Changes in ocean denitrification during Late Carboniferous glacial–interglacial cycles

Article metrics


Denitrification (the process by which nitrate and nitrite are reduced to nitrogen gas) in the oxygen-minimum zones of modern oceans is an important part of the global nitrogen cycle. Variations in rates of denitrification over Quaternary glacial–interglacial timescales may have affected global climate. Evidence of denitrification has been reported from some older marine systems, but it is unclear whether denitrification rates varied during pre-Quaternary glacial cycles. Here we present ratios of organic carbon to nitrogen and nitrogen isotope data from the Upper Carboniferous black shales of the North American mid-continent. In these cyclic deposits, we find evidence of variations in the intensity of denitrification in the eastern tropical Panthalassic Ocean associated with glacially driven sea-level changes. Sedimentary δ15N increases during the interval of rapid sea-level rise in each cycle, indicative of intensified denitrification, before returning to background levels as sea level stabilized during the interglacial phase. Nearly identical patterns of denitrification have been observed in the eastern tropical Pacific during the Quaternary period. We therefore conclude that ice ages have produced similar oceanographic conditions and nitrogen cycle dynamics in these regions over the past 300 million years.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Palaeogeography of Late Carboniferous North America during interglacial sea-level highstands.
Figure 2: Study sections.
Figure 3: δ15Ntot versus δ13Corg for study units.
Figure 4: Sea-level curve and upwelling-zone δ15N data for 20 kyr BP to present.


  1. 1

    Soreghan, G. S. & Giles, K. A. Amplitudes of Late Pennsylvanian glacioeustasy. Geology 27, 255–258 (1999).

  2. 2

    Joachimski, M. M., von Bitter, P. H. & Buggisch, W. Constraints on Pennsylvanian glacio-eustatic sea-level changes using oxygen isotopes of conodont apatite. Geology 34, 277–280 (2006).

  3. 3

    Heckel, P. H. Sea-level curve for Pennsylvanian eustatic marine transgressive-regressive depositional cycles along midcontinent outcrop belt, North America. Geology 14, 330–334 (1986).

  4. 4

    Heckel, P. H. in Modern and Ancient Continental Shelf Anoxia (eds Tyson, R. V. & Pearson, T. H.) 259–273 (Spec. Publ. 58, Geol. Soc. London, Oxford, 1991).

  5. 5

    Algeo, T. J., Schwark, L. & Hower, J. C. High-resolution geochemistry and sequence stratigraphy of the Hushpuckney Shale (Swope Formation, eastern Kansas): Implications for climato-environmental dynamics of the Late Pennsylvanian Midcontinent Sea. Chem. Geol. 206, 259–288 (2004).

  6. 6

    Algeo, T. J., Heckel, P. H., Maynard, J. B., Blakey, R. & Rowe, H. in Dynamics of Epeiric Seas: Sedimentological, Paleontological and Geochemical Perspectives (eds Holmden, C & Pratt, B R) (Spec. Publ., Geol. Assoc., Canada, 2007) in the press.

  7. 7

    Meyers, P. A. Preservation of elemental and isotopic source identification of sedimentary organic matter. Chem. Geol. 114, 289–302 (1994).

  8. 8

    Prokopenko, M. G. et al. Nitrogen cycling in the sediments of Santa Barbara basin and Eastern Subtropical North Pacific: Nitrogen isotopes, diagenesis and possible chemosymbiosis between two lithotrophs (Thioploca and Anammox)—riding on a glider. Earth Planet. Sci. Lett. 242, 186–204 (2006).

  9. 9

    Hansell, D. A. & Waterhouse, T. Y. Controls on the distributions of organic carbon and nitrogen in the eastern Pacific Ocean. Deep-Sea Res. I 44, 843–857 (1997).

  10. 10

    Copin-Montégut, C. Consumption and production on scales of a few days of inorganic carbon, nitrate and oxygen by the planktonic community: Results of continuous measurements at the Dyfamed Station in the northwestern Mediterranean Sea (May 1995). Deep-Sea Res. I 47, 447–477 (2000).

  11. 11

    François, R., Altabet, M. A. & Burckle, L. H. Glacial to interglacial changes in surface nitrate utilization in the Indian section of the Southern Ocean as recorded by sediment δ15N. Paleoceanography 7, 589–606 (1992).

  12. 12

    Altabet, M. A., François, 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).

  13. 13

    Altabet, M. A., Higginson, M. J. & Murray, D. W. The effect of millennial-scale changes in Arabian Sea denitrification on atmospheric CO2 . Nature 415, 159–162 (2002).

  14. 14

    Suthhof, A., Ittekkot, V. & Gaye-Haake, B. Millennial-scale oscillation of denitrification intensity in the Arabian Sea during the late Quaternary and its potential influence on atmospheric N2O and global climate. Glob. Biogeochem. Cycles 15, 637–649 (2001).

  15. 15

    Ganeshram, R. S., Pedersen, T. F., Calvert, S. E., McNeill, G. W. & Fontugne, M. R. Glacial-interglacial variability in denitrification in the world’s oceans: Causes and consequences. Paleoceanography 15, 361–376 (2000).

  16. 16

    Ganeshram, R., Pedersen, T., Calvert, S. & François, R. Reduced nitrogen fixation in the glacial ocean inferred from changes in marine nitrogen and phosphorus inventories. Nature 415, 156–159 (2002).

  17. 17

    Pride, C. et al. Nitrogen isotopic variations in the Gulf of California since the last deglaciation: Response to global climate change. Paleoceanography 14, 397–409 (1999).

  18. 18

    Kienast, S. S., Calvert, S. E. & Pedersen, T. Nitrogen isotope and productivity variations along the northeast Pacific margin over the last 120 kyr: Surface and subsurface paleoceanography. Paleoceanography 17, 1–17 (2002).

  19. 19

    Thunell, R. C. & Kepple, A. B. Glacial-Holocene δ15N record from the Gulf of Tehuantepec, Mexico: Implications for denitrification in the eastern equatorial Pacific and changes in atmospheric N2O. Glob. Biogeochem. Cycles 18, GB1001 (2004).

  20. 20

    Voss, M., Dippner, J. W. & Montoya, J. P. Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical Pacific Ocean. Deep-Sea Res. I 48, 1905–1921 (2001).

  21. 21

    Altabet, M. A. & François, R. Sedimentary nitrogen isotopic ratio as a recorder for surface ocean nitrate utilization. Glob. Biogeochem. Cycles 8, 103–116 (1994).

  22. 22

    Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997).

  23. 23

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

  24. 24

    Sigman, D. M., Altabet, M. A., François, R., McCorkle, D. C. & Gaillard, J.-F. The isotopic composition of diatom-bound nitrogen in Southern Ocean sediments. Paleoceanography 14, 118–134 (1999).

  25. 25

    Sigman, D. M., Altabet, M. A., McCorkle, D. C., François, R. & Fischer, G. The δ15N of nitrate in the Southern Ocean: Consumption of nitrate in surface waters. Glob. Biogeochem. Cycles 13, 1149–1166 (1999).

  26. 26

    Holmes, M. E., Fischer, G., Lavik, G. & Wefer, G. in South Atlantic in the Late Quaternary; Reconstruction of Material Budgets and Current Systems (eds Mulitza, S. & Ratmeyer, V.) 143–165 (Springer, Berlin, 2003).

  27. 27

    Murray, J. W., Fuchsman, C., Kirkpatrick, J., Paul, B. & Konovalov, S. K. Species and δ15N signatures of nitrogen transformations in the suboxic zone of the Black Sea. Oceanography 18, 36–47 (2005).

  28. 28

    Liu, Z., Altabet, M. A. & Herbert, T. D. Glacial–interglacial modulation of eastern tropical North Pacific denitrification over the last 1.8-Myr. Geophys. Res. Lett. 32, L23607 (2005).

  29. 29

    Higginson, M. J., Maxwell, J. R. & Altabet, M. A. Nitrogen isotope and chlorin paleoproductivity records from the Northern South China Sea: Remote versus local forcing of millennial- and orbital-scale variability. Mar. Geol. 201, 223–250 (2003).

  30. 30

    Siddall, M. et al. Sea-level fluctuations during the last glacial cycle. Nature 423, 853–858 (2003).

  31. 31

    Andreasen, D. H., Ravelo, A. C. & Broccoli, A. J. Remote forcing at the Last Glacial Maximum in the tropical Pacific Ocean. J. Geophy. Res. 106, 879–897 (2001).

  32. 32

    Meissner, K. J., Galbraith, E. D. & Volker, C. Denitrification under glacial and interglacial conditions: A physical approach. Paleoceanography 20, PA3001 (2005).

  33. 33

    Zheng, Y., van Geen, A., Anderson, R., Gardner, J. & Dean, W. Intensification of the northeast Pacific oxygen minimum zone during the Bölling/Allerød warm period. Paleoceanography 15, 528–536 (2000).

  34. 34

    Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997).

  35. 35

    Sigman, D. M. et al. Distinguishing between water column and sedimentary denitrification in the Santa Barbara Basin using the stable isotopes of nitrate. Geochem. Geophys. Geosyst. 4, 1040 (2003).

  36. 36

    Lehmann, M. F., Bernasconi, S. M., Barbieri, A. & McKenzie, J. A. Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochim. Cosmochim. Acta 66, 3573–3584 (2002).

  37. 37

    Naqvi, S. W. A. et al. Budgetary and biogeochemical implications of N2O isotope signatures in the Arabian Sea. Nature 394, 462–464 (1998).

  38. 38

    Lashof, D. A. & Ahuja, R. D. Relative contributions of greenhouse gas emissions to global warming. Nature 344, 529–531 (1990).

  39. 39

    Flückiger, J. et al. Variations in atmospheric N2O concentration during abrupt climatic changes. Science 285, 227–230 (1999).

  40. 40

    Jenkyns, H. C., Gröcke, D. R. & Hesselbo, S. P. Nitrogen isotope evidence for water mass denitrification during the early Toarcian (Jurassic) oceanic anoxic event. Paleoceanography 16, 593–603 (2001).

  41. 41

    Rau, G. H., Arthur, M. A. & Dean, W. E. 15N/14N variations in Cretaceous Atlantic sedimentary sequences: Implication for past changes in marine nitrogen biogeochemistry. Earth Planet. Sci. Lett. 82, 269–279 (1987).

  42. 42

    Saelen, G., Tyson, R. V., Telnaes, N. & Talbot, M. R. Contrasting watermass conditions during deposition of the Whitby Mudstone (Lower Jurassic) and Kimmeridge Clay (Upper Jurassic) formations, UK. Palaeogeogr. Palaeoclimatol. Palaeoecol. 163, 163–196 (2000).

  43. 43

    Junium, C. K. & Arthur, M. A. Nitrogen cycling during the Cretaceous, Cenomanian-Turonian Oceanic Anoxic Event II. Geochem. Geophys. Geosyst. 8, Q03002 (2007).

  44. 44

    Thunell, R. C., Sigman, D. M., Muller-Karger, F., Astor, Y. & Varela, R. Nitrogen isotope dynamics of the Cariaco Basin, Venezuela. Glob. Biogeochem. Cycles 18, GB3001 (2004).

  45. 45

    Emmer, E. & Thunell, R. C. Nitrogen isotopic variation in Santa Barbara Basin sediments: Implications for denitrification in the Eastern Tropical North Pacific during the last 50,000 years. Paleoceanography 15, 377–387 (2000).

Download references


We thank W. Lynn Watney and the Kansas Geological Survey for access to the study cores, T. Phillips for drafting services and M. Altabet for a review of the manuscript. This project was supported by grants to T.J.A. from the National Science Foundation (EAR-0310072, EAR-0618003 and EAR-0745574) and the University of Cincinnati Research Council.

Author information

Correspondence to Thomas Algeo.

Supplementary information

Supplementary Information

Supplementary figures S1-S5 (PDF 1358 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Algeo, T., Rowe, H., Hower, J. et al. Changes in ocean denitrification during Late Carboniferous glacial–interglacial cycles. Nature Geosci 1, 709–714 (2008) doi:10.1038/ngeo307

Download citation

Further reading