Drought of early time in growing season decreases community aboveground biomass, but increases belowground biomass in a desert steppe

Churkina G, Running SW. Contrasting climatic controls on the estimated productivity of global terrestrial biomes. Ecosystems. 1998;1(2):206–15. Cleland EE, Collins SL, Dickson TL, Farrer EC, Gross KL, Gherardi LA, Hallett LM, Hobbs RJ, Hsu JS, Turnbull L, et al. Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. Ecology. 2013;94(8):1687–96. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO. Climate extremes: observations, modeling, and impacts. Science. 2000;289(5487):2068–74. Smith MD. An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J Ecol. 2011;99(3):656–63. Knapp AK, Hoover DL, Wilcox KR, Avolio ML, Koerner SE, La Pierre KJ, Loik ME, Luo YQ, Sala OE, Smith MD. Characterizing differences in precipitation regimes of extreme wet and dry years: implications for climate change experiments. Global Change Biol. 2015;21(7):2624–33. Copeland SM, On SPH, Latimer AM, Damschen EI, Eskelinen AM, Fernandez-Going B, Spasojevic MJ, Anacker BL, Thorne JH. Ecological effects of extreme drought on Californian herbaceous plant communities. Ecol Monogr. 2016;86(3):295–311. Huxman TE, Smith MD, Fay PA, Knapp AK, Shaw MR, Loik ME, Smith SD, Tissue DT, Zak JC, Weltzin JF, et al. Convergence across biomes to a common rain-use efficiency. Nature. 2004;429(6992):651–4. McConnaughay KDM, Coleman JS. Biomass allocation in plants: Ontogeny or optimality? A test along three resource gradients. Ecology. 1999;80(8):2581–93. Frank DA. Drought effects on above- and belowground production of a grazed temperate grassland ecosystem. Oecologia. 2007;152(1):131–9. Kreyling J, Beierkuhnlein C, Elmer M, Pritsch K, Radovski M, Schloter M, Wollecke J, Jentsch A. Soil biotic processes remain remarkably stable after 100-year extreme weather events in experimental grassland and heath. Plant Soil. 2008;308(1–2):175–88. Harrison S, Spasojevic MJ, Li D. Climate and plant community diversity in space and time. Proc Natl Acad Sci U S A. 2020;117(9):4464–70. Griffin-Nolan RJ, Bushey JA, Carroll CJW, Challis A, Chieppa J, Garbowski M, Hoffman AM, Post AK, Slette IJ, Spitzer D, et al. Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes. Funct Ecol. 2018;32(7):1746–56. Wu GL, Zhang ZN, Wang D, Shi ZH, Zhu YJ. Interactions of soil water content heterogeneity and species diversity patterns in semi-arid steppes on the Loess Plateau of China. J Hydrol. 2014;519:1362–7. Yin QL, Tian TT, Han XH, Xu JS, Chai YF, Mo J, Lei ML, Wang L, Yue M. The relationships between biomass allocation and plant functional trait. Ecol Indic. 2019;102:302–8. Schaeffer SM, Homyak PM, Boot CM, Roux-Michollet D, Schimel JP. Soil carbon and nitrogen dynamics throughout the summer drought in a California annual grassland. Soil Biol Biochem. 2017;115:54–62. Knapp AK, Smith MD. Variation among biomes in temporal dynamics of aboveground primary production. Science. 2001;291(5503):481–4. Bradford JB, Schlaepfer DR, Lauenroth WK, Palmquist KA. Robust ecological drought projections for drylands in the 21st century. Global Change Biol. 2020;26(7):3906–19. Knapp AK, Fay PA, Blair JM, Collins SL, Smith MD, Carlisle JD, Harper CW, Danner BT, Lett MS, McCarron JK. Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science. 2002;298(5601):2202–5. Felton AJ, Slette IJ, Smith MD, Knapp AK. Precipitation amount and event size interact to reduce ecosystem functioning during dry years in a mesic grassland. Global Change Biol. 2020;26(2):658–68. Harrison S, Spasojevic MJ, Li DJ. Climate and plant community diversity in space and time. P Natl Acad Sci USA. 2020;117(9):4464–70. Chen YX, Huang YY, Niklaus PA, Castro-Izaguirre N, Clark AT, Bruelheide H, Ma KP, Schmid B. Directed species loss reduces community productivity in a subtropical forest biodiversity experiment. Nat Ecol Evol. 2020;4(4):660–660. Grace JB, Anderson TM, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hautier Y, Hillebrand H, Lind EM, Partel M, et al. Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature. 2016;529(7586):390. Rabosky DL, Hurlbert AH. Species richness at continental scales is dominated by ecological limits. Am Nat. 2015;185(5):572–83. Li Y, Dong S, Liu S, Su X, Wang X, Zhang Y, Zhao Z, Gao X, Li S, Tang L. Relationships between plant diversity and biomass production of alpine grasslands are dependent on the spatial scale and the dimension of biodiversity. Ecol Eng. 2019;127:375–82. Gastine A, Scherer-Lorenzen M, Leadley PW. No consistent effects of plant diversity on root biomass, soil biota and soil abiotic conditions in temperate grassland communities. Appl Soil Ecol. 2003;24(1):101–11. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C. Diversity and productivity in a long-term grassland experiment. Science. 2001;294(5543):843–5. Craine JM, Reich PB, Tilman GD, Ellsworth D, Fargione J, Knops J, Naeem S. The role of plant species in biomass production and response to elevated CO2 and N. Ecol Lett. 2003;6(7):623–30. Wu GL, Liu Y, Tian FP, Shi ZH. Legumes functional group promotes soil organic carbon and nitrogen storage by increasing plant diversity. Land Degrad Dev. 2017;28(4):1336–44. Kimball S, Funk JL, Spasojevic MJ, Suding KN, Parker S, Goulden ML. Can functional traits predict plant community response to global change? Ecosphere. 2016;7:12. Costa DS, Gerschlauer F, Pabst H, Kuhnel A, Huwe B, Kiese R, Kuzyakov Y, Kleyer M. Community-weighted means and functional dispersion of plant functional traits along environmental gradients on Mount Kilimanjaro. J Veg Sci. 2017;28(4):684–95. Bruelheide H, Dengler J, Purschke O, Lenoir J, Jimenez-Alfaro B, Hennekens SM, Botta-Dukat Z, Chytry M, Field R, Jansen F, et al. Global trait-environment relationships of plant communities. Nat Ecol Evol. 2018;2(12):1906–17. Zuo XA, Zhang J, Lv P, Zhou X, Li YL, Luo YY, Luo YQ, Lian J, Yue XY. Plant functional diversity mediates the effects of vegetation and soil properties on community-level plant nitrogen use in the restoration of semiarid sandy grassland. Ecol Indic. 2016;64:272–80. Sandel B, Goldstein LJ, Kraft NJ, Okie JG, Shuldman MI, Ackerly DD, Cleland EE, Suding KN. Contrasting trait responses in plant communities to experimental and geographic variation in precipitation. New Phytol. 2010;188(2):565–75. Le Bagousse-Pinguet Y, Gross N, Maestre FT, Maire V, de Bello F, Fonseca CR, Kattge J, Valencia E, Leps J, Liancourt P. Testing the environmental filtering concept in global drylands. J Ecol. 2017;105(4):1058–69. Forrestel EJ, Donoghue MJ, Edwards EJ, Jetz W, du Toit JCO, Smith MD. Different clades and traits yield similar grassland functional responses. P Natl Acad Sci USA. 2017;114(4):705–10. Yue XY, Zuo XA, Yu Q, Xu C, Lv P, Zhang J, Knapp AK, Smith MD. Response of plant functional traits of Leymus chinensis to extreme drought in Inner Mongolia grasslands. Plant Ecol. 2019;220(2):141–9. Kobe RK, Iyer M, Walters MB. Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology. 2010;91(1):166–79. van Wijk MT. Understanding plant rooting patterns in semi-arid systems: an integrated model analysis of climate, soil type and plant biomass. Global Ecol Biogeogr. 2011;20(2):331–42. Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, Korner C, de Boeck HJ, Christensen JH, Leuzinger S, Janssens IA, et al. Precipitation manipulation experiments—challenges and recommendations for the future. Ecol Lett. 2012;15(8):899–911. Sardans J, Penuelas J. Potassium: a neglected nutrient in global change. Global Ecol Biogeogr. 2015;24(3):261–75. He MZ, Dijkstra FA. Drought effect on plant nitrogen and phosphorus: a metaanalysis. New Phytol. 2014;204(4):924–31. Gessler A, Schaub M, McDowell NG. The role of nutrients in drought-induced tree mortality and recovery. New Phytol. 2017;214(2):513–20. Griffin-Nolan RJ, Carroll CJW, Denton EM, Johnston MK, Collins SL, Smith MD, Knapp AK. Legacy effects of a regional drought on aboveground net primary production in six central US grasslands. Plant Ecol. 2018;219(5):505–15. Grime JP, Brown VK, Thompson K, Masters GJ, Hillier SH, Clarke IP, Askew AP, Corker D, Kielty JP. The response of two contrasting limestone grasslands to simulated climate change. Science. 2000;289(5480):762–5. Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG. Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology. 2008;89(8):2140–53. Luo WT, Zuo XA, Griffin-Nolan RJ, Xu C, Ma W, Song L, Helsen K, Lin YC, Cai JP, Yu Q, et al. Long term experimental drought alters community plant trait variation, not trait means, across three semiarid grasslands. Plant Soil. 2019;442(1–2):343–53. Cornwell WK, Ackerly DD. Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr. 2009;79(1):109–26. Stampfli A, Zeiter M. Mechanisms of structural change derived from patterns of seedling emergence and mortality in a semi-natural meadow. J Veg Sci. 2008;19(4):563-U516. Zeiter M, Scharrer S, Zweifel R, Newbery DM, Stampfli A. Timing of extreme drought modifies reproductive output in semi-natural grassland. J Veg Sci. 2016;27(2):238–48. Muscarella R, Uriarte M. Do community-weighted mean functional traits reflect optimal strategies? Proc Biol Sci. 1827;2016(283):20152434. Mudrak O, de Bello F, Dolezal J, Leps J. Changes in the functional trait composition and diversity of meadow communities induced by Rhinanthus minor L. Folia Geobot. 2016;51(1):1–11. Al Haj Khaled R, Duru M, Theau JP, Plantureux S, Cruz P. Variation in leaf traits through seasons and N-availability levels and its consequences for ranking grassland species. J Veg Sci. 2005;16(4):391–8. Li YL, Johnson DA, Su YZ, Cui JY, Zhang TH. Specific leaf area and leaf dry matter content of plants growing in sand dunes. Bot Bull Acad Sinica. 2005;46(2):127–34. He JS, Wang ZH, Wang XP, Schmid B, Zuo WY, Zhou M, Zheng CY, Wang MF, Fang JY. A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytol. 2006;170(4):835–48. Wright IJ, Reich PB, Westoby M. Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol. 2001;15(4):423–34. Deleglise C, Meisser M, Mosimann E, Spiegelberger T, Signarbieux C, Jeangros B, Buttler A. Drought-induced shifts in plants traits, yields and nutritive value under realistic grazing and mowing managements in a mountain grassland. Agr Ecosyst Environ. 2015;213:94–104. Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T. Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol. 2014;102(1):45–53. Ren CJ, Zhao FZ, Shi Z, Chen J, Han XH, Yang GH, Feng YZ, Ren GX. Differential responses of soil microbial biomass and carbon-degrading enzyme activities to altered precipitation. Soil Biol Biochem. 2017;115:1–10. Deng L, Peng CH, Kim DG, Li JW, Liu YL, Hai XY, Liu QY, Huang CB, Shangguan ZP, Kuzyakov Y. Drought effects on soil carbon and nitrogen dynamics in global natural ecosystems. Earth-Sci Rev. 2021;214:25. Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. P Natl Acad Sci USA. 2004;101(30):11001–6. Luo W, Elser JJ, Lü XT, Wang Z, Bai E, Yan C, Wang C, Li MH, Zimmermann NE, Han X, et al. Plant nutrients do not covary with soil nutrients under changing climatic conditions. Global Biogeochem Cycles. 2015;29(8):1298–308. de la Riva EG, Perez-Ramos IM, Tosto A, Navarro-Fernandez CM, Olmo M, Maranon T, Villar R. Disentangling the relative importance of species occurrence, abundance and intraspecific variability in community assembly: a trait-based approach at the whole-plant level in Mediterranean forests. Oikos. 2016;125(3):354–63. Luo W, Zuo X, Ma W, Xu C, Li A, Yu Q, Knapp AK, Tognetti R, Dijkstra FA, Li MH, et al. Differential responses of canopy nutrients to experimental drought along a natural aridity gradient. Ecology. 2018;99(10):2230–9. He M, Dijkstra FA. Drought effect on plant nitrogen and phosphorus: a meta-analysis. New Phytol. 2014;204(4):924–31. Zhang BW, Cadotte MW, Chen SP, Tan XR, You CH, Ren TT, Chen ML, Wang SS, Li WJ, Chu CJ, et al. Plants alter their vertical root distribution rather than biomass allocation in response to changing precipitation. Ecology. 2019;100:11. Bai YF, Han XG, Wu JG, Chen ZZ, Li LH. Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature. 2004;431(7005):181–4. Ansley RJ, Boutton TW, Jacoby PW. Root biomass and distribution patterns in a semi-arid mesquite savanna: responses to long-term rainfall manipulation. Rangeland Ecol Manag. 2014;67(2):206–18. Zhang B, Cadotte MW, Chen S, Tan X, You C, Ren T, Chen M, Wang S, Li W, Chu C, et al. Plants alter their vertical root distribution rather than biomass allocation in response to changing precipitation. Ecology. 2019;100(11):e02828. Sala OE, Gherardi LA, Reichmann L, Jobbagy E, Peters D. Legacies of precipitation fluctuations on primary production: theory and data synthesis. Philos T R Soc B. 2012;367(1606):3135–44. Bai Y, Wu J, Pan Q, Huang J, Wang Q, Li F, Buyantuyev A, Han X. Positive linear relationship between productivity and diversity: evidence from the Eurasian Steppe. J Appl Ecol. 2007;44(5):1023–34. Bhandari J, Zhang Y. Effect of altitude and soil properties on biomass and plant richness in the grasslands of Tibet, China, and Manang District. Nepal Ecosphere. 2019;10:788. Schumacher J, Roscher C. Differential effects of functional traits on aboveground biomass in semi-natural grasslands. Oikos. 2009;118(11):1659–68. Zuo XA, Zhang J, Lv P, Wang SK, Yang Y, Yue XY, Zhou X, Li YL, Chen M, Lian J, et al. Effects of plant functional diversity induced by grazing and soil properties on above- and belowground biomass in a semiarid grassland. Ecol Indic. 2018;93:555–61. Lavorel S. Plant functional effects on ecosystem services. J Ecol. 2013;101(1):4–8. Zhang Q, Buyantuev A, Li FY, Jiang L, Niu JM, Ding Y, Kang S, Ma WJ. Functional dominance rather than taxonomic diversity and functional diversity mainly affects community aboveground biomass in the Inner Mongolia grassland. Ecol Evol. 2017;7(5):1605–15. Shi Y, Su C, Wang M, Liu X, Liang C, Zhao L, Zhang X, Minggagud H, Feng G, Ma W. Modern climate and soil properties explain functional structure better than phylogenetic structure of plant communities in Northern China. Front Ecol Evol. 2020;8:24. Shi Z, Thomey ML, Mowll W, Litvak M, Brunsell NA, Collins SL, Pockman WT, Smith MD, Knapp AK, Luo Y. Differential effects of extreme drought on production and respiration: synthesis and modeling analysis. Biogeosciences. 2014;11(3):621–33. Denton EM, Dietrich JD, Smith MD, Knapp AK. Drought timing differentially affects above- and belowground productivity in a mesic grassland. Plant Ecol. 2017;218(3):317–28. Zheng SX, Ren HY, Lan ZC, Li WH, Wang KB, Bai YF. Effects of grazing on leaf traits and ecosystem functioning in Inner Mongolia grasslands: scaling from species to community. Biogeosciences. 2010;7(3):1117–32. Liu LX, Zhao XY, Chang XL, Lian J. Impact of Precipitation Fluctuation on Desert-Grassland ANPP. Sust Basel. 2016;8:12. Yahdjian L, Sala OE. A rainout shelter design for intercepting different amounts of rainfall. Oecologia. 2002;133(2):95–101. Valencia E, Maestre FT, Le Bagousse-Pinguet Y, Quero JL, Tamme R, Borger L, Garcia-Gomez M, Gross N. Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol. 2015;206(2):660–71. Guittar J, Goldberg D, Klanderud K, Telford RJ, Vandvik V. Can trait patterns along gradients predict plant community responses to climate change? Ecology. 2016;97(10):2791–801. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, et al. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot. 2003;51(4):335–80. Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT. Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct Ecol. 2013;27(5):1254–61. Debouk H, de Bello F, Sebastia MT. Functional trait changes, productivity shifts and vegetation stability in mountain grasslands during a short-term warming. Plos One. 2015;10:10.