Changes in North Atlantic nitrogen fixation controlled by ocean circulation

Abstract

In the ocean, the chemical forms of nitrogen that are readily available for biological use (known collectively as ‘fixed’ nitrogen) fuel the global phytoplankton productivity that exports carbon to the deep ocean1,2,3. Accordingly, variation in the oceanic fixed nitrogen reservoir has been proposed as a cause of glacial–interglacial changes in atmospheric carbon dioxide concentration2,3. Marine nitrogen fixation, which produces most of the ocean’s fixed nitrogen, is thought to be affected by multiple factors, including ocean temperature4 and the availability of iron2,3,5 and phosphorus6. Here we reconstruct changes in North Atlantic nitrogen fixation over the past 160,000 years from the shell-bound nitrogen isotope ratio (15N/14N) of planktonic foraminifera in Caribbean Sea sediments. The observed changes cannot be explained by reconstructed changes in temperature, the supply of (iron-bearing) dust or water column denitrification. We identify a strong, roughly 23,000-year cycle in nitrogen fixation and suggest that it is a response to orbitally driven changes in equatorial Atlantic upwelling7, which imports ‘excess’ phosphorus (phosphorus in stoichiometric excess of fixed nitrogen) into the tropical North Atlantic surface5,6. In addition, we find that nitrogen fixation was reduced during glacial stages 6 and 4, when North Atlantic Deep Water had shoaled to become glacial North Atlantic intermediate water8, which isolated the Atlantic thermocline from excess phosphorus-rich mid-depth waters that today enter from the Southern Ocean. Although modern studies have yielded diverse views of the controls on nitrogen fixation1,2,4,5, our palaeobiogeochemical data suggest that excess phosphorus is the master variable in the North Atlantic Ocean and indicate that the variations in its supply over the most recent glacial cycle were dominated by the response of regional ocean circulation to the orbital cycles.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Core locations, surface winds, excess P at 20-m depth and main surface currents.
Figure 2: FB-δ15N in ODP Site 999 and its relationship to SST, dust flux and water column denitrification.
Figure 3: Comparison of FB-δ15N with changes in precession-paced equatorial Atlantic upwelling and glacial–interglacial Atlantic intermediate water source.
Figure 4: Effect of changes in glacial–interglacial circulation on N fixation in the Atlantic.

References

  1. 1

    Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008)

    CAS  ADS  Article  Google Scholar 

  2. 2

    Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997)

    CAS  ADS  Article  Google Scholar 

  3. 3

    Broecker, W. S. & Henderson, G. M. The sequence of events surrounding Termination II and their implications for the cause of glacial-interglacial CO2 changes. Paleoceanography 13, 352–364 (1998)

    ADS  Article  Google Scholar 

  4. 4

    Houlton, B. Z., Wang, Y., Vitousek, P. M. & Field, C. B. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008)

    CAS  ADS  Article  Google Scholar 

  5. 5

    Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci. 2, 867–871 (2009)

    CAS  ADS  Article  Google Scholar 

  6. 6

    Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007)

    CAS  ADS  Article  Google Scholar 

  7. 7

    Molfino, B. & McIntyre, A. Precessional forcing of nutricline dynamics in the equatorial Atlantic. Science 249, 766–769 (1990)

    CAS  ADS  Article  Google Scholar 

  8. 8

    Piotrowski, A. M., Goldstein, S. L., Hemming, S. R. & Fairbanks, R. G. Temporal relationships of carbon cycling and ocean circulation at glacial boundaries. Science 307, 1933–1938 (2005)

    CAS  ADS  Article  Google Scholar 

  9. 9

    Brandes, J. A., Devol, A. H., Yoshinari, T., Jayakumar, D. A. & Naqvi, S. W. A. Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: a tracer for mixing and nitrogen cycles. Limnol. Oceanogr. 43, 1680–1689 (1998)

    CAS  ADS  Article  Google Scholar 

  10. 10

    Brandes, J. A. & Devol, A. H. A global marine-fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Glob. Biogeochem. Cycles 16, 1120 (2002)

  11. 11

    Altabet, M. A., Francois, R., Murray, D. W. & Prell, W. L. Climate-related variations in denitrification in the Arabian Sea from sediment 15N/14N ratios. Nature 373, 506–509 (1995)

    CAS  ADS  Article  Google Scholar 

  12. 12

    Christensen, J. P. Carbon export from continental shelves, denitrification and atmospheric carbon dioxide. Cont. Shelf Res. 14, 547–576 (1994)

    ADS  Article  Google Scholar 

  13. 13

    Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999)

    CAS  ADS  Article  Google Scholar 

  14. 14

    Knapp, A. N., DiFiore, P. J., Deutsch, C., Sigman, D. M. & Lipschultz, F. Nitrate isotopic composition between Bermuda and Puerto Rico: implications for N2 fixation in the Atlantic Ocean. Glob. Biogeochem. Cycles 22, GB3014 (2008)

    ADS  Article  Google Scholar 

  15. 15

    Ren, H. et al. Foraminiferal isotope evidence of reduced nitrogen fixation in the ice age Atlantic Ocean. Science 323, 244–248 (2009)

    CAS  Article  Google Scholar 

  16. 16

    Ren, H., Sigman, D. M., Thunell, R. C. & Prokopenko, M. G. Nitrogen isotopic composition of planktonic foraminifera from the modern ocean and recent sediments. Limnol. Oceanogr. 57, 1011–1024 (2012)

    CAS  ADS  Article  Google Scholar 

  17. 17

    Meckler, A. N. et al. Deglacial nitrogen isotope changes in the Gulf of Mexico: evidence from bulk sedimentary and foraminifera-bound nitrogen in Orca Basin sediments. Paleoceanography 26, PA4216 (2011)

    ADS  Article  Google Scholar 

  18. 18

    Ren, H., Sigman, D. M., Chen, M. C. & Kao, S. Elevated foraminifera-bound nitrogen isotopic composition during the last ice age in the South China Sea and its global and regional implications. Glob. Biogeochem. Cycles 26, GB1031 (2012)

    ADS  Article  Google Scholar 

  19. 19

    Imbrie, J. et al. On the structure and origin of major glaciation cycles 1. Linear responses to Milankovitch forcing. Paleoceanography 7, 701–738 (1992)

    ADS  Article  Google Scholar 

  20. 20

    Schmidt, M. W., Vautravers, M. J. & Spero, H. J. Western Caribbean sea surface temperatures during the late Quaternary. Geochem. Geophys. Geosyst. 7, Q02P10 (2006)

    Article  Google Scholar 

  21. 21

    Tiedemann, R., Sarnthein, M. & Shackleton, N. J. Astronomic timescale for the Pliocene Atlantic δ18O and dust flux records of Ocean Drilling Program site 659. Paleoceanography 9, 619–638 (1994)

    ADS  Article  Google Scholar 

  22. 22

    deMenocal, P. B., Ruddiman, W. F. & Pokras, E. M. Influences of high- and low-latitude processes on African terrestrial climate: Pleistocene eolian records from equatorial Atlantic Ocean Drilling Program Site 663. Paleoceanography 8, 209–242 (1993)

    ADS  Article  Google Scholar 

  23. 23

    Mora, G. & Martínez, J. I. Sedimentary metal ratios in the Colombia Basin as indicators for water balance change in northern South America during the past 400,000 years. Paleoceanography 20, PA4013 (2005)

    ADS  Article  Google Scholar 

  24. 24

    Pokras, E. M. & Mix, A. C. Earth’s precession cycle and Quaternary climatic change in tropical Africa. Nature 326, 486–487 (1987)

    ADS  Article  Google Scholar 

  25. 25

    Coles, V. J. & Hood, R. R. Modeling the impact of iron and phosphorus limitations on nitrogen fixation in the Atlantic Ocean. Biogeosciences 4, 455–479 (2007)

    CAS  ADS  Article  Google Scholar 

  26. 26

    Subramaniam, A., Mahaffey, C., Johns, W. & Mahowald, N. Equatorial upwelling enhances nitrogen fixation in the Atlantic Ocean. Geophys. Res. Lett. 40, 1766–1771 (2013)

    ADS  Article  Google Scholar 

  27. 27

    Harris, S. E. & Mix, A. C. Pleistocene precipitation balance in the Amazon basin recorded in deep sea sediments. Quat. Res. 51, 14–26 (1999)

    Article  Google Scholar 

  28. 28

    Marchitto, T. M., Curry, W. B. & Oppo, D. W. Millennial-scale changes in North Atlantic circulation since the last glaciation. Nature 393, 557–561 (1998)

    CAS  ADS  Article  Google Scholar 

  29. 29

    Ganeshram, R. S., Pedersen, T. F., Calvert, S. E. & Murray, D. W. Large changes in oceanic nutrient inventories from glacial to interglacial periods. Nature 376, 755–758 (1995)

    CAS  ADS  Article  Google Scholar 

  30. 30

    Jia, G. & Li, Z. Easterly denitrification signal and nitrogen fixation feedback documented in the western Pacific sediments. Geophys. Res. Lett. 38, L24605 (2011)

    ADS  Article  Google Scholar 

  31. 31

    Yu, J. et al. An evaluation of benthic foraminiferal B/Ca and δ11B for deep ocean carbonate ion and pH reconstructions. Earth Planet. Sci. Lett. 293, 114–120 (2010)

    CAS  ADS  Article  Google Scholar 

  32. 32

    Marchitto, T. M. & Broecker, W. S. Deep water mass geometry in the glacial Atlantic Ocean: a review of constraints from the paleonutrient proxy Cd/Ca. Geochem. Geophys. Geosyst. 7, Q12003 (2006)

    ADS  Google Scholar 

  33. 33

    Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal. Chem. 61, 2715–2718 (1989)

    CAS  Article  Google Scholar 

  34. 34

    Sigman, D. M. et al. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 73, 4145–4153 (2001)

    CAS  Article  Google Scholar 

  35. 35

    Schmidt, D. W., Spero, H. J. & Lea, D. W. Links between salinity variation in the Caribbean and North Atlantic thermohaline circulation. Nature 428, 160–163 (2004)

    CAS  ADS  Article  Google Scholar 

  36. 36

    Lisiecki, L. E. & Raymo, M. E. A. Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20, PA1003 (2005)

    ADS  Google Scholar 

  37. 37

    Sarnthein, M. & Tiedemann, R. Toward a high-resolution stable isotope stratigraphy of the last 3.4 million years: Sites 658 and 659 off Northwest Africa. Proc. ODP Sci. Res. 108, 167–661 (1989)

    Google Scholar 

  38. 38

    deMenocal, P. et al. Abrupt onset and termination of the African Humid Period: rapid climate responses to gradual insolation forcing. Quat. Sci. Rev. 19, 347–361 (2000)

    ADS  Article  Google Scholar 

  39. 39

    Adkins, J., deMenocal, P. & Eshel, G. The “African humid period” and the record of marine upwelling from excess 230Th in Ocean Drilling Program Hole 658C. Paleoceanography 21, PA4203 (2006)

    ADS  Article  Google Scholar 

  40. 40

    Tjallingii, R. Application and Quality of X-Ray Fluorescence Core Scanning in Reconstructing Late Pleistocene NW African Continental Margin Sedimentation Patterns and Paleoclimate Variations 65–84. PhD thesis, Univ. Bremen. (2006)

  41. 41

    Tjallingii, R. et al. Coherent high- and low-latitude control of the northwest African hydrological balance. Nature Geosci. 1, 670–675 (2008)

    CAS  ADS  Article  Google Scholar 

  42. 42

    Matthewson, A. P., Shimmield, G. B., Kroon, D. & Fallick, A. E. A 300-kyr high-resolution aridity record of the North-African continent. Paleoceanography 10, 677–692 (1995)

    ADS  Article  Google Scholar 

  43. 43

    Holz, C., Stuut, J. B. W. & Henrich, R. Terrigenous sedimentation processes along the continental margin off NW Africa: implications from grain-size analysis of seabed sediments. Sedimentology 51, 1145–1154 (2004)

    ADS  Article  Google Scholar 

  44. 44

    Garcia, H. E. et al. World Ocean Atlas 2009 Vol. 4, 398 (Government Printing Office, 2010)

  45. 45

    Schlitzer, R. Ocean Data View. http://odv.awi.de (2012)

Download references

Acknowledgements

We thank M. A. Weigand, S. Oleynik and S. Bishop for technical assistance and U. Röhl and V. Lukies for X-ray fluorescence scanning support. Funding was from SNF grant 200021-131886/1, US NSF grant OCE-1060947 and the Grand Challenges Program of Princeton University. This research used samples provided by the ODP, which is sponsored by the NSF and participating countries under the management of the Joint Oceanographic Institutions. X-ray fluorescence scanning was supported by the DFG-Leibniz Center for Surface Process and Climate Studies at the University of Potsdam.

Author information

Affiliations

Authors

Contributions

M.S., D.M.S. and G.H.H. designed the study. M.S. performed the FB-δ15N analysis and wrote the first version of the manuscript with D.M.S.; A.N.M. generated the Zr/Al record at ODP Site 658. A.M.-G. performed the statistical analysis of the data with M.S.; H.R. was involved in the laboratory and data analysis. All authors contributed to the interpretation of the data and provided significant input to the final manuscript.

Corresponding author

Correspondence to Marietta Straub.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-12, a Supplementary Discussion and Supplementary References. (PDF 1499 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Straub, M., Sigman, D., Ren, H. et al. Changes in North Atlantic nitrogen fixation controlled by ocean circulation. Nature 501, 200–203 (2013). https://doi.org/10.1038/nature12397

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.