Long term experimental drought alters community plant trait variation, not trait means, across three semiarid grasslands

  • Wentao Luo
  • Xiaoan ZuoEmail author
  • Robert J. Griffin-Nolan
  • Chong Xu
  • Wang Ma
  • Lin Song
  • Kenny Helsen
  • Yingchao Lin
  • Jiangping Cai
  • Qiang Yu
  • Zhengwen WangEmail author
  • Melinda D. Smith
  • Xingguo Han
  • Alan K. Knapp
Regular Article


Background and aims

Grasslands are expected to experience droughts of unprecedented magnitude and duration in this century. Plant traits can be useful for understanding community and ecosystem responses to climate extremes. Few studies, however, have investigated the response of community-scale traits to extreme drought on broad spatial/temporal scales, with even less research on the relative contribution of species turnover vs. intraspecific trait variation to such responses.


We experimentally removed ~66% of growing season rainfall for three years across three semi-arid grasslands of northern China and tracked changes in community functional composition, defined as the community mean and variation of several leaf economic traits.


Community trait variations were more sensitive to drought than community trait means, which suggests this component of functional composition may be a better indicator of initial community drought responses than trait values themselves. The greatest change in trait variation was observed at the high aridity site and was driven largely by intraspecific trait variability. Apart from specific leaf area, trait variability increased with increasing aridity across sites, largely due to species turnover. Variations in soil moisture and fertility likely mediated the responses of community trait variations to water stress.


These results highlight the importance of measuring community trait variability in response to drought and support the well-documented pattern of increased community drought sensitivity of more arid ecosystems.


Climate change Plant functional traits Grasslands Intraspecific trait variability Species turnover 



This study was supported by funding from National Natural Science Foundation of China (41603080, 41600302, 41622103, 31822006 and 41320104002), National Key Research and Development Program of China (2016YFC0500601 and 2016YFC0500602), and Strategic Priority Research Program of Chinese Academic of Sciences (XDA23080401). We thank all who worked in Extreme Drought in Grasslands Experiment (EDGE) project for assistance in planning and conducting the field experiment. Qiang Yu designed the experiment, all questions and correspondence about the experiment should be forwarded to him (

Supplementary material

11104_2019_4176_MOESM1_ESM.docx (1.4 mb)
ESM 1 (DOCX 1398 kb)


  1. Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145CrossRefGoogle Scholar
  2. Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Funct Ecol 24:1192–1201CrossRefGoogle Scholar
  3. Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc Natl Acad Sci 113:5024–5029CrossRefGoogle Scholar
  4. Auger S, Shipley B (2013) Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest. J Veg Sci 24:419–428CrossRefGoogle Scholar
  5. Benedetti-Cecchi L (2003) The importance of the variation around the mean effect size if ecology processes. Ecology 84:2335–2346CrossRefGoogle Scholar
  6. Bernard-Verdier M, Navas ML, Vellend M, Violle C, Fayolle A, Garnier E (2012) Community assembly along a soil depth gradient: contrasting patterns of plant trait convergence and divergence in a Mediterranean rangeland. J Ecol 100:1422–1433CrossRefGoogle Scholar
  7. Bruelheide H, Dengler J, Purschke O, Lenoir J, Jiménez-Alfaro B, Hennekens SM, Botta-Dukát Z, Chytrý M, Field R, Jansen F, Kattge J, Pillar VD, Schrodt F, Mahecha MD, Peet RK, Sandel B, van Bodegom P, Altman J, Alvarez-Dávila E, Arfin Khan MAS, Attorre F, Aubin I, Baraloto C, Barroso JG, Bauters M, Bergmeier E, Biurrun I, Bjorkman AD, Blonder B, Čarni A, Cayuela L, Černý T, Cornelissen JHC, Craven D, Dainese M, Derroire G, de Sanctis M, Díaz S, Doležal J, Farfan-Rios W, Feldpausch TR, Fenton NJ, Garnier E, Guerin GR, Gutiérrez AG, Haider S, Hattab T, Henry G, Hérault B, Higuchi P, Hölzel N, Homeier J, Jentsch A, Jürgens N, Kącki Z, Karger DN, Kessler M, Kleyer M, Knollová I, Korolyuk AY, Kühn I, Laughlin DC, Lens F, Loos J, Louault F, Lyubenova MI, Malhi Y, Marcenò C, Mencuccini M, Müller JV, Munzinger J, Myers-Smith IH, Neill DA, Niinemets Ü, Orwin KH, Ozinga WA, Penuelas J, Pérez-Haase A, Petřík P, Phillips OL, Pärtel M, Reich PB, Römermann C, Rodrigues AV, Sabatini FM, Sardans J, Schmidt M, Seidler G, Silva Espejo JE, Silveira M, Smyth A, Sporbert M, Svenning JC, Tang Z, Thomas R, Tsiripidis I, Vassilev K, Violle C, Virtanen R, Weiher E, Welk E, Wesche K, Winter M, Wirth C, Jandt U (2018) Global trait-environment relationships of plant communities. Nature Ecology and Evolution 2:1906–1917CrossRefGoogle Scholar
  8. Cherwin K, Knapp A (2012) Unexpected patterns of sensitivity to drought in three semi-arid grasslands. Oecologia 169:845–852CrossRefGoogle Scholar
  9. Cleland EE, Collins SL, Dickson TL, Farrer EC, Gross KL, Gherardi LA, Hallett LM, Hobbs RJ, Hsu JS, Turnbull L, Suding KN (2013) Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. Ecology 94:1687–1696CrossRefGoogle Scholar
  10. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126CrossRefGoogle Scholar
  11. Dai AG (2011) Drought under global warming: a review. Wiley Interdisciplinary Reviews-Climate Change 2:45–65CrossRefGoogle Scholar
  12. Dunne JA, Saleska SR, Fischer ML, Harte J (2004) Integrating experimental and gradient methods in ecological climate change research. Ecology 85:904–916CrossRefGoogle Scholar
  13. Elmendorf SC, Henry GHR, Hollister RD, Fosaa AM, Gould WA, Hermanutz L, Hofgaard A, Jónsdóttir IS, Jorgenson JC, Lévesque E, Magnusson B, Molau U, Myers-Smith IH, Oberbauer SF, Rixen C, Tweedie CE, Walker MD (2015) Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns. Proc Natl Acad Sci 112:448–452CrossRefGoogle Scholar
  14. Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol 15:688–695CrossRefGoogle Scholar
  15. Griffin-Nolan RJ, Bushey Julie A, Carroll Charles JW et al (2018a) Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes. Funct Ecol 32:1746–1756CrossRefGoogle Scholar
  16. Griffin-Nolan RJ, Carroll CJW, Denton EM, Johnston MK, Collins SL, Smith MD, Knapp AK (2018b) Legacy effects of a regional drought on aboveground net primary production in six central US grasslands. Plant Ecol 219:505–515CrossRefGoogle Scholar
  17. Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. J Veg Sci 17:255–260CrossRefGoogle Scholar
  18. Grime JP, Brown VK, Thompson K, Masters GJ, Hillier SH, Clarke IP, Askew AP, Corker D, Kielty JP (2000) The response of two contrasting limestone grasslands to simulated climate change. Science 289:762–765CrossRefGoogle Scholar
  19. Handmer, Honda Y, Kundzewicz ZW et al. (2012) Changes in impacts of climate extremes: Human systems and ecosystems, in Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (IPCC SREX Report), edited by Field CB et al., pp. 231–290, Cambridge Univ. Press, Cambridge, U. K., and New YorkGoogle Scholar
  20. He N, Liu C, Piao S et al (2018) Ecosystem traits linking functional traits to macroecology. Trends Ecol Evol 34:200–210CrossRefGoogle Scholar
  21. Hewitt JE, Thrush SF, Dayton PK, Bonsdorff E (2007) The effect of spatial and temporal heterogeneity on the design and analysis of empirical studies of scale-dependent systems. Am Nat 169:398–408CrossRefGoogle Scholar
  22. Hoover DL, Knapp AK, Smith MD (2014) Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95:2646–2656CrossRefGoogle Scholar
  23. Huxman TE, Smith MD, Fay PA, Knapp AK, Shaw MR, Loik ME, Smith SD, Tissue DT, Zak JC, Weltzin JF, Pockman WT, Sala OE, Haddad BM, Harte J, Koch GW, Schwinning S, Small EE, Williams DG (2004) Convergence across biomes to a common rain-use efficiency. Nature 429:651–654CrossRefGoogle Scholar
  24. Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102:45–53CrossRefGoogle Scholar
  25. Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140CrossRefGoogle Scholar
  26. Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct Ecol 27:1254–1261CrossRefGoogle Scholar
  27. Knapp AK, Avolio ML, Beier C et al (2016) Pushing precipitation to the extremes in distributed experiments: recommendations for simulating wet and dry years. Glob Chang Biol 23:1774–1782CrossRefGoogle Scholar
  28. Knapp AK, Carroll CJW, Griffin-Nolan RJ, Slette IJ, Chaves FA, Baur LE, Felton AJ, Gray JE, Hoffman AM, Lemoine NP, Mao W, Post AK, Smith MD (2018) A reality check for climate change experiments: do they reflect the real world? Ecology 99:2145–2151CrossRefGoogle Scholar
  29. Lepš J, De Bello F, Smilauer P, Dolezal J (2011) Community trait response to environment: disentangling species turnover vs. intraspecific trait variability effects. Ecography 34:856–863CrossRefGoogle Scholar
  30. Luo W, Elser JJ, Lü XT, Wang Z, Bai E, Yan C, Wang C, Li MH, Zimmermann NE, Han X, Xu Z, Li H, Wu Y, Jiang Y (2015) Plant nutrients do not covary with soil nutrients under changing climatic conditions. Glob Biogeochem Cycles 29:1298–1308CrossRefGoogle Scholar
  31. Luo W, Zuo X, Ma W, Xu C, Li A, Yu Q, Knapp AK, Tognetti R, Dijkstra FA, Li MH, Han G, Wang Z, Han X (2018) Differential responses of canopy nutrients to experimental drought along a natural aridity gradient. Ecology 99:2230–2239CrossRefGoogle Scholar
  32. Luo YQ, Melillo J, Niu SL et al (2011) Coordinated approaches to quantify long-term ecosystem dynamics in response to global change. Glob Chang Biol 17:843–854CrossRefGoogle Scholar
  33. Mason NWH, Richardson SJ, Peltzer DA, De Bello F, Wardle DA, Allen RB (2012) Changes in coexistence mechanisms along a long-term soil chronosequence revealed by functional trait diversity. J Ecol 100:678–689CrossRefGoogle Scholar
  34. Matthew C, van Loo EN, Thom ER, Dawson LA, Care DA (2001) Understanding shoot and root development. In: Proceedings of the XIX International Grassland Congress, São Paulo, BrazilGoogle Scholar
  35. Nogueira C, Nunes A, Bugalho MN, Branquinho C, McCulley RL, Caldeira MC (2018) Nutrient addition and drought interact to change the structure and decrease the functional diversity of a Mediterranean grassland. Front Ecol Evol 6:155CrossRefGoogle Scholar
  36. Pérez-Harguindeguy N, Diaz S, Garnier E et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234CrossRefGoogle Scholar
  37. Reich PB (2014) The world-wide 'fast-slow' plant economics spectrum: a traits manifesto. J Ecol 102:275–301CrossRefGoogle Scholar
  38. Sandel B, Goldstein LJ, Kraft NJ et al (2010) Contrasting trait responses in plant communities to experimental and geographic variation in precipitation. New Phytol 188:565–575CrossRefGoogle Scholar
  39. Smith MD (2011) An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J Ecol 99:656–663CrossRefGoogle Scholar
  40. Smith MD, Knapp AK, Collins SL (2009) A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 90:3279–3289CrossRefGoogle Scholar
  41. Smith MD, Wilcox KR, Power SA, Tissue DT, Knapp AK (2017) Assessing community and ecosystem sensitivity to climate change-toward a more comparative approach. J Veg Sci 28:235–237CrossRefGoogle Scholar
  42. Suding KN, Lavorel S, Chapin FS et al (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Chang Biol 14:1125–1140CrossRefGoogle Scholar
  43. Tielbörger K, Bilton MC, Metz J, Kigel J, Holzapfel C, Lebrija-Trejos E, Konsens I, Parag HA, Sternberg M (2014) Middle-eastern plant communities tolerate 9 years of drought in a multi-site climate manipulation experiment. Nat Commun 5:5102CrossRefGoogle Scholar
  44. Violle C, Enquist BJ, Mcgill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252CrossRefGoogle Scholar
  45. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefGoogle Scholar
  46. Yuan ZY, Jiao F, Shi XR, Sardans J, Maestre FT, Delgado-Baquerizo M, Reich PB, Peñuelas J (2017) Experimental and observational studies find contrasting responses of soil nutrients to climate change. Elife 6:e23255CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Erguna Forest-Steppe Ecotone Research Station, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.Urat Desert-Grassland Research Station, Northwest Institute of Eco-Environment and ResourcesChinese Academy of ScienceLanzhouChina
  3. 3.Department of Biology and Graduate Degree Program in EcologyColorado State UniversityFort CollinsUSA
  4. 4.Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingChina
  5. 5.Plant Conservation and Population Biology, Department of BiologyUniversity of LeuvenHeverleeBelgium
  6. 6.Guizhou Academy of Tobacco ScienceGuiyangChina
  7. 7.State Key Laboratory of Vegetation and Environmental Change, Institute of BotanyChinese Academy of SciencesBeijingChina

Personalised recommendations