Folia Geobotanica

, Volume 53, Issue 4, pp 365–376 | Cite as

Aboveground facilitation and not complementary resource use cause overyielding among grasses in Tibetan alpine ecosystems

  • Xin Yin
  • Wei Qi
  • Johannes M. H. Knops
  • Xuexue Qin
  • GuoZhen DuEmail author


Although plant-plant interactions and their effects on ecological functioning have been examined in communities composed of different functional groups, they have rarely been studied in communities that contained a single functional group. We established a five-year experiment using three grass species with different nutrient addition and mowing treatments to explore overyielding and species interactions. We found strong overyielding caused by trait-independent complementarity effects. Nutrient addition increased overyielding via increasing trait-independent complementarity effects whereas mowing eliminated overyielding. One possible mechanism underlying the responses observed is the changes of positive aboveground species interactions. This result is consistent with the considerable literature identifying facilitation in alpine ecosystems by which coexisting plant species improve the microclimate and thereby promote the performance of all species. Complimentary resource use and selection effect have been demonstrated frequently as the mechanisms driving overyielding in grasslands. However, as we identify here, and positive interactions may be especially important in driving overyielding and positive interactions may be especially important in stressful environments such as alpine grasslands.


aboveground biomass light partitioning interspecific interactions intraspecific interactions grass species 



The study is supported by the Project of the National Natural Science Foundation of China granted to Guozhen Du (41430749) and Wei Qi (31600329,31770448), and the Fundamental Research Funds for the Central Universities granted to Wei Qi (lzujbky-2016-90). We thank Ang Li, Menghe Gu and other field assistants for their help with field work and Jeremy Fox for clarifying the partitioning of overyielding.

Supplementary material

12224_2018_9325_MOESM1_ESM.doc (1.6 mb)
ESM 1 (DOC 1.63 mb)
12224_2018_9325_MOESM2_ESM.doc (234 kb)
ESM 2 (DOC 234 kb)


  1. Alberda TH (1957) The effects of cutting, light intensity and night temperature on growth and soluble carbohydrate content of Lolium perenne L. Pl & Soil 8:199–230CrossRefGoogle Scholar
  2. Alhamad MN, Alrababah MA (2008) Defoliation and competition effects in a productivity gradient for a semiarid Mediterranean annual grassland community. Basic Appl Ecol 9:224–232CrossRefGoogle Scholar
  3. Anthelme F, Dangles O (2012) Plant-plant interactions in tropical alpine environments. Perspect Pl Ecol Evol Syst 14:363–372CrossRefGoogle Scholar
  4. Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260CrossRefGoogle Scholar
  5. Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184CrossRefGoogle Scholar
  6. Berendse F (1983) Interspecific competition and niche differentiation between Plantago lanceolata and Anthoxanthum odoratum in a natural hayfield. J Ecol 71:397–390CrossRefGoogle Scholar
  7. Bobbink R (1998) Impacts of tropospheric ozone and airborne nitrogenous pollutants on natural and semi-natural ecosystems: a commentary. New Phytol 139:161–168CrossRefGoogle Scholar
  8. Borer ET, Seabloom EW, Gruner DS, Harpole WS, Hillebrand H, Lind EM, Adler PB, Alberti J, Anderson TM, Bakker JD, Biederman L, Blumenthal D, Brown CS, Brudvig AL, Buckley YM, Cadotte M, Chu C, Cleland E, Crawley M, Daleo P, Damschen EI, Davies KF, DeCrappeo NM, Du G, Firn J, Hautier Y, Heckman RW, Hector A, HilleRisLambers J, Iribarne O, Klein JA, Knops JMH, Pierre KJL, Leakey ADB, Li W, MacDougall AS, McCulley RL, Melbourne BA, Mitchell C, Moore JL, Mortensen B, O’Halloran LR, Orrock RL, Pascual J, Sullivan LL, Williams R, Wragg PB, Wright JP, Yang LH (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520CrossRefGoogle Scholar
  9. Brooker RW, Kikvidze Z, Pugnaire F, Callaway RM, Choler P, Lortie CJ, Michalet R. (2005) The importance of importance. Oikos 109: 63–70Google Scholar
  10. Brooker RW (2006) Plant-plant interactions and environmental change. New Phytol 171:271–284CrossRefGoogle Scholar
  11. Byun C, de Blois S, Brisson J (2013) Plant functional group identity and diversity determine biotic resistance to invasion by an exotic grass. J Ecol 101:128–139CrossRefGoogle Scholar
  12. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  13. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefGoogle Scholar
  14. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67CrossRefGoogle Scholar
  15. Carlen C, Kölliker R, Reidy B, Lüscher A, Nösberger J (2002) Effect of season and cutting frequency on root and shoot competition between Festuca pratensis and Dactylis glomerata. Grass Forage Sci 57:247–254CrossRefGoogle Scholar
  16. Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Letters 17:193–202CrossRefGoogle Scholar
  17. Chen DD, Zhang SH, Dong SK, Wang XT, Du GZ (2010) Effect of land-use on soil nutrients and microbial biomass of an alpine region on the northeastern Tibetan Plateau, China. Land Degrad Developm 21:446–452Google Scholar
  18. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308CrossRefGoogle Scholar
  19. Chu C, Wang Y, Li Q, Zhao L, Ren Z, Xiao S, Yuan J, Wang G (2009) Effects of traits, species identity and local environmental conditions on the assessment of interactions: insights from an alpine meadow community. J Pl Ecol 2:135–141CrossRefGoogle Scholar
  20. Ergon Å, Kirwan L, Fystro G, Bleken MA, Collins RP, Rognli OA (2016) Spaces interactions in a grassland mixture under low nitrogen fertilization and two cutting frequencies. II. Nutritional quality. Grass Forage Sci 72:333–342CrossRefGoogle Scholar
  21. Farrer EC, Suding KN (2016) Teasing apart plant community responses to N enrichment: the roles of resource limitation, competition and soil microbes. Ecol Letters 19:1287–1296CrossRefGoogle Scholar
  22. Fox JW (2005) Interpreting the selection effect of biodiversity on ecosystem function. Ecol Letters 8:846–856CrossRefGoogle Scholar
  23. Fridley JD (2002) Resource availability dominates and alters the relationship between species diversity and ecosystem productivity in experimental plant communities. Oecologia 132:271–277CrossRefGoogle Scholar
  24. Fridley JD (2003) Diversity effects on production in different light and fertility environments: an experiment with communities of annual plants. J Ecol 91:396–406CrossRefGoogle Scholar
  25. Fridley JD, Grime JP (2010) Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity. Ecology 91:2272–2283CrossRefGoogle Scholar
  26. Geijzendorffer IR, van der Werf W, Bianchi FJJA, Schulte RPO (2011) Sustained dynamic transience in a Lotka-Volterra competition model system for grassland species. Ecol Modelling 222:2817–2824CrossRefGoogle Scholar
  27. Götzenberger L, de Bello F, Bråthen KA, Davison J, Dubuis A, Guisan A, Lepš J, Lindborg R, Moora M, Pärtel M, Pellissier L, Pottier J, Vittoz P, Zobel K, Zobel M (2012) Ecological assembly rules in plant communities-approaches, patterns and prospects. Biol Rev 87:111–127CrossRefGoogle Scholar
  28. Greenlee JT and Callaway RM (1996) Abiotic stress and the relative importance of interference and facilitation in montane bunchgrass community in western Montana. Amer Naturalist 148:386–396CrossRefGoogle Scholar
  29. Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347CrossRefGoogle Scholar
  30. Gross K (2008) Positive interactions among competitors can produce species-rich communities. Ecol Letters 11:929–936CrossRefGoogle Scholar
  31. Gross N, Suding KN, Lavorel S, Roumet C (2007) Complementarity as a mechanism of coexistence between functional groups of grasses. J Ecol 95:1296–1305CrossRefGoogle Scholar
  32. Gross N, Robson TM, Lavorel S, Albert C, Bagousse-Pinguet YL, Guillemin R (2008) Plant response traits mediate the effects of subalpine grasslands on soil moisture. New Phytol 180:652–662CrossRefGoogle Scholar
  33. Gubsch M, Buchmann N, Schmid B, Schulze E, Lipowsky A, Roscher C (2011) Differential effects of plant diversity on functional trait variation of grass species. Ann Bot (Oxford) 107:157–169CrossRefGoogle Scholar
  34. Gupta S, Narayan R (2011) Plant diversity and dry-matter dynamics of peri-urban plant communities in an Indian dry tropical region. Ecol Res 26:67–78CrossRefGoogle Scholar
  35. Halada L, Evans D, Romão C, Petersen J-E (2011) Which habitats of European importance depend on agricultural practices? Biodivers Conservation 20:2365–2378CrossRefGoogle Scholar
  36. Harris W, Forde BJ, Hardacre AK (1981) Temperature and cutting effects on the growth and competitive interaction of ryegrass and paspalum. II. Interspecific competition. New Zealand J Agric Res 24:309–320CrossRefGoogle Scholar
  37. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Nature 324:636–638Google Scholar
  38. Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975CrossRefGoogle Scholar
  39. Hooper DU, Dukes JS (2004) Overyielding among plant functional groups in a long-term experiment. Ecol Letters 7:95–105CrossRefGoogle Scholar
  40. Isbell F, Polley HW, Wilsey BJ (2009) Species interaction mechanisms maintain grassland plant species diversity. Ecology 90:1821–1830CrossRefGoogle Scholar
  41. Kelemen A, Lazzaro L, Besnyői V, Albert ÁJ, Konečná M, Dobay G, Memelink I, Adamec V, Götzenberger L, Bello F, Bagousse-Pinguet YL, Lepš J (2015a) Net outcome of competition and facilitation in a wet meadow changes with plant’s life stage and community productivity. Preslia 87:347–361Google Scholar
  42. Kelemen A, Török P, Valkó O, Deák B, Tóth K, Tóthmérész B (2015b) Both facilitation and limiting similarity shape the species coexistence in dry alkali grasslands. Ecol Complex 21:34–38CrossRefGoogle Scholar
  43. Knops JMH, Reinhart K (2000) Specific leaf area among a nitrogen fertilization gradient. Amer Midl Naturalist 144:265–272CrossRefGoogle Scholar
  44. Li W, Knops JMH, Brassil CE, Lu J, Qi W, Li J, Liu M, Chang S, Li W (2016) Functional group dominance and not productivity drives species richness. Pl Ecol Divers 9:2 141–150CrossRefGoogle Scholar
  45. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76CrossRefGoogle Scholar
  46. Ma MJ, Zhou XH, Wang G, Ma Z, Du GZ (2010) Seasonal dynamics in alpine meadow seed banks along an altitudinal gradient on the Tibetan Plateau. Pl & Soil 336:291–302CrossRefGoogle Scholar
  47. Maalouf JP, Bagousse-Pinguet YL, Marchand L, Touzard B, Michalet R (2012) The interplay of stress and mowing disturbance for the intensity and importance of plant interactions in dry calcareous grasslands. Ann Bot (Oxford) 110:821–828CrossRefGoogle Scholar
  48. Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Letters 13:1085–1093CrossRefGoogle Scholar
  49. Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valiente-Banuet A, Calaway RM (2006) Do biotic interactions shape both sides of the humped back model of species richness in plant communities? Ecol Letters 9:767–773CrossRefGoogle Scholar
  50. Nyfeler D, Huguenin-Elie O, Suter M, Forssard E, Connolly J, Lüscher A (2009) Strong mixture effects among four species in fertilized agricultural grassland led to persistent and consistent transgressive overyielding. J Appl Ecol 46:683–691CrossRefGoogle Scholar
  51. Öpik M, Bello F, Price JN, Fraser LH (2014) New insights into vegetation patterns and processes New Phytol 201:383–387CrossRefGoogle Scholar
  52. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Letters 9:741–758CrossRefGoogle Scholar
  53. Petersen U, Isselstein J (2015) Nitrogen addition and harvest frequency rather than initial plant composition determine vertical structure and light interception in grasslands. AoB Pl 7:plv089CrossRefGoogle Scholar
  54. Pistón N, Armas C, Schöb C, Macek P, Pugnaire FI (2015) Phylogenetic distance among beneficiary species in a cushion plant species explains interaction outcome. Oikos 124:1354–1359CrossRefGoogle Scholar
  55. Polley HW, Wilsey BJ, Tischler CR (2007) Species abundances influence the net biodiversity effect in mixtures of two plant species. Basic Appl Ecol 8:209–218CrossRefGoogle Scholar
  56. Pontes LS, Maire V, Louault F, Soussana J, Carrère P (2012) Impacts of species interactions on grass community productivity under contrasting management regimes. Oecologia 168:761–771CrossRefGoogle Scholar
  57. Pugnaire F, Zhang L, Li R, Luo T (2015) No evidence of facilitation collapse in the Tibetan plateau. J Veg Sci 26:233–242CrossRefGoogle Scholar
  58. Qin GL, Du GZ, Luo YJ, Dong GS, Ma JY (2003) A reexamination of the relationships among phonological complementarity, species diversity, and ecosystem function. Bot Bull Acad Sin 44:239–244Google Scholar
  59. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at
  60. Roscher C, Schumacher J (2016) Positive diversity effects on productivity in mixtures of arable weed species as related to density-size relationships. J Pl Ecol 9:792–804CrossRefGoogle Scholar
  61. Roscher C, Schumacher J, Weisser WW, Schmid B, Schulze ED (2007) Detecting the role of individual species for overyielding in experimental grassland communities composed of potentially dominant species. Oecologia 154:535–549CrossRefGoogle Scholar
  62. Roscher C, Schmid B, Kolle O, Schulze ED (2016) Complementarity among four highly productive grassland species depends on resource availability. Oecologia 181:571–582CrossRefGoogle Scholar
  63. Saiz H, Bittebiere AK, Benot ML, Jung V, Mony C (2016) Understanding clonal plant competition for space over time: a fine-scale spatial approach based on experimental communities. J Veg Sci 27:759–770CrossRefGoogle Scholar
  64. Schöb C, Kerle S, Karley AJ, Morcillo L, Pakeman, RJ, Newton AC, Brooker RW (2015) Intraspecific genetic diversity and composition modify species-level diversity-productivity relationships. New Phytol 205:720–730CrossRefGoogle Scholar
  65. Sheley RL, James JJ (2014) Simultaneous intraspecific facilitation and interspecific competition between native and annual grasses. J Arid Environm 104:80–87CrossRefGoogle Scholar
  66. Siebenkäs A, Schumacher J, Roscher C (2016) Resource availability alters biodiversity effects in experimental grass-forb mixtures. PLOS ONE 11:e0158110CrossRefGoogle Scholar
  67. Soliveres S, Smit C, Maestre FT (2015) Moving forward on facilitation research: response to changing environments and effects on the diversity, functioning and evolution of plant communities. Biol Rev 90:297–313CrossRefGoogle Scholar
  68. Tilman D (1989) On the meaning of competition and the mechanisms of competition superiority. Funct Ecol 1:304–315CrossRefGoogle Scholar
  69. Tilman D, Wedin D (1991) Dynamics of nitrogen competition between successional grasses. Ecology 72:1038–1049CrossRefGoogle Scholar
  70. van Ruijven J, Berendse F (2009) Long-term persistence of a positive plant diversity-productivity in the absence of legumes. Ecol Letters 6:170–175CrossRefGoogle Scholar
  71. Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP, Parmenter R (1999) The relationship between productivity and species richness. Annual Rev Ecol Syst 30:257–300CrossRefGoogle Scholar
  72. Wang H, Chen H (2016) The importance of plant functional groups under different fertilization and mowing regimes: implications for sustainable meadows. Agric Eco-Syst Environm 224:67–74CrossRefGoogle Scholar
  73. Wang Y, Chu C, Maestre FT, Wang G (2007) On the relevance of facilitation in alpine meadow communities: an experimental assessment with multiple species differing in their ecological optimum. Acta Oecol 33:108–113CrossRefGoogle Scholar
  74. Weigelt A, Weisser WW, Buchmann N, Scherer-Lorenzen M (2009) Biodiversity for multifunctional grasslands: equal productivity in high-diversity low-input and low-diversity high-input systems. Biogeosciences 6:1695–1706CrossRefGoogle Scholar
  75. Wright A, Schnitzer SA, Reich PB (2014) Living close to your neighbors: the importance of both competition and facilitation in plant communities. Ecology 95:2213–2223CrossRefGoogle Scholar
  76. Yang ZL, van Ruijven J, Du GZ (2011) The effects of long-term fertilization on the temporal stability of alpine meadow communities. Pl & Soil 345:315–324CrossRefGoogle Scholar
  77. Young K, Mangold J (2008) Medusahead (Taeniatherum caput-medusae) outperforms squirreltail (Elymus elymoides) through interference and growth rate. Invasive Pl Sci Managem 1:73–81CrossRefGoogle Scholar
  78. Zhang ST, Liu JP, Bao XH, Niu KC (2011) Seed-to-seed potential allelopathic effects between Ligularia virgaurea and native grass species of Tibetan alpine grasslands. Ecol Res 26:47–52CrossRefGoogle Scholar
  79. Zuppinger-Dingley D, Schmid B, Petermann JS, Yadav V, De Deyn GB, Flynn DFB (2014) Selection for niche differentiation in plant communities increases biodiversity effects. Nature 515:108–111CrossRefGoogle Scholar

Copyright information

© Institute of Botany, Academy of Sciences of the Czech Republic 2018

Authors and Affiliations

  • Xin Yin
    • 1
  • Wei Qi
    • 1
  • Johannes M. H. Knops
    • 2
  • Xuexue Qin
    • 3
  • GuoZhen Du
    • 1
    Email author
  1. 1.State Key Laboratory of Grassland Agroecosystems, School of Life SciencesLanzhou UniversityLanzhouChina
  2. 2.School of Biological SciencesUniversity of NebraskaLincolnUSA
  3. 3.College of Life Science and TechnologyLongdong UniversityQingyang, GansuPeople’s Republic of China

Personalised recommendations