It has been suggested, on the basis of modern hydrology and fully coupled palaeoclimate simulations, that the warm greenhouse conditions1 that characterized the early Palaeogene period (55–45 Myr ago) probably induced an intensified hydrological cycle2 with precipitation exceeding evaporation at high latitudes3. Little field evidence, however, has been available to constrain oceanic conditions in the Arctic during this period. Here we analyse Palaeogene sediments obtained during the Arctic Coring Expedition, showing that large quantities of the free-floating fern Azolla grew and reproduced in the Arctic Ocean by the onset of the middle Eocene epoch (50 Myr ago). The Azolla and accompanying abundant freshwater organic and siliceous microfossils indicate an episodic freshening of Arctic surface waters during an 800,000-year interval. The abundant remains of Azolla that characterize basal middle Eocene marine deposits of all Nordic seas4,5,6,7 probably represent transported assemblages resulting from freshwater spills from the Arctic Ocean that reached as far south as the North Sea8. The termination of the Azolla phase in the Arctic coincides with a local sea surface temperature rise from 10 °C to 13 °C, pointing to simultaneous increases in salt and heat supply owing to the influx of waters from adjacent oceans. We suggest that onset and termination of the Azolla phase depended on the degree of oceanic exchange between Arctic Ocean and adjacent seas.

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  1. 1

    Zachos, J. C., Pagani, M., Sloan, L. C., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001)

  2. 2

    Barron, E. J., Hay, W. W. & Thompson, S. The hydrologic cycle: A major variable during Earth history. Glob. Planet. Change 1, 157–174 (1989)

  3. 3

    Huber, M., Sloan, L. C. & Shellito, C. J. in Causes and Consequences of Globally Warm Climates in the Early Palaeogene (eds Wing, S. L., Gingerich, P. D., Schmitz, B. & Thomas, E.) 25–47 (GSA Special Paper 369, Geological Society of America, Boulder, Colorado, 2003)

  4. 4

    Boulter, M. C. Pollen and spore events from the marine Tertiary of North Europe. J. Micropalaeontol. 5, 75–84 (1986)

  5. 5

    Bujak, J. P. & Mudge, D. C. A high-resolution North Sea Eocene dinocyst zonation. J. Geol. Soc. Lond. 151, 449–462 (1994)

  6. 6

    Eldrett, J. S., Harding, I. C., Firth, J. V. & Roberts, A. P. Magnetostratigraphic calibration of Eocene-Oligocene dinoflagellate cyst biostratigraphy from the Norwegian-Greenland Sea. Mar. Geol. 204, 91–127 (2004)

  7. 7

    Gradstein, F. M. & Agterberg, F. in Quantitative Stratigraphic Correlation (eds Cubitt, J. M. & Reyment, R. A.) 119–175 (Wiley & Sons, Chichester, UK, 1982)

  8. 8

    Heilmann-Clausen, C. in Early Paleogene Stage Boundaries. Abstracts and Field Trip Guides (ed. Molina, E.) 19 (University of Zaragoza, Zaragoza, Spain, 1996)

  9. 9

    Backman, J., Moran, K., McInroy, D. B., Mayer, L. A. & the Expedition 302 Scientists. Proc. IODP 302 doi:10.2204/iodp.proc.302.2006 (Integrated Ocean Drilling Program Management International, Inc., Edinburgh, 2006).

  10. 10

    Moran, K. et al. The cenozoic palaeoenvironment of the Arctic Ocean. Nature doi:10.1038/nature04800 (this issue)

  11. 11

    Rai, V. & Rai, A. K. Growth behaviour of Azolla pinnata at various salinity levels and induction of high salt tolerance. Plant Soil 206, 79–84 (1998)

  12. 12

    Arora, A. & Singh, P. K. Comparison of biomass productivity and nitrogen fixing potential of Azolla SPP. Biomass Bioenergy 24, 175–178 (2003)

  13. 13

    Collinson, M. E. The ecology of Cainozoic ferns. Rev. Palaeobot. Palynol. 119, 51–68 (2002)

  14. 14

    Collinson, M. E. Cainozoic ferns and their distribution. Brittonia 53, 173–235 (2001)

  15. 15

    Collinson, M. E. Palaeofloristic assemblages and palaeoecology of the Lower Oligocene Bembridge Marls, Hamstead Ledge, Isle of Wight. Bot. J. Linn. Soc. 86, 177–225 (1983)

  16. 16

    Sweet, A. R. & Hills, L. V. Early Tertiary species of Azolla subg. Azolla sect Kremastospora from western and arctic Canada. Can. J. Bot. 54, 334–351 (1976)

  17. 17

    Hopmans, E. C. et al. A novel proxy for terrestrial organic matter in sediments based on branched and isoprenoid tetraether lipids. Earth Planet. Sci. Lett. 224, 107–116 (2004)

  18. 18

    Sluijs, A. et al. Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum. Nature doi:10.1038/nature04668 (this issue)

  19. 19

    Schouten, S., Hopmans, E. C., Schefuß, E. & Sinninghe Damsté, J. S. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet. Sci. Lett. 204, 265–274 (2002)

  20. 20

    Wuchter, C., Schouten, S., Coolen, M. J. L. & Sinninghe Damsté, J. S. Temperature-dependent variation in the distribution of tetraether membrane lipids of marine Crenarchaeota: Implications for TEX86 paleothermometry. Paleoceanography 19, doi:10.1029/2004PA001041 (2004)

  21. 21

    Powers, L. A. et al. Crenarchaeotal membrane lipids in lake sediments: A new paleotemperature proxy for continental paleoclimate reconstruction? Geology 32, 613–616 (2004)

  22. 22

    Greenwood, D. R. & Wing, S. L. Eocene continental climates and latitudinal temperature gradients. Geology 23, 1044–1048 (1995)

  23. 23

    Markwick, P. J. Fossil crocodilians as indicators of Late Cretaceous and Cenozoic climates: Implications for using palaeontological data in reconstructing palaeoclimate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 137, 205–271 (1998)

  24. 24

    Tripati, A., Zachos, J., Marincovich, L. Jr & Bice, K. Late Paleocene Arctic coastal climate inferred from molluscan stable and radiogenic isotope ratios. Palaeogeogr. Palaeoclimatol. Palaeoecol. 170, 101–113 (2001)

  25. 25

    Jahren, A. H. & Sternberg, L. S. L. Humidity estimate for the middle Eocene Arctic rain forest. Geology 31, 463–466 (2003)

  26. 26

    Fricke, H. C. & Wing, S. L. Oxygen isotope and paleobotanical estimates of temperature and δ18O-latitude gradients over North America during the early Eocene. Am. J. Sci. 304, 612–635 (2004)

  27. 27

    Huber, M. & Nof, D. The ocean circulation in the southern hemisphere and its climatic impacts in the Eocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 231, 9–28 (2006)

  28. 28

    Sloan, L. C. & Rea, D. K. Atmospheric carbon dioxide and early Eocene climate: A general circulation modeling sensitivity study. Palaeogeogr. Palaeoclimatol. Palaeoecol. 119, 275–292 (1996)

  29. 29

    Pagani, M., Zachos, J. C., Freeman, K. H., Tipple, B. & Bohaty, S. Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309, 600–603 (2005)

  30. 30

    Pearson, P. N. & Palmer, M. R. Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406, 695–699 (2000)

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H.B. thanks the Netherlands Organization for Scientific Research (NWO) and Utrecht University for enabling participation in the ACEX expedition. A.S. thanks the Utrecht Biogeology Centre for funding. M.H. thanks the Purdue Research Foundation for funding. This research used samples and data provided by the Integrated Ocean Drilling Program (IODP). We thank L. Bik, T. Brain, S. Gibbons, P. Goggin, N. Holloway, J. van Tongeren, N. Welters and M. Woltering for technical support and L.J. Lourens, H. Nohr-Hansen, M. Pagani, C.E. Stickley, G.L. Williams and J.C. Zachos for discussions. Author Contributions H.B., A.S., F.S. and J.S.E. carried out the palynology, S.S. and J.S.S.D. the TEX86 and BIT analyses, M.E.C., J.v.d.B. and H.v.K.-v.C. the palaeobotany, J.O. and K.T. generated siliceous microfossil numbers, while R.S. generated the TOC data. M.H. carried out the comparison to climate models. J.B. and K.M. were co-chiefs on the ACEX. J.P.B. and H.B. compiled the unpublished industrial palynological records. All authors contributed to writing the paper.

Author information


  1. Laboratory of Palaeobotany and Palynology, Palaeoecology, Institute of Environmental Biology, Utrecht University, Budapestlaan 4, 3584 CD, Utrecht, The Netherlands

    • Henk Brinkhuis
    • , Appy Sluijs
    • , Johan van der Burgh
    • , André F. Lotter
    • , Francesca Sangiorgi
    • , Han van Konijnenburg-van Cittert
    •  & Jan W. de Leeuw
  2. Department of Marine Biogeochemistry and Toxicology, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB, DenBurg, Texel, The Netherlands

    • Stefan Schouten
    • , Jaap S. Sinninghe Damsté
    • , Francesca Sangiorgi
    •  & Jan W. de Leeuw
  3. Department of Geology, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK

    • Margaret E. Collinson
  4. Department of Earth Sciences, Utrecht University, Budapestlaan 4, 3584 CD, Utrecht, The Netherlands

    • Jaap S. Sinninghe Damsté
  5. Department of Earth Sciences, Rice University, Houston, 6100 Main Street, Texas, 77005, USA

    • Gerald R. Dickens
  6. Earth and Atmospheric Sciences Department and the Purdue Climate Change Research Center, Purdue University, 550 Stadium Mall Drive, Indiana, 47906, West Lafayette, USA

    • Matthew Huber
  7. USGS National Center, Reston, 12201 Sunrise Valley Drive, Virginia, 20192, USA

    • Thomas M. Cronin
  8. Department of Earth and Planetary Sciences, Kyushu University, Fukuoka, 812-8581, Japan

    • Jonaotaro Onodera
    •  & Kozo Takahashi
  9. Bujak Research International, Blackpool, 105 North Park Drive, FY3 8NE, UK

    • Jonathan P. Bujak
  10. Alfred Wegener Institute for Polar and Marine Research, Columbusstrasse, 27568, Bremerhaven, Germany

    • Ruediger Stein
    •  & Jens Matthiessen
  11. Shell UK Exploration and Production, 1 Altens Farm Road, AB12 3FY, Nigg, Aberdeen, UK

    • James S. Eldrett
  12. School of Ocean & Earth Science, Southampton Oceanography Centre, University of Southampton, European Way, SO14 3ZH, Southampton, UK

    • Ian C. Harding
  13. Earth Science, Southampton Oceanography Centre, University of Southampton, European Way

    • Ian C. Harding
  14. National Museum of Natural History, ‘Naturalis’, PO Box 9517, 2300 RA, Leiden, The Netherlands

    • Han van Konijnenburg-van Cittert
  15. Department of Geology and Geochemistry, Stockholm University, SE-10691, Stockholm, Sweden

    • Jan Backman
  16. University of Rhode Island, Bay Campus, Rhode Island, 02882, Narragansett, USA

    • Kathryn Moran


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  1. the Expedition 302 Scientists

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    Reprints and permissions information is available at The authors declare no competing financial interests.

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    Correspondence to Henk Brinkhuis.

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