, Volume 174, Issue 4, pp 1117–1126 | Cite as

Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree

  • Nina Wurzburger
  • Chelcy Ford Miniat
Physiological ecology - Original research


General circulation models project more intense and frequent droughts over the next century, but many questions remain about how terrestrial ecosystems will respond. Of particular importance, is to understand how drought will alter the species composition of regenerating temperate forests wherein symbiotic dinitrogen (N2)-fixing plants play a critical role. In experimental mesocosms we manipulated soil moisture to study the effect of drought on the physiology, growth and competitive interactions of four co-occurring North American tree species, one of which (Robinia pseudoacacia) is a symbiotic N2-fixer. We hypothesized that drought would reduce growth by decreasing stomatal conductance, hydraulic conductance and increasing the water use efficiency of species with larger diameter xylem vessel elements (Quercus rubra, R. pseudoacacia) relative to those with smaller elements (Acer rubrum and Liriodendron tulipifera). We further hypothesized that N2 fixation by R. pseudoacacia would decline with drought, reducing its competitive ability. Under drought, growth declined across all species; but, growth and physiological responses did not correspond to species’ hydraulic architecture. Drought triggered an 80 % increase in nodule biomass and N accrual for R. pseudoacacia, improving its growth relative to other species. These results suggest that drought intensified soil N deficiency and that R. pseudoacacia’s ability to fix N2 facilitated competition with non-fixing species when both water and N were limiting. Under scenarios of moderate drought, N2 fixation may alleviate the N constraints resulting from low soil moisture and improve competitive ability of N2-fixing species, and as a result, supply more new N to the ecosystem.


Climate change Biogeochemistry Hydraulic conductance Plant physiology Stomatal conductance 



This study was supported by the United States Department of Agriculture Forest Service, Southern Research Station, and by cooperative agreement number 11-CA-11330140-095 to N. Wurzburger at the University of Georgia. Any opinions, findings, conclusions, or recommendations expressed in the material are those of the authors and do not necessarily reflect the views of the USDA Forest Service or the University of Georgia. We thank Neal Muldoon, Shialoh Wilson, Sheena Zhang, Courtney Collins, Steven T. Brantley, and Jeff Minucci for their assistance with this research. We are grateful to Lindsay Boring, Ford Ballantyne and two anonymous reviewers for their constructive comments on the manuscript.

Supplementary material

442_2013_2851_MOESM1_ESM.docx (86 kb)
Supplementary material 1 (DOCX 87 kb)


  1. Allen CD et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684CrossRefGoogle Scholar
  2. Apsley DK (1987) Growth interactions and comparative water relations of Liriodendron tulipifera L. and Robinia pseudoacacia L.. MSc, University of Georgia, AthensGoogle Scholar
  3. Aranibar JN et al (2004) Nitrogen cycling in the soil–plant system along a precipitation gradient in the Kalahari sands. Glob Change Biol 10:359–373CrossRefGoogle Scholar
  4. Boring LR, Swank WT (1984a) The role of black locust (Robinia pseudoacacia) in forest succession. J Ecol 72:749–766CrossRefGoogle Scholar
  5. Boring LR, Swank WT (1984b) Symbiotic nitrogen fixation in regenerating black locust (Robinia pseudoacacia L.) stands. For Sci 30:528–537Google Scholar
  6. Boring LR, Swank WT, Monk CD (1988) Dynamics of early succional forest structure and processes in the Coweeta Basin. In: Swank WT, Crossley DA (eds) Ecological studies, vol 66. Forest hydrology and ecology at Coweeta. Springer, New York, pp 162–179Google Scholar
  7. Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley centre climate model. J Hydrometeorol 7:1113–1125CrossRefGoogle Scholar
  8. Cai J, Tyree MT (2010) The impact of vessel size on vulnerability curves: data and models for within-species variability in saplings of aspen, Populus tremuloides Michx. Plant Cell Environ 33:1059–1069PubMedCrossRefGoogle Scholar
  9. Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc Natl Acad Sci 108:1474–1478PubMedCentralPubMedCrossRefGoogle Scholar
  10. Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol 193:713–720PubMedCrossRefGoogle Scholar
  11. Clark JS, Bell DM, Hersh MH, Nichols L (2011) Climate change vulnerability of forest biodiversity: climate and competition tracking of demographic rates. Glob Change Biol 17:1834–1849CrossRefGoogle Scholar
  12. Clark JS, Bell DM, Kwit M, Stine A, Vierra B, Zhu K (2012) Individual-scale inference to anticipate climate-change vulnerability of biodiversity. Philos Trans R Soc B: Biol Sci 367:236–246CrossRefGoogle Scholar
  13. Clinton BD, Boring LR, Swank WT (1993) Canopy gap characteristics and drought influences in oak forests of the Coweeta Basin. Ecology 74:1551–1558CrossRefGoogle Scholar
  14. Cramer MD, Van Cauter A, Bond WJ (2010) Growth of N2-fixing African savanna Acacia species is constrained by below-ground competition with grass. J Ecol 98:156–167CrossRefGoogle Scholar
  15. Domec J-C, Gartner BL (2001) Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees. Trees Struct Funct 15:204–214CrossRefGoogle Scholar
  16. Du S et al (2011) Sapflow characteristics and climatic responses in three forest species in the semiarid Loess Plateau region of China. Agric For Meteorol 151:1–10CrossRefGoogle Scholar
  17. Elliott KJ, Swank WT (1994a) Changes in tree species diversity after successive clearcuts in the Southern Appalachians. Vegetatio 115:11–18Google Scholar
  18. Elliott KJ, Swank WT (1994b) Impacts of drought on tree mortality and growth in a mixed hardwood forest. J Veg Sci 5:229–236CrossRefGoogle Scholar
  19. Elliott KJ, Swank WT (2008) Long-term changes in forest composition and diversity following early logging (1919–1923) and the decline of American chestnut (Castanea dentata). Plant Ecol 197:155–172CrossRefGoogle Scholar
  20. Farquhar G, Ehleringer J, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  21. Ford CR, Laseter SH, Swank WT, Vose JM (2011) Can forest management be used to sustain water-based ecosystem services in the face of climate change? Ecol Appl 21:2049–2067PubMedCrossRefGoogle Scholar
  22. Freiberg E (1998) Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a Costa Rican premontane rain forest. Oecologia 117:9–18CrossRefGoogle Scholar
  23. Gerber S, Hedin LO, Keel SG, Pacala SW, Shevliakova E (2013) Land use change and nitrogen feedbacks constrain the trajectory of the land carbon sink. Geophys Res Lett 40:2013GL057260Google Scholar
  24. Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311CrossRefGoogle Scholar
  25. Hinchee MW, Mullinax L, Rottmann W (2010) Woody biomass and purpose-grown trees as feedstocks for renewable energy. In: Mascia PN, Scheffran J, Widholm JM (eds) Plant biotechnology for sustainable production of energy and co-products, vol 66. Springer, Berlin, Heidelberg, pp 155–208CrossRefGoogle Scholar
  26. Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121CrossRefGoogle Scholar
  27. Jeffers ES, Bonsall MB, Willis KJ (2011) Stability in ecosystem functioning across a climatic threshold and contrasting forest regimes. PLoS One 6:e16134PubMedCentralPubMedCrossRefGoogle Scholar
  28. Johnsen KH, Bongarten BC (1991) Allometry of acetylene reduction and nodule growth of Robinia pseudoacacia families subjected to varied root zone nitrate concentrations. Tree Physiol 9:507–522PubMedCrossRefGoogle Scholar
  29. Johnsen KH, Bongarten BC (1992) Relationships between nitrogen fixation and growth in Robinia pseudoacacia seedlings: a functional growth-analysis approach using 15N. Physiol Plant 85:77–84CrossRefGoogle Scholar
  30. Leng H, Lu M, Wan X (2013) Variation in embolism occurrence and repair along the stem in drought-stressed and re-watered seedlings of a poplar clone. Physiol Plant 147:329–339PubMedCrossRefGoogle Scholar
  31. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723PubMedCrossRefGoogle Scholar
  32. Lindenmayer DB, Hobbs RJ, Likens GE, Krebs CJ, Banks SC (2011) Newly discovered landscape traps produce regime shifts in wet forests. Proc Natl Acad Sci 108:15887–15891PubMedCentralPubMedCrossRefGoogle Scholar
  33. Maherali H, Pockman WT, Brooks JR (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 84:2184–2199CrossRefGoogle Scholar
  34. Maherali H, Moura C, Caldeira MC, Willson CJ, Jackson RB (2006) Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. Plant Cell Environ 29:571–583PubMedCrossRefGoogle Scholar
  35. Marino D et al (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974PubMedCentralPubMedCrossRefGoogle Scholar
  36. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532PubMedCrossRefGoogle Scholar
  37. Meinzer FC, McCulloh KA (2013) Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? Tree Physiol 33:331–334PubMedCrossRefGoogle Scholar
  38. Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477PubMedCrossRefGoogle Scholar
  39. Monks A, Cieraad E, Burrows L, Walker S (2012) Higher relative performance at low soil nitrogen and moisture predicts field distribution of nitrogen-fixing plants. Plant Soil 359:363–374CrossRefGoogle Scholar
  40. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373PubMedCentralPubMedCrossRefGoogle Scholar
  41. Ogasa M, Miki NH, Murakami Y, Yoshikawa K (2013) Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiol 33:335–344PubMedCrossRefGoogle Scholar
  42. Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299PubMedCrossRefGoogle Scholar
  43. Rastetter EB, Vitousek PM, Field C, Shaver GR, Herbert D, Ågren GI (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems 4:369–388CrossRefGoogle Scholar
  44. Schulze ED, Gebauer G, Ziegler H, Lange OL (1991) Estimates of nitrogen fixation by trees on an aridity gradient in Namibia. Oecologia 88:451–455CrossRefGoogle Scholar
  45. Sperry J (2011) Hydraulics of vascular water transport. In: Wojtaszek P (ed) Mechanical integration of plant cells and plants, vol 9. Springer, Berlin, Heidelberg, pp 303–327CrossRefGoogle Scholar
  46. Taneda H, Sperry JS (2008) A case-study of water transport in co-occurring ring- versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol 28:1641–1651PubMedCrossRefGoogle Scholar
  47. Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Mol Biol 40:19–38CrossRefGoogle Scholar
  48. Tyree MT, Engelbrecht BMJ, Vargas G, Kursar TA (2003) Desiccation tolerance of five tropical seedlings in Panama: relationship to a field assessment of drought performance. Plant Physiol 132:1439–1447PubMedCentralPubMedCrossRefGoogle Scholar
  49. USDA Forest Service (2012) Future of America’s forest and rangelands: Forest Service 2010 Resources Planning Act assessment. Gen Tech Rep WO-87. Washington, DCGoogle Scholar
  50. Vitousek P, Howarth R (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  51. Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812CrossRefGoogle Scholar
  52. Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5:475–482CrossRefGoogle Scholar
  53. Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. Proc Natl Acad Sci 104:5738–5742PubMedCentralPubMedCrossRefGoogle Scholar
  54. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Coweeta Hydrologic LabUSDA Forest Service, Southern Research StationOttoUSA

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