Designing mixtures of varieties for multifunctional agriculture with the help of ecology. A review

  • Sébastien Barot
  • Vincent Allard
  • Amélie Cantarel
  • Jérôme Enjalbert
  • Arnaud Gauffreteau
  • Isabelle Goldringer
  • Jean-Christophe Lata
  • Xavier Le Roux
  • Audrey Niboyet
  • Emanuelle Porcher
Review Article

Abstract

The study of natural ecosystems and experiments using mixtures of plant species demonstrates that both species and genetic diversity generally promote ecosystem functioning. Therefore, mixing crop varieties is a promising alternative practice to transform modern high-input agriculture that is associated with a drastic reduction of within-field crop genetic diversity and is widely recognized as unsustainable. Here, we review the effects of mixtures of varieties on ecosystem functioning, and their underlying ecological mechanisms, as studied in ecology and agronomy, and outline how this knowledge can help designing more efficient mixtures. We recommend the development of two complementary strategies to optimize variety mixtures by fostering the ecological mechanisms leading to a positive relationship between biodiversity and ecosystem functioning and its stability through time, i.e., sampling and complementarity effects. (1) In the “trait-blind” approach, the design of high-performance mixtures is based on estimations of the mixing abilities of varieties. While this approach is operational because it does not require detailed trait knowledge, it relies on heavy experimental designs to evaluate mixing ability. (2) The trait-based approach is particularly efficient to design mixtures of varieties to provide particular baskets of services but requires building databases of traits for crop varieties and documenting the relations between traits and services. The performance of mixtures requires eventually to be evaluated in real economic, social, and agronomic contexts. We conclude that the need of a multifunctional low-input agriculture strongly increases the attractiveness of mixtures but that new breeding approaches are required to create varieties with higher mixing abilities, to foster complementarity and selection effects through an increase in the variance of relevant traits and to explore new combinations of trait values.

Keywords

Biodiversity Mixtures of varieties Sampling effect Complementarity effect Crop breeding Crop traits Multifunctional agriculture Mixing ability 

References

  1. Aanderud Z, Bledsoe CS (2009) Preference for 15N-ammonium, 15N-nitrate, and 15N-glycine differ among dominant exotic and subordinate native grasses from a California oak woodland. Env Exp Bot 65:205–209CrossRefGoogle Scholar
  2. Abakumova M, Zobel K, Lepik A, Semchenko M (2016) Plasticity in plant functional traits is shaped by variability in neighbourhood species composition. New Phytol 211(2):455–463. doi:10.1111/nph.13935 PubMedCrossRefGoogle Scholar
  3. Allan E, Weisser WW, Fischer M, Schulze ED, Weigelt A et al (2013) A comparison of the strength of biodiversity effects across multiple functions. Oecologia 173(1):223–237. doi:10.1007/s00442-012-2589-0 PubMedCrossRefGoogle Scholar
  4. Allard RW, Adams J (1969) Population studies in predominantly self-pollinating species. XIII. Intergenotypic competition and population structure in barley and wheat. Am Nat 103:621–645CrossRefGoogle Scholar
  5. Altieri MA (1989) Agroecology—a new research and development paradigm for world agriculture. Agriculture Ecos Envir 27(1–4):37–46. doi:10.1016/0167-8809(89)90070-4 Google Scholar
  6. Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agri Ecos Env 74(1–3):19–31. doi:10.1016/S0167-8809(99)00028-6 CrossRefGoogle Scholar
  7. Barot S, Lata J-C, Lacroix G (2012) Meeting the relational challenge of ecological engineering. Ecol Eng 45:13–23. doi:10.1016/j.ecoleng.2011.04.006 CrossRefGoogle Scholar
  8. Bavec F, Bavec M (2001) Chlorophyll meter readings of winter wheat cultivars and grain yield prediction. Commun Soil Sci Plan 32:2709–2719. doi:10.1081/CSS-120000956 CrossRefGoogle Scholar
  9. de Bello F, Lavorel S, Diaz S, Harrington R, Cornelissen JHC et al (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodi Cons 19(10):2873–2893. doi:10.1007/s10531-010-9850-9 CrossRefGoogle Scholar
  10. Bertness MD, Callaway R (1994) Positive interactions in communities. Tree 9:191–193. doi:10.1016/0169-5347(94)90088-4 PubMedGoogle Scholar
  11. Besag JE, Kempton RA (1986) Statistical analysis of field experiments using neighboring plots. Biometrics 42:231–251. doi:10.2307/2531047 CrossRefGoogle Scholar
  12. Bessler H, Temperton VM, Roscher C, Buchmann N, Schmid B et al (2009) Aboveground overyielding in grassland mixtures is associated with reduced biomass partitioning to belowground organs. Ecology 90(6):1520–1530. doi:10.1890/08-0867.1 PubMedCrossRefGoogle Scholar
  13. Bøckman OC (1997) Fertilizers and biological nitrogen fixation as sources of plant nutrients: perspectives for future agriculture. Plant Soil 194:11–14. doi:10.1023/A:1004212306598 CrossRefGoogle Scholar
  14. Bonnin I, Bonneuil C, Goffaux R, Montalent P, Goldringer I (2014) Explaining the decrease in the genetic diversity of wheat in France over the 20th century. Agri Ecos Envir 195:183–192. doi:10.1016/j.agee.2014.06.003 CrossRefGoogle Scholar
  15. Boudsocq S, Lata JC, Mathieu J, Abbadie L, Barot S (2009) Modelling approach to analyze the effects of nitrification inhibition on primary production. Func Ecol 23:220–230. doi:10.1111/j.1365-2435.2008.01476.x CrossRefGoogle Scholar
  16. Brisson N, Gate P, Gouache D, Charmet G, Oury F-X et al (2010) Why are wheat yields stagnating in Europe? A comprehensive data analysis for France. Field Crops Res 119(1):201–212. doi:10.1016/j.fcr.2010.07.012 CrossRefGoogle Scholar
  17. Brooker RW, Bennett AE, Cong W-F, Daniell TJ, George TS et al (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206(1):107–117. doi:10.1111/nph.13132 PubMedCrossRefGoogle Scholar
  18. Burns JH, Strauss SY (2012) Effects of competition on phylogenetic signal and phenotypic plasticity in plant functional traits. Ecology 93:S126–S137CrossRefGoogle Scholar
  19. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ et al (2002) Positive interactions among alpine plants increase with stress. Nature 417(6891):840–847. doi:10.1038/nature00805 CrossRefGoogle Scholar
  20. Campbell BD, Grime JP, Mackey JML (1991) A trade-off between scale and precision in resource foraging. Oecologia 87:532–538. doi:10.1007/BF00320417 PubMedCrossRefGoogle Scholar
  21. Cantarel AA, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M et al (2015) Using plant traits to explain plant–microbe relationships involved in nitrogen acquisition. Ecology 96:788–799. doi:10.1890/13-2107.1 PubMedCrossRefGoogle Scholar
  22. Cardinale BJ, Palmer MA, Collins SL (2003) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429. doi:10.1038/415426a CrossRefGoogle Scholar
  23. Chateil C, Goldringer I, Tarallo L, Kerbiriou C, Le Viol I et al (2013) Crop genetic diversity benefits farmland biodiversity in cultivated fields. Agri Ecosys Envir 171:25–32. doi:10.1016/j.agee.2013.03.004 CrossRefGoogle Scholar
  24. Cianciaruso MV, Batalha MA, Gaston KJ, Petchey OL (2009) Including intraspecific variability in functional diversity. Ecology 90(1):81–89. doi:10.1890/07-1864.1 PubMedCrossRefGoogle Scholar
  25. Comstock RE, Robinson HF, Harvey PH (1949) A breeding procedure designed to make maximum use of both general and specific combining ability. Agro J 41:360–367CrossRefGoogle Scholar
  26. Cook-Patton SC, McArt SH, Parachnowitsch AL, Thaler JS, Agrawal AA (2011) A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92(4):915–923. doi:10.1890/10-0999.1 PubMedCrossRefGoogle Scholar
  27. Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Global Env Change 19(2):292–305. doi:10.1016/j.gloenvcha.2008.10.009 CrossRefGoogle Scholar
  28. Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aus J Bot 51:335–380. doi:10.1071/BT02124 CrossRefGoogle Scholar
  29. Crawford KM, Rudgers JA, Cahill J (2012) Plant species diversity and genetic diversity within a dominant species interactively affect plant community biomass. J Ecol 100(6):1512–1521. doi:10.1111/j.1365-2745.2012.02016.x CrossRefGoogle Scholar
  30. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC et al (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313(5789):966–968. doi:10.1126/science.1128326 PubMedCrossRefGoogle Scholar
  31. Dawson JC, Goldringer I (2012) Breeding for genetically diverse populations: variety mixtures and evolutionary populations. In: van Bueren ETL, Myers JR (eds) Organic crop breeding. Wiley-Blackwell, pp 77–98. doi:10.1002/9781119945932.ch5
  32. Debaeke P, Rouet P, Justes E (2006) Relationship between the normalized SPAD index and the nitrogen nutrition index: application to durum wheat. J Plant Nutr 29:75–92. doi:10.1080/01904160500416471 CrossRefGoogle Scholar
  33. Debaeke P, Gauffreteau A, Durel C-E, Jeuffroy M-H (2014) Conception d’idéotypes variétaux en réponse aux nouveaux contextes agricoles et environnementaux. Agro Envir Soc 4:65–73Google Scholar
  34. Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem process. Trends Ecol Evol 16(11):646–655. doi:10.1016/S0169-5347(01)02283-2 CrossRefGoogle Scholar
  35. Dornbusch T, Baccar R, Watt J, Hillier J, Bertheloot J et al (2011) Plasticity of winter wheat modulated by sowing date, plant population density and nitrogen fertilisation: dimensions and size of leaf blades, sheaths and internodes in relation to their position on a stem. Field Crops Res 121(1):116–124. doi:10.1016/j.fcr.2010.12.004 CrossRefGoogle Scholar
  36. Drummond EB, Vellend M (2012) Genotypic diversity effects on the performance of Taraxacum officinale populations increase with time and environmental favorability. PLoS One 7(2):e30314. doi:10.1371/journal.pone.0030314 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ecarnot M, Compan F, Roumet P (2013) Assessing leaf nitrogen content and leaf mass per unit area of wheat in the field throughout plant cycle with a portable spectrometer. Field Crop Res 140:44–50. doi:10.1016/j.fcr.2012.10.013 CrossRefGoogle Scholar
  38. Eggermont H, Balian E, Azevedo J, Beumer V, Brodin T et al (2015) Nature-based solutions: new influence for environmental management and research in Europe. Gaia 24:243–248. doi:10.14512/gaia.24.4.9 CrossRefGoogle Scholar
  39. FAO (2010) The second report on the state of the world’s plant genetic resources for food and agriculture. FAO, RomeGoogle Scholar
  40. Finckh MR (2008) Integration of breeding and technology into diversification strategies for disease control in modern agriculture. Eur J Plant Path 121(3):399–409. doi:10.1007/s10658-008-9273-6 CrossRefGoogle Scholar
  41. Finckh MR, Mundt CC (1992) Stripe rust, yield, and plant competition in wheat cultivar mixtures. Phytopathology 82:905–913CrossRefGoogle Scholar
  42. Finckh MR, Gacek ES, Goyeau H, Lannou C, Merz U et al (2000) Cereal variety and species mixtures in practice, with emphasis on disease resistance. Agronomie 20:813–837. doi:10.1051/agro:2000177 CrossRefGoogle Scholar
  43. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS et al (2011) Solutions for a cultivated planet. Nature 478(7369):337–342. doi:10.1038/nature10452 PubMedCrossRefGoogle Scholar
  44. Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity-productivity relationship in an N-limited grassland. Ecology 90(2):408–418. doi:10.1890/08-0325.1 PubMedCrossRefGoogle Scholar
  45. Foucteau V, Brabant P, Monod H, David O, Goldringer I (2000) Correction models for intergenotypic competition in winter wheat. Agronomie 20:943–995. doi:10.1051/agro:2000170 CrossRefGoogle Scholar
  46. Fridley JD, Grime JP (2010) Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity. Ecology 91(8):2272–2283PubMedCrossRefGoogle Scholar
  47. Gaba S, Lescourret F, Boudsocq S, Enjalbert J, Hinsinger P et al (2015) Multiple cropping systems as drivers for providing multiple ecosystem services: from concepts to design. Agro Sust Dev 35(2):607–623. doi:10.1007/s13593-014-0272-z CrossRefGoogle Scholar
  48. Gallandt ER, Dofing SM, Reisenauer PE, Donaldson E (2001) Diallel analysis of cultivar mixtures in winter wheat. Crop Sci 41:792–796. doi:10.2135/cropsci2001.413792x CrossRefGoogle Scholar
  49. Gamfeldt L, Snall T, Bagchi R, Jonsson M, Gustafsson L et al (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Comm 4:1340. doi:10.1038/ncomms2328 CrossRefGoogle Scholar
  50. Garcia-Palacios P, Maestre FT, Gallardo A (2011) Soil nutrient heterogeneity modulates ecosystem responses to changes in the identity and richness of plant functional groups. J Ecol 99(2):551–562. doi:10.1111/j.1365-2745.2010.01765.x PubMedPubMedCentralGoogle Scholar
  51. Gizlice Z, Carter TE, Burton JW, Emigh TH (1989) Partitioning of blending ability using two-way blends and component lines of soybean. Crop Sci 29:885–889CrossRefGoogle Scholar
  52. Goldringer I, Brabant P, Kempton RA (1994) Adjustment for competition between genotypes in single-row-plot trials of winter wheat (Triticum aestivum). Plant Breed 112:294–300. doi:10.1111/j.1439-0523.1994.tb00687.x CrossRefGoogle Scholar
  53. Griffing B (1956) Concept of general and specific combining ability in relation to diallel crossing systems. Austr J Biol Sci 9:463–493. doi:10.1071/BI9560463 CrossRefGoogle Scholar
  54. Grime JP, Cornelissen JHC, Thompson K, Hodgson JG (1996) Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77:489–494. doi:10.2307/3545938 CrossRefGoogle Scholar
  55. Gross K, Cardinale BJ, Fox JW, Gonzalez A, Loreau M et al (2014) Species richness and the temporal stability of biomass production: a new analysis of recent biodiversity experiments. Am Nat 183:1–12. doi:10.1086/673915 PubMedCrossRefGoogle Scholar
  56. Hajjar R, Jarvis DI, Gemmill-Herren B (2008) The utility of crop genetic diversity in maintaining ecosystem services. Agri Ecosys Envir 123(4):261–270. doi:10.1016/j.agee.2007.08.003 CrossRefGoogle Scholar
  57. Hauggaard-Nielsen H, Jensen ES (2005) Facilitative root interactions in intercrops. Plant Soil 274(1–2):237–250. doi:10.1007/s11104-004-1305-1 CrossRefGoogle Scholar
  58. Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS et al (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521–525. doi:10.1038/nature13014 PubMedCrossRefGoogle Scholar
  59. He J-S, Bazzaz FA, Schmid B (2002) Interactive effects of diversity, nutrients and elevated CO2 on experimental plant communities. Oikos 97:337–348CrossRefGoogle Scholar
  60. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448(7150):188–190. doi:10.1038/nature05947 PubMedCrossRefGoogle Scholar
  61. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M et al (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1126. doi:10.1126/science.286.5442.1123 PubMedCrossRefGoogle Scholar
  62. Hector A, Joshi J, Scherer-Lorenzen M, Schmid B, Spehn EM et al (2007) Biodiversity and ecosystem functioning: reconciling the results of experimental and observational studies. Func Ecol 21(5):998–1002. doi:10.1111/j.1365-2435.2007.01308.x CrossRefGoogle Scholar
  63. Hector A, Hautier Y, Saner P, Wacker L, Bagchi R et al (2010) General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91(8):2213–2220. doi:10.1890/09-1162.1 PubMedCrossRefGoogle Scholar
  64. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quat Rev Biol 67(3):283–335CrossRefGoogle Scholar
  65. Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestrors. Can J Bot 70:2032–2040. doi:10.1139/b92-253 CrossRefGoogle Scholar
  66. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195. doi:10.1023/A:1013351617532 CrossRefGoogle Scholar
  67. Holmgren M, Scheffer M (2010) Strong facilitation in mild environments: the stress gradient hypothesis revisited. J Ecol 98(6):1269–1275. doi:10.1111/j.1365-2745.2010.01709.x CrossRefGoogle Scholar
  68. Howden SM, Soussana JF, Tubiello FN, Chhetri N, Dunlop M et al (2007) Adapting agriculture to climate change. Proc Natl Acad Sci U S A 104(50):19691–19696. doi:10.1073/pnas.0701890104 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci U S A 101(24):8998–9002. doi:10.1073/pnas.0402642101 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecolog Lett 11(6):609–623. doi:10.1111/j.1461-0248.2008.01179.x CrossRefGoogle Scholar
  71. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  72. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477(7363):199–202. doi:10.1038/nature10282 PubMedCrossRefGoogle Scholar
  73. Jarvis DI, Brown AH, Cuong PH, Collado-Panduro L, Latournerie-Moreno L et al (2008) A global perspective of the richness and evenness of traditional crop-variety diversity maintained by farming communities. Proc Natl Acad Sci U S A 105(14):5326–5331. doi:10.1073/pnas.0800607105 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Jiang L, Pu Z, Nemergut DR (2008) On the importance of the negative selection effect for the relationship between biodiversity and ecosystem functioning. Oikos 117:488–493. doi:10.1111/j.2007.0030-1299.16401.x CrossRefGoogle Scholar
  75. Johnson MTJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9(1):24–34. doi:10.1111/j.1461-0248.2005.00833.x PubMedGoogle Scholar
  76. Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P et al (2011) TRY—a global database of plant traits. Global Chan Biol 17(9):2905–2935. doi:10.1111/j.1365-2486.2011.02451.x CrossRefGoogle Scholar
  77. Kempton RA (1982) Adjustment for competition between varieties in plant breeding trials. J Agri Sci 98:599–611. doi:10.1017/S0021859600054381 CrossRefGoogle Scholar
  78. Kempton RA (1985) Statistical models for interplot competition. Asp Appl Biol 10:110–120Google Scholar
  79. Kiær LP, Skovgaard IM, Østergård H (2009) Grain yield increase in cereal variety mixtures: a meta-analysis of field trials. Field Crops Res 114(3):361–373. doi:10.1016/j.fcr.2009.09.006 CrossRefGoogle Scholar
  80. Kiær LP, Skovgaard IM, Østergård H (2012) Effects of inter-varietal diversity, biotic stresses and environmental productivity on grain yield of spring barley variety mixtures. Euphytica 185(1):123–138. doi:10.1007/s10681-012-0640-1 CrossRefGoogle Scholar
  81. Knott EA, Mundt CC (1990) Mixing ability analysis of wheat cultivar mixtures under diseased and nondiseased conditions. Theoret Appl Gen 80:313–320. doi:10.1007/BF00210065 CrossRefGoogle Scholar
  82. Kotowska AM, Cahill JF, Keddie BA (2010) Plant genetic diversity yields increased plant productivity and herbivore performance. J Ecol 98(1):237–245. doi:10.1111/j.1365-2745.2009.01606.x CrossRefGoogle Scholar
  83. Lata J-C, Degrange V, Raynaud X, Maron P-A, Lensi R et al (2004) Grass populations control nitrification in savanna soils. Funct Ecol 18:605–611. doi:10.1111/j.0269-8463.2004.00880.x CrossRefGoogle Scholar
  84. Latz E, Eisenhauer N, Rall BC, Allan E, Roscher C et al (2012) Plant diversity improves protection against soil-borne pathogens by fostering antagonistic bacterial communities. J Ecol 100(3):597–604. doi:10.1111/j.1365-2745.2011.01940.x CrossRefGoogle Scholar
  85. Laughlin DC (2011) Nitrification is linked to dominant leaf traits rather than functional diversity. J Ecol 99(5):1091–1099. doi:10.1111/j.1365-2745.2011.01856.x CrossRefGoogle Scholar
  86. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Func Ecol 16:545–556. doi:10.1046/j.1365-2435.2002.00664.x CrossRefGoogle Scholar
  87. Le Roux X, Schmid B, Poly F, Barnard RL, Niklaus PA et al (2013) Soil environmental conditions and microbial build-up mediate the effect of plant diversity on soil nitrifying and denitrifying enzyme activities in temperate grasslands. PLoS One 8(4):e61069. doi:10.1371/journal.pone.0061069 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Leff B (2004) Geographic distribution of major crops across the world. Glob Biogeo Cycles 18(1). doi:10.1029/2003gb002108
  89. Li L, Li S-M, Sun J-H, Bao X-G, Zhang H-G et al (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci U S A 104:11192–11196. doi:10.1073/pnas.0704591104 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Li L, Tilman D, Lambers H, Zhang F-S (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203(1):63–69. doi:10.1111/nph.12778 PubMedCrossRefGoogle Scholar
  91. Litrico I, Violle C (2015) Diversity in plant breeding: a new conceptual framework. Trends Plant Sci 20(10):604–613. doi:10.1016/j.tplants.2015.07.007 PubMedCrossRefGoogle Scholar
  92. Loeuille N, Barot S, Georgelin E, Kylafis G, Lavigne C (2013) Eco-evolutionary dynamics of agricultural networks: implications for a sustainable management. Adv Ecol Res 49:339–435. doi:10.1016/B978-0-12-420002-9.00006-8 CrossRefGoogle Scholar
  93. Lopez CG, Mundt CC (2000) Using mixing ability analysis from two-way cultivar mixtures to predict the performance of cultivars in complex mixtures. Field Crops Res 68:121–132. doi:10.1016/S0378-4290(00)00114-3 CrossRefGoogle Scholar
  94. Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82(3):600–602CrossRefGoogle Scholar
  95. Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91:3–17. doi:10.1034/j.1600-0706.2000.910101.x CrossRefGoogle Scholar
  96. Loreau M (2004) Does functional redundancy exist? Oikos 104(3):606–611. doi:10.1111/j.0030-1299.2004.12685.x CrossRefGoogle Scholar
  97. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. doi:10.1038/35083573 PubMedCrossRefGoogle Scholar
  98. Lynch JP, Brown KM (2012) New roots for agriculture: exploiting the root phenome. Philos Trans Royal Soc Lond B 367(1595):1598–1604. doi:10.1098/rstb.2011.0243 CrossRefGoogle Scholar
  99. Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97(2):199–205. doi:10.1111/j.1365-2745.2008.01476.x CrossRefGoogle Scholar
  100. Malézieux E (2011) Designing cropping systems from nature. Agro Sustain Develop 32(1):15–29. doi:10.1007/s13593-011-0027-z CrossRefGoogle Scholar
  101. Marquard E, Weigelt A, Roscher C, Gubsch M, Lipowsky A et al (2009) Positive biodiversity-productivity relationship due to increased plant density. J Ecol 97(4):696–704. doi:10.1111/j.1365-2745.2009.01521.x CrossRefGoogle Scholar
  102. Martin AR, Isaac ME, Manning P (2015) Plant functional traits in agroecosystems: a blueprint for research. J Appl Ecol 52(6):1425–1435. doi:10.1111/1365-2664.12526 CrossRefGoogle Scholar
  103. de Miranda-Filho JB, Chaves LJ (1991) Procedures for selecting composites based on prediction methods. Theoret Appl Genetics 81:265–271. doi:10.1007/BF00215732 CrossRefGoogle Scholar
  104. Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Func Ecol 24(4):867–876. doi:10.1111/j.1365-2435.2010.01695.x CrossRefGoogle Scholar
  105. Murphy KM, Campbell KG, Lyon SR, Jones SS (2007) Evidence of varietal adaptation to organic farming systems. Field Crops Res 102:172–177. doi:10.1016/j.fcr.2007.03.011 CrossRefGoogle Scholar
  106. Nakhforoosh A, Grausgruber H, Kaul H-P, Bodner G (2014) Wheat root diversity and root functional characterization. Plant Soil 380(1–2):211–229. doi:10.1007/s11104-014-2082-0 CrossRefGoogle Scholar
  107. Newton AC, Swanston JS, Guy DC, Ellis RP (1998) The effect of cultivar mixtures on malting quality in winter and spring barley. J Inst Brew 104:41–45. doi:10.1002/j.2050-0416.1998.tb00973.x CrossRefGoogle Scholar
  108. Østergård H, Finckh MR, Fontaine L, Goldringer I, Hoad SP et al (2009) Time for a shift in crop production: embracing complexity through diversity at all levels. J Sci Food Agric 89:1439–1445. doi:10.1002/jsfa.3615 CrossRefGoogle Scholar
  109. Palma J, Graves AR, Burgess PJ, van der Werf W, Herzog F (2007) Integrating environmental and economic performance to assess modern silvoarable agroforestry in Europe. Ecol Econ 63(4):759–767. doi:10.1016/j.ecolecon.2007.01.011 CrossRefGoogle Scholar
  110. Parker JD, Salminen JP, Agrawal AA (2010) Herbivory enhances positive effects of plant genotypic diversity. Ecol Lett 13(5):553–563. doi:10.1111/j.1461-0248.2010.01452.x PubMedCrossRefGoogle Scholar
  111. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aus J Bot 61(3):167. doi:10.1071/bt12225 CrossRefGoogle Scholar
  112. Postma JA, Lynch JP (2012) Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann Bot 110(2):521–534. doi:10.1093/aob/mcs082 PubMedPubMedCentralCrossRefGoogle Scholar
  113. del Pozo A, Matus I, Serret MD, Araus JL (2014) Agronomic and physiological traits associated with breeding advances of wheat under high-productive Mediterranean conditions. The case of Chile. Envir Exp Bot 103:180–189. doi:10.1016/j.envexpbot.2013.09.016 CrossRefGoogle Scholar
  114. Prieto I, Violle C, Barre P, Durand J-L, Ghesquiere M et al (2015) Complementary effects of species and genetic diversity on productivity and stability of sown grasslands. Nature Plants. doi:10.1038/nplants.2015.33 PubMedGoogle Scholar
  115. Quetier F, Lavorel S, Thuiller W, Davies I (2007) Plant-trait-based modeling assessment of ecosystem-service sensitivity to land-use change. Ecol Appl 17(8):2377–2386PubMedCrossRefGoogle Scholar
  116. Reich PB, Knops J, Tilman D, Craine J, Ellsworth D et al (2001) Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–812PubMedCrossRefGoogle Scholar
  117. Reich PB, Tilman D, Naeem S, Ellsworth DS, Knops J et al (2004) Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N. Proc Natl Acad Sci U S A 101(27):10101–10106. doi:10.1073/pnas.0306602101 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Renting H, Rossing WA, Groot JC, Van der Ploeg JD, Laurent C et al (2009) Exploring multifunctional agriculture. A review of conceptual approaches and prospects for an integrative transitional framework. J Environ Manag 90(Suppl 2):S112–S123. doi:10.1016/j.jenvman.2008.11.014 CrossRefGoogle Scholar
  119. Richards RA (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J Exp Bot 51:447–458. doi:10.1093/jexbot/51.suppl_1.447 PubMedCrossRefGoogle Scholar
  120. de Roman M, Fernandez I, Wyatt T, Sahrawy M, Heil M et al (2011) Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J Ecol 99(1):36–45. doi:10.1111/j.1365-2745.2010.01752.x CrossRefGoogle Scholar
  121. Roscher C, Thein S, Schmid B, Scherer-Lorenzen M (2008) Complementary nitrogen use among potentially dominant species in a biodiversity experiment varies between two years. J Ecol 96(3):477–488. doi:10.1111/j.1365-2745.2008.01353.x CrossRefGoogle Scholar
  122. Sarandon SJ, Sarandon R (1995) Mixture of cultivars: pilot field trial of an ecological alternative to improve production or quality of wheat (Triticum aestivum). J Appl Ecol 32:288–294. doi:10.2307/2405096 CrossRefGoogle Scholar
  123. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W et al (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468(7323):553–556. doi:10.1038/nature09492 PubMedCrossRefGoogle Scholar
  124. Scherer-Lorenzen M, Palmborg C, Prinz A, Schulze E-D (2003) The role of plant diversity and composition for nitrate leaching in grasslands. Ecology 84(6):1539–1552. doi:10.1890/0012-9658(2003)084[1539:TROPDA]2.0.CO;2 CrossRefGoogle Scholar
  125. Schöb C, Kerle S, Karley AJ, Morcillo L, Pakeman RJ et al (2015) Intraspecific genetic diversity and composition modify species-level diversity-productivity relationships. New Phytol 205:720–730. doi:10.1111/nph.13043 PubMedCrossRefGoogle Scholar
  126. Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840. doi:10.1890/04-1955 CrossRefGoogle Scholar
  127. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV et al (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89(3):773–781. doi:10.1890/07-0337.1 PubMedCrossRefGoogle Scholar
  128. Shahzad T, Chenu C, Genet P, Barot S, Perveen N et al (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155. doi:10.1016/j.soilbio.2014.09.023 CrossRefGoogle Scholar
  129. Smithson JB, Lenne´ JM (1996) Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Ann Appl Biol 128:127–158. doi:10.1111/j.1744-7348.1996.tb07096.x
  130. Spehn EM, Scherer-Lorenzen M, Schmid B, Hector A, Caldeira MC et al (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98:205–218. doi:10.1034/j.1600-0706.2002.980203.x CrossRefGoogle Scholar
  131. Sprague GF, Tatum LA (1942) General vs. specific combining ability in single crosses of corn. J Am Soc Agron 34:923–932CrossRefGoogle Scholar
  132. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17(6):278–285. doi:10.1016/S0169-5347(02)02483-7 CrossRefGoogle Scholar
  133. Swanston JS, Gacek E, Guy DC, Newton AC (2000) Malting performance of barley cultivar mixtures from the UK and Poland. J Inst Brew 106:239–244. doi:10.1002/j.2050-0416.2000.tb00063.x CrossRefGoogle Scholar
  134. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822. doi:10.1126/science.1183700 PubMedCrossRefGoogle Scholar
  135. Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365. doi:10.1007/978-1-4612-4018-1_1 CrossRefGoogle Scholar
  136. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720. doi:10.1038/379718a0 CrossRefGoogle Scholar
  137. Tilman D, Knops J, Wedin D, Reich P, Ritchie M et al (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302. doi:10.1126/science.277.5330.1300 CrossRefGoogle Scholar
  138. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. doi:10.1038/nature01014 PubMedCrossRefGoogle Scholar
  139. Tooker JF, Frank SD, Steffan-Dewenter I (2012) Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J Appl Ecol 49(5):974–985. doi:10.1111/j.1365-2664.2012.02173.x CrossRefGoogle Scholar
  140. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C et al (2007) Let the concept of trait be functional! Oikos 116:882–892. doi:10.1111/j.0030-1299.2007.15559.x CrossRefGoogle Scholar
  141. Weiner J (1990) Asymmetric competition in plant populations. Trends Ecol Evol 5(11):360–364. doi:10.1016/0169-5347(90)90095-U PubMedCrossRefGoogle Scholar
  142. Wilson GWT, Hartnett DC, Rice CW (2006) Mycorrhizal-mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludovician. Func Ecol 20(3):427–435. doi:10.1111/j.1365-2435.2006.01134.x CrossRefGoogle Scholar
  143. Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P et al (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7(9):776–780. doi:10.1111/j.1461-0248.2004.00635.x CrossRefGoogle Scholar
  144. Wissuwa M, Mazzola M, Picard C (2008) Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321(1–2):409–430. doi:10.1007/s11104-008-9693-2 Google Scholar
  145. Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Phil Trans R Soc B 363:703–716. doi:10.1098/rstb.2007.2179 PubMedCrossRefGoogle Scholar
  146. Wolfe MS (1985) The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Ann Rev Phytopath 23:251-273. doi: 10.1146/annurev.py.23.090185.001343
  147. Xu S, Zhu D, Zhang Q (2014) Predicting hybrid performance in rice using genomic best linear unbiased prediction. Proc Natl Acad Sci U S A 111:12456–12461. doi:10.1073/pnas.1413750111 PubMedPubMedCentralCrossRefGoogle Scholar
  148. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci U S A 96:1463–1468. doi:10.1073/pnas.96.4.1463 PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD (2010) Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc Natl Acad Sci U S A 107(4):1443–1446. doi:10.1073/pnas.0906829107 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Zeller SL, Kalinina O, Flynn DFB, Schmid B (2012) Mixtures of genetically modified wheat lines outperform monocultures. Ecol Appl 22(6):1817–1826PubMedCrossRefGoogle Scholar
  151. Zhang W, Ricketts TH, Kremen C, Carney K, Swinton SM (2007) Ecosystem services and dis-services to agriculture. Ecol Econ 64(2):253–260. doi:10.1016/j.ecolecon.2007.02.024 CrossRefGoogle Scholar
  152. Zhang X, Pérez-Rodríguez P, Semagn K, Beyene Y, Babu R et al (2015) Genomic prediction in biparental tropical maize populations in water-stressed and well-watered environments using low-density and GBS SNPs. Heredity 114:291–299. doi:10.1038/hdy.2014.99 PubMedCrossRefGoogle Scholar
  153. Zhu Y, Chen H, Fan J, Wang Y, Li Y et al (2000) Genetic diversity and disease control in rice. Nature 406:718–722. doi:10.1038/35021046 PubMedCrossRefGoogle Scholar
  154. Zhu J, van der Werf W, Anten NP, Vos J, Evers JB (2015) The contribution of phenotypic plasticity to complementary light capture in plant mixtures. New Phytol 207(4):1213–1222. doi:10.1111/nph.13416 PubMedCrossRefGoogle Scholar
  155. Zuppinger-Dingley D, Schmid B, Petermann JS, Yadav V, De Deyn GB et al (2014) Selection for niche differentiation in plant communities increases biodiversity effects. Nature 515(7525):108–111. doi:10.1038/nature13869 PubMedCrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France 2017

Authors and Affiliations

  • Sébastien Barot
    • 1
  • Vincent Allard
    • 2
  • Amélie Cantarel
    • 3
  • Jérôme Enjalbert
    • 4
  • Arnaud Gauffreteau
    • 5
  • Isabelle Goldringer
    • 4
  • Jean-Christophe Lata
    • 1
    • 6
  • Xavier Le Roux
    • 3
  • Audrey Niboyet
    • 1
  • Emanuelle Porcher
    • 7
  1. 1.IEES-P (IRD, CNRS, UPEC)ParisFrance
  2. 2.INRA, UMR 1095 Génétique, Diversité et Ecophysiologie des CéréalesClermont-FerrandFrance
  3. 3.UMR CNRS 5557, UMR 1418 INRA, Ecologie MicrobienneUniversité Lyon1, Université de LyonVilleurbanneFrance
  4. 4.UMR 0320 (INRA–CNRS–UPS) Génétique VégétaleGif-sur-YvetteFrance
  5. 5.INRA, UMR 211 Agronomie, AgroParisTechUniversité Paris-SaclayThiverval-GrignonFrance
  6. 6.Department of Geoecology and Geochemistry, Institute of Natural ResourcesTomsk Polytechnic UniversityTomskRussia
  7. 7.UMR 7204, Centre d’Ecologie et des Sciences de la ConservationSorbonne Universités-MNHN-CNRS-UPMC, Muséum national d’Histoire naturelleParisFrance

Personalised recommendations