Consequences of elevated temperatures on legume biomass and nitrogen cycling in a field warming and biodiversity experiment in a North American prairie
Heather R. Whittington A C , David Tilman B and Jennifer S. Powers A BA Department of Plant Biology, University of Minnesota, 1445 Gortner Avenue, Saint Paul, MN 55108, USA.
B Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, MN 55108, USA.
C Corresponding author. Email: whitt092@umn.edu
Functional Plant Biology 40(11) 1147-1158 https://doi.org/10.1071/FP12345
Submitted: 17 November 2012 Accepted: 17 May 2013 Published: 28 June 2013
Abstract
Increases in global temperature are likely to have effects on the nitrogen cycle, including those mediated through effects on legumes, which have a role in the N cycle by fixing N2. These effects may alter plant functioning and community structure, especially in N-limited ecosystems. We manipulated temperature and plant diversity in the field to investigate the effects of elevated temperature on aboveground biomass, shoot N concentration ([N]), and reliance on N2 fixation of four prairie legumes (Amorpha canescens Pursh., Dalea purpurea Vent., Lespedeza capitata Michx. and Lupinus perennis L.) planted in plots of varying species numbers. We monitored the effect of warming on soil microclimate and net N mineralisation rates, as these variables may mediate the effect of warming on legumes. Warming decreased soil moisture and increased soil temperature, but had no effect on net N mineralisation. Warming increased the aboveground biomass of D. purpurea and L. perennis, but decreased shoot [N] for all species in one year. Though the data were not optimal for quantifying N2 fixation using stable isotopes, they suggest that warming did not affect the reliance on N2 fixation. Species diversity did not have strong effects on the response to warming. These results suggest that legume-mediated effects of temperature on N cycling will arise from changes in biomass and tissue chemistry, not N2 fixation. We observed strong interannual variation between a wet and dry year for N mineralisation, shoot [N] and reliance on N2 fixation, suggesting that these may be more responsive to precipitation changes than elevated temperature.
Additional keywords: Amorpha canescens, Dalea purpurea, grassland, Lespedeza capitata, Lupinus perennis, Petalostemum purpureum.
References
Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology 14, 2898–2909.| Warming and drying suppress microbial activity and carbon cycling in boreal forest soils.Crossref | GoogleScholarGoogle Scholar |
Allos HF, Bartholomew WV (1955) Effect of available nitrogen on symbiotic fixation. Soil Science Society of America Journal 19, 182–184.
| Effect of available nitrogen on symbiotic fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXnsFSkuw%3D%3D&md5=3f8e40b8e43f31dd36fab8c1f6cb5ec4CAS |
An YA, Wan SQ, Zhou XH, Subedar AA, Wallace LL, Luo YQ (2005) Plant nitrogen concentration, use efficiency, and contents in a tallgrass prairie ecosystem under experimental warming. Global Change Biology 11, 1733–1744.
| Plant nitrogen concentration, use efficiency, and contents in a tallgrass prairie ecosystem under experimental warming.Crossref | GoogleScholarGoogle Scholar |
Aranjuelo I, Irigoyen JJ, Sanchez-Diaz M (2007) Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. Environmental and Experimental Botany 59, 99–108.
| Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1CqtbzO&md5=fda31a8e8e92fd97282ca1af4307ecb3CAS |
Barrios S, Raggio N, Raggio M (1963) Effect of temperature on infection of isolated bean roots by rhizobia. Plant Physiology 38, 171–174.
| Effect of temperature on infection of isolated bean roots by rhizobia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zhtl2rsw%3D%3D&md5=6ea9047f3aa3031b5a9f300b9c5400d5CAS | 16655768PubMed |
Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutrient Cycling in Agroecosystems 57, 235–270.
| Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials.Crossref | GoogleScholarGoogle Scholar |
Carlsson G, Palmborg C, Jumpponen A, Scherer-Lorenzen M, Hogberg P, Huss-Danell K (2009) N2 fixation in three perennial Trifolium species in experimental grasslands of varied plant species richness and composition. Plant Ecology 205, 87–104.
| N2 fixation in three perennial Trifolium species in experimental grasslands of varied plant species richness and composition.Crossref | GoogleScholarGoogle Scholar |
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters 11, 1065–1071.
| Plant species traits are the predominant control on litter decomposition rates within biomes worldwide.Crossref | GoogleScholarGoogle Scholar | 18627410PubMed |
Cedar Creek Ecosystem Science Reserve (CCESR) (2009) Weather data. (CCESR, St Paul). Available online at www.cedarcreek.umn.edu/research/weather [Verified 4 June 2013].
Craine JM, Jackson RD (2010) Plant nitrogen and phosphorus limitation in 98 North American grassland soils. Plant and Soil 334, 73–84.
| Plant nitrogen and phosphorus limitation in 98 North American grassland soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqur%2FM&md5=9db2df536fd676e2848a55bed47222ebCAS |
Craine JM, Tilman D, Wedin D, Reich P, Tjoelker M, Knops J (2002) Functional traits, productivity and effects on nitrogen cycling of 33 grassland species. Functional Ecology 16, 563–574.
| Functional traits, productivity and effects on nitrogen cycling of 33 grassland species.Crossref | GoogleScholarGoogle Scholar |
De Boeck HJ, Lemmens C, Bossuyt H, Malchair S, Carnol M, Merckx R, Nijs I, Ceulemans R (2006) How do climate warming and plant species richness affect water use in experimental grasslands? Plant and Soil 288, 249–261.
| How do climate warming and plant species richness affect water use in experimental grasslands?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFaksLzP&md5=befbcb7eb0c9d3b053b4522c68a62d11CAS |
De Boeck HJ, Lemmens C, Zavalloni C, Gielen B, Malchair S, Carnol M, Merckx R, Van den Berge J, Ceulemans R, Nijs I (2008) Biomass production in experimental grasslands of different species richness during three years of climate warming. Biogeosciences 5, 585–594.
| Biomass production in experimental grasslands of different species richness during three years of climate warming.Crossref | GoogleScholarGoogle Scholar |
Dijkstra FA, Wrage K, Hobbie SE, Reich PB (2006) Tree patches show greater N losses but maintain higher soil N availability than grassland patches in a frequently burned oak savanna. Ecosystems 9, 441–452.
| Tree patches show greater N losses but maintain higher soil N availability than grassland patches in a frequently burned oak savanna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVaqtb4%3D&md5=ef98387387579f63cd43ab830c92f917CAS |
Doane TA, Horwath WR (2003) Spectrophotometric determination of nitrate with a single reagent. Analytical Letters 36, 2713–2722.
| Spectrophotometric determination of nitrate with a single reagent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFGqsLY%3D&md5=0f93d03ea07238f7c35aa61761cdd7b9CAS |
Fargione JE, Tilman D (2005) Diversity decreases invasion via both sampling and complementarity effects. Ecology Letters 8, 604–611.
| Diversity decreases invasion via both sampling and complementarity effects.Crossref | GoogleScholarGoogle Scholar |
Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Frontiers in Ecology and the Environment 9, 61–67.
| Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar |
Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity-productivity relationship in an N-limited grassland. Ecology 90, 408–418.
| Ecological mechanisms associated with the positive diversity-productivity relationship in an N-limited grassland.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3jsF2mtQ%3D%3D&md5=aa00527b2ad5a22aaea0d7bc02f3a6b2CAS | 19323225PubMed |
Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. Journal of Ecology 97, 48–56.
| Linkages between plant functional composition, fine root processes and potential soil N mineralization rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFeqtrw%3D&md5=fa13a9ac77cccb8c2db768964dfcd3c8CAS |
Fritschi FB, Boote KJ, Sollenberger LE, Allen LHJ (1999) Carbon dioxide and temperature effects on forage establishment: tissue composition and nutritive value. Global Change Biology 5, 743–753.
| Carbon dioxide and temperature effects on forage establishment: tissue composition and nutritive value.Crossref | GoogleScholarGoogle Scholar |
Garten CT, Classen AT, Norby RJ, Brice DJ, Weltzin JF, Souza L (2008) Role of N2-fixation in constructed old-field communities under different regimes of [CO2], temperature, and water availability. Ecosystems 11, 125–137.
| Role of N2-fixation in constructed old-field communities under different regimes of [CO2], temperature, and water availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1Wisr0%3D&md5=e252e5640b2f57dd4f15826b04fcdef6CAS |
Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell & Environment 15, 965–985.
| The use of natural abundance of nitrogen isotopes in plant physiology and ecology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvVOju74%3D&md5=24bca36d183b5fb5647132d9bf5335f7CAS |
Harding SC, Sheehy JE (1980) Influence of shoot and root temperature on leaf growth, photosynthesis and nitrogen-fixation of lucerne. Annals of Botany 45, 229–233.
Harte J, Torn MS, Chang F-R, Feifarek B, Kinzig AP, Shaw R, Shen K (1995) Global warming and soil microclimate: results from a meadow-warming experiment. Ecological Applications 5, 132–150.
| Global warming and soil microclimate: results from a meadow-warming experiment.Crossref | GoogleScholarGoogle Scholar |
Hille Ris Lambers J, Harpole WS, Tilman D, Knops J, Reich PB (2004) Mechanisms responsible for the positive diversity–productivity relationship in Minnesota grasslands. Ecology Letters 7, 661–668.
| Mechanisms responsible for the positive diversity–productivity relationship in Minnesota grasslands.Crossref | GoogleScholarGoogle Scholar |
Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends in Ecology & Evolution 7, 336–339.
| Effects of plant species on nutrient cycling.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itVOrug%3D%3D&md5=19a4b4075ca469f04b318190ed40b009CAS |
Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecological Monographs 75, 3–35.
| Effects of biodiversity on ecosystem functioning: A consensus of current knowledge.Crossref | GoogleScholarGoogle Scholar |
Hungate BA, Dukes JS, Shaw MR, Luo YQ, Field CB (2003) Nitrogen and climate change. Science 302, 1512–1513.
| Nitrogen and climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVKmt7Y%3D&md5=a5d890a64ef25ae972fe2f57bf0b8bf0CAS | 14645831PubMed |
Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant and Soil 149, 95–102.
| Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVOqtrw%3D&md5=5ccd52ed320e5c755786a115efa64a61CAS |
Kessler W, Boller BC, Nosberger J (1990) Distinct influence of root and shoot temperature on nitrogen fixation by white clover. Annals of Botany 65, 341–346.
Kindscher K, Tieszen LL (1998) Floristic and soil organic matter changes after five and thirty-five years of native tallgrass prairie restoration. Restoration Ecology 6, 181–196.
| Floristic and soil organic matter changes after five and thirty-five years of native tallgrass prairie restoration.Crossref | GoogleScholarGoogle Scholar |
Larsen KS, Andresen LC, Beier C, Jonasson S, Albert KR, Ambus P, Arndal MF, Carter MS, Christensen S, Holmstrup M, Ibrom A, Kongstad J, van der Linden L, Maraldo K, Michelsen A, Mikkelsen TN, Pilegaard K, Prieme A, Ro-Poulsen H, Schmidt IK, Selsted MB, Stevnbak K (2011) Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Global Change Biology 17, 1884–1899.
| Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments.Crossref | GoogleScholarGoogle Scholar |
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379.
| Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed.Crossref | GoogleScholarGoogle Scholar | 18409427PubMed |
Ledgard SF, Peoples MB (1988) Measurement of nitrogen fixation in the field. In ‘Advances in nitrogen cycling in agricultural ecosystems’. (Ed. JR Wilson) pp. 351–367. (CAB International: Wallingford, UK)
Lee TD, Reich PB, Tjoelker MG (2003) Legume presence increases photosynthesis and N concentrations of co-occurring non-fixers but does not modulate their responsiveness to carbon dioxide enrichment. Oecologia 137, 22–31.
| Legume presence increases photosynthesis and N concentrations of co-occurring non-fixers but does not modulate their responsiveness to carbon dioxide enrichment.Crossref | GoogleScholarGoogle Scholar | 12802677PubMed |
Lilley JM, Bolger TP, Peoples MB, Gifford RM (2001) Nutritive value and the nitrogen dynamics of Trifolium subterraneum and Phalaris aquatica under warmer, high CO2 conditions. New Phytologist 150, 385–395.
| Nutritive value and the nitrogen dynamics of Trifolium subterraneum and Phalaris aquatica under warmer, high CO2 conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVegsrk%3D&md5=e1d1f717cf0731d1dc67f6088f057d94CAS |
Lira Junior MA, Lima AST, Arruda JRF, Smith DL (2005) Effect of root temperature on nodule development of bean, lentil, and pea. Soil Biology & Biochemistry 37, 235–239.
| Effect of root temperature on nodule development of bean, lentil, and pea.Crossref | GoogleScholarGoogle Scholar |
Meyer DR, Anderson AJ (1959) Temperature and symbiotic nitrogen fixation. Nature 183, 61
| Temperature and symbiotic nitrogen fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1MXnsVeltQ%3D%3D&md5=5194c47d5f93f7306d1e471fde05c412CAS |
Oelmann Y, Buchmann N, Gleixner G, Habekost M, Roscher C, Rosenkranz S, Schulze ED, Steinbeiss S, Temperton VM, Weigelt A, Weisser WW, Wilcke W (2011) Plant diversity effects on aboveground and belowground N pools in temperate grassland ecosystems: development in the first 5 years after establishment. Global Biogeochemical Cycles 25, GB2014
| Plant diversity effects on aboveground and belowground N pools in temperate grassland ecosystems: development in the first 5 years after establishment.Crossref | GoogleScholarGoogle Scholar |
Piha MI, Munns DN (1987) Sensitivity of the common bean (Phaseolus vulgaris L.) symbiosis to high soil temperature. Plant and Soil 98, 183–194.
| Sensitivity of the common bean (Phaseolus vulgaris L.) symbiosis to high soil temperature.Crossref | GoogleScholarGoogle Scholar |
Piper JK, Schmidt ES, Janzen AJ (2007) Effects of species richness on resident and target species components in a prairie restoration. Restoration Ecology 15, 189–198.
| Effects of species richness on resident and target species components in a prairie restoration.Crossref | GoogleScholarGoogle Scholar |
Purwantari ND, Date RA, Dart PJ (1995) Nodulation and N2 fixation by Calliandra calothyrsus and Sesbania sesban grown at different root temperatures. Soil Biology & Biochemistry 27, 421–425.
| Nodulation and N2 fixation by Calliandra calothyrsus and Sesbania sesban grown at different root temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt12rsL0%3D&md5=dbcc971e58387402261880928835b3f9CAS |
Roscher C, Thein S, Weigelt A, Temperton VM, Buchmann N, Schulze ED (2011) N2 fixation and performance of 12 legume species in a 6-year grassland biodiversity experiment. Plant and Soil 341, 333–348.
| N2 fixation and performance of 12 legume species in a 6-year grassland biodiversity experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1Wjtro%3D&md5=08b7487ea6ce1065a3cdda0362e4d0c4CAS |
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562.
| A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming.Crossref | GoogleScholarGoogle Scholar |
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602.
| Nitrogen mineralization: challenges of a changing paradigm.Crossref | GoogleScholarGoogle Scholar |
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. Journal of Experimental Botany 50, 143–155.
Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50, 871–882.
| Global warming and terrestrial ecosystems: a conceptual framework for analysis.Crossref | GoogleScholarGoogle Scholar |
Shaw MR, Harte J (2001) Response of nitrogen cycling to simulated climate change: differential responses along a subalpine ecotone. Global Change Biology 7, 193–210.
| Response of nitrogen cycling to simulated climate change: differential responses along a subalpine ecotone.Crossref | GoogleScholarGoogle Scholar |
Shearer G, Kohl DH (1989) Estimates of N2 fixation in ecosystems: the need for and basis of the 15N natural abundance method. In ‘Stable isotopes in ecological research’. (Eds PW Rundel, JR Ehleringer, KA Nagy) pp. 342–374. (Springer-Verlag: New York)
Sprent J (2001) ‘Nodulation in legumes.’ (Royal Botanic Gardens: Kew)
Thornton PE, Doney SC, Lindsay K, Moore JK, Mahowald N, Randerson JT, Fung I, Lamarque JF, Feddema JJ, Lee YH (2009) Carbon–nitrogen interactions regulate climate–carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosciences 6, 2099–2120.
| Carbon–nitrogen interactions regulate climate–carbon cycle feedbacks: results from an atmosphere-ocean general circulation model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltVCkuw%3D%3D&md5=1e6eb3bc1f91d841afc3d3fd08c53d47CAS |
Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294, 843–845.
| Diversity and productivity in a long-term grassland experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVChsb0%3D&md5=f6fb170c54ee29bdfc4e832b8876f54fCAS | 11679667PubMed |
Verburg PSJ, Johnson DW, Schorran DE, Wallace LL, Luo Y, Arnone JA (2009) Impacts of an anomalously warm year on soil nitrogen availability in experimentally manipulated intact tallgrass prairie ecosystems. Global Change Biology 15, 888–900.
| Impacts of an anomalously warm year on soil nitrogen availability in experimentally manipulated intact tallgrass prairie ecosystems.Crossref | GoogleScholarGoogle Scholar |
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i – plant demography, nitrogen fixation, ecosystem effects. Ecological Monographs 59, 247–265.
| Biological invasion by Myrica faya in Hawai’i – plant demography, nitrogen fixation, ecosystem effects.Crossref | GoogleScholarGoogle Scholar |
Wan SQ, Hui DF, Wallace L, Luo YQ (2005) Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Global Biogeochemical Cycles 19, GB2014
| Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie.Crossref | GoogleScholarGoogle Scholar |
Weatherburn MW (1967) Phenol–hypochlorite reaction for determination of ammonia. Analytical Chemistry 39, 971–974.
| Phenol–hypochlorite reaction for determination of ammonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXksFSqtLY%3D&md5=494c8d68f0be438422b2cbedf7968ab0CAS |
Wedin DA, Tilman D (1990) Species effects on nitrogen cycling – a test with perennial grasses. Oecologia 84, 433–441.
Welker JM, Fahnestock JT, Sullivan PF, Chimner RA (2005) Leaf mineral nutrition of Arctic plants in response to warming and deeper snow in northern Alaska. Oikos 109, 167–177.
| Leaf mineral nutrition of Arctic plants in response to warming and deeper snow in northern Alaska.Crossref | GoogleScholarGoogle Scholar |
West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytologist 167, 523–530.
| Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2].Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpt1ersbY%3D&md5=09fb8b652e1b767d96774fb0c20fbd31CAS | 15998403PubMed |
Whittington HR (2012) ‘Consequences of elevated temperature on prairie plants: legumes, nitrogen, and phenology.’ (University of Minnesota: Minneapolis).
Whittington HR, Deede L, Powers JS (2012) Growth responses, biomass partitioning, and nitrogen isotopes of prairie legumes in response to elevated temperature and varying nitrogen source in a growth chamber experiment. American Journal of Botany 99, 838–846.
| Growth responses, biomass partitioning, and nitrogen isotopes of prairie legumes in response to elevated temperature and varying nitrogen source in a growth chamber experiment.Crossref | GoogleScholarGoogle Scholar | 22539505PubMed |
Woodmansee RG, Vallis I, Mott JJ (1981) Grassland nitrogen. In ‘Terrestrial nitrogen cycles’. (Eds FE Clark, T Rosswell) pp. 443–462. (Swedish National Science Research Council: Stockholm)
Zaehle S, Friedlingstein P, Friend AD (2010) Terrestrial nitrogen feedbacks may accelerate future climate change. Geophysical Research Letters 37, L01401
| Terrestrial nitrogen feedbacks may accelerate future climate change.Crossref | GoogleScholarGoogle Scholar |
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84, 2042–2050.
| Plant diversity, soil microbial communities, and ecosystem function: are there any links?Crossref | GoogleScholarGoogle Scholar |
Zhou XH, Liu XZ, Wallace LL, Luo YQ (2007) Photosynthetic and respiratory acclimation to experimental warming for four species in a tallgrass prairie ecosystem. Journal of Integrative Plant Biology 49, 270–281.
| Photosynthetic and respiratory acclimation to experimental warming for four species in a tallgrass prairie ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1Gks7s%3D&md5=561221d71b70da8b5137bf4962f4c13fCAS |