Grass to legume facilitation in saline-sodic steppes: influence of vegetation seasonality and root symbionts

  • Carla E. Di Bella
  • Pablo A. García-ParisiEmail author
  • Fernando A. Lattanzi
  • Magdalena Druille
  • Hans Schnyder
  • Agustín A. Grimoldi
Regular Article



Identify key factors driving legume seedlings performance in saline-sodic soils.


Five plots were established in paired sub-humid steppes with saline-sodic soils dominated by Distichlis spicata or Panicum coloratum. In each plot, Lotus tenuis was sown in autumn and individual plants were collected close to nurse plants (dominant species), and in open areas, at the end of the cold and warm seasons. Carbon and nutrient acquisition (through C and O isotopic composition and N and P content measurements) and plant symbiotic functioning (through N fixation by rhizobia and mycorrhizal colonization measurements) were determined.


Biomass of legume grown close to a nurse plant was always higher than in open areas. This increase was higher close to P. coloratum and to D. spicata in the cold and warm seasons, respectively. In both cases, L. tenuis improved its nutrient acquisition and symbiosis functioning. N-acquisition and rhizobia efficiency increased in the most facilitated L. tenuis plants in the cold season while P-acquisition was greater in the warm season.


Grass-to-legume facilitation in sub-humid steppes with saline-sodic soils was detected in cold and warm seasons, differing between steppes in relationship with the vegetation growing rate and the establishment and functioning of legume-rhizobia-mycorrhiza symbioses.


Dual isotope approach Lotus tenuis N fixation N isotopic composition Mycorrhiza Halomorphic soils 



arbuscular mycorrhizal fungi






stomatal conductance


assimilation rate


water use efficiency


carbon isotope composition


nitrogen isotope composition


oxygen isotope composition



This work formed part of the project HALOSYMB, supported by BAYLAT-CONICET (Bilateral Cooperation Project, Germany-Argentina). We also thank José Otondo for facilitating the access to the study site. CEDB and PAGP were supported by a postdoctoral fellowship from CONICET (Argentina). PAGP was also supported by a short-term grant from the DAAD (German Academic Exchange Service) number 57314022. We want to thank Dr. Gustavo Striker, the editor and two anonymous reviewers for their comments on the early version of the manuscript.


  1. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  2. Bertness MD, Callaway R (1994) Positive interactions in communities. TREE 9(5):191–193. CrossRefPubMedGoogle Scholar
  3. Bertness MD, Ewanchuk PJ (2002) Latitudinal and climate-driven variation in the strength and nature of biological interactions in New England salt marshes. Oecologia 132(3):392–401. CrossRefPubMedGoogle Scholar
  4. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134(2):189–207. CrossRefGoogle Scholar
  5. Brendel O, Iannetta PPM, Stewart D (2000) A rapid and simple method to isolate pure alpha-cellulose. Phytochem Anal 11(1):7–10.<7::AID-PCA488>3.0.CO;2-U CrossRefGoogle Scholar
  6. Burkart SE, Leon RJC, Movia CP (1990) Inventario fitosociologico del pastizal de la depresion del salado (prov. Bs. As.) en un area representativa de sus principales ambientes. Darwiniana 30(1/4):27–69Google Scholar
  7. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78(7):1958–1965CrossRefGoogle Scholar
  8. Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S, Anthelme F, Björk RG, Dickinson KJM, Cranston BH, Gavilán R, Gutiérrez-Girón A, Kanka R, Maalouf JP, Mark AF, Noroozi J, Parajuli R, Phoenix GK, Reid AM, Ridenour WM, Rixen C, Wipf S, Zhao L, Escudero A, Zaitchik BF, Lingua E, Aschehoug ET, Callaway RM (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Lett 17(2):193–202. CrossRefPubMedGoogle Scholar
  9. Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55(407):2447–2460. CrossRefPubMedGoogle Scholar
  10. Di Bella CE, Striker GG, Loreti J, Cosentino DJ, Grimoldi AA (2016) Soil water regime of grassland communities along subtle topographic gradient in the flooding Pampa (Argentina). Soil Water Res 11(2):90–96. CrossRefGoogle Scholar
  11. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137Google Scholar
  12. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40(1):503–537. CrossRefGoogle Scholar
  13. Farquhar GD, Cernusak LA, Barnes B (2007) Heavy water fractionation during transpiration. Plant Physiol 143(1):11–18. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Flores J, Jurado E (2003) Are nurse-protégé interactions more common among plants from arid environments? J Veg Sci 14(6):911–916. CrossRefGoogle Scholar
  15. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Los AngelesGoogle Scholar
  16. Fuka, D. R., Walter, M. T., Archibald, J. A., Steenhuis, T. S., & Easton, Z. M. (2014). EcoHydRology: a community modeling foundation for eco-hydrology. R package version 0.4.12. Retrieved from
  17. García Parisi PA, Lattanzi FA, Grimoldi AA, Omacini M (2015) Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses. Oikos 124(5):553–560. CrossRefGoogle Scholar
  18. García-Parisi PA, Lattanzi FA, Grimoldi AA, Druille M, Omacini M (2017) Three symbionts involved in interspecific plant-soil feedback: Epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis. Plant Soil 412:151–162.
  19. Gaudinski JB, Dawson TE, Quideau S, Schuur EAG, Roden JS, Trumbore SE, Sandquist DR, Oh SW, Wasylishen RE (2005) Comparative analysis of cellulose preparation techniques for use with 13C, 14C, and 18O isotopic measurements. Anal Chem 77(22):7212–7224. CrossRefPubMedGoogle Scholar
  20. Gerz M, Bueno GC, Ozinga WA, Zobel M, Moora M (2018) Niche differentiation and expansion of plant species are associated with mycorrhizal symbiosis. J Ecol 106(1):254–264. CrossRefGoogle Scholar
  21. Gómez-Aparicio L, Valladares F, Zamora R, Quero JL (2005) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28(6):757–768. CrossRefGoogle Scholar
  22. Hanson WC (1950) The photometric determination of phosphorus in fertilizers using the phosphovanado-molybdate complex. J Sci Food Agric 1(6):172–173. CrossRefGoogle Scholar
  23. Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, Chase J, Fay PA, Hautier Y, Hillebrand H, MacDougall AS, Seabloom EW, Williams R, Bakker JD, Cadotte MW, Chaneton EJ, Chu C, Cleland EE, D’Antonio C, Davies KF, Gruner DS, Hagenah N, Kirkman K, Knops JMH, la Pierre KJ, McCulley RL, Moore JL, Morgan JW, Prober SM, Risch AC, Schuetz M, Stevens CJ, Wragg PD (2016) Addition of multiple limiting resources reduces grassland diversity. Nature 537(7618):93–96. CrossRefPubMedGoogle Scholar
  24. Harrison MJ, Dewbre GR, Liu J, (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14(10):2413-2429CrossRefPubMedPubMedCentralGoogle Scholar
  25. Herben T, Mayerová H, Skálová H, Hadincová V, Pecháčková S, Krahulec F (2017) Long-term time series of legume cycles in a semi-natural montane grassland: evidence for nitrogen-driven grass dynamics? Funct Ecol 31(7):1430–1440. CrossRefGoogle Scholar
  26. Högberg P (1997) Tansley review no. 95. 15Natural abundance in soil-plant systems. New Phytol 137(2):179–203. CrossRefGoogle Scholar
  27. Høgh-Jensen H, Schjoerring JK (1997) Interactions between white clover and ryegrass under contrasting nitrogen availability: N2 fixation, N fertilizer recovery, N transfer and water use efficiency. Plant Soil 197:187–199CrossRefGoogle Scholar
  28. INTA. (2017). SIGA - Sistema de Información y Gestión Agrometeorológica. Retrieved May 23, 2018, from Accessed 23 May 2018
  29. INTA. (2018). Carta de suelos de la provincia de Buenos Aires. Retrieved from Accessed 23 May 2018
  30. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bucking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. CrossRefPubMedGoogle Scholar
  31. Kikvidze Z, Khetsuriani L, Kikodze D, Callaway RM (2006) Seasonal shifts in competition and facilitation in subalpine plant communities of the central Caucasus. J Veg Sci 17(1):77–82. CrossRefGoogle Scholar
  32. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70CrossRefPubMedPubMedCentralGoogle Scholar
  33. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33(6):1441. CrossRefGoogle Scholar
  34. Laliberté E, Zemimik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345(6204):1602–1605. CrossRefGoogle Scholar
  35. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115(3):495–501. CrossRefGoogle Scholar
  36. McIntire EJB, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201(2):403–416. CrossRefPubMedGoogle Scholar
  37. Moreno-Gutiérrez C, Dawson TE, Nicolás E, Querejeta JI (2012) Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytol 196(2):489–496. CrossRefPubMedGoogle Scholar
  38. Mortier V, Holsters M, Goormachtig S (2011) Never too many? How legumes control nodule numbers. Plant Cell Environ 3:245–258. CrossRefGoogle Scholar
  39. Naidu R, Rengasamy P (1993) Ion interactions and constraints to plant nutrition in australian sodic soils. Aust J Soil Res 31(6):801–819. CrossRefGoogle Scholar
  40. Paruelo JM, Epstein HE, Lauenroth WK, Burke IC (1997) ANPP estimates from NDVI for the central grassland region of the United States. Ecology 78(3):953. CrossRefGoogle Scholar
  41. Perelman SB, Leon RJC, Oesterheld M (2001) Cross-scale vegetation patterns of flooding Pampa grasslands. J Ecol 89(4):562–577. CrossRefGoogle Scholar
  42. Phillips JM, Hayman DS, (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158-161CrossRefGoogle Scholar
  43. Pinheiro, J. C., Bates, D., DebRoy, S., Sarkar, D., & Team, R. C. (2015). {nlme}: linear and nonlinear mixed effects models. R package version: 3.1-141. Retrieved from Accessed 20 Dec 2015
  44. Priestley CHB, Taylor RJ (1972) On the assessment of surface heat flux and evaporation using large-scale parameters. Mon Weather Rev 100(2):81–92.<0081:OTAOSH>2.3.CO;2 CrossRefGoogle Scholar
  45. Qadir M, Oster JD, Schubert S, Noble AD, Sahrawat KL (2007) Phytoremediation of sodic and saline-sodic soils. Adv Agron 96(07):197–247. CrossRefGoogle Scholar
  46. Quinos PM, Insausti P, Soriano A (1998) Facilitative effect of Lotus tenuis on Paspalum dilatatum in a lowland grassland of Argentina. Oecologia 114(3):427–431. CrossRefPubMedGoogle Scholar
  47. R Core Team. (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, AustriaGoogle Scholar
  48. Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57(5):1017–1023. CrossRefGoogle Scholar
  49. Rengasamy P (2010) Soil processes affecting crop production in salt-affected soils. Funct Plant Biol 37(7):613–620. CrossRefGoogle Scholar
  50. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125(3):350–357. CrossRefPubMedGoogle Scholar
  51. Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137. CrossRefGoogle Scholar
  52. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  53. 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(2):205–218. CrossRefGoogle Scholar
  54. Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation: Tansley review. New Phytol 174(1):11–25. CrossRefPubMedGoogle Scholar
  55. Sonmez S, Buyuktas D, Okturen F, Citak S, (2008) Assessment of different soil to water ratios (1:1, 1:2.5, 1:5) in soil salinity studies. Geoderma 144(1-2):361-369CrossRefGoogle Scholar
  56. Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. J Exp Bot 68(8):1851–1872. CrossRefPubMedGoogle Scholar
  57. Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355(6321):173–176. CrossRefPubMedGoogle Scholar
  58. Valladares F, Bastias CC, Godoy O, Granda E, Escudero A (2015) Species coexistence in a changing world. Front Plant Sci 6(October):1–16. CrossRefGoogle Scholar
  59. Van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97(6):1139–1150. CrossRefGoogle Scholar
  60. van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310. CrossRefPubMedGoogle Scholar
  61. van der Heijden MGA, de Bruin S, Luckerhoff L, van Logtestijn RSP, Schlaeppi K (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10(2):389–399. CrossRefPubMedGoogle Scholar
  62. Wang C, Wan S, Xing X, Zhang L, Han X (2006) Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in northern China. Soil Biol Biochem 38(5):1101–1110. CrossRefGoogle Scholar
  63. Yang Z, Liu J, Tischer SV, Christmann A, Windisch W, Schnyder H, Grill E (2016) Leveraging abscisic acid receptors for efficient water use in Arabidopsis. Proc Natl Acad Sci 113(24):6791–6796. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.IFEVA, Universidad de Buenos Aires, CONICET, Facultad de AgronomíaBuenos AiresArgentina
  2. 2.Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Producción Animal, Cátedra de ForrajiculturaBuenos AiresArgentina
  3. 3.Technische Universität MünchenFreising-WeihenstephanGermany
  4. 4.INIA La EstanzuelaInstituto Nacional de Investigación Agropecuaria (INIA)ColoniaUruguay

Personalised recommendations