Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Plant spore walls as a record of long-term changes in ultraviolet-B radiation

Nature Geoscience volume 1, pages 592–596 (2008)Cite this article

Abstract

Stratospheric ozone screens the Earth’s surface from harmful ultraviolet-B radiation. Concentrations of stratospheric ozone are governed by a variety of natural and anthropogenic factors, including solar cycles1, volcanic aerosols2, ozone-depleting substances3 and climate change4. However, assessing this variability before instrumental records has proved difficult owing to the lack of a well-constrained proxy5. Here, we use microspectroscopy to analyse the chemical composition of herbarium samples of clubmoss (Lycophyta) spores originating from high- and low-latitude localities, where they were exposed to different ultraviolet-B histories. We show that the concentration of two ultraviolet-B-absorbing compounds in the walls of high-northern- and southern-latitude spores is strongly regulated by historical variations in ultraviolet-B radiation. Conversely, we find little change in the concentration of these compounds in spores originating from tropical Ecuador, where ultraviolet levels have remained relatively stable. Using spores from Greenland, we reconstruct past (1907–1993) changes in ozone concentration and ultraviolet-B flux; we reveal strong similarities between spore-wall reconstructions, and independent instrumental records6 and model results7. Our findings suggest that ultraviolet-B-absorbing compounds in plant spore walls have the potential to act as a proxy for past changes in terrestrial ultraviolet-B radiation and stratospheric ozone. The chemical signature of plant spore walls in herbaria, and possibly also in sedimentary and ice-core archives, may therefore prove valuable for reconstructing past variations in stratospheric ozone and their connections with changes in solar radiation and climate.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Lycopodium spore-wall chemistry diagnostics.
Figure 2: Historical changes in stratospheric ozone regimes.
Figure 3: Spore-chemistry responses to changes in stratospheric ozone and ultraviolet-B fluxes.
Figure 4: Historical changes in Greenland spore-wall chemistry, stratospheric ozone and ultraviolet-B radiation.

Similar content being viewed by others

References

  1. Rozema, J., van Geel, B., Bjorn, L. O., Lean, J. & Madronich, S. Paleoclimate: Toward solving the UV puzzle. Science 296, 1621–1622 (2002).

    Article  Google Scholar 

  2. Tabazadeh, A., Drdla, K., Schoeberl, M. R., Hamill, P. & Toon, O. B. Arctic ‘ozone hole’ in a cold volcanic stratosphere. Proc. Natl Acad. Sci. 99, 2609–2612 (2002).

    Article  Google Scholar 

  3. Farman, J. C., Gardiner, B. G. & Shanklin, J. D. Large losses of total ozone in Antarctica reveal seasonal ClOx/NOx interaction. Nature 315, 207–210 (1985).

    Article  Google Scholar 

  4. Goutail, F. et al. Early unusual ozone loss during the Arctic winter 2002/2003 compared to other winters. Atmos. Chem. Phys. 5, 665–677 (2005).

    Article  Google Scholar 

  5. World Meteorological Organisation (WMO). Scientific assessment of ozone depletion: 2006 Global Ozone Research and Monitoring Project-Report No. 50 (Geneva, 2007).

  6. Hansen, G. & Svenøe, T. Multi-linear regression analysis of the 65-year Tromsø total ozone series. J. Geophys. Res. 110, D10103 (2005).

    Article  Google Scholar 

  7. Lindfors, A., Holmgren, B. & Hansen, G. Long-term erythemal UV at Abisko and Helsinki estimated using total ozone, sunshine duration, and snow depth. Remote Sens. Clouds Atmos. XI, Proc. SPIE 6362, doi:10.1117/12.689742 (2006).

  8. Herman, J. R., Bhartia, P.K., Ziemke, J., Ahmad, Z.N. & Larko, D. UV-B increases (1979–1992) from decreases in total ozone. Geophys. Res. Lett. 23, 2117–2120 (1996).

    Article  Google Scholar 

  9. Vogler, C., Brönnimann, S., Staehelin, J. & Griffin, R. E. M. Dobson total ozone series of Oxford: Re-evaluation and applications. J. Geophys. Res. 112, D20116 (2007).

    Article  Google Scholar 

  10. Dobson, G. M. B. & Harrison, D. N. Measurements of the amount of ozone in the Earth’s atmosphere and its relation to other geophysical conditions. Proc. Phys. Soc. Lond. A 110, 660–693 (1926).

    Article  Google Scholar 

  11. Vogler, C., S., Brönnimann, S. & Hansen, G. Re-evaluation of the 1950–1962 total ozone record from Longyearbyen, Svalbard. Atmos. Chem. Phys. 6, 4763–4773 (2006).

    Article  Google Scholar 

  12. Searles, P. S., Flint, S. D. & Caldwell, M. M. A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127, 1–10 (2001).

    Article  Google Scholar 

  13. Xiong, F. S. & Day, T. A. Effect of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of Antarctic vascular plants. Plant Phys. 125, 738–751 (2001).

    Article  Google Scholar 

  14. Ruhland, C. T. & Day, T. A. Size and longevity of seed banks in Antarctica and the influence of ultraviolet-B radiation on survivorship, growth and pigment concentrations of Colobanthus quitensis seedlings. Environ. Exp. Bot. 45, 143–154 (2001).

    Article  Google Scholar 

  15. Newsham, K. K. UV-B radiation arising from stratospheric ozone depletion influences the pigmentation of the Antarctic moss Andreaea regularis. Oecologia 135, 327–331 (2003).

    Article  Google Scholar 

  16. Markham, K. R., Franke, A., Given, D. R. & Brownsey, P. Historical Antarctic ozone trends from herbarium specimen flavonoids. Bull. Liais. Group Polyphenols 15, 230–235 (1990).

    Google Scholar 

  17. Blokker, P., Yeloff, D., Boelen, P., Broekman, R. A. & Rozema, J. 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. 77, 6026–6031 (2005).

    Article  Google Scholar 

  18. Rozema, J. et al. 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. Photo. B. 62, 108–117 (2001).

    Article  Google Scholar 

  19. Watson, J. S. et al. Rapid determination of spore chemistry using thermochemolysis gas chromatography–mass spectrometry and micro-Fourier transform infrared spectroscopy. Photochem. Photobiol. Sci. 6, 689–694 (2007).

    Article  Google Scholar 

  20. Alonso-Amelot, M. E., Oliveros-Bastidas, A. & Calcagno-Pisarelli, M. P. Phenolics and condensed tannins of high altitude Pteridium arachnoideum in relation to sunlight exposure, elevation, and rain regime. Biochem. Syst. Ecol. 35, 1–10 (2007).

    Article  Google Scholar 

  21. Piazena, H. The effect of altitude upon the solar UV-B and UV-A irradiance in the tropical Chilean. Sol. Energy 57, 133–140 (1996).

    Article  Google Scholar 

  22. Weatherhead, B., Tanskanen, A. & Stevermer, A. in Arctic Climate Impact Assessment (eds Corell, R. et al.) 151–182 (Cambridge Univ. Press, Cambridge, 2005).

    Google Scholar 

  23. WMO (World Meteorological Organization), Scientific Assessment of Ozone Depletion: 1998, WMO Global Ozone Research and Monitoring Project-Report No. 44 (Geneva, 1998).

  24. McKenzie, R. L., Aucamp, P. J., Bais, A. F., Björn, L. O. & Ilyas, M. Changes in biologically-active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 6, 218–231 (2007).

    Article  Google Scholar 

  25. Draper, N. R. & Smith, H. Applied regression analysis 2nd edn (Wiley, New York, 1987).

    Google Scholar 

  26. Jones, P. D., Jonsson, T. & Wheeler, D. Extension to the North Atlantic Oscillation using early instrumental pressure observations from Gibraltar and south-west Iceland. Int. J. Clim. 17, 1433–1450 (1997).

    Article  Google Scholar 

  27. Orsolini, Y. J. & Doblas-Reyes, F. J. Ozone signatures of climate patterns over the Euro-Atlantic sector in the spring. Q. J. R. Meteorol. Soc. 329, 3251–3263 (2003).

    Article  Google Scholar 

  28. Hahlbrock, K. & Scheel, D. Physiology and molecular-biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 347–369 (1989).

    Article  Google Scholar 

  29. Lean, J. Evolution of the sun’s spectral irradiance since the Maunder minimum. Geophys. Res. Lett. 27, 2425–2428 (2000).

    Article  Google Scholar 

  30. Bubert, H., Lambert, J., Steuernagel, S., Ahlers, F. & Wiermann, R. Continuous decomposition of sporopollenin from pollen of Typha angustifolia L. by acidic methanolysis. Z. Naturforsch. 57, 1035–1041 (2002).

    Article  Google Scholar 

Download references

Acknowledgements

We thank F. I. Woodward and W. P. Quick for critical comments on an earlier version of the manuscript, and D. Cameron and P. Mitchell for statistical assistance. We are also grateful to the following individuals for herbarium loans: H. Peat (British Antarctic Survey); B. Øllgaard (University of Aarhus); O. Ryding (The Botanical Museum, Copenhagen). We gratefully acknowledge financial support through a Natural Environment Research Council (NERC) studentship and CASE award to W.T.F. from Thermo Fisher Scientific and an NERC award (NER/A/S/2002/00865) and a Leverhulme Trust Early Career Fellowship to B.H.L. (ECF/2006/0492).

Author information

Author notes

  1. Barry H. Lomax

    Present address: Present address: The School of Biosciences, Division of Agricultural and Environmental Sciences, The University of Nottingham, Nottingham NG72RD, UK,

Authors and Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

    Barry H. Lomax, Terry V. Callaghan, Charles H. Wellman & David J. Beerling

  2. Department of Earth Sciences, The Open University, Walton Hall, Milton Keynes MK7 6AA, UK

    Wesley T. Fraser & Stephen Self

  3. Department of Earth Science and Engineering, Imperial College London, South Kensington Campus, London SW7 2AZ, UK

    Mark A. Sephton

  4. Abisko Scientific Research Station, SE-981 07 Abisko, Sweden

    Terry V. Callaghan

  5. Department of Chemistry, Centre for Atmospheric Science, University of Cambridge, Cambridge CB1 1EW, UK

    Michael Harfoot & John A. Pyle

  6. National Centre for Atmospheric Science, Global Composition, University of Cambridge, Cambridge CB2 1EW, UK

    John A. Pyle

Authors
  1. Barry H. Lomax
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wesley T. Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark A. Sephton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Terry V. Callaghan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephen Self
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Harfoot
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John A. Pyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Charles H. Wellman
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. David J. Beerling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barry H. Lomax.

Supplementary information

Supplementary Information

Supplementary figures S1-S2 and tables S1-S4 (PDF 223 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lomax, B., Fraser, W., Sephton, M. et al. Plant spore walls as a record of long-term changes in ultraviolet-B radiation. Nature Geosci 1, 592–596 (2008). https://doi.org/10.1038/ngeo278

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo278

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing