Plant and Soil

, Volume 414, Issue 1–2, pp 339–354 | Cite as

Rainfall reduction impacts rhizosphere biogeochemistry in eucalypts grown in a deep Ferralsol in Brazil

  • Céline Pradier
  • Philippe Hinsinger
  • Jean-Paul Laclau
  • Jean-Pierre Bouillet
  • Irae Amaral Guerrini
  • José Leonardo Moraes Gonçalves
  • Verónica Asensio
  • Cassio H. Abreu-Junior
  • Christophe JourdanEmail author
Regular Article


Background and aims

Comparing root functioning under contrasting rainfall regimes can help assessing the capacity of plant species to cope with more intense and frequent drought predicted under climate change context. While the awareness of the need to study the whole root system is growing, most of the studies of root functioning through rhizosphere analyses have been restricted to the topsoil. Our study aimed to assess whether the depth in the soil and the rainfall amount affect root functioning, and notably the fate of nutrients within the rhizosphere.


We compared pH and nutrient availability within the rhizosphere and bulk soil along a 4-m deep soil profile in a 5-year-old eucalypt (Eucalyptus grandis) plantation under undisturbed and reduced rainfall treatments.


The exchangeable K concentration and the pH of the bulk soil were not influenced by the reduced rainfall treatment. By contrast, the H3O+ concentration in the rhizosphere was significantly greater than that of the bulk soil, only in the reduced rainfall plot. The concentrations of exchangeable K in the rhizosphere were significantly larger than those of the bulk soil in both treatments but this difference was higher in the reduced rainfall plot, notably below the depth of 2 m. Both exchangeable K and H3O+ concentration significantly increased within the rhizosphere in the reduced rainfall treatment at soil depth down to 4 m.


The amount of K brought to the roots by mass flow was estimated and could not explain the observed increase in exchangeable K concentration within the rhizosphere. A more likely explanation was root-induced weathering of K-bearing minerals, partly related to enhanced rhizosphere acidification. Our results demonstrate that root functioning can be considerably altered as a response to drought down to large depths.


Eucalyptus grandis Fine root Soil depth pH Exchangeable potassium cation 



We acknowledge the staff at the Itatinga Experimental Station (ESALQ-USP) as well as Eder Araujo da Silva and Floragro ( for their technical support. This project was funded by the University of São Paulo, the Centre de coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), the Agence Nationale de la Recherche (MACACC project ANR-13-AGRO-0005, Viabilité et Adaptation des Ecosystèmes Productifs, Territoires et Ressources face aux Changements Globaux AGROBIOSPHERE 2013 program), USP-COFECUB (Project 2011–25), FAPESP (grant number 2013/25998-4) and AGREENIUM (Plantrotem project). This site belongs to the SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French national research infrastructure ANAEE-F (

Supplementary material

11104_2016_3107_MOESM1_ESM.jpg (68 kb)
Fig. S1 Volumetric soil water content (SWC) in the + W (a) and –W (b) treatments between topsoil and the depth of 4 m, from March 2015 to October 2015. The arrows indicate the collection period. (JPG 67 kb)
11104_2016_3107_MOESM2_ESM.jpg (19 kb)
Fig. S2 Soil pseudo-total K concentration of the bulk soil along the soil profile for both treatments (+W = full symbol; –W = open symbol) upon sampling time, B stands for bulk soil. (JPG 18 kb)
11104_2016_3107_MOESM3_ESM.docx (27 kb)
Table S1 Circumference and aboveground biomass of the trees in the three blocks for –W and + W treatments. Data were collected in April 2015. Significant treatment effect were found on circumference (p < 0.01) and aboveground biomass (p < 0.01) but not on block. The study was made in the block 3 (bold values). (DOCX 26 kb)
11104_2016_3107_MOESM4_ESM.docx (28 kb)
Table S2 Concentrations (mg kg- 1) obtained for the available Ca and Mg in the bulk soil (Bulk) and in the rhizosphere (Rhizo) in the + W and –W treatments for the 4 repetitions (Rep). The limit of detection for Ca was 1.12 mg kg- 1 and 0.56 mg kg- 1 for Mg. Hence, only the values above the determination threshold are meaningful (2.24 mg kg- 1 for Ca and 1.12 mg kg- 1 for Mg). Values below the determination threshold were indicated by a hyphen (DOCX 28 kb)


  1. Aroca R (2012) Plant responses to drought stress: from morphological to molecular features. Springer Science & Business MediaGoogle Scholar
  2. Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach, 2 edn. WileyGoogle Scholar
  3. Barré P, Montagnier C, Chenu C et al (2007) Clay minerals as a soil potassium reservoir: observation and quantification through X-ray diffraction. Plant Soil 302:213–220. doi: 10.1007/s11104-007-9471-6 CrossRefGoogle Scholar
  4. Battie-Laclau P, Laclau JP, Domec JC et al (2014) Effects of potassium and sodium supply on drought-adaptive mechanisms in Eucalyptus grandis plantations. New Phytol 203:401–413. doi: 10.1111/nph.12810 CrossRefPubMedGoogle Scholar
  5. Battie-Laclau P, Delgado-Rojas JS, Christina M et al (2016) Potassium fertilization increases water-use efficiency for stem biomass production without affecting intrinsic water-use efficiency in Eucalyptus grandis plantations. For Ecol Manag 364:77–89. doi: 10.1016/j.foreco.2016.01.004 CrossRefGoogle Scholar
  6. Benedetti MF, Menard O, Noack Y et al (1994) Water-rock interactions in tropical catchments: field rates of weathering and biomass impact. Chem Geol 118:203–220CrossRefGoogle Scholar
  7. Blossfeld S (2013) Light for the dark side of plant life: Planar optodes visualizing rhizosphere processes. Plant Soil 369:29–32CrossRefGoogle Scholar
  8. Bravin MN, Martí AL, Clairotte M, Hinsinger P (2008) Rhizosphere alkalisation - a major driver of copper bioavailability over a broad pH range in an acidic, copper-contaminated soil. Plant Soil 318:257–268. doi: 10.1007/s11104-008-9835-6 CrossRefGoogle Scholar
  9. Callesen I, Harrison R, Stupak I et al (2016) Carbon storage and nutrient mobilization from soil minerals by deep roots and rhizospheres. For Ecol Manag 359:322–331. doi: 10.1016/j.foreco.2015.08.019 CrossRefGoogle Scholar
  10. Calvaruso C, N’Dira V, Turpault MP (2011) Impact of common European tree species and Douglas-fir (Pseudotsuga menziesii [Mirb.] Franco) on the physicochemical properties of the rhizosphere. Plant Soil 342:469–480. doi: 10.1007/s11104-010-0710-x CrossRefGoogle Scholar
  11. Calvaruso C, Collignon C, Kies A, Turpault MP (2014) Seasonal evolution of the rhizosphere effect on major and trace elements in soil solutions of Norway Spruce (Picea abies Karst) and beech (Fagus sylvatica) in an acidic forest soil. Open J Soil Sci 4:323–336. doi: 10.4236/ojss.2014.49034 CrossRefGoogle Scholar
  12. Christina M, Laclau JP, Goncalves JLM et al (2011) Almost symmetrical vertical growth rates above and below ground in one of the world’s most productive forests. Ecosphere 2:2710CrossRefGoogle Scholar
  13. Christina M, Le Maire G, Battie-Laclau P et al (2015) Measured and modeled interactive effects of potassium deficiency and water deficit on gross primary productivity and light-use efficiency in Eucalyptus grandis plantations. Glob Chang Biol 21:2022–2039. doi: 10.1111/gcb.12817 CrossRefPubMedGoogle Scholar
  14. Christina M, Nouvellon Y, Laclau JP, Stape JL, Bouillet JP, Lambais GR, le Maire G (2016). Importance of deep water uptake in tropical eucalypt forest. Funct Ecol, in pressGoogle Scholar
  15. Christoffersen BO, Restrepo-Coupe N, Arain MA et al (2014) Mechanisms of water supply and vegetation demand govern the seasonality and magnitude of evapotranspiration in Amazonia and Cerrado. Agric For Meteorol 191:33–50CrossRefGoogle Scholar
  16. Clegg S, Gobran GR (1997) Rhizospheric P and K in forest soil manipulated with ammonium sulfate and water. Can J Soil Sci 77:525–533CrossRefGoogle Scholar
  17. Cocco S, Agnelli A, Gobran GR, Corti G (2013) Changes induced by the roots of Erica arborea L. to create a suitable environment in a soil developed from alkaline and fine-textured marine sediments. Plant Soil 368:297–313. doi: 10.1007/s11104-012-1501-3 CrossRefGoogle Scholar
  18. Collignon C, Calvaruso C, Turpault M-P (2011) Temporal dynamics of exchangeable K, Ca and Mg in acidic bulk soil and rhizosphere under Norway spruce (Picea abies Karst.) and beech (Fagus sylvatica L.) stands. Plant Soil 349:355–366. doi: 10.1007/s11104-011-0881-0 CrossRefGoogle Scholar
  19. Courchesne F, Gobran GR (1997) Mineralogical variations of bulk and rhizosphere soils from a Norway spruce stand. Soil Sci Soc Am J 61:1245. doi: 10.2136/sssaj1997.03615995006100040034x CrossRefGoogle Scholar
  20. da Silva EV, Bouillet JP, de Moraes Gonçalves JL et al (2011) Functional specialization of eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths. Funct Ecol 25:996–1006. doi: 10.1111/j.1365-2435.2011.01867.x CrossRefGoogle Scholar
  21. Darunsontaya T, Suddhiprakarn A, Kheoruenromne I et al (2012) The forms and availability to plants of soil potassium as related to mineralogy for upland Oxisols and Ultisols from Thailand. Geoderma 170:11–24. doi: 10.1016/j.geoderma.2011.10.002 CrossRefGoogle Scholar
  22. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. doi: 10.1038/nature04514 CrossRefPubMedGoogle Scholar
  23. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42CrossRefGoogle Scholar
  24. EMBRAPA (1999) Sistema brasileiro de classificação de solos. Embrapa Solos, Centro Nacional de Pesquisa de Solos, Rio de JaneiroGoogle Scholar
  25. Epron D, Cabral OMR, Laclau JP et al (2016) In situ (CO2)-C-13 pulse labelling of field-grown eucalypt trees revealed the effects of potassium nutrition and throughfall exclusion on phloem transport of photosynthetic carbon. Tree Physiol 36:6–21. doi: 10.1093/treephys/tpv090 CrossRefPubMedGoogle Scholar
  26. FAO (1998) World reference base for soil resources FAO. ISRIC and ISSS, RomeGoogle Scholar
  27. Fontaine S, Delvaux B, Dufey JE, Herbillon AJ (1989) Potassium exchange behaviour in Carribean volcanic ash soils under banana cultivation. Plant Soil 120:283–290CrossRefGoogle Scholar
  28. Göransson H, Rosengren U (2006) Nutrient acquisition from different soil depths by pedunculate oak. Trees-Struct Funct 20:292–298CrossRefGoogle Scholar
  29. Göransson H, Fransson A-M, Jonsson-Belyazid U (2007) Do oaks have different strategies for uptake of N, K and P depending on soil depth? Plant Soil 297:119–125. doi: 10.1007/s11104-007-9325-2 CrossRefGoogle Scholar
  30. Göransson H, Ingerslev M, Wallander H (2008) The vertical distribution of N and K uptake in relation to root distribution and root uptake capacity in mature Quercus robur, Fagus sylvatica and Picea abies stands. Plant Soil 306:129–137. doi: 10.1007/s11104-007-9524-x CrossRefGoogle Scholar
  31. Hinsinger P, Elsass F, Jaillard B, Robert M (1993) Root-induced irreversible transformation of a trioctahedral mica in the rhizosphere of rape. J Soil Sci 44:535–545. doi: 10.1111/j.1365-2389.1993.tb00475.x CrossRefGoogle Scholar
  32. Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. (Special issue: Structure and functioning of cluster roots and plant responses to phosphate deficiency). Plant Soil 248:43–59CrossRefGoogle Scholar
  33. Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303. doi: 10.1111/j.1469-8137.2005.01512.x CrossRefPubMedGoogle Scholar
  34. Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. (Special Issue: Rhizosphere: achievements and challenges.). Plant Soil 321:117–152CrossRefGoogle Scholar
  35. Hinsinger P, Betencourt E, Bernard L et al (2011a) P for Two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086. doi: 10.1104/pp.111.175331 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hinsinger P, Brauman A, Devau N et al (2011b) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61. doi: 10.1007/s11104-011-0903-y CrossRefGoogle Scholar
  37. Huang B, Duncan RR, Carrow RN (1997) Drought-resistance mechanisms of seven warm-season turfgrasses under surface soil drying: II. Root aspects. Crop Sci 37:1863–1869CrossRefGoogle Scholar
  38. 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. In: Stocker TF, Qin D, Plattner G-K, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM. eds. Cambridge, UK & New York, NY, USA: Cambridge University PressGoogle Scholar
  39. Jaillard B, Hinsinger P (1993) Root-induced release of interlayer potassium and vermiculitization of phlogopite as related to potassium depletion in the rhizosphere of ryegrass. J Soil Sci 44:525–534CrossRefGoogle Scholar
  40. Kell DB (2011) Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Ann Bot 108:407–418. doi: 10.1093/aob/mcr175 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Laclau JP, Almeida JCR, Gonçalves JLM et al (2009) Influence of nitrogen and potassium fertilization on leaf lifespan and allocation of above-ground growth in Eucalyptus plantations. Tree Physiol 29:111–124. doi: 10.1093/treephys/tpn010 CrossRefPubMedGoogle Scholar
  42. Laclau JP, Ranger J, de Moraes Gonçalves JL et al (2010) Biogeochemical cycles of nutrients in tropical Eucalyptus plantations. For Ecol Manag 259:1771–1785. doi: 10.1016/j.foreco.2009.06.010 CrossRefGoogle Scholar
  43. Laclau JP, da Silva EA, Rodrigues Lambais G et al (2013) Dynamics of soil exploration by fine roots down to a depth of 10 m throughout the entire rotation in Eucalyptus grandis plantations. Front Plant Sci. doi: 10.3389/fpls.2013.00243 PubMedPubMedCentralGoogle Scholar
  44. Maeght JL, Rewald B, Pierret A (2013) How to study deep roots-and why it matters. Front Plant Sci. doi: 10.3389/fpls.2013.00299 PubMedPubMedCentralGoogle Scholar
  45. Maquère V (2008) Dynamics of mineral elements under a fast-growing eucalyptus plantation in Brazil. Implications for soil sustainability, Ph.D thesis Agro Paris Tech and USP-ESALQ, BrazilGoogle Scholar
  46. Maurice J, Laclau JP, Re DS et al (2010) Fine root isotropy in Eucalyptus grandis plantations. Towards the prediction of root length densities from root counts on trench walls. Plant Soil 334:261–275CrossRefGoogle Scholar
  47. Melo VF, Corrêa GF, Ribeiro AN et al (2005) Cinética de liberação de potássio e magnésio pelos minerais da fração argila de solos do Triângulo Mineiro. Rev Brasil Ciênc Solo 29:533–545. doi: 10.1590/S0100-06832005000400006 CrossRefGoogle Scholar
  48. Melo VF, Schaefer CEGR, Novais RF et al (2007) Potassium and magnesium in clay minerals of some Brazilian soils as indicated by a sequential extraction procedure. Commun Soil Sci Plant Anal 33:2203–2225. doi: 10.1081/CSS-120005757 CrossRefGoogle Scholar
  49. Nadezhdina N, David TS, David JS et al (2010) Trees never rest: the multiple facets of hydraulic redistribution. Ecohydrology 3:431–444. doi: 10.1002/eco.148 CrossRefGoogle Scholar
  50. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. doi: 10.5194/hess-11-1633-2007 CrossRefGoogle Scholar
  51. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. doi: 10.1038/nrmicro3109 CrossRefPubMedGoogle Scholar
  52. Pinheiro RC, de Deus JC, Nouvellon Y et al (2016) A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil. For Ecol Manag 366:143–152. doi: 10.1016/j.foreco.2016.02.012 CrossRefGoogle Scholar
  53. Reinhold-Hurek B, Bünger W, Burbano CS et al (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424. doi: 10.1146/annurev-phyto-082712-102342 CrossRefPubMedGoogle Scholar
  54. Rewald B, Godbold DL, Falik O, Rachmilevitch S (2014) Root and rhizosphere processes - high time to dig deeper. Front Plant Sci 5:278CrossRefPubMedPubMedCentralGoogle Scholar
  55. Römheld V, Kirkby EA (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180. doi: 10.1007/s11104-010-0520-1 CrossRefGoogle Scholar
  56. Santiago LS, Wright SJ, Harms KE et al (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316. doi: 10.1111/j.1365-2745.2011.01904.x CrossRefGoogle Scholar
  57. Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–494CrossRefGoogle Scholar
  58. Silva IR, Novais RF, Jham GN et al (2004) Responses of eucalypt species to aluminum: the possible involvement of low molecular weight organic acids in the Al tolerance mechanism. Tree Physiol 24:1267–1277CrossRefPubMedGoogle Scholar
  59. Sokolova TA (2015) Specificity of soil properties in the rhizosphere: analysis of literature data. Eurasian Soil Sci 48:968–980. doi: 10.1134/S1064229315050099 CrossRefGoogle Scholar
  60. Taylor AB, Velbel MA (1991) Geochemical mass balances and weathering rates in forested watersheds of the southern blue ridge II. Effects of botanical uptake terms. Geoderma 51:29–50CrossRefGoogle Scholar
  61. Thom D, Seidl R (2015) Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests. Biol Rev Camb Philos Soc. doi: 10.1111/brv.12193 PubMedPubMedCentralGoogle Scholar
  62. Turpault MP, Uterano C, Boudot JP, Ranger J (2005) Influence of mature Douglas fir roots on the solid soil phase of the rhizosphere and its solution chemistry. Plant Soil 275:327–336CrossRefGoogle Scholar
  63. Turpault M-P, Gobran GR, Bonnaud P (2007) Temporal variations of rhizosphere and bulk soil chemistry in a Douglas fir stand. Geoderma 137:490–496. doi: 10.1016/j.geoderma.2006.10.005 CrossRefGoogle Scholar
  64. Van Raij B, Quaggio JA (2001) Determinação de fósforo, cálcio, magnésio e potássio extraídos com resina trocadora de íons. In: van Raij B, de Andrade JC, Cantarella H, Quaggio JA (eds) Análise química para avaliação da fertilidade de solos tropicais. Instituto Agronômico, Campinas, Brazil, pp 189–199Google Scholar
  65. Velbel MA, Price JR (2007) Solute geochemical mass-balances and mineral weathering rates in small watersheds: Methodology, recent advances, and future directions. Appl Geochem 22:1682–1700. doi: 10.1016/j.apgeochem.2007.03.029 CrossRefGoogle Scholar
  66. West A, Galy A, Bickle M (2005) Tectonic and climatic controls on silicate weathering. Earth Planet Sci Lett 235:211–228. doi: 10.1016/j.epsl.2005.03.020 CrossRefGoogle Scholar
  67. Wu Z, Dijkstra P, Koch GW, Peñuelas J, Hungate BA (2011) Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Chang Biol 17:927–942CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Céline Pradier
    • 1
  • Philippe Hinsinger
    • 2
  • Jean-Paul Laclau
    • 1
  • Jean-Pierre Bouillet
    • 1
  • Irae Amaral Guerrini
    • 3
  • José Leonardo Moraes Gonçalves
    • 4
  • Verónica Asensio
    • 5
  • Cassio H. Abreu-Junior
    • 5
  • Christophe Jourdan
    • 1
    Email author
  1. 1.CIRAD, UMR Eco&SolsMontpellierFrance
  2. 2.INRA, UMR Eco&SolsMontpellierFrance
  3. 3.FCA, UNESPBotucatuBrazil
  4. 4.LCF, ESALQPiracicabaBrazil
  5. 5.CENA, ESALQPiracicabaBrazil

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