Plant and Soil

, Volume 384, Issue 1–2, pp 113–129 | Cite as

Drought changes the structure and elemental composition of very fine roots in seedlings of ten woody tree species. Implications for a drier climate

  • Manuel Olmo
  • Bárbara Lopez-Iglesias
  • Rafael Villar
Regular Article


Background and aims

Water availability is often one of the most limiting factors for plants. Climate change predictions for many areas suggest an intensification of water limitation. The ability of a plant to modify its root characteristics can be an important mechanism for preventing drought stress.


We studied the drought response of seedlings of 10 woody species and compared the biomass allocation, vertical root distribution across different root diameters, and the key traits of very fine roots (root diameter <0.5 mm) under two water regimes (no water limitation and severe drought).


Under drought conditions, the very fine roots had a higher specific root length (SRL, root length: biomass ratio), smaller root diameter and higher root tissue mass density, as well as a lower nitrogen concentration. A higher value of the mean root plasticity index was related to higher drought resistance. A quantitative literature review showed that there was a wide variation in the effect of the drought on SRL, thus there was not a clear effect of drought on SRL.


Certain species have the necessary root traits and plasticity to survive drought. We have identified plasticity in root characteristics as a whole-plant trait which plays a significant role in separating out species into those which are vulnerable and those which are resistant to drought.


Biomass allocation Drought Plasticity Vertical root distribution Root traits Specific root length Survival 



This study was supported by an FPI-MEC pre-doctoral fellowship awarded to BL (BES-2009-016985), the coordinated Spanish MEC projects INTERBOS (CGL2008-04503-CO3-02) and DIVERBOS (CGL2011-30285-C02-02), the ANASINQUE project (PGC2010-RNM-5782), the Life + Biodehesa Project (11/BIO/ES/000726) and FEDER funding. We thank the Consejería de Medio Ambiente (Junta de Andalucía, Spain) for providing the seedlings for this experiment. Mar Ávila and Daniel Sánchez helped in the experiment and Simón Cuadros let us use the WinRHIZO analysis equipment. Thanks to Enrique Garcia de la Riva and José Luis Quero for their comments aimed at improving the manuscript. Our research group is a member of the GLOBIMED network (

Supplementary material

11104_2014_2178_MOESM5_ESM.doc (160 kb)
Figure S1 Annual rainfall in the South of Spain (Córdoba) from 1920 to 2013. (Data from AEMET, Agencia Estatal de Meteorología). Pearson correlation coefficient and significance levels are given: (* P < 0.05). (DOC 160 kb)
11104_2014_2178_MOESM6_ESM.doc (660 kb)
Figure S2 (a) Experimental design diagram with harvests and treatments: initial control plants (C1); watered plants (final control plants, C2) and plants in drought (D). (b) Mean ± SE of plant biomass for each species and treatments. (DOC 660 kb)
11104_2014_2178_MOESM7_ESM.doc (223 kb)
Figure S3 Mean ± SE of relative soil water content for all species during drought. (DOC 223 kb)
11104_2014_2178_MOESM8_ESM.doc (472 kb)
Figure S4 Mean ± SE of vertical root distribution (proportion of total root biomass in one layer, g g−1). Layer 1: 0–10 cm; Layer 2: 10–20 cm; Layer 3: 20–30 cm; Layer 4: 30–40 cm for the ten species and two treatments (control in red and drought in yellow). (DOC 472 kb)
11104_2014_2178_MOESM9_ESM.doc (582 kb)
Figure S5 Relationship between specific root length (SRL) and: (a) root diameter (RD); (b) root tissue mass density (TMDr) for the two treatments (control in red and drought in yellow). Pearson correlation coefficient and significance levels are given: (n.s. P > 0.1; * P < 0.05; ** P < 0.01) (DOC 582 kb)
11104_2014_2178_MOESM1_ESM.doc (34 kb)
Table S1 (DOC 33 kb)
11104_2014_2178_MOESM2_ESM.doc (130 kb)
Table S2 (DOC 130 kb)
11104_2014_2178_MOESM3_ESM.doc (74 kb)
Appendix S1 (DOC 74 kb)
11104_2014_2178_MOESM4_ESM.doc (34 kb)
Appendix S2 (DOC 33 kb)


  1. AEMET. Agencia Estatal de Meteorologia. (Spain). (accessed 29 September 2012).
  2. Alameda D, Villar R (2009) Moderate soil compaction: Implications on growth and architecture in seedlings of 17 woody plant species. Soil Tillage Res 103:325–331CrossRefGoogle Scholar
  3. Alameda D, Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia seedlings under soil compaction conditions. Environ Exp Bot 79:49–57CrossRefGoogle Scholar
  4. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg E, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684CrossRefGoogle Scholar
  5. Antúnez I, Retamosa EC, Villar R (2001) Relative growth rate in phylogenetically related deciduous and evergreen woody species. Oecologia 128:172–180CrossRefGoogle Scholar
  6. Auclair AND (1993) Extreme climatic fluctuations as a cause of forest dieback in the Pacific rim. Water Air Soil Pollut 66:207–229Google Scholar
  7. Baburai N (2006) The physiological and genetic bases of water-use efficiency in winter wheat. PhD Thesis, Nottingham, University of Nottingham, UK.Google Scholar
  8. Bell DL, Sultan SE (1999) Dynamic phenotypic plasticity for root growth in Polygonum: a comparative study. Am J Bot 86:807–819PubMedCrossRefGoogle Scholar
  9. Bigler C, Braker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9:330–343CrossRefGoogle Scholar
  10. Blum A (2002) Drought tolerance is it a complex trait? In: Saxena NP, O’Toole JC (eds) Field screening for drought tolerance in crop plants with emphasis on rice. New York, ICRISAT and The Rockefeller Foundation, pp 17–22Google Scholar
  11. Boisvenue C, Running SW (2006) Impacts of climate change on natural forest productivity-evidence since the middle of the 20th century. Glob Chang Biol 12:862–882CrossRefGoogle Scholar
  12. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155CrossRefGoogle Scholar
  13. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long–term consequences. Ann For Sci 63:625–644CrossRefGoogle Scholar
  14. Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Buchmann N, Aubinet M, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend A, Friedlingstein P, Gobron N, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533PubMedCrossRefGoogle Scholar
  15. Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytol 182:919–928PubMedCrossRefGoogle Scholar
  16. Cortina J, Green JJ, Baddeley JA, Watson CA (2008) Root morphology and water transport of Pistacia lentiscus seedlings under contrasting water supply: a test of the pipe stem theory. Environ Exp Bot 62:343–350CrossRefGoogle Scholar
  17. Ebrahim NM (2008) Responses of root and shoot growth of durum wheat (Triticum turgidum) and barley (Hordeum vulgare) plants to different water and nitrogen levels. PhD Thesis, University of Jordan, Amman, JordanGoogle Scholar
  18. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  19. 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
  20. Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82PubMedCrossRefGoogle Scholar
  21. Finér L, Messier C, Grandpré L (1997) Fine-root dynamics in mixed boreal conifer broad-leafed forest stands at different successional stages after fire. Can J For Res 27:304–314CrossRefGoogle Scholar
  22. Fitter AH (1985) Functional significance of root morphology and root system architecture. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological Interactions in Soil. Blackwell Scientific Publications, Oxford, pp 87–106Google Scholar
  23. Fitter AH (1987) An architectural approach to the comparative ecology of plant root systems. New Phytol 106:61–77CrossRefGoogle Scholar
  24. Gregory PJ, Palta JA, Batts GR (1997) Root systems and root: mass ratio-carbon allocation under current and projected atmospheric conditions in arable crops. Plant Soil 187:221–228CrossRefGoogle Scholar
  25. Grime JP (1994) The role of plasticity in exploiting environmental heterogeneity. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York, pp 1–21CrossRefGoogle Scholar
  26. Grime JP, Mackey JML (2002) The role of plasticity in resource capture by plants. Evol Ecol 16:299–307CrossRefGoogle Scholar
  27. Grime JP, Crick JC, Rincon JC (1986) The ecological significance of plasticity. In: Trewavas AJ (ed) Plasticity in Plants. Cambridge University, Cambridge, pp 5–29Google Scholar
  28. Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a long leaf pine forest. Oecologia 140:450–457PubMedCrossRefGoogle Scholar
  29. Hamblin A, Tennant D, Perry MW (1990) The cost of stress–dry–matter partitioning changes with seasonal supply of water and nitrogen to dryland wheat. Plant Soil 122:47–58CrossRefGoogle Scholar
  30. Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architecture tradeoffs for water and phosphorus acquisition. Funct Plant Biol 32:737–748CrossRefGoogle Scholar
  31. Hoad SP, Russell G, Lucas ME, Bingham IJ (2001) The management of wheat, barley, and oat root systems. Adv Agron 74:193–246CrossRefGoogle Scholar
  32. Holl KD (1998) Effects of above- and below-ground competition of shrubs and grass on Calophyllum brasiliense (Camb.) seedling growth in abandoned tropical pasture. Forest Ecol Manag 109:187–195CrossRefGoogle Scholar
  33. Hoogenboom G, Huck MG, Peterson CM (1987) Root growth rate of soybean as affected by drought stress. Agron J 79:607–614CrossRefGoogle Scholar
  34. Huang B, Gao H (2000) Root physiological characteristics associated with drought resistance in tall fescue cultivars. Crop Sci 40:196–203CrossRefGoogle Scholar
  35. Jackson RB, Canadell J, Ehleringer JA, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411CrossRefGoogle Scholar
  36. Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci U S A 94:7362–7366PubMedPubMedCentralCrossRefGoogle Scholar
  37. Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535PubMedCrossRefGoogle Scholar
  38. King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398CrossRefGoogle Scholar
  39. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, San DiegoGoogle Scholar
  40. Larcher W (1995) Physiological plant ecology, 3rd edn. Springer, Berlin-Heidelberg, GermanyCrossRefGoogle Scholar
  41. Lauenroth WK, Sala OE, Milchunas DG, Lathrop RW (1987) Root dynamics of Bouteloua gracilis during short-term recovery from drought. Funct Ecol 1:117–124CrossRefGoogle Scholar
  42. Lehto T (1992) Effect of drought on Picea sitchensis seedlings inoculated with mycorrhizal fungi. Scand J For Res 7:177–182CrossRefGoogle Scholar
  43. Li FM, Liu XL, Li SQ (2001) Effects of early soil water distribution on the dry matter partition between roots and shoots of winter wheat. Agric Water Manag 49:163–171CrossRefGoogle Scholar
  44. Lloret F, Casanovas C, Peñuelas J (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216CrossRefGoogle Scholar
  45. Lloret F, Siscart D, Dalmases C (2004) Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain). Glob Chang Biol 10:2092–2099CrossRefGoogle Scholar
  46. López González GA (2001) Los árboles y arbustos de la Peninsula Iberica e Islas Baleares: especies silvestres y las principales cultivadas. Mundi-Prensa, MadridGoogle Scholar
  47. Markejstein L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade tolerance. J Ecol 97:311–325CrossRefGoogle Scholar
  48. Martínez F, Merino O, Martín A, García Martín D, Merino JA (1998) Belowground structure and production in a Mediterranean shrub community. Plant Soil 201:209–216CrossRefGoogle Scholar
  49. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831CrossRefGoogle Scholar
  50. Meier IC, Leuschner C (2007) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiol 28:297–309CrossRefGoogle Scholar
  51. Metcalfe DB, Meir P, Aragao L, da Costa ACL, Braga AP, Goncalves PHL, Silva JD, de Almeida SS, Dawson LA, Malhi Y, Williams M (2008) The effects of water availability on root growth and morphology in an Amazon rainforest. Plant Soil 311:189–199CrossRefGoogle Scholar
  52. Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root:shoot ratios in terrestrial biomes. Glob Chang Biol 11:1–13Google Scholar
  53. Nicotra AB, Babicka N, Westoby M (2002) Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130:136–145Google Scholar
  54. Niklas KJ, Enquist BJ (2002) Global allocation rules for patterns of biomass partitioning in seed plants. Science 295:1517–1520PubMedCrossRefGoogle Scholar
  55. Nuckolls AE, Wurzburger N, Ford CR, Hendrick RL, Vose JM, Dloeppel BD (2009) Hemlock declines rapidly with hemlock wooly adelgid infestation: impacts on the carbon cycle of southern appalachian forest. Ecosystems 12:179–190CrossRefGoogle Scholar
  56. Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442CrossRefGoogle Scholar
  57. Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495CrossRefGoogle Scholar
  58. Padilla FM, Miranda JD, Jorquera MJ, Pugnaire FI (2009) Variability in amount and frequency of water supply affects roots but not growth of arid shrubs. Plant Ecol 204:261–270CrossRefGoogle Scholar
  59. Palátová E (2002) Effect of increased nitrogen depositions and drought stress on the development of Scots pine (Pinus sylvestris) – II. Root system response. J Forensic Sci 48:237–247Google Scholar
  60. Passioura JB (1983) Roots and drought resistance. Agric Water Manag 7:265–280CrossRefGoogle Scholar
  61. Persson H, Fircks Y, Majdi H, Nilsson LO (1995) Root distribution in Norway spruce (Picea abies) stand subjected to drought and ammonium-sulphate application. Plant Soil 169:161–165CrossRefGoogle Scholar
  62. Phillips OL, Van Der Heijden G, Lewis SL, López-González G, Aragão LEOC, Lloyd J, Malhi Y et al (2010) Drought–mortality relationships for tropical forests. New Phytol 187(3):631–646PubMedCrossRefGoogle Scholar
  63. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50PubMedCrossRefGoogle Scholar
  64. Pregitzer KS, Burton AJ, King JS, Zak DR (2008) Soil respiration, root biomass, and root turnover following long-term exposure of northern forests to elevated atmospheric CO2 and tropospheric O3. New Phytol 180:153–161PubMedCrossRefGoogle Scholar
  65. Quero JL, Villar R, Marañon T, Zamora R (2006) Interactions of drought and shade effects on seedlings of four Quercus species: physiological and structural leaf responses. New Phytol 170:819–834PubMedCrossRefGoogle Scholar
  66. Quero JL, Sterck FJ, Villar R, Martínez-Vilalta J (2011) Water use strategies of six co-existing Mediterranean woody species during a summer drought. Oecologia 166:45–57PubMedCrossRefGoogle Scholar
  67. Ryser P (1998) Intra– and interspecific variation in root length, root turnover and the underlying parameters. In: Lambers H, Poorter H, van Vuuren MMI (eds) Variation in plant growth. Backhuys Publishers, Leiden, pp 441–465Google Scholar
  68. Ryser P (2006) The mysterious root length. Plant Soil 286:1–6CrossRefGoogle Scholar
  69. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) IPCC climate change 2007. In: The physical science basis. Cambridge University Press, CambridgeGoogle Scholar
  70. Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–359CrossRefGoogle Scholar
  71. Sponchiado B, White J, Castillo J, Jones P (1989) Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Exp Agric 25:249–257CrossRefGoogle Scholar
  72. Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542PubMedCrossRefGoogle Scholar
  73. Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Bot Neerl 44:363–383CrossRefGoogle Scholar
  74. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542PubMedCrossRefGoogle Scholar
  75. Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates Inc. Publishers, Sunderland, p 764Google Scholar
  76. Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol 167:493–508PubMedCrossRefGoogle Scholar
  77. Trubat R, Cortina J, Vilagrosa A (2006) Plant morphology and root hydraulics are altered by nutrient deficiency in Pistacia lentiscus. Trees 20:334–339CrossRefGoogle Scholar
  78. Valenzuela-Estrada LR, Vera-Caraballo V, Eissenstat DM (2008) Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). Am J Bot 95:1506–1514PubMedCrossRefGoogle Scholar
  79. Valladares F, Sánchez‐Gómez D (2006) Ecophysiological traits associated with drought in mediterranean tree seedlings: individual responses versus interspecific trends in eleven species. Plant Biol 8:688–697PubMedCrossRefGoogle Scholar
  80. Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  81. Villar R, Ruiz-Robleto J, De Jong Y, Poorter H (2006) Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant Cell Environ 29:1629–1643PubMedCrossRefGoogle Scholar
  82. Vogt KA, Publicover DA, Bloomfield J, Perez JM, Vogt DJ, Silver WL (1993) Belowground responses as indicators of environmental change. Environ Exp Bot 133:189–205CrossRefGoogle Scholar
  83. Wahl S, Ryser P (2000) Root tissue structure is linked to ecological strategies of grasses. New Phytol 148:459–471CrossRefGoogle Scholar
  84. Walther G-R, Post E, Convey P, Menzel A, Parmesank C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  85. White J, Castillo J (1989) Relative effect of root and shoot genotypes on yield of common bean under drought stress. Crop Sci 29:360–362CrossRefGoogle Scholar
  86. Wright IJ, Westoby M (1999) Differences in seedling growth behaviour among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. J Ecol 87:85–97CrossRefGoogle Scholar
  87. Wright GC, Nageswara RC, Farquhar GD (1994) Water-use efficiency and carbon isotope discrimination in peanut under water deficit conditions. Crop Sci 34:92–97CrossRefGoogle Scholar
  88. Zhu WQ, Wu LH, Tao QN (2002) Advances in the studies on crop root against drought stress. Soil Environ 11:430–433Google Scholar
  89. Zhu YH, Ren LL, Skaggs TH, Lu HS, Yu ZB, Wu Y, Fang X (2009) Simulation of Populus euphratica root uptake of groundwater in an arid woodland of the Ejina Basin, China. Hydrol Process 23:2460–2469CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Manuel Olmo
    • 1
  • Bárbara Lopez-Iglesias
    • 1
  • Rafael Villar
    • 1
  1. 1.Area de Ecología, Facultad de CienciasUniversidad de CórdobaCórdobaSpain

Personalised recommendations