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:

Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests

Abstract

There is wide agreement that anthropogenic climate warming has influenced the phenology of forests during the late twentieth and early twenty-first centuries1,2. Longer growing seasons can lead to increased photosynthesis and productivity3, which would represent a negative feedback to rising CO2 and consequently warming4,5. Alternatively, increased demand for soil resources because of a longer photosynthetically active period in conjunction with other global change factors might exacerbate resource limitation6,7, restricting forest productivity response to a longer growing season8,9. In this case, increased springtime productivity has the potential to increase plant nitrogen limitation by increasing plant demand for nitrogen more than nitrogen supplies, or increasing early-season ecosystem nitrogen losses10,11. Here we show that for 222 trees representing three species in eastern North America earlier spring phenology during the past 30 years has caused declines in nitrogen availability to trees by increasing demand for nitrogen relative to supply. The observed decline in nitrogen availability is not associated with reduced wood production, suggesting that other environmental changes such as increased atmospheric CO2 and water availability are likely to have overwhelmed reduced nitrogen availability. Given current trajectories of environmental changes, nitrogen limitation is likely to continue to increase for these forests, possibly further limiting carbon sequestration potential.

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

Access options

Buy this article

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

Figure 1: Vegetation fractions using pre- and post-2000 data.
Figure 2: Path diagram illustrating relationships between time, spring (DOYspr) and autumn (DOYaut) phenology, wood production (BAI), nitrogen availability (δ15N) and discrimination against 13C (Δ13C).
Figure 3: Relationships between mean δ15N, Δ13C, and spring anomaly.

Similar content being viewed by others

References

  1. Schwartz, M. D., Ahas, R. & Aasa, A. Onset of spring starting earlier across the Northern Hemisphere. Glob. Change Biol. 12, 343–351 (2006).

    Article  Google Scholar 

  2. Jeong, S.-J., Ho, C.-H., Gim, H.-J. & Brown, M. E. Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982–2008. Glob. Change Biol. 17, 2385–2399 (2011).

    Article  Google Scholar 

  3. Hyvonen, R. et al. The likely impact of elevated CO2, nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol. 173, 463–480 (2007).

    Article  Google Scholar 

  4. Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Phil. Trans. R. Soc. B 365, 3227–3246 (2010).

    Article  Google Scholar 

  5. Keenan, T. F. et al. Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat. Clim. Change 4, 598–604 (2014).

    Article  CAS  Google Scholar 

  6. 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).

    Article  CAS  Google Scholar 

  7. Sigurdsson, B. D., Medhurst, J. L., Wallin, G., Eggertsson, O. & Linder, S. Growth of mature boreal Norway spruce was not affected by elevated CO2 and/or air temperature unless nutrient availability was improved. Tree Physiol. 33, 1192–1205 (2013).

    Article  CAS  Google Scholar 

  8. Piao, S. L. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).

    Article  CAS  Google Scholar 

  9. Zaehle, S., Jones, C. D., Houlton, B., Lamarque, J.-F. & Robertson, E. Nitrogen availability reduces CMIP5 projections of twenty-first-century land carbon uptake. J. Clim. 28, 2494–2511 (2015).

    Article  Google Scholar 

  10. Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001).

    Article  CAS  Google Scholar 

  11. Campbell, J. L. et al. Consequences of climate change for biogeochemical cycling in forests of northeastern North America. Can. J. Forest Res. 39, 264–284 (2009).

    Article  CAS  Google Scholar 

  12. Elmore, A. J., Guinn, S. M., Minsley, B. J. & Richardson, A. D. Landscape controls on the timing of spring, autumn, and growing season length in mid-Atlantic forests. Glob. Change Biol. 18, 656–674 (2012).

    Article  Google Scholar 

  13. 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).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Bukata, A. R. & Kyser, T. K. Carbon and nitrogen isotope variations in tree-rings as records of perturbations in regional carbon and nitrogen cycles. Environ. Sci. Technol. 41, 1331–1338 (2007).

    Article  CAS  Google Scholar 

  16. Ehleringer, J. R. & Cerling, T. E. Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol. 15, 105–111 (1995).

    Article  CAS  Google Scholar 

  17. Melaas, E. K., Friedl, M. A. & Zhu, Z. Detecting interannual variation in deciduous broadleaf forest phenology using Landsat TM/ETM plus data. Remote Sens. Environ. 132, 176–185 (2013).

    Article  Google Scholar 

  18. Becklin, K. M., Medeiros, J. S., Sale, K. R. & Ward, J. K. Evolutionary history underlies plant physiological responses to global change since the last glacial maximum. Ecol. Lett. 17, 691–699 (2014).

    Article  Google Scholar 

  19. Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).

    Article  CAS  Google Scholar 

  20. Phipps, R. L. & Whiton, J. C. Decline in long-term growth trends of white oak. Can. J. Forest Res. 18, 24–32 (1988).

    Article  Google Scholar 

  21. Fenn, M. E. et al. Nitrogen excess in North American ecosystems: Predisposing factors, ecosystem responses, and management strategies. Ecol. Appl. 8, 706–733 (1998).

    Article  Google Scholar 

  22. Frank, D. C. et al. Water-use efficiency and transpiration across European forests during the Anthropocene. Nat. Clim. Change 5, 579–583 (2015).

    Article  CAS  Google Scholar 

  23. Eshleman, K. N., Sabo, R. D. & Kline, K. M. Surface water quality is improving due to declining atmospheric N deposition. Environ. Sci. Technol. 47, 12193–12200 (2013).

    Article  CAS  Google Scholar 

  24. Steffen, W. et al. Planetary boundaries: Guiding human development on a changing planet. Science 347 (2015).

  25. Duran, J. et al. Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7, e01251 (2016).

    Article  Google Scholar 

  26. Jonard, M. et al. Tree mineral nutrition is deteriorating in Europe. Glob. Change Biol. 21, 418–430 (2015).

    Article  Google Scholar 

  27. Aber, J. D. et al. Forest processes and global environmental change: predicting the effects of individual and multiple stressors. Bioscience 51, 735–751 (2001).

    Article  Google Scholar 

  28. Masek, J. G. et al. A Landsat surface reflectance dataset for North America, 1990–2000. IEEE Geosci. Remote Sens. Lett. 3, 68–72 (2006).

    Article  Google Scholar 

  29. Elmore, A. J., Mustard, J. F., Manning, S. J. & Lobell, D. B. Quantifying vegetation change in semiarid environments: Precision and accuracy of spectral mixture analysis and the Normalized Difference Vegetation Index. Remote Sens. Environ. 73, 87–102 (2000).

    Article  Google Scholar 

  30. McCarroll, D. & Loader, N. J. Stable isotopes in tree rings. Quat. Sci. Rev. 23, 771–801 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

Funding provided by the National Aeronautics and Space Administration (no. NNX12AK17G). We thank S.M. Guinn for remote sensing data processing and database development, R. Paulman for dendrochronology and analytical measurements, V. Cunningham and H. Ding for field assistance, D. Taillie for assistance with Fig. 2, and K. McLauchlan for insightful conversation.

Author information

Authors and Affiliations

Authors

Contributions

A.J.E. and D.M.N. conceived the study, collected the data and oversaw analytical and geospatial measurements. A.J.E., D.M.N. and J.M.C. performed statistical analyses and wrote the manuscript.

Corresponding author

Correspondence to Andrew J. Elmore.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Description of Figure 2, and Supplementary Table for figure 2, Supplementary Figures 1-10, Supplementary Tables 1-19 (PDF 3234 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elmore, A., Nelson, D. & Craine, J. Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nature Plants 2, 16133 (2016). https://doi.org/10.1038/nplants.2016.133

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2016.133

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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