A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics

New Phytologist

Volumn 199, Issue 2, 2013, Pages 441-451

  Bai, Edith ^a   Li, Shanlong ^a,b   Xu, Wenhua ^a   Li, Wei ^a   Dai, Weiwei ^a   Jiang, Ping ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Increased temperature; Mineralization; N cycling processes; Nitrification; Nitrogen fluxes

Indexed keywords

ECOSYSTEM DYNAMICS; ECOSYSTEM FUNCTION; EXPERIMENTAL STUDY; GLOBAL WARMING; GRASSLAND; HEATHLAND; IMMOBILIZATION; META-ANALYSIS; NITRIFICATION; NITROGEN; NITROGEN CYCLE; SHRUBLAND; SOIL MICROORGANISM; SOIL MOISTURE; TEMPERATURE EFFECT;

EID: 84879687371     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12252     Document Type: Article

References (84)

1. Aronson EL, McNulty SG. 2009. Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality. Agricultural and Forest Meteorology 149: 1791-1799.
2. Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8: 343-351.
3. Avrahami S, Conrad R. 2003. Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Applied and Environmental Microbiology 69: 6152-6164.
4. Bai E, Houlton BZ. 2009. Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Global Biogeochemical Cycles 23: doi: 10.1029/2008GB003361.
5. Banning NC, Murphy DV. 2008. Effect of heat-induced disturbance on microbial biomass and activity in forest soil and the relationship between disturbance effects and microbial community structure. Applied Soil Ecology 40: 109-119.
6. Barnard R, Leadley PW, Hungate BA. 2005. Global change, nitrification, and denitrification: a review. Global Biogeochemical Cycles 19: GB1007, doi: 10.1029/2004GB002282.
7. Bassirirad H. 2000. Kinetics of nutrient uptake by roots: responses to global change. New Phytologist 147: 155-169.
8. Beier C, Emmett BA, Penuelas J, Schmidt IK, Tietema A, Estiarte M, Gundersen P, Llorens L, Riis-Nielsen T, Sowerby A et al. 2008. Carbon and nitrogen cycles in European ecosystems respond differently to global warming. Science of the Total Environment 407: 692-697.
9. Bijoor NS, Czimczik CI, Pataki DE, Billings SA. 2008. Effects of temperature and fertilization on nitrogen cycling and community composition of an urban lawn. Global Change Biology 14: 2119-2131.
10. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD. 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters 11: 1316-1327.
11. Braker G, Schwarz J, Conrad R. 2010. Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiology Ecology 73: 134-148.
12. Brzostek ER, Blair JM, Dukes JS, Frey SD, Hobbie SE, Melillo JM, Mitchell RJ, Pendall E, Reich PB, Shaver GR et al. 2012. The effect of experimental warming and precipitation change on proteolytic enzyme activity: positive feedbacks to nitrogen availability are not universal. Global Change Biology 18: 2617-2625.
13. Butler S, Melillo J, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Smith R, Vario C, Scott L et al. 2012. Soil warming alters nitrogen cycling in a New England forest: implications for ecosystem function and structure. Oecologia 168: 819-828.
14. 2O fluxes in an upland grassland ecosystem. Global Change Biology 18: 2520-2531.
15. 2 and warming. Ecosystems 15: 761-774.
16. Castaldi S. 2000. Responses of nitrous oxide, dinitrogen and carbon dioxide production and oxygen consumption to temperature in forest and agricultural light-textured soils determined by model experiment. Biology and Fertility of Soils 32: 67-72.
17. Cookson WR, Osman M, Marschner P, Abaye DA, Clark I, Murphy DV, Stockdale EA, Watson CA. 2007. Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biology and Biochemistry 39: 744-756.
18. 2 effects on woody plant mass, form, and physiology. Oecologia 113: 299-313.
19. Dalias P, Anderson JM, Bottner P, Coûteaux M-M. 2001. Temperature responses of carbon mineralization in conifer forest soils from different regional climates incubated under standard laboratory conditions. Global Change Biology 7: 181-192.
20. Dalias P, Anderson JM, Bottner P, Coûteauxa M-M. 2002. Temperature responses of net nitrogen mineralization and nitrification in conifer forest soils incubated under standard laboratory conditions. Soil Biology and Biochemistry 34: 691-701.
21. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165-173.
22. 2 and warming on nitrogen cycling in a semiarid grassland. New Phytologist 187: 426-437.
23. Dijkstra FA, Prior SA, Runion GB, Torbert HA, Tian H, Lu C, Venterea RT. 2012. Effects of elevated carbon dioxide and increased temperature on methane and nitrous oxide fluxes: evidence from field experiments. Frontiers in Ecology and the Environment 10: 520-527.
24. Dong S, Scagel CF, Cheng L, Fuchigami LH, Rygiewicz PT. 2001. Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth. Tree Physiology 21: 541-547.
25. 2 flux to soil warming. Global Change Biology 11: 167-181.
26. Ellsworth DS, Reich PB. 1992. Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments. Functional Ecology 6: 423-435.
27. Fan JW, Wang K, Harris W, Zhong HP, Hu ZM, Han B, Zhang WY, Wang JB. 2009. Allocation of vegetation biomass across a climate-related gradient in the grasslands of Inner Mongolia. Journal of Arid Environments 73: 521-528.
28. 2 and temperature on soil enzyme activity in the subalpine fir forest. Acta Ecologica Sinica 27: 4019-4026.
29. Fierer N, Schimel JP, Holden PA. 2003. Influence of drying-rewetting frequency on soil bacterial community structure. Microbial Ecology 45: 63-71.
30. Frey SD, Drijber R, Smith H, Melillo J. 2008. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biology and Biochemistry 40: 2904-2907.
31. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320: 889-892.
32. Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H. 1998. Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist 138: 275-285.
33. Gödde M, Conrad R. 1999. Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biology and Fertility of Soils 30: 33-40.
34. Groffman P, Butterbach-Bahl K, Fulweiler R, Gold A, Morse J, Stander E, Tague C, Tonitto C, Vidon P. 2009. Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93: 49-77.
35. Groffman P, Driscoll C, Fahey T, Hardy J, Fitzhugh R, Tierney G. 2001. Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochemistry 56: 191-213.
36. Gruber N, Galloway JN. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451: 293-296.
37. Gurevitch J, Hedges LV. 1993. Meta-analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J, eds. Design and analysis of ecological experiments. New York, NY, USA: Chapman and Hall, 378-398.
38. Hedges LV, Gurevitch J, Curtis PS. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156.
39. Hopkins FM, Torn MS, Trumbore SE. 2012. Warming accelerates decomposition of decades-old carbon in forest soils. Proceedings of the National Academy of Sciences, USA 109: E1753-E1761.
40. Kattge J, Knorr W, Raddatz T, Wirth C. 2009. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15: 976-991.
41. Koch O, Tscherko D, Kandeler E. 2007. Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochemical Cycles 21: GB4017, doi: 10.1029/2007GB002983.
42. Liu W, Zhang Z, Wan S. 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology 15: 184-195.
43. 2, temperature and N fertilization on nitrogen fluxes in a temperate grassland ecosystem. Global Change Biology 6: 953-965.
44. Lu M, Zhou X, Yang Q, Li H, Luo Y, Fang C, Chen J, Yang X, Li B. (in press). Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology, doi: 10.1890/12-0279.1
45. 2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87: 53-63.
46. Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ et al. 2004. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54: 731-739.
47. Maag M, Vinther FP. 1996. Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Applied Soil Ecology 4: 5-14.
48. Mahendrappa MK, Smith RL, Christiansen AT. 1966. Nitrifying organisms affected by climatic region in Western United States. Soil Science Society of America Journal 30: 60-62.
49. Malhi SS, McGill WB. 1982. Nitrification in three Alberta soils: effect of temperature, moisture and substrate concentration. Soil Biology and Biochemistry 14: 393-399.
50. Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298: 2173-2176.
51. Niklińska M, Maryański M, Laskowski R. 1999. Effect of temperature on humus respiration rate and nitrogen mineralization: implications for global climate change. Biogeochemistry 44: 239-257.
52. Ollinger SV, Richardson AD, Martin ME, Hollinger DY, Frolking SE, Reich PB, Plourde LC, Katul GG, Munger JW, Oren R et al. 2008. Canopy nitrogen, carbon assimilation, and albedo in temperate and boreal forests: functional relations and potential climate feedbacks. Proceedings of the National Academy of Sciences, USA 105: 19336-19341.
53. Owen JS, Wang MK, Wang CH, King HB, Sun HL. 2003. Net N mineralization and nitrification rates in a forested ecosystem in northeastern Taiwan. Forest Ecology and Management 176: 519-530.
54. 2 Enrichment experiment. New Phytologist 174: 823-834.
55. Patil RH, Laegdsmand M, Olesen JE, Porter JR. 2010. Effect of soil warming and rainfall patterns on soil N cycling in Northern Europe. Agriculture, Ecosystems & Environment 139: 195-205.
56. 2 and temperature: a discussion of observations, measurement methods, and models. New Phytologist 162: 311-322.
57. Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Høye TT et al. 2009. Ecological dynamics across the arctic associated with recent climate change. Science 325: 1355-1358.
58. 2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326: 123-125.
59. Reich PB, Walters MB, Ellsworth DS, Uhl C. 1994. Photosynthesis-nitrogen relations in Amazonian tree species. Oecologia 97: 62-72.
60. Reich PB, Walters MB, Kloeppel BD, Ellsworth DS. 1995. Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104: 24-30.
61. Rogelj J, Meinshausen M, Knutti R. 2012. Global warming under old and new scenarios using IPCC climate sensitivity range estimates. Nature Climate Change 2: 248-253.
62. Rosenberg M, Adams D, Gurevitch J. 2000. MetaWin: Statistical software for meta-analysis. Sunderland, MA, USA: Sinauer Associates.
63. 4 flux from a low elevation spruce-fir forest soil in Maine, USA. Global Change Biology 4: 597-605.
64. Rustad LR, Campbell JC, Marion GM, Norby RN, Mitchell MM, Hartley AH, Cornelissen JC, Gurevitch JG, Gcte-News G-N. 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.
65. Saad OALO, Conrad R. 1993. Temperature dependence of nitrification, denitrification, and turnover of nitric oxide in different soils. Biology and Fertility of Soils 15: 21-27.
66. Saxe H, Cannell MGR, Johnsen Ø, Ryan MG, Vourlitis G. 2001. Tree and forest functioning in response to global warming. New Phytologist 149: 369-399.
67. 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.
68. Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A. 2003. Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. European Journal of Soil Science 54: 779-791.
69. Stres B, Danevčič T, Pal L, Fuka MM, Resman L, Leskovec S, Hacin J, Stopar D, Mahne I, Mandic-Mulec I. 2008. Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiology Ecology 66: 110-122.
70. Szukics U, Abell GCJ, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S. 2010. Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiology Ecology 72: 395-406.
71. Thorup-Kristensen K, Salmerón Cortasa M, Loges R. 2009. Winter wheat roots grow twice as deep as spring wheat roots, is this important for N uptake and N leaching losses? Plant and Soil 322: 101-114.
72. Tiedje JM. 1988. Ecology of denitrification and dissimilatory nitrate reduction. In: Zehnder AJB, ed. Biology of anaerobic organisms. New York, NY, USA: John Wiley & Sons, 179-244.
73. 2 levels. Soil Biology and Biochemistry 33: 491-501.
74. Turnbull MH, Murthy R, Griffin KL. 2002. The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides. Plant, Cell & Environment 25: 1729-1737.
75. Turner M, Henry H. 2010. Net nitrogen mineralization and leaching in response to warming and nitrogen deposition in a temperate old field: the importance of winter temperature. Oecologia 162: 227-236.
76. Venterea RT, Lovett GM, Groffman PM, Schwarz PA. 2003. Landscape patterns of net nitrification in a Northern Hardwood-Conifer Forest. Soil Science Society of America Journal 67: 527-539.
77. Verburg PSJ, Johnson DW, Schorran DE, Wallace LL, Luo Y, Arnone Iii 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.
78. Wan S, Hui D, Wallace L, Luo Y. 2005. Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Global Biogeochemical Cycles 19: GB2014.
79. Weih M, Karlsson PS. 2002. Low winter soil temperature affects summertime nutrient uptake capacity and growtht rate of mountain birch seedlings in the subarctic, Swedish lapland. Arctic, Antarctic, and Alpine Research 34: 434-439.
80. Wisser D, Marchenko S, Talbot J, Treat C, Frolking S. 2011. Soil temperature response to 21st century global warming: the role of and some implications for peat carbon in thawing permafrost soils in North America. Earth System Dynamics 2: 121-138.
81. Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N. 2009. Initial community evenness favours functionality under selective stress. Nature 458: 623-626.
82. Wu Z, Dijkstra P, Koch GW, Hungate BA. 2012. Biogeochemical and ecological feedbacks in grassland responses to warming. Nature Climate Change 2: 458-461.
83. Yin H, Chen Z, Liu Q. 2012. Effects of experimental warming on soil N transformations of two coniferous species, Eastern Tibetan Plateau, China. Soil Biology and Biochemistry 50: 77-84.
84. Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S. 2005. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Global Change Biology 11: 266-277.