Abstract
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.
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References
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 259:660–684
Apsley DK (1987) Growth interactions and comparative water relations of Liriodendron tulipifera L. and Robinia pseudoacacia L.. MSc, University of Georgia, Athens
Aranibar JN et al (2004) Nitrogen cycling in the soil–plant system along a precipitation gradient in the Kalahari sands. Glob Change Biol 10:359–373
Boring LR, Swank WT (1984a) The role of black locust (Robinia pseudoacacia) in forest succession. J Ecol 72:749–766
Boring LR, Swank WT (1984b) Symbiotic nitrogen fixation in regenerating black locust (Robinia pseudoacacia L.) stands. For Sci 30:528–537
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 162–179
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 7:1113–1125
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 33:1059–1069
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 108:1474–1478
Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol 193:713–720
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 17:1834–1849
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 367:236–246
Clinton BD, Boring LR, Swank WT (1993) Canopy gap characteristics and drought influences in oak forests of the Coweeta Basin. Ecology 74:1551–1558
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 98:156–167
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 15:204–214
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 151:1–10
Elliott KJ, Swank WT (1994a) Changes in tree species diversity after successive clearcuts in the Southern Appalachians. Vegetatio 115:11–18
Elliott KJ, Swank WT (1994b) Impacts of drought on tree mortality and growth in a mixed hardwood forest. J Veg Sci 5:229–236
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 197:155–172
Farquhar G, Ehleringer J, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
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 21:2049–2067
Freiberg E (1998) Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a Costa Rican premontane rain forest. Oecologia 117:9–18
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 40:2013GL057260
Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311
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 155–208
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 24:113–121
Jeffers ES, Bonsall MB, Willis KJ (2011) Stability in ecosystem functioning across a climatic threshold and contrasting forest regimes. PLoS One 6:e16134
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 9:507–522
Johnsen KH, Bongarten BC (1992) Relationships between nitrogen fixation and growth in Robinia pseudoacacia seedlings: a functional growth-analysis approach using 15N. Physiol Plant 85:77–84
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 147:329–339
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 190:709–723
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 108:15887–15891
Maherali H, Pockman WT, Brooks JR (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 84:2184–2199
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 29:571–583
Marino D et al (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974
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 26:523–532
Meinzer FC, McCulloh KA (2013) Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? Tree Physiol 33:331–334
Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477
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 359:363–374
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 107:19368–19373
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 33:335–344
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299
Rastetter EB, Vitousek PM, Field C, Shaver GR, Herbert D, Ågren GI (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems 4:369–388
Schulze ED, Gebauer G, Ziegler H, Lange OL (1991) Estimates of nitrogen fixation by trees on an aridity gradient in Namibia. Oecologia 88:451–455
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 303–327
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 28:1641–1651
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Mol Biol 40:19–38
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 132:1439–1447
USDA Forest Service (2012) Future of America’s forest and rangelands: Forest Service 2010 Resources Planning Act assessment. Gen Tech Rep WO-87. Washington, DC
Vitousek P, Howarth R (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
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 28:800–812
Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5:475–482
Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. Proc Natl Acad Sci 104:5738–5742
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Acknowledgments
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.
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Communicated by Allan T. G. Green.
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Wurzburger, N., Ford Miniat, C. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174, 1117–1126 (2014). https://doi.org/10.1007/s00442-013-2851-0
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DOI: https://doi.org/10.1007/s00442-013-2851-0