Plant and Soil

, Volume 424, Issue 1–2, pp 171–182 | Cite as

Neighbourhood stories: role of neighbour identity, spatial location and order of arrival in legume and non-legume initial interactions

  • Emanuela W. A. Weidlich
  • Vicky M. Temperton
  • Marc Faget
Regular Article


Backgrounds and aims

Interactions between plants can be both positive and negative, denoting facilitation and competition. Although facilitative effects of having legume neighbours (focus on yield productivity) are well studied, a better mechanistic understanding of how legumes interact with non-legumes in terms of root distribution is needed. We tested the effects of neighbour identity, its spatial location, as well as the effects of plant order of arrival on above and belowground traits and root distribution.


We performed a rhizotron experiment (4 weeks duration) in which we grew maize alone, with only a legume, only another grass, or with both species and tracked roots of the plant species using green and red fluorescent markers.


Maize grew differently when it had a neighbour, with reduced development when growing with wheat compared to alone. Growing with a legume generally equated to the same outcome as not having a neighbour. Roots grew towards the legume species and away from the wheat. Order of arrival affected aboveground traits to a certain extent, but its effects on maize roots were dependent on spatial location.


Our study provides evidence of facilitation, showing the importance of the identity of the neighbours, together with their spatial location, and how order of arrival can modulate the outcome of these initial interactions.


Plant-plant interactions Green fluorescent protein (GFP) Legumes Priority effect Competition Nitrogen facilitation Rhizotrons Roots 



We thank Marlene Mueller, Edelgard Schoelgens and the ZEA in the Forschungszentrum Jülich for analysing the soil and plant samples. We thank also Mark Müller-Linow for image alignment. We also thank Benjamin M. Delory for his valuable suggestions on how to improve our manuscript. This research was funded by Forschungszentrum Jülich (IBG2) and Ministry of Science, Technology and Innovation of Brazil (CNPq) with the PhD scholarship of E.W.A.W.

Supplementary material

11104_2017_3398_MOESM1_ESM.docx (485 kb)
ESM 1 (DOCX 485 kb)


  1. Andersen SN, Dresbøll DB, Thorup-Kristensen K (2014) Root interactions between intercropped legumes and non-legumes—a competition study of red clover and red beet at different nitrogen levels. Plant Soil 378:59–72. CrossRefGoogle Scholar
  2. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686Google Scholar
  3. Bessler H, Oelmann Y, Roscher C, Buchmann N, Scherer-Lorenzen M, Schulze ED, Temperton VM, Wilcke W, Engels C (2012) Nitrogen uptake by grassland communities: contribution of N2 fixation, facilitation, complementarity, and species dominance. Plant Soil 358:301–322. CrossRefGoogle Scholar
  4. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielb??rger K, JMJ T, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34.
  5. 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 417:844–848. CrossRefPubMedGoogle Scholar
  6. Casper BB, Jackson RB (1997) Plant competition underground. Nature 337:122–123. Google Scholar
  7. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Soc Nat 111:1119–1144.
  8. de Mendiburu F (2015) Agricolae: statistical procedures for agricultural research. R Package Version 1:2–3 Google Scholar
  9. Duchene O, Vian JF, Celette F (2017) Intercropping with legume for agroecological cropping systems: complementarity and facilitation processes and the importance of soil microorganisms. A review. Agric Ecosyst Environ 240:148–161. CrossRefGoogle Scholar
  10. Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dudley SA, File AL (2008) Yes, kin recognition in plants! Int J Plant Sci 4:69–70. Google Scholar
  12. Eriksson O, Eriksson Å (1998) Effects of arrival order and seed size on germination of grassland plants: are there assembly rules during recruitment? Ecol Res 13:229–239. CrossRefGoogle Scholar
  13. Faget M (2009) Green fluorescent protein (GFP). A tool to study root interactions in mixed plant stands. PhD Thesis 75Google Scholar
  14. Faget M, Liedgens M, Stamp P, Flütsch P, Herrera JM (2010) A minirhizotron imaging system to identify roots expressing the green fluorescent protein. Comput Electron Agric 74:163–167. CrossRefGoogle Scholar
  15. Faget M, Liedgens M, Feil B, Stamp P, Herrera JM (2012) Root growth of maize in an Italian ryegrass living mulch studied with a non-destructive method. Eur J Agron 36:1–8. CrossRefGoogle Scholar
  16. Faget M, Blossfeld S, von Gillhaussen P, Schurr U, Temperton VM (2013a) Disentangling who is who during rhizosphere acidification in root interactions: combining fluorescence with optode techniques. Front Plant Sci 4:1–8. CrossRefGoogle Scholar
  17. Faget M, Nagel KA, Walter A, Herrera JM, Jahnke S, Schurr U, Temperton VM (2013b) Root-root interactions: extending our perspective to be more inclusive of the range of theories in ecology and agriculture using in-vivo analyses. Ann Bot 112:253–266. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Falik O, Reides P, Gersani M, Novoplansky A (2003) Self/non-self discrimination in roots. J Ecol 91:525–531. CrossRefGoogle Scholar
  19. Fan F, Zhang F, Song Y, Sun J, Bao X, Guo T, Li L (2006) Nitrogen fixation of faba bean (Vicia Faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283:275–286. CrossRefGoogle Scholar
  20. Fukami T (2015) Historical contingency in community assembly : integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23. CrossRefGoogle Scholar
  21. Hauggaard-Nielsen H, Jensen ES (2005) Facilitative root interactions in intercrops. Plant Soil 274:237–250. CrossRefGoogle Scholar
  22. Hauggaard-Nielsen H, Jørnsgaard B, Kinane J, Jensen ES (2008) Grain legume–cereal intercropping: the practical application of diversity, competition and facilitation in arable and organic cropping systems. Renewable Agric Food Syst 23:3–12. CrossRefGoogle Scholar
  23. Hecht VL, Temperton VM, Nagel KA, Rascher U, Postma JA (2016) Sowing density: a neglected factor fundamentally affecting root distribution and biomass allocation of field grown spring barley (Hordeum vulgare L.) Front Plant Sci 7:1–14. CrossRefGoogle Scholar
  24. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus Acquisition in the Rhizosphere of intercropped species. Plant Physiol 156:1078–1086. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hobbs RJ, Norton DA (2004) Ecological filters, thresholds, and gradients in resistance to ecosystem reassembly. In: Temperton V, Hobbs RJ, Nuttle T, Halle S (eds) Assembly Rules and Restoration Ecology: Bridging the Gap Between Theory and Practice. Island Press, Washington, pp 72–95Google Scholar
  26. Joseph H, Connell ROS (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  27. Kardol P, Souza L, Classen AT (2013) Resource availability mediates the importance of priority effects in plant community assembly and ecosystem function. Oikos 122:84–94. CrossRefGoogle Scholar
  28. Klemens JA (2008) Kin recognition in plants? Biol Lett 4:67–68. CrossRefPubMedGoogle Scholar
  29. Körner C, Stöcklin J, Reuther-Thiébaud L, Pelaez-Riedl S (2008) Small differences in arrival time influence composition and productivity of plant communities. New Phytol 177:698–705. CrossRefPubMedGoogle Scholar
  30. Li L, Yang S, Li X, Zhang F, Christie P (1999) Interspecific complementary and competitive interactions between intercropped maize and faba bean. Plant Soil 212:105–114. CrossRefGoogle Scholar
  31. Li L, Sun J, Zhang F, Li X, Yang S, Rengel Z (2001) Wheat / maize or wheat / soybean strip intercropping I. Yield advantage and interspeci ® c interactions on nutrients. F Crop Res 71:123–137. CrossRefGoogle Scholar
  32. Li L, Zhang F, Li X, Christie P, Sun J, Yang S, Tang C (2003) Interspecific facilitation of nutrient uptake by intercropped maize and faba bean. Nutr Cycl Agroecosyst 65:61–71. CrossRefGoogle Scholar
  33. Nabel M, Temperton VM, Poorter H, Lücke A, Jablonowski ND (2016) Energizing marginal soils - the establishment of the energy crop Sida Hermaphrodita as dependent on digestate fertilization, NPK, and legume intercropping. Biomass Bioenergy 87:9–16. CrossRefGoogle Scholar
  34. Nagel KA, Kastenholz B, Jahnke S, van Dusschoten D, Aach T, Mühlich M, Truhn D, Scharr H, Terjung S, Walter A, Schurr U (2009) Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping. Funct Plant Biol 36:947–959.
  35. Neugschwandtner RW, Kaul HP (2014) Sowing ratio and N fertilization affect yield and yield components of oat and pea in intercrops. F Crop Res 155:159–163. CrossRefGoogle Scholar
  36. Nord EA, Zhang C, Lynch JP (2011) Root responses to neighbouring plants in common bean are mediated by nutrient concentration rather than self/non-self recognition. Funct Plant Biol 38:941–952. CrossRefGoogle Scholar
  37. Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21:243–255. CrossRefPubMedGoogle Scholar
  38. Padilla FM, Mommer L, de Caluwe H, Smit-Tiekstra AE, Wagemaker CAM, Ouborg NJ, de Kroon H (2013) Early root overproduction not triggered by nutrients decisive for competitive success belowground. PLoS One 8:1–9. CrossRefGoogle Scholar
  39. Postma JA, Lynch JP (2012) Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann Bot 110:521–534. CrossRefPubMedPubMedCentralGoogle Scholar
  40. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL Google Scholar
  41. Ramirez-Garcia J, Martens HJ, Quemada M, Thorup-Kristensen K (2014) Intercropping effect on root growth and nitrogen uptake at different nitrogen levels. J Plant Ecol 8:1–10. Google Scholar
  42. Roscher C, Temperton VM, Scherer-Lorenzen M, Schmitz M, Schumacher J, Schmid B, Buchmann N, Weisser WW, Schulze ED (2005) Overyielding in experimental grassland communities - irrespective of species pool or spatial scale. Ecol Lett 8:419–429. CrossRefGoogle Scholar
  43. Roscher C, Scherer-Lorenzen M, Schumacher J, Temperton VM, Buchmann N, Schulze ED (2011) Plant resource-use characteristics as predictors for species contribution to community biomass in experimental grasslands. Perspect Plant Ecol Evol Syst 13:1–13. CrossRefGoogle Scholar
  44. Sarneel JM, Kardol P, Nilsson C, Bartha S (2016) The importance of priority effects for riparian plant community dynamics. J Veg Sci 27:658–667. CrossRefGoogle Scholar
  45. Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739. CrossRefGoogle Scholar
  46. Semchenko M, Saar S, Lepik A (2014) Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. New Phytol 204:631–637. CrossRefPubMedGoogle Scholar
  47. Sikes BA, Hawkes CV, Fukami T (2016) Plant and root-endophyte assembly history: interactive effects on native and exotic plants. Ecology 97:484–493. CrossRefPubMedGoogle Scholar
  48. Spehn EM, Scherer-Lorenzen M, Schmid B, Hector A, Caldeira MC, Dimitrakopoulos PG, Finn JA, Jumpponen A, O’Donnovan G, Pereira JS, Schulze ED, Troumbis AY, Korner C (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98:205–218. CrossRefGoogle Scholar
  49. Temperton VM, Mwangi PN, Scherer-Lorenzen M, Schmid B, Buchmann N (2007) Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 151:190–205. CrossRefPubMedGoogle Scholar
  50. Tosti G, Thorup-Kristensen K (2010) Using coloured roots to study root interaction and competition in intercropped legumes and non-legumes. J Plant Ecol 3:191–199. CrossRefGoogle Scholar
  51. Valiente-Banuet A, Rumebe AV, Verdú M, Callaway RM (2006) Modern quaternary plant lineages promote diversity through facilitation of ancient tertiary lineages. Proc Natl Acad Sci U S A 103:16812–16817. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Vaughn KJ, Young TP (2015) Short-term priority over exotic annuals increases the initial density and longer-term cover of native perennial grasses. Ecol Appl 25:791–799. CrossRefGoogle Scholar
  53. von Felten S, Hector A, Buchmann N, Niklaus PA, Schmid B, Scherer-lorenzen M, Ecology S, May N, Felten S Von, Hector A, Buchmann N, Niklaus PA, Schmid B, Scherer-lorenzen M (2016) Belowground nitrogen partitioning in experimental grassland plant communities of varying species richness. Ecology 90:1389–1399Google Scholar
  54. Von Gillhaussen P, Rascher U, Jablonowski ND, Plückers C, Beierkuhnlein C, Temperton VM (2014) Priority effects of time of arrival of plant functional groups override sowing interval or density effects: a grassland experiment. PLoS One.
  55. Weidlich EWA, von Gillhaussen P, Delory BM, Blossfeld S, Poorter H, Temperton VM (2017a) The importance of being first: exploring priority and diversity effects in a grassland field experiment. Front Plant Sci 7:1–12. CrossRefGoogle Scholar
  56. Weidlich EWA, von Gillhaussen P, Max JFJ, Delory BM, Jablonowski ND, Rascher U, Temperton VM (2017b) Priority effects caused by plant order of arrival affect belowground productivity. J Ecol.
  57. Zhang F, Li L (2003) Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248:305–312. CrossRefGoogle Scholar
  58. Zhang X, Huang G, Bian X, Zhao Q (2013) Effects of nitrogen fertilization and root interaction on the agronomic traits of intercropped maize, and the quantity of microorganisms and activity of enzymes in the rhizosphere. Plant Soil 368:407–417. CrossRefGoogle Scholar
  59. Zhang C, Postma JA, York LM, Lynch JP (2014) Root foraging elicits niche complementarity-dependent yield advantage in the ancient “three sisters” (maize/bean/squash) polyculture. Ann Bot 114:1719–1733. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute for Bio & Geosciences (IBG-2), Plant Sciences, Forschungszentrum Jülich GmbHJülichGermany
  2. 2.Institute of EcologyLeuphana University LüneburgLüneburgGermany

Personalised recommendations