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.

Changes in global nitrogen cycling during the Holocene epoch

Nature volume 495, pages 352–355 (2013)Cite this article

Subjects

Abstract

Human activities have doubled the pre-industrial supply of reactive nitrogen on Earth, and future rates of increase are expected to accelerate1. Yet little is known about the capacity of the biosphere to buffer increased nitrogen influx. Past changes in global ecosystems following deglaciation at the end of the Pleistocene epoch provide an opportunity to understand better how nitrogen cycling in the terrestrial biosphere responded to changes in carbon cycling. We analysed published records of stable nitrogen isotopic values (δ15N) in sediments from 86 lakes on six continents. Here we show that the value of sedimentary δ15N declined from 15,000 years before present to 7,056 ± 597 years before present, a period of increasing atmospheric carbon dioxide concentrations and terrestrial carbon accumulation2. Comparison of the nitrogen isotope record with concomitant carbon accumulation on land and nitrous oxide in the atmosphere suggests millennia of declining nitrogen availability in terrestrial ecosystems during the Pleistocene–Holocene transition around 11,000 years before present. In contrast, we do not observe a consistent change in global sedimentary δ15N values during the past 500 years, despite the potential effects of changing temperature and nitrogen influx from anthropogenic sources. We propose that the lack of a single response may indicate that modern increases in atmospheric carbon dioxide and net carbon sequestration in the biosphere have the potential to offset recent increased supplies of reactive nitrogen in some ecosystems.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Figure 1: Locations of the 86 sites analysed for lacustrine sedimentary δ15N in this study.
Figure 2: Changes in lacustrine sedimentary δ15N during the late Pleistocene and Holocene.
Figure 3: Three local environmental variables explain site-specific trajectories of sedimentary δ15N in the past 500 yr.
Figure 4: Conceptual diagram of hypothesized drivers of isotopic signatures of sedimentary N.

References

  1. Galloway, J. N. et al. Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226 (2004)

    CAS  Google Scholar 

  2. Schmitt, J. et al. Carbon isotope constraints on the deglacial CO2 rise from ice cores. Science 336, 711–714 (2012)

    ADS  CAS  PubMed  Google Scholar 

  3. Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Dentener, F. et al. Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob. Biogeochem. Cycles 20, GB4003, http://dx.doi.org/10.1029/2005GB002672 (2006)

    ADS  Google Scholar 

  5. Rockström, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009)

    ADS  PubMed  Google Scholar 

  6. Davidson, E. A. et al. Excess Nitrogen in the U.S. Environment: Trends, Risks, and Solutions Vol. 15 (Ecological Society of America, 2012)

  7. Bernal, S., Hedin, L. O., Likens, G. E., Gerber, S. & Buso, D. C. Complex response of the forest nitrogen cycle to climate change. Proc. Natl Acad. Sci. USA 109, 3406–3411 (2012)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Craine, J. M. et al. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980–992 (2009)

    CAS  PubMed  Google Scholar 

  9. Bai, E. & Houlton, B. Z. Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Glob. Biogeochem. Cycles 23, GB2011, http://dx.doi.org/10.1029/2008GB003361 (2009)

    ADS  Google Scholar 

  10. McLauchlan, K. K., Ferguson, C. J., Wilson, I. E., Ocheltree, T. W. & Craine, J. M. Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytol. 187, 1135–1145 (2010)

    CAS  PubMed  Google Scholar 

  11. Hietz, P. et al. Long-term change in the nitrogen cycle of tropical forests. Science 334, 664–666 (2011)

    ADS  CAS  PubMed  Google Scholar 

  12. Perakis, S. S., Sinkhorn, E. R. & Compton, J. E. δ15N constraints on long-term nitrogen balances in temperate forests. Oecologia 167, 793–807 (2011)

    ADS  PubMed  Google Scholar 

  13. Mayr, C. et al. Isotopic fingerprints on lacustrine organic matter from Laguna Potrok Aike (southern Patagonia, Argentina) reflect environmental changes during the last 16,000 years. J. Paleolimnol. 42, 81–102 (2009)

    ADS  Google Scholar 

  14. Houlton, B. Z. & Bai, E. Imprint of denitrifying bacteria on the global terrestrial biosphere. Proc. Natl Acad. Sci. USA 106, 21713–21716 (2009)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. McLauchlan, K. K., Craine, J. M., Oswald, W. W., Leavitt, P. R. & Likens, G. E. Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc. Natl Acad. Sci. USA 104, 7466–7470 (2007)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sanderson, E. W. et al. The human footprint and the last of the wild. Bioscience 52, 891–904 (2002)

    Google Scholar 

  17. Prentice, I. C., Harrison, S. P. & Bartlein, P. J. Global vegetation and terrestrial carbon cycle changes after the last ice age. New Phytol. 189, 988–998 (2011)

    CAS  PubMed  Google Scholar 

  18. Engstrom, D. R., Fritz, S. C., Almendinger, J. E. & Juggins, S. Chemical and biological trends during lake evolution in recently deglaciated terrain. Nature 408, 161–166 (2000)

    ADS  CAS  PubMed  Google Scholar 

  19. Bunting, L., Leavitt, P. R., Weidman, R. P. & Vinebrooke, R. D. Regulation of the nitrogen biogeochemistry of mountain lakes by subsidies of terrestrial dissolved organic matter and the implications for climate studies. Limnol. Oceanogr. 55, 333–345 (2010)

    ADS  CAS  Google Scholar 

  20. Talbot, M. R. in Tracking Environmental Change Using Lake Sediments Vol. 2, Physical and Geochemical Methods (eds Last, W. M. & Smol, J. P. ) 401–439 (Kluwer Academic, 2001)

    Google Scholar 

  21. Högberg, P. Tansley Review No. 95 15N natural abundance in soil-plant systems. New Phytol. 137, 179–203 (1997)

    PubMed  Google Scholar 

  22. Perakis, S. S. & Sinkhorn, E. R. Biogeochemistry of a temperate forest nitrogen gradient. Ecology 92, 1481–1491 (2011)

    PubMed  Google Scholar 

  23. Schilt, A. et al. Glacial-interglacial and millennial-scale variations in the atmospheric nitrous oxide concentration during the last 800,000 years. Quat. Sci. Rev. 29, 182–192 (2010)

    ADS  Google Scholar 

  24. Petit, J. R. et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436 (1999)

    ADS  CAS  Google Scholar 

  25. Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Hastings, M. G., Sigman, D. M. & Steig, E. J. Glacial/interglacial changes in the isotopes of nitrate from the Greenland Ice Sheet Project 2 (GISP2) ice core. Glob Biogeochem. Cycles 19, GB4024, http://dx.doi.org/10.1029/2005GB002502 (2005)

    ADS  Google Scholar 

  28. Le Quéré, C. et al. Trends in the sources and sinks of carbon dioxide. Nature Geosci. 2, 831–836 (2009)

    ADS  Google Scholar 

  29. Holtgrieve, G. W. et al. A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the Northern Hemisphere. Science 334, 1545–1548 (2011)

    ADS  CAS  PubMed  Google Scholar 

  30. Xu-Ri & Prentice, I. C. Terrestrial nitrogen cycle simulation with a dynamic global vegetation model. Glob. Change Biol. 14, 1745–1764 (2008)

    ADS  Google Scholar 

  31. Nadelhoffer, K. J. & Fry, B. in Stable Isotopes in Ecology and Environmental Science (eds Lajtha, K. & Michener, R. H. ) 22–44 (Blackwell Scientific, 1994)

    Google Scholar 

  32. Brodie, C. R. et al. Evidence for bias in C/N, δ13C and δ15N values of bulk organic matter, and on environmental interpretation, from a lake sedimentary sequence by pre-analysis acid treatment methods. Quat. Sci. Rev. 30, 3076–3087 (2011)

    ADS  Google Scholar 

  33. Leavitt, P. R., Schindler, D. E., Paul, A. J., Hardie, A. K. & Schindler, D. W. Fossil pigment records of phytoplankton in trout-stocked alpine lakes. Can. J. Fish. Aquat. Sci. 51, 2411–2423 (1994)

    CAS  Google Scholar 

  34. Lascu, I., McLauchlan, K. K., Myrbo, A., Leavitt, P. R. & Banerjee, S. K. Sediment-magnetic evidence for last millennium drought conditions at the prairie-forest ecotone of northern United States. Palaeogeogr. Palaeoclimatol. Palaeoecol. 337–338, 99–107 (2012)

    Google Scholar 

  35. Laird, K., Cumming, B. & Nordin, R. A regional paleolimnological assessment of the impact of clear-cutting on lakes from the west coast of Vancouver Island, British Columbia. Can. J. Fish. Aquat. Sci. 58, 479–491 (2001)

    CAS  Google Scholar 

  36. Laird, K. & Cumming, B. A regional paleolimnological assessment of the impact of clear-cutting on lakes from the central interior of British Columbia. Can. J. Fish. Aquat. Sci. 58, 492–505 (2001)

    CAS  Google Scholar 

  37. Jeffers, E. S., Bonsall, M. B. & Willis, K. J. Stability in ecosystem functioning across a climatic threshold and contrasting forest regimes. PLoS One 6, e16134 (2011)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  38. Jeffers, E. S., Bonsall, M. B., Watson, J. E. & Willis, K. J. Climate change impacts on ecosystem functioning: evidence from an Empetrum heathland. New Phytol. 193, 150–164 (2012)

    PubMed  Google Scholar 

  39. Xu, Y. P. & Jaffe, R. Geochemical record of anthropogenic impacts on Lake Valencia, Venezuela. Appl. Geochem. 24, 411–418 (2009)

    CAS  Google Scholar 

  40. Wooller, M., Wang, Y. M. & Axford, Y. A multiple stable isotope record of Late Quaternary limnological changes and chironomid paleoecology from northeastern Iceland. J. Paleolimnol. 40, 63–77 (2008)

    ADS  Google Scholar 

  41. Wolfe, B. B. et al. Effect of varying oceanicity on early- to mid-Holocene palaeohydrology, Kola Peninsula, Russia: isotopic evidence from treeline lakes. Holocene 13, 153–160 (2003)

    ADS  Google Scholar 

  42. Wolfe, B. B., Edwards, T. W. D. & Aravena, R. Changes in carbon and nitrogen cycling during tree-line retreat recorded in the isotopic content of lacustrine organic matter, western Taimyr Peninsula, Russia. Holocene 9, 215–222 (1999)

    ADS  Google Scholar 

  43. Wolfe, A. P., Van Gorp, A. C. & Baron, J. S. Recent ecological and biogeochemical changes in alpine lakes of Rocky Mountain National Park (Colorado, USA): a response to anthropogenic nitrogen deposition. Geobiology 1, 153–168 (2003)

    CAS  Google Scholar 

  44. Wolfe, A. P., Cooke, C. A. & Hobbs, W. O. Are current rates of atmospheric nitrogen deposition influencing lakes in the Eastern Canadian Arctic? Arct. Antarct. Alp. Res. 38, 465–476 (2006)

    Google Scholar 

  45. Vreca, P. & Muri, G. Changes in accumulation of organic matter and stable carbon and nitrogen isotopes in sediments of two Slovenian mountain lakes (Lake Ledvica and Lake Planina), induced by eutrophication changes. Limnol. Oceanogr. 51, 781–790 (2006)

    ADS  CAS  Google Scholar 

  46. Teranes, J. L. & Bernasconi, S. M. The record of nitrate utilization and productivity limitation provided by δ15N values in lake organic matter — a study of sediment trap and core sediments from Baldeggersee, Switzerland. Limnol. Oceanogr. 45, 801–813 (2000)

    ADS  CAS  Google Scholar 

  47. Tenzer, G. E. et al. Sedimentary organic matter record of recent environmental changes in the St. Marys River ecosystem, Michigan-Ontario border. Org. Geochem. 30, 133–146 (1999)

    CAS  Google Scholar 

  48. Tareq, S. M., Kitagawa, H. & Ohta, K. Lignin biomarker and isotopic records of paleovegetation and climate changes from Lake Erhai, southwest China, since 18.5 ka BP. Quat. Int. 229, 47–56 (2011)

    Google Scholar 

  49. Talbot, M. R. & Johannessen, T. A high-resolution palaeoclimatic record for the last 27,500 years in tropical west Africa from the carbon and nitrogen isotopic composition of lacustrine organic matter. Earth Planet. Sci. Lett. 110, 23–37 (1992)

    ADS  CAS  Google Scholar 

  50. Talbot, M. R. & Laerdal, T. The Late Pleistocene-Holocene palaeolimnology of Lake Victoria, East Africa, based upon elemental and isotopic analyses of sedimentary organic matter. J. Paleolimnol. 23, 141–164 (2000)

    ADS  Google Scholar 

  51. Talbot, M. R., Jensen, N. B., Laerdal, T. & Filippi, M. L. Geochemical responses to a major transgression in giant African Lakes. J. Paleolimnol. 35, 467–489 (2006)

    ADS  Google Scholar 

  52. Street-Perrott, F. A. et al. Towards an understanding of late Quaternary variations in the continental biogeochemical cycle of silicon: multi-isotope and sediment-flux data for Lake Rutundu, Mt Kenya, East Africa, since 38 ka BP. J. Quat. Sci. 23, 375–387 (2008)

    Google Scholar 

  53. Selbie, D. T., Lewis, B. A., Smol, J. P. & Finney, B. P. Long-term population dynamics of the endangered Snake River sockeye salmon: evidence of past influences on stock decline and impediments to recovery. Trans. Am. Fisheries Soc. 136, 800–821 (2007)

    Google Scholar 

  54. Selbie, D. T. Climate change modulates structural and functional lake ecosystem responses to introduced anadromous salmon. Can. J. Fish. Aquat. Sci. 68, 675–692 (2011)

    CAS  Google Scholar 

  55. Schindler, D. E., Leavitt, P. R., Johnson, S. P. & Brock, C. S. A 500-year context for the recent surge in sockeye salmon (Oncorhynchus nerka) abundance in the Alagnak River, Alaska. Can. J. Fish. Aquat. Sci. 63, 1439–1444 (2006)

    Google Scholar 

  56. Schindler, D. E., Leavitt, P. R., Brock, C. S., Johnson, S. P. & Quay, P. D. Marine-derived nutrients, commercial fisheries, and production of salmon and lake algae in Alaska. Ecology 86, 3225–3231 (2005)

    Google Scholar 

  57. Saros, J. E., Michel, T. J., Interlandi, S. J. & Wolfe, A. P. Resource requirements of Asterionella formosa and Fragilaria crotonensis in oligotrophic alpine lakes: implications for recent phytoplankton community reorganizations. Can. J. Fish. Aquat. Sci. 62, 1681–1689 (2005)

    CAS  Google Scholar 

  58. Ryner, M., Gasse, F., Rumes, B. & Verschuren, D. Climatic and hydrological instability in semi-arid equatorial East Africa during the late Glacial to Holocene transition: a multi-proxy reconstruction of aquatic ecosystem response in northern Tanzania. Palaeogeogr. Palaeoclimatol. Palaeoecol. 248, 440–458 (2007)

    Google Scholar 

  59. Russell, J. M., McCoy, S. J., Verschuren, D., Bessems, I. & Huang, Y. Human impacts, climate change, and aquatic ecosystem response during the past 2000 yr at Lake Wandakara, Uganda. Quat. Res. 72, 315–324 (2009)

    CAS  Google Scholar 

  60. Routh, J., Meyers, P. A., Hjorth, T., Baskaran, M. & Hallberg, R. Sedimentary geochemical record of recent environmental changes around Lake Middle Marviken, Sweden. J. Paleolimnol. 37, 529–545 (2007)

    ADS  Google Scholar 

  61. Routh, J. et al. Sedimentary geochemical record of human-induced environmental changes in the Lake Brunnsviken watershed, Sweden. Limnol. Oceanogr. 49, 1560–1569 (2004)

    ADS  CAS  Google Scholar 

  62. Routh, J., Choudhary, P., Meyers, P. A. & Kumar, B. A sediment record of recent nutrient loading and trophic state change in Lake Norrviken, Sweden. J. Paleolimnol. 42, 325–341 (2009)

    ADS  Google Scholar 

  63. Reuss, N. S. et al. Lake ecosystem responses to Holocene climate change at the subarctic tree-line in northern Sweden. Ecosystems 13, 393–409 (2010)

    CAS  Google Scholar 

  64. Pueyo, J. J. et al. Carbonate and organic matter sedimentation and isotopic signatures in Lake Chungara, Chilean Altiplano, during the last 12.3 kyr. Palaeogeogr. Palaeoclimatol. Palaeoecol. 307, 339–355 (2011)

    Google Scholar 

  65. Pessenda, L. C. R. et al. Last millennium environmental changes and climate inferences in the Southeastern Atlantic forest, Brazil. An. Acad. Bras. Cienc. 82, 717–729 (2010)

    PubMed  Google Scholar 

  66. Parplies, J. et al. Late glacial environment and climate development in northeastern China derived from geochemical and isotopic investigations of the varved sediment record from Lake Sihailongwan (Jilin Province). J. Paleolimnol. 40, 471–487 (2008)

    ADS  Google Scholar 

  67. Olsen, J., Noe-Nygaard, N. & Wolfe, B. B. Mid- to late-Holocene climate variability and anthropogenic impacts: multi-proxy evidence from Lake Bliden, Denmark. J. Paleolimnol. 43, 323–343 (2010)

    ADS  Google Scholar 

  68. Muzuka, A. N. N., Ryner, M. & Holmgren, K. 12,000-year, preliminary results of the stable nitrogen and carbon isotope record from the Empakai Crater lake sediments, Northern Tanzania. J. Afr. Earth Sci. 40, 293–303 (2004)

    ADS  CAS  Google Scholar 

  69. McLauchlan, K. K., Craine, J. M., Oswald, W. W., Leavitt, P. R. & Likens, G. E. Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc. Natl Acad. Sci. USA 104, 7466–7470 (2007)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  70. Mayr, C. et al. Isotopic fingerprints on lacustrine organic matter from Laguna Potrok Aike (southern Patagonia, Argentina) reflect environmental changes during the last 16,000 years. J. Paleolimnol. 42, 81–102 (2009)

    ADS  Google Scholar 

  71. Lucke, A. & Brauer, A. Biogeochemical and micro-facial fingerprints of ecosystem response to rapid Late Glacial climatic changes in varved sediments of Meerfelder Maar (Germany). Palaeogeogr. Palaeoclimatol. Palaeoecol. 211, 139–155 (2004)

    Google Scholar 

  72. Lobo, I., Mozeto, A. A. & Aravena, R. Paleohydrological investigation of Infernao Lake, Moji-Guaccu River watershed, Sao Paulo, Brazil. J. Paleolimnol. 26, 119–129 (2001)

    Google Scholar 

  73. Abbott, M. B., Wolfe, B. B., Aravena, R., Wolfe, A. P. & Seltzer, G. O. Holocene hydrological reconstructions from stable isotopes and paleolimnology, Cordillera Real, Bolivia. Quat. Sci. Rev. 19, 1801–1820 (2000)

    ADS  Google Scholar 

  74. Alin, S. R. et al. Effects of land-use change on aquatic biodiversity: A view from the paleorecord at Lake Tanganyika, East Africa. Geology 30, 1143–1146 (2002)

    ADS  Google Scholar 

  75. Anderson, L., Abbott, M. B. & Finney, B. P. Holocene climate inferred from oxygen isotope ratios in lake sediments, central Brooks Range, Alaska. Quat. Res. 55, 313–321 (2001)

    CAS  Google Scholar 

  76. Bertrand, S. et al. Bulk organic geochemistry of sediments from Puyehue Lake and its watershed (Chile, 40 degrees S): implications for paleoenvironmental reconstructions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 294, 56–71 (2010)

    Google Scholar 

  77. Brahney, J., Clague, J. J., Menounos, B. & Edwards, T. W. D. Timing and cause of water level fluctuations in Kluane Lake, Yukon Territory, over the past 5000 years. Quat. Res. 70, 213–227 (2008)

    Google Scholar 

  78. Brenner, M., Whitmore, T. J., Curtis, J. H., Hodell, D. A. & Schelske, C. L. Stable isotope (δ13C and δ15N) signatures of sedimented organic matter as indicators of historic lake trophic state. J. Paleolimnol. 22, 205–221 (1999)

    ADS  Google Scholar 

  79. Choudhary, P., Routh, J. & Chakrapani, G. J. An environmental record of changes in sedimentary organic matter from Lake Sattal in Kumaun Himalayas, India. Sci. Total Environ. 407, 2783–2795 (2009)

    ADS  CAS  PubMed  Google Scholar 

  80. Choudhary, P., Routh, J., Chakrapani, G. J. & Kumar, B. Biogeochemical records of paleoenvironmental changes in Nainital Lake, Kumaun Himalayas, India. J. Paleolimnol. 42, 571–586 (2009)

    ADS  Google Scholar 

  81. Chu, G. Q. et al. A 1600 year multiproxy record of paleoclimatic change from varved sediments in Lake Xiaolongwan, northeastern China. J. Geophys. Res.. 114, D22108, http://dx.doi.org/10.1029/2009JD012077 (2009)

    ADS  Google Scholar 

  82. Drew, S., Flett, I., Wilson, J., Heijnis, H. & Skilbeck, C. G. The trophic history of Myall Lakes, New South Wales, Australia: interpretations using δ13C and δ15N of the sedimentary record. Hydrobiologia 608, 35–47 (2008)

    CAS  Google Scholar 

  83. Enders, S. K. et al. Compound-specific stable isotopes of organic compounds from lake sediments track recent environmental changes in an alpine ecosystem, Rocky Mountain National Park, Colorado. Limnol. Oceanogr. 53, 1468–1478 (2008)

    ADS  CAS  Google Scholar 

  84. Engstrom, D. R., Schottler, S. P., Leavitt, P. R. & Havens, K. E. A reevaluation of the cultural eutrophication of Lake Okeechobee using multiproxy sediment records. Ecol. Appl. 16, 1194–1206 (2006)

    PubMed  Google Scholar 

  85. Enters, D. et al. Climate change and human impact at Sacrower See (NE Germany) during the past 13,000 years: a geochemical record. J. Paleolimnol. 43, 719–737 (2010)

    ADS  Google Scholar 

  86. Fagel, N. et al. Geochemical evidence (C, N and Pb isotopes) of recent anthropogenic impact in south-central Chile from two environmentally distinct lake sediment records. J. Quat. Sci. 25, 1100–1112 (2010)

    Google Scholar 

  87. Filippi, M. L. & Talbot, M. R. The palaeolimnology of northern Lake Malawi over the last 25 ka based upon the elemental and stable isotopic composition of sedimentary organic matter. Quat. Sci. Rev. 24, 1303–1328 (2005)

    ADS  Google Scholar 

  88. Hassan, K. M., Swinehart, J. B. & Spalding, R. F. Evidence for Holocene environmental change from C/N ratios, and δ13C and δ15N values in Swan Lake sediments, western Sand Hills, Nebraska. J. Paleolimnol. 18, 121–130 (1997)

    ADS  Google Scholar 

  89. Heikkilä, M., Edwards, T. W. D., Seppa, H. & Sonninen, E. Sediment isotope tracers from Lake Saarikko, Finland, and implications for Holocene hydroclimatology. Quat. Sci. Rev. 29, 2146–2160 (2010)

    ADS  Google Scholar 

  90. Herczeg, A. L., Smith, A. K. & Dighton, J. C. A 120 year record of changes in nitrogen and carbon cycling in Lake Alexandrina, South Australia: C:N, δ15N and δ13C in sediments. Appl. Geochem. 16, 73–84 (2001)

    CAS  Google Scholar 

  91. Hobbs, W. O., Vinebrooke, R. D. & Wolfe, A. P. Biogeochemical responses of two alpine lakes to climate change and atmospheric deposition, Jasper and Banff National parks, Canadian Rocky Mountains. Can. J. Fish. Aquat. Sci. 68, 1480–1494 (2011)

    Google Scholar 

  92. Holmgren, S. U., Bigler, C., Ingolfsson, O. & Wolfe, A. P. The Holocene-Anthropocene transition in lakes of western Spitsbergen, Svalbard (Norwegian High Arctic): climate change and nitrogen deposition. J. Paleolimnol. 43, 393–412 (2010)

    ADS  Google Scholar 

  93. Holtgrieve, G. W. et al. A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the Northern Hemisphere. Science 334, 1545–1548 (2011)

    ADS  CAS  PubMed  Google Scholar 

  94. Hu, F. S., Finney, B. P. & Brubaker, L. B. Effects of Holocene Alnus expansion on aquatic productivity, nitrogen cycling, and soil development in southwestern Alaska. Ecosystems 4, 358–368 (2001)

    CAS  Google Scholar 

  95. Hyodo, F. et al. Changes in stable isotopes, lignin-derived phenols, and fossil pigments in sediments of Lake Biwa, Japan: implications for anthropogenic effects over the last 100 years. Sci. Total Environ. 403, 139–147 (2008)

    ADS  CAS  PubMed  Google Scholar 

  96. Janbu, A. D., Paasche, O. & Talbot, M. R. Paleoclimate changes inferred from stable isotopes and magnetic properties of organic-rich lake sediments in Arctic Norway. J. Paleolimnol. 46, 29–44 (2011)

    ADS  Google Scholar 

  97. Li, L., Yu, Z., Moeller, R. E. & Bebout, G. E. Complex trajectories of aquatic and terrestrial ecosystem shifts caused by multiple human-induced environmental stress. Geochim. Cosmochim. Acta 72, 4338–4351 (2008)

    ADS  CAS  Google Scholar 

  98. Jeffers, E. S., Bonsall, M. B., Brooks, S. J. & Willis, K. J. Abrupt environmental changes drive shifts in tree-grass interaction outcomes. J. Ecol. 99, 1063–1070 (2011)

    Google Scholar 

  99. McCormac, F. G. SHCal04 Southern Hemisphere calibration 0-11.0 cal kyr BP. Radiocarbon 46, 1087–1092 (2004)

    CAS  Google Scholar 

  100. Reimer, P. J. et al. IntCal09 and Marine09 radiocarbon age calibration curves, 0-50,000 years cal BP. Radiocarbon 51, 1111–1150 (2009)

    CAS  Google Scholar 

  101. Blaauw, M. Methods and code for “classical” age-modelling of radiocarbon sequences. Quat. Geochronol. 5, 512–518 (2010)

    Google Scholar 

  102. Team, R. D. C. R: A Language and Environment for Statistical Computing, Reference Index Version 2.15.0 (R Foundation for Statistical Computing, 2005)

    Google Scholar 

  103. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)

    Google Scholar 

  104. Dentener, F. et al. Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob. Biogeochem. Cycles 20, GB4003, http://dx.doi.org/10.1029/2005GB002672 (2006)

    ADS  Google Scholar 

  105. Farr, T. G. et al. The shuttle radar topography mission. Rev. Geophys. 45, RG2004 (2007)

    ADS  Google Scholar 

  106. Sanderson, E. W. et al. The human footprint and the last of the wild. Bioscience 52, 891–904 (2002)

    Google Scholar 

  107. Woodward, C. A., Potito, A. P. & Beilman, D. W. Carbon and nitrogen stable isotope ratios in surface sediments from lakes of western Ireland: implications for inferring past lake productivity and nitrogen loading. J. Paleolimnol. 47, 167–184 (2012)

    ADS  Google Scholar 

  108. Keeling, C. D., Piper, S. C., Whorf, T. P. & Keeling, R. F. Evolution of natural and anthropogenic fluxes of atmospheric CO2 from 1957 to 2003. Tellus B 63, 1–22 (2011)

    ADS  CAS  Google Scholar 

  109. Petit, J. R. et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436 (1999)

    ADS  CAS  Google Scholar 

  110. Vito, M. & Muggeo, R. segmented: an R package to fit regression models with broken-line relationships. R News 8, 20–25 (2008)

    Google Scholar 

  111. Canty, A. & Ripley, B. Resampling methods in R: the boot package. R News 2, 2–7 (2002)

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Science Foundation (BCS-0955225 and EPS-0903806) and a James Martin Fellowship at the University of Oxford. We thank the many authors who contributed their data for the purpose of this analysis. We appreciate technical assistance from C. Morris, P. Long and S. McConaghy. We thank J. Marlon, S. Enders, C. Baird and S. Perakis for comments.

Author information

Authors and Affiliations

  1. Department of Geography, Kansas State University, Manhattan, 66506, Kansas, USA

    Kendra K. McLauchlan & Joseph J. Williams

  2. Division of Biology, Kansas State University, Manhattan, 66506, Kansas, USA

    Joseph M. Craine

  3. Department of Zoology, Biodiversity Institute, University of Oxford, Oxford OX1 3PS, UK,

    Elizabeth S. Jeffers

Authors
  1. Kendra K. McLauchlan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph J. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph M. Craine
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth S. Jeffers
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

K.K.M. and E.S.J. designed research, K.K.M., E.S.J. and J.J.W. performed research, K.K.M., J.J.W. and J.M.C. analysed the data, and K.K.M. led the writing of the paper with substantial input from E.S.J., J.J.W. and J.M.C.

Corresponding author

Correspondence to Kendra K. McLauchlan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-7, Supplementary Text, Supplementary References and Supplementary Tables 1-2. (PDF 1101 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

McLauchlan, K., Williams, J., Craine, J. et al. Changes in global nitrogen cycling during the Holocene epoch. Nature 495, 352–355 (2013). https://doi.org/10.1038/nature11916

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11916

This article is cited by

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.

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