, Volume 129, Issue 3, pp 389–400 | Cite as

Responses of aboveground C and N pools to rainfall variability and nitrogen deposition are mediated by seasonal precipitation and plant community dynamics

  • Michael J. SchusterEmail author
  • Nicholas G. Smith
  • Jeffrey S. Dukes


Plant productivity and tissue chemistry in temperate ecosystems are largely driven by water and nitrogen (N) availability. Although changes in rainfall patterns may influence nutrient limitation, few studies have considered how these two global change factors could interact to influence terrestrial ecosystem productivity and stoichiometry. Here, we examined the influence of experimentally-increased intra-annual rainfall variability and low-level nitrogen addition on aboveground productivity, C and N pools, and C:N ratios in a restored tallgrass prairie across two growing seasons. In the drier first year of the experiment, increased rainfall variability boosted productivity and C pools. In the wetter second year, aboveground productivity and C pools increased with N addition, suggesting a switch in primary resource limitation from water to N. Increased rainfall variability also reduced aboveground N pools in the second year. Community-level C:N increased under increased rainfall variability in the wetter second year and N addition slightly reduced community C:N in both years. These changes in element pools and stoichiometry were mostly a result of increased forb dominance in response to both treatments. Overall, our findings from a restored prairie indicate that increased rainfall variability and N addition can enhance aboveground productivity and C pools, but that N pools may not have a consistent response to either global change factor. Our study also suggests that these effects are dependent on growing season precipitation patterns and are mediated by shifts in plant community composition.


Precipitation manipulation Global change Ecological stoichiometry Nitrogen Productivity Grassland 



We thank Siying Long, Raj Lal, Tanvi Lad, Alejandro Salazar, and Emmalyn Terracciano for field assistance. The PRICLE project was supported by the Purdue Climate Change Research Center (PCCRC). M.J.S. was supported by USDA Agro-ecosystem Services National Need Fellowship. N.G.S. was supported by a NASA Earth and Space Science Fellowship and a PCCRC Graduate Fellowship. J.S.D. gratefully acknowledges support from NSF (DEB-0955771). This is publication 1637 of the PCCRC.

Supplementary material

10533_2016_240_MOESM1_ESM.docx (3.1 mb)
Supplementary material 1 (DOCX 3176 kb)


  1. Alexander LV, Zhang X, Peterson TC et al (2006) Global observed changes in daily climate extremes of temperature and precipitation. J Geophys Res Atmos 111:D05109. doi: 10.1029/2005JD006290 Google Scholar
  2. Baer SG, Kitchen DJ, Blair JM, Rice CW (2002) Changes in ecosystem structure and function along a chronosequence of restored grasslands. Ecol Appl 12:1688–1701. doi: 10.1890/1051-0761(2002)012[1688:CIESAF]2.0.CO;2 CrossRefGoogle Scholar
  3. Bloor JMG, Bardgett RD (2012) Stability of above-ground and below-ground processes to extreme drought in model grassland ecosystems: interactions with plant species diversity and soil nitrogen availability. Perspect Plant Ecol Evol Syst 14:193–204. doi: 10.1016/j.ppees.2011.12.001 CrossRefGoogle Scholar
  4. Borer ET, Seabloom EW, Gruner DS et al (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520. doi: 10.1038/nature13144 CrossRefGoogle Scholar
  5. Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Change Biol 15:808–824. doi: 10.1111/j.1365-2486.2008.01681.x CrossRefGoogle Scholar
  6. Chapin FSI, Vitousek PM, Cleve KV (1986) The Nature of Nutrient Limitation in Plant Communities. Am Nat 127:48–58CrossRefGoogle Scholar
  7. Dickson TL, Gross KL (2013) Plant community responses to long-term fertilization: changes in functional group abundance drive changes in species richness. Oecologia 173:1513–1520. doi: 10.1007/s00442-013-2722-8 CrossRefGoogle Scholar
  8. Dupre C, Stevens CJ, Ranke T et al (2010) Changes in species richness and composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Change Biol 16:344–357. doi: 10.1111/j.1365-2486.2009.01982.x CrossRefGoogle Scholar
  9. Eskelinen A, Harrison S (2013) Exotic plant invasions under enhanced rainfall are constrained by soil nutrients and competition. Ecology 95:682–692. doi: 10.1890/13-0288.1 CrossRefGoogle Scholar
  10. Eskelinen A, Harrison SP (2015) Resource colimitation governs plant community responses to altered precipitation. Proc Natl Acad Sci 112:13009–13014. doi: 10.1073/pnas.1508170112 CrossRefGoogle Scholar
  11. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19. doi: 10.1007/BF00377192 CrossRefGoogle Scholar
  12. Fay PA, Carlisle JD, Danner BT et al (2002) Altered rainfall patterns, gas exchange, and growth in grasses and forbs. Int J Plant Sci 163:549–557. doi: 10.1086/339718 CrossRefGoogle Scholar
  13. Fay PA, Carlisle JD, Knapp AK et al (2003) Productivity responses to altered rainfall patterns in a C 4-dominated grassland. Oecologia 137:245–251. doi: 10.1007/s00442-003-1331-3 CrossRefGoogle Scholar
  14. Fierer N, Schimel JP (2002) Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787. doi: 10.1016/S0038-0717(02)00007-X CrossRefGoogle Scholar
  15. Foster BL, Gross KL (1998) Species Richness in a successional Grassland: effects of Nitrogen Enrichment and Plant Litter. Ecology 79:2593–2602. doi: 10.1890/0012-9658(1998)079[2593:SRIASG]2.0.CO;2 CrossRefGoogle Scholar
  16. Galloway J, Dentener F, Capone D et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. doi: 10.1007/s10533-004-0370-0 CrossRefGoogle Scholar
  17. Grant K, Kreyling J, Dienstbach LFH et al (2014) Water stress due to increased intra-annual precipitation variability reduced forage yield but raised forage quality of a temperate grassland. Agric Ecosyst Environ 186:11–22. doi: 10.1016/j.agee.2014.01.013 CrossRefGoogle Scholar
  18. Harmon ME, Silver WL, Fasth B et al (2009) Long-term patterns of mass loss during the decomposition of leaf and fine root litter: an intersite comparison. Glob Change Biol 15:1320–1338. doi: 10.1111/j.1365-2486.2008.01837.x CrossRefGoogle Scholar
  19. Harpole W, Tilman D (2006) Non-neutral patterns of species abundance in grassland communities. Ecol Lett 9:15–23Google Scholar
  20. Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Change Biol 13:2341–2348. doi: 10.1111/j.1365-2486.2007.01447.x CrossRefGoogle Scholar
  21. Hautier Y, Seabloom EW, Borer ET et al (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521–525. doi: 10.1038/nature13014 CrossRefGoogle Scholar
  22. Heisler-White JL, Knapp AK, Kelly EF (2008) Increasing precipitation event size increases aboveground net primary productivity in a semi-arid grassland. Oecologia 158:129–140. doi: 10.1007/s00442-008-1116-9 CrossRefGoogle Scholar
  23. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293. doi: 10.1007/BF01007582 Google Scholar
  24. Humbert J-Y, Dwyer JM, Andrey A, Arlettaz R (2016) Impacts of nitrogen addition on plant biodiversity in mountain grasslands depend on dose, application duration and climate: a systematic review. Glob Change Biol 22:110–120. doi: 10.1111/gcb.12986 CrossRefGoogle Scholar
  25. IPCC (2012) Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  26. Isbell FI, Polley HW, Wilsey BJ (2009) Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol Lett 12:443–451. doi: 10.1111/j.1461-0248.2009.01299.x CrossRefGoogle Scholar
  27. Jentsch A, Kreyling J, Elmer M et al (2011) Climate extremes initiate ecosystem-regulating functions while maintaining productivity. J Ecol 99:689–702. doi: 10.1111/j.1365-2745.2011.01817.x CrossRefGoogle Scholar
  28. Jones MB, Donnelly A (2004) Carbon sequestration in temperate grassland ecosystems and the influence of management, climate and elevated CO(2). New Phytol 164:423–439. doi: 10.1111/j.1469-8137.2004.01201.x CrossRefGoogle Scholar
  29. Kinugasa T, Tsunekawa A, Shinoda M (2012) Increasing nitrogen deposition enhances post-drought recovery of grassland productivity in the Mongolian steppe. Oecologia 170:857–865. doi: 10.1007/s00442-012-2354-4 CrossRefGoogle Scholar
  30. Knapp AK, Fay PA, Blair JM et al (2002) Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298:2202–2205. doi: 10.1126/science.1076347 CrossRefGoogle Scholar
  31. Knapp AK, Beier C, Briske DD et al (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–821. doi: 10.1641/B580908 CrossRefGoogle Scholar
  32. Knapp AK, Hoover DL, Wilcox KR et al (2015) Characterizing differences in precipitation regimes of extreme wet and dry years: implications for climate change experiments. Glob Change Biol 21:2624–2633. doi: 10.1111/gcb.12888 CrossRefGoogle Scholar
  33. Kreyling J, Beier C (2013) Complexity in climate change manipulation experiments. Bioscience 63:763–767. doi: 10.1525/bio.2013.63.9.12 CrossRefGoogle Scholar
  34. Kreyling J, Wenigmann M, Beierkuhnlein C, Jentsch A (2008) Effects of extreme weather events on plant productivity and tissue die-back are modified by community composition. Ecosystems 11:752–763. doi: 10.1007/s10021-008-9157-9 CrossRefGoogle Scholar
  35. Kulmatiski A, Beard KH (2013) Woody plant encroachment facilitated by increased precipitation intensity. Nat Clim Change 3:833–837. doi: 10.1038/nclimate1904 CrossRefGoogle Scholar
  36. Laungani R, Knops JMH (2009) The impact of co-occurring tree and grassland species on carbon sequestration and potential biofuel production. GCB Bioenergy 1:392–403. doi: 10.1111/j.1757-1707.2009.01031.x CrossRefGoogle Scholar
  37. Leuzinger S, Luo Y, Beier C et al (2011) Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol Evol 26:236–241. doi: 10.1016/j.tree.2011.02.011 CrossRefGoogle Scholar
  38. Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115. doi: 10.1111/ele.12073 CrossRefGoogle Scholar
  39. Lu M, Yang Y, Luo Y et al (2011a) Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytol 189:1040–1050. doi: 10.1111/j.1469-8137.2010.03563.x CrossRefGoogle Scholar
  40. Lu M, Zhou X, Luo Y et al (2011b) Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agric Ecosyst Environ 140:234–244. doi: 10.1016/j.agee.2010.12.010 CrossRefGoogle Scholar
  41. Manning P, Newington JE, Robson HR et al (2006) Decoupling the direct and indirect effects of nitrogen deposition on ecosystem function. Ecol Lett 9:1015–1024. doi: 10.1111/j.1461-0248.2006.00959.x CrossRefGoogle Scholar
  42. Mueller KE, Hobbie SE, Tilman D, Reich PB (2013) Effects of plant diversity, N fertilization, and elevated carbon dioxide on grassland soil N cycling in a long-term experiment. Glob Change Biol 19:1249–1261. doi: 10.1111/gcb.12096 CrossRefGoogle Scholar
  43. Mulder CPH, Jumpponen A, Hogberg P, Huss-Danell K (2002) How plant diversity and legumes affect nitrogen dynamics in experimental grassland communities. Oecologia 133:412–421. doi: 10.1007/s00442-002-1043-0 CrossRefGoogle Scholar
  44. Novotny AM, Schade JD, Hobbie SE et al (2007) Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696. doi: 10.1007/s00442-006-0599-5 CrossRefGoogle Scholar
  45. Oelmann Y, Buchmann N, Gleixner G et al (2011) Plant diversity effects on aboveground and belowground N pools in temperate grassland ecosystems: development in the first 5 years after establishment. Glob Biogeochem Cycles 25:GB2014. doi: 10.1029/2010GB003869 CrossRefGoogle Scholar
  46. Ordonez JC, van Bodegom PM, Witte J-PM et al (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. doi: 10.1111/j.1466-8238.2008.00441.x CrossRefGoogle Scholar
  47. Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149. doi: 10.1007/s10533-010-9439-0 CrossRefGoogle Scholar
  48. Reich PB, Knops J, Tilman D et al (2001) Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–812. doi: 10.1038/35071062 CrossRefGoogle Scholar
  49. Reichstein M, Bahn M, Ciais P et al (2013) Climate extremes and the carbon cycle. Nature 500:287–295. doi: 10.1038/nature12350 CrossRefGoogle Scholar
  50. Rennenberg H, Dannenmann M, Gessler A et al (2009) Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol 11:4–23. doi: 10.1111/j.1438-8677.2009.00241.x CrossRefGoogle Scholar
  51. Schimel D (1995) Terrestrial ecosystems and the carbon-cycle. Glob Change Biol 1:77–91. doi: 10.1111/j.1365-2486.1995.tb00008.x CrossRefGoogle Scholar
  52. Schimel DS, Braswell BH, Parton WJ (1997) Equilibration of the terrestrial water, nitrogen, and carbon cycles. Proc Natl Acad Sci 94:8280–8283CrossRefGoogle Scholar
  53. Schuster MJ (2015) Increased rainfall variability and N addition accelerate litter decomposition in a restored prairie. Oecologia. doi: 10.1007/s00442-015-3396-1 Google Scholar
  54. Skogen KA, Holsinger KE, Cardon ZG (2011) Nitrogen deposition, competition and the decline of a regionally threatened legume, Desmodium cuspidatum. Oecologia 165:261–269. doi: 10.1007/s00442-010-1818-7 CrossRefGoogle Scholar
  55. Smith NG, Schuster MJ, Dukes JS (2016) Rainfall variability and nitrogen addition synergistically reduce plant diversity in a restored tallgrass prairie. J Appl Ecol. doi: 10.1111/1365-2664.12593 Google Scholar
  56. Stevens CJ, Lind EM, Hautier Y et al (2015) Anthropogenic nitrogen deposition predicts local grassland primary production worldwide. Ecology 96:1459–1465. doi: 10.1890/14-1902.1 CrossRefGoogle Scholar
  57. Stocker T, Qin D, Plattner G-K et al (2014) Climate change 2013: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
  58. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632. doi: 10.1038/nature04742 CrossRefGoogle Scholar
  59. Turner CL, Knapp AK (1996) Responses of a C4 grass and three C3 forbs to variation in nitrogen and light in tallgrass prairie. Ecology 77:1738–1749. doi: 10.2307/2265779 CrossRefGoogle Scholar
  60. Vitousek PM, Aber JD, Howarth RW et al (1997) Technical report: human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. doi: 10.2307/2269431 Google Scholar
  61. Yang Y, Fang J, Ma W, Wang W (2008) Relationship between variability in aboveground net primary production and precipitation in global grasslands. Geophys Res Lett 35:L23710. doi: 10.1029/2008GL035408 CrossRefGoogle Scholar
  62. Yue K, Peng Y, Peng C et al (2016) Stimulation of terrestrial ecosystem carbon storage by nitrogen addition: a meta-analysis. Sci Rep 6:19895. doi: 10.1038/srep19895 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Forestry and Natural ResourcesPurdue UniversityWest LafayetteUSA
  2. 2.Department of Biological SciencesPurdue UniversityWest LafayetteUSA

Personalised recommendations