environ., 1997, 20, 1079–1085.

    Article  Google Scholar 

  84. J. Rozema, M. Tosserams, H. J. M. Nelissen, L. van Heerwaarden, R. A. Broekman and N. Flierman, Stratospheric ozone reduction and ecosystem processes: enhanced UV-B radiation affects chemical quality and decomposition of leaves of the dune grassland species Calamagrostis epigeios, Plant Ecol., 1997, 128, 285–294.

    Article  Google Scholar 

  85. E. A. Tripp, Y. Zhuang, M. Schreiber, H. Stone and A. E. Berardi, Evolutionary and ecological drivers of plant flavonoids across a large latitudinal gradient, Mol. Phylogenet. Evol., 2018, 128, 147–161.

    Article  CAS  PubMed  Google Scholar 

  86. L. Jaakola and A. Hohtola, Effect of latitude on flavonoid biosynthesis in plants, Plant, Cell Environ., 2010, 160, 1239–1247.

    Google Scholar 

  87. M. Tattini, C. Galardi, P. Pinelli, R. Massai, D. Remorini and G. Agati, Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress, New Phytol., 2004, 163, 547–561.

    Article  CAS  PubMed  Google Scholar 

  88. F. Sato, Plant Secondary Metabolism in eLS, John Wiley & Sons, Ltd, Chichester, UK, 2014.

  89. T. M. Robson, S. M. Hartikainen and P. J. Aphalo, How does solar ultraviolet-B radiation improve drought tolerance of silver birch (Betula pendula Roth.) seedlings?, Plant, Cell Environ., 2014, 38, 953–967.

    Article  CAS  Google Scholar 

  90. L. von Post, Einige Südschwedischen Quellmoore, Bulletin of the Geological Institute of Uppsala University, 1916.

  91. L. von Post, Skogsträdpollen i sydsvenska torvmosselagerföljder, Förhandlingar Skandinavia Naturforskermøte, 1918, 43–465.

  92. H. J. B. Birks and B. E. Berglund, One hundred years of Quaternary pollen analysis 1916–2016, Veg. Hist. Archaeobot., 2018, 27, 271–309.

  93. A. Dawson, C. J. Paciorek, J. S. McLachlan, S. Goring, J. W. Williams and S. T. Jackson, Quantifying pollen-vegetation relationships to reconstruct ancient forests using 19th-century forest composition and pollen data, Quat. Sci. Rev., 2016, 137, 156–175.

    Article  Google Scholar 

  94. S. Sugita, Pollen representation of vegetation in quaternary sediments - theory and method in patchy vegetation, J. Ecol., 1994, 82, 881–897.

  95. I. C. Prentice, Pollen representation, source area, and basin size - toward a unified theory of pollen analysis, Quat. Res., 1985, 23, 76–86.

  96. M. Blaauw and E. Heegaard, in, Tracking Environmental Change Using Lake Sediments, Volume 5: Data Handling and Numerical Techniques, ed. H. J. B. Birks, A. F. Lotter, S. Juggins and J. P. Smol, Springer, Dordrecht, 2012, pp. 379–413.

  97. M. Blaauw and J. A. Christen, Flexible paleoclimate age-depth models using an autoregressive gamma process, Bayesian Anal., 2011, 6, 457–474.

    Article  Google Scholar 

  98. M. B. Davis, Palynology after Y2 K - Understanding the source area of pollen in sediments, Annu. Rev. Earth Planet. Sci., 2000, 28, 1–18.

  99. S. Sugita, S. Hicks and H. Sormunen, Absolute pollen productivity and pollen-vegetation relationships in northern Finland, J. Quat. Sci., 2009, 25, 724–736.

    Article  Google Scholar 

  100. H. Seppä and H. J. B. Birks, July mean temperature and annual precipitation trends during the Holocene in the Fennoscandian tree-line area: pollen-based climate reconstructions, Holocene, 2001, 11, 527–539.

    Article  Google Scholar 

  101. W. T. Fraser, J. S. Watson, M. A. Sephton, B. H. Lomax, G. Harrington, W. D. Gosling and S. Self, Changes in spore chemistry and appearance with increasing maturity, Rev. Palaeobot. Palynol., 2014, 201, 41–46.

    Article  Google Scholar 

  102. K. D. Bennett and K. J. Willis, in, Tracking Environmental Change Using Lake Sediments, Volume 3: Terrestrial, Algal, and Siliceous Indicators, ed. J. P. Smol, H. J. B. Birks and W. M. Last, R. S. Kluwer Academic Publishers, Dordrecht, 2002, vol. 3.

  103. A. Traverse, Paleopalynology, Massachusetts, 1988.

  104. P. E. Jardine, W. T. Fraser, B. H. Lomax and W. D. Gosling, The impact of oxidation on spore and pollen chemistry, J. Micropalaeontol., 2015, 34, 139–149.

    Article  Google Scholar 

  105. G. D. Wood, A. M. Gabriel and J. C. Lawson, in, Palynology Principles and Applications, ed. J. Jansonius and D. C. McGregor, American Association of Stratigraphic Palynologists Foundation, Dallas, 1996.

  106. N. G. Johnson, Early Silurian palynomorphs from the tuscarora formation in central Pennsylvania and their paleo-botanical and geological significance, Rev. Palaeobot. Palynol., 1985, 45, 307–359.

  107. V. Lebreton, E. Messager, L. Marquer and J. Renault-Miskovsky, A neotaphonomic experiment in pollen oxidation and its implications for archaeopalynology, Rev. Palaeobot. Palynol., 2010, 162, 29–38.

    Article  Google Scholar 

  108. A. R. Hemsley, A. C. Scott, P. J. Barrie and W. G. Chaloner, Studies of fossil and modern spore wall biomacromolecules using 13C solid state NMR, Ann. Bot., 1996, 78, 83–94.

    Article  Google Scholar 

  109. B. Zimmermann, Characterization of pollen by vibrational spectroscopy, Appl. Spectrosc., 2010, 64, 1364–1373.

  110. B. Zimmermann, M. Bağcıoğlu, V. Tafinstseva, A. Kohler, M. Ohlson and S. Fjellheim, A high-throughput FTIR spectroscopy approach to assess adaptive variation in the chemical composition of pollen, Ecol. Evol., 2017, 7, 10839–10849.

    Article  PubMed  PubMed Central  Google Scholar 

  111. M. Bağcıoğlu, A. Kohler, S. Seifert, J. Kneipp and B. Zimmermann, Monitoring of plant-environment interactions by high-throughput FTIR spectroscopy of pollen, Methods Ecol. Evol., 2016, 8, 870–880.

    Article  Google Scholar 

  112. B. Zimmerman, V. Tafintseva, M. Bağcıoğlu, M. Høegh Berdahl and A. Kohler, Analysis of allergenic pollen by FTIR microspectroscopy, Anal. Chem., 2015, 88, 803–811.

    Article  PubMed  CAS  Google Scholar 

  113. B. Zimmermann, Chemical characterization and identification of Pinaceae pollen by infrared microspectroscopy, Planta, 2017, 247, 171–180.

  114. P. E. Jardine, F. A. J. Abernethy, B. H. Lomax, W. D. Gosling and W. T. Fraser, Shedding light on sporopollenin chemistry, with reference to UV reconstructions, Rev. Palaeobot. Palynol., 2016, 1–28.

  115. R. Blümel, R. Lukacs, B. Zimmermann, M. Bağcıoğlu and A. Kohler, Observation of Mie ripples in the synchrotron Fourier transform infrared spectra of spheroidal pollen grains, J. Opt. Soc. Am. A, 2018, 35, 1769–1711.

    Article  Google Scholar 

  116. R. Lukacs, R. Blümel, B. Zimmerman, M. Bağcıoğlu and A. Kohler, Recovery of absorbance spectra of micrometer-sized biological and inanimate particles, Analyst, 2015, 140, 3273–3284.

    Article  CAS  PubMed  Google Scholar 

  117. P. W. Barnes, M. A. K. Jansen, G. I. Jenkins, F. Vandenbussche, C. C. Brelsford, A. K. Banas, W. Bilger, A. Castagna, D. Festi, A. Gaberščik, M. Germ, A. Golob, M.-T. Hauser, L. Llorens, J. Martinez-Abaigar, L. O. Morales, S. Neugart, M. Pieristè, N. Rai, L. Ryan, M. Santin, A. W. R. Seddon, J. Stelzner, E. Tavridou, J. Łabuz and T. M. Robson, The importance and direction of current and future plant-UV research, UV Plants Bull., 2018, 3, 19–32.

    Google Scholar 

  118. D. Magri, Past UV-B flux from fossil pollen: prospects for climate, environment and evolution, New Phytol., 2011, 192, 310–312.

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Seddon, A.W.R., Festi, D., Robson, T.M. et al. Fossil pollen and spores as a tool for reconstructing ancient solar-ultraviolet irradiance received by plants: an assessment of prospects and challenges using proxy-system modelling. Photochem Photobiol Sci 18, 275–294 (2019). https://doi.org/10.1039/c8pp00490k

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