Advertisement

Trees

, Volume 33, Issue 1, pp 293–303 | Cite as

Rooting big and deep rapidly: the ecological roots of pine species distribution in southern Europe

  • Enrique Andivia
  • Paolo Zuccarini
  • Beatriz Grau
  • Felicidad de Herralde
  • Pedro Villar-Salvador
  • Robert SavéEmail author
Original Article

Abstract

Key message

The rapid production of a large, deep root system during seedling establishment is critical for pines to colonize dry Mediterranean locations.

Abstract

Root properties can influence plant drought resistance, and consequently plant species distribution. Root structure strongly varies across biomes partly as a result of phylogeny. However, whether the spatial distribution of phylogenetically close plant species is linked to differences in root properties remains unclear. We examined whether root properties mediate the strong correlation between summer drought intensity and the spatial segregation of pine species native to southern Europe. For this, we compared the seedling root growth and structure of five ecologically distinct pine species grown in 360 L rhizotrons for 19 months under typical hot and dry Mediterranean conditions. We studied the mountain and boreo-alpine pines Pinus sylvestris and Pinus nigra, and the Mediterranean pines Pinus pinaster, Pinus pinea, and Pinus halepensis. Mediterranean pines formed deep roots faster than mountain pines, their shoots and roots grew faster and had higher root growth, especially P. halepensis, at low air temperature. By the end of the study, Mediterranean pines had larger root systems than mountain pines. Neither distribution of root mass with depth nor root-to-shoot mass ratio varied significantly among species. Across species, minimal annual rainfall to which species are exposed in their range related negatively to root growth but positively to specific root length and the time needed for roots to reach a depth of 40 cm. This study highlights the importance of root growth as a driver of pine distribution in southern Europe and suggests that rapidly producing a large, deep root system may be a key attribute for pines to colonize dry Mediterranean locations.

Keywords

Drought resistance Pinus Rhizotron Root growth Root structure Rooting depth Specific root length 

Notes

Acknowledgements

Research was supported by the projects Life MEDACC, AGL2011-24296 ECOLPIN (MICIIN), CGL2014-53308-P (SERAVI), Centres CERCA of Generalitat de Catalunya and the network REMEDINAL 3 (S2013/MAE-2719) of the CAM. EA was supported by postdoctoral grant “Ayudas para contratos para la formación postdoctoral” (FPDI-2013-15573) from the Spanish Government. We thank Laia Serra and Christian Morales for their technical assistance and Verónica Cruz-Alonso for figure preparation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2018_1777_MOESM1_ESM.docx (789 kb)
Supplementary material 1 (DOCX 789 KB)

References

  1. Alía Miranda R, García del Barrio JM, Iglesias Sauce S, Mancha Núñez JA de (2009) Miguel y del Ánge, l J. Nicolás Peragón JL, Pérez Martín F, Sánchez. In: de Ron D Regiones de procedencia de especies forestales españolas. Organismo Autónomo de Parques Nacionales, MadridGoogle Scholar
  2. Alsina MM, Smart DR, Bauerle T, De Herralde F, Biel C, Stockert C, Negron C, Save R (2011) Seasonal changes of whole root system conductance by a drought-tolerant grape root system. J Exp Bot 62:99–109.  https://doi.org/10.1093/jxb/erq247 CrossRefGoogle Scholar
  3. Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218CrossRefGoogle Scholar
  4. Barbero M, Loisel R, Quezel P, Richardson DM, Romane F, Barbéro M, Loisel P, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean Basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 153–170Google Scholar
  5. Blanco E, Casado MA, Costa M, Escribano R, García M, Génova M, Gómez A, Gómez F, Moreno JC, Morla C, Regato P, Sainz H (1998) Los bosques Ibéricos. Una interpretación geobotánica. Editorial Planeta S.A., BarcelonaGoogle Scholar
  6. Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc Natl Acad Sci USA 111:14489–14493.  https://doi.org/10.1073/pnas.1407930111 CrossRefGoogle Scholar
  7. Brum M, Teodoro GS, Abrahão A, Oliveira RS (2017) Coordination of rooting depth and leaf hydraulic traits defines drought-related strategies in the campos rupestres, a tropical montane biodiversity hotspot. Plant Soil.  https://doi.org/10.1007/s11104-017-3330-x Google Scholar
  8. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:1–16.  https://doi.org/10.3389/fpls.2015.00547 CrossRefGoogle Scholar
  9. Burdett AN (1990) Physiological processes in plantation establishment and the development of specifications for forest planting stock. Can J For Res 20:415–427CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, USA, p 488Google Scholar
  11. Calama R, Manso R, Lucas-Borja ME, Espelta JM, Piqué M, Bravo F, del Peso C, Pardos M (2017) Natural regeneration in iberian pines: a review of dynamic processes and proposals for management. For Syst 26:eR02SGoogle Scholar
  12. Canadell J, Jackson R, Ehleringer J, Mooney HA, Sala OE, Schulze E-D (1996) Maximum rooting depth of vegetation types at the global scale. Oecologia 108:583–595.  https://doi.org/10.1007/BF00329030 CrossRefGoogle Scholar
  13. Castro J (2006) Short delay in timing of emergence determines establishment success in Pinus sylvestris across microhabitats. Ann Bot 98:1233–1240.  https://doi.org/10.1093/aob/mcl208 CrossRefGoogle Scholar
  14. Castro J, Zamora R, Hodar JA, Gomez JM (2004) Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: consequences of being in a marginal Mediterranean habitat. J Ecol 92:266–277.  https://doi.org/10.1111/j.0022-0477.2004.00870.x CrossRefGoogle Scholar
  15. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  16. Christensen JH, Christensen OB (2007) A summary of the PRUDENCE model projections of changes in European climate by the end of this century. Clim Change 81:7–30CrossRefGoogle Scholar
  17. Climent J, Costa e Silva F, Chambel MR, Pardos M, Almeida MH (2009) Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Ann For Sci 66:407–407.  https://doi.org/10.1051/forest/2009016 CrossRefGoogle Scholar
  18. Climent J, San-Martín R, Chambel MR, Mutke S (2011) Ontogenetic differentiation between Mediterranean and Eurasian pines (sect. Pinus) at the seedling stage. Trees Struct Funct 25:175–186.  https://doi.org/10.1007/s00468-010-0496-8 CrossRefGoogle Scholar
  19. Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum tree species rate among 11 mature temperate. Funct Ecol 18:388–397CrossRefGoogle Scholar
  20. Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling DJ (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. Int J Plant Sci 173:584–595.  https://doi.org/10.1086/665823 CrossRefGoogle Scholar
  21. Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442.  https://doi.org/10.3389/fpls.2013.00442 CrossRefGoogle Scholar
  22. Cuesta B, Villar-Salvador P, Puértolas J, Jacobs DF, Rey Benayas JM (2010) Why do large, nitrogen rich seedlings better resist stressful transplanting conditions? A physiological analysis in two functionally contrasting Mediterranean forest species. For Ecol Manag 260:71–78.  https://doi.org/10.1016/j.foreco.2010.04.002 CrossRefGoogle Scholar
  23. De Micco V, Aronne G (2012) Morpho-anatomical traits for plant adapatation to drought. In: Aroca R (ed) Plant responses to drought stress: from morphological to molecular features. Springer, Berlin HeidelbergGoogle Scholar
  24. De Luis M, Verdú M, Raventós J (2008) Early to rise makes a plant healthy, wealthy, and wise. Ecology 89:3061–3071CrossRefGoogle Scholar
  25. De Herralde F, Savé R, Aranda X, Biel C (2010) Grapevine roots and soil environment: growth, distribution and function. In: Methodologies and results in grapevine research. Springer, Dordrecht, pp 1–20Google Scholar
  26. de la Riva EG, Tosto A, Pérez-Ramos IM, Navarro-Fernández CM, Olmo M, Anten NPR, Marañón T, Villar R (2016) A plant economics spectrum in Mediterranean forests along environmental gradients: Is there coordination among leaf, stem and root traits? J Veg Sci 27:187–199.  https://doi.org/10.1111/jvs.12341 CrossRefGoogle Scholar
  27. de la Riva EG, Marañón T, Pérez-Ramos IM, Olmo M, Villar R (2017) Plant and soil root traits across environmental gradients in Mediterranean woody communities: are they aligned along a single acquisition-conservation axis ? Plant Soil.  https://doi.org/10.1007/s11104-017-3433-4 (in press) Google Scholar
  28. Fernández L, Villar-Salvador P, Martínez-Vilalta J, Toca AO, Zavala MA (2018) Distribution of pines in Europe agrees with seedling differences in foliage frost tolerance, not with xylem embolism vulnerability. Tree Physiol 38:507–516CrossRefGoogle Scholar
  29. Freschet GT, Valverde-Barrantes OJ, Tucker CM, Craine JM, McCormack ML, Violle C, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM, Bonis A, Comas LH, Cornelissen JHC, Dong M, Guo D, Hobbie SE, Holdaway RJ, Kembel SW, Makita N, Onipchenko VG, Picon-Cochard C, Reich PB, de la Riva EG, Smith SW, Soudzilovskaia NA, Tjoelker MG, Wardle DA, Roumet C (2017) Climate, soil and plant functional types as drivers of global fine-root trait variation. J Ecol 105:1182–1196.  https://doi.org/10.1111/1365-2745.12769 CrossRefGoogle Scholar
  30. Gonzalo J (2008) Diagnosis fitoclimática de la España peninsular. Actualización y análisis geoestadístico aplicado. Universidad Politécnica de Madrid, MadridGoogle Scholar
  31. Grossnickle SC (2005) Importance of root growth in overcoming planting stress. New For 30:273–294.  https://doi.org/10.1007/s11056-004-8303-2 CrossRefGoogle Scholar
  32. Grossnickle SC (2012) Why seedlings survive: influence of plant attributes. New For 43:711–738CrossRefGoogle Scholar
  33. He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol 194:751–759.  https://doi.org/10.1111/j.1469-8137.2012.04079.x CrossRefGoogle Scholar
  34. Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2010) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207:233–244.  https://doi.org/10.1007/s11258-009-9668-2 CrossRefGoogle Scholar
  35. Holmgren M, López BC, Gutiérrez JR, Squeo FA (2006) Herbivory and plant growth rate determine the success of El Niño Southern Oscillation-driven tree establishment in semiarid South America. Glob Change Biol 12:2263–2271.  https://doi.org/10.1111/j.1365-2486.2006.01261.x CrossRefGoogle Scholar
  36. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411.  https://doi.org/10.1007/BF00333714 CrossRefGoogle Scholar
  37. Körner CH, Renhardt U (1987) Dry matter partitioning and root length/leaf area ratios in herbaceous perennial plants with diverse altitudinal distribution. Oecologia 74:411–418CrossRefGoogle Scholar
  38. Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310.  https://doi.org/10.1111/1365-2745.12562 CrossRefGoogle Scholar
  39. Levitt J (1980) Responses of plants to environmental stresses. Volume II. Water, radiation, salt, and other stresses, 2nd edn. Academic Press, New YorkGoogle Scholar
  40. Lyr H (1996) Effect of the root temperature on growth parameters of various European tree species. In: Annales des sciences forestières. EDP Sciences, pp 317–323Google Scholar
  41. Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol 97:311–325.  https://doi.org/10.1111/j.1365-2745.2008.01466.x CrossRefGoogle Scholar
  42. Matías L, González-Díaz P, Jump AS (2014) Larger investment in roots in southern range-edge populations of Scots pine is associated with increased growth and seedling resistance to extreme drought in response to simulated climate change. Environ Exp Bot 105:32–38CrossRefGoogle Scholar
  43. Matías L, Castro J, Villar-Salvador P, Quero JL, Jump AS (2017) Differential impact of hotter drought on seedling performance of five ecologically distinct pine species. Plant Ecol 218:201–212.  https://doi.org/10.1007/s11258-016-0677-7 CrossRefGoogle Scholar
  44. Mitrakos K (1980) A theory for Mediterranean plant life. Acta Oecol Oecol Plant 1:245–252Google Scholar
  45. Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root: shoot ratios in terrestrial biomes. Glob Change Biol 12:84–96.  https://doi.org/10.1111/j.1365-2486.2005.001043.x CrossRefGoogle Scholar
  46. 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 141:426–442.  https://doi.org/10.1080/11263500701626069 CrossRefGoogle Scholar
  47. Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495CrossRefGoogle Scholar
  48. Poorter H, Bühler J, Van Dusschoten D, Climent J, Postma J (2012a) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850.  https://doi.org/10.1071/FP12049 CrossRefGoogle Scholar
  49. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012b) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50.  https://doi.org/10.1111/j.1469-8137.2011.03952.x CrossRefGoogle Scholar
  50. Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115CrossRefGoogle Scholar
  51. Pulido F, García E, Obrador JJ, Moreno G (2010) Multiple pathways for tree regeneration in anthropogenic savannas: incorporating biotic and abiotic drivers into management schemes. J Appl Ecol 47:1272–1281.  https://doi.org/10.1111/j.1365-2664.2010.01865.x CrossRefGoogle Scholar
  52. Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Buschena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Funct Ecol 12:327–338CrossRefGoogle Scholar
  53. Richter S, Kipfer T, Wohlgemuth T, Guerrero CC, Ghazoul J, Moser B (2012) Phenotypic plasticity facilitates resistance to climate change in a highly variable environment. Oecologia 169:269–279CrossRefGoogle Scholar
  54. Ruiz-Benito P, Gómez-Aparicio L, Zavala MA (2012) Large-scale assessment of regeneration and diversity in Mediterranean planted pine forests along ecological gradients. Divers Distrib 18:1092–1106.  https://doi.org/10.1111/j.1472-4642.2012.00901.x CrossRefGoogle Scholar
  55. Salazar-Tortosa D, Castro J, De Casas RR, Viñegla B, Sánchez-Cañete EP, Villar-Salvador PP (2018a) Gas exchange at whole plant level shows that a less conservative water use is linked to a higher performance in three ecologically distinct pine species. Environ Res Lett 13:045004CrossRefGoogle Scholar
  56. Salazar-Tortosa D, Castro J, Villar-Salvador P, Viñegla B, Matías L, Michelsen A, Rubio de Casas R, Querejeta JI (2018b) The “isohydric trap”: a proposed feedback between water shortage, stomatal regulation, and nutrient acquisition drives differential growth and survival of European pines under climatic dryness. Glob Change Biol 24:4069–4083CrossRefGoogle Scholar
  57. Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads and belowground aboveground allometries of plants in water limited ecosystems. J Ecol.  https://doi.org/10.1046/j.1365-2745.2002.00682.x Google Scholar
  58. Schulze ED, Mooney HA, Sala OE, Jobbagy E, Buchmann N, Bauer G, Canadell J, Jackson RB, Loreti J, Oesterheld M, Ehleringer JR (1996) Rooting depth, water availability, and vegetation cover along an aridity gradient in Patagonia. Oecologia 108:503–511CrossRefGoogle Scholar
  59. Stella JC, Battles JJ (2010) How do riparian woody seedlings survive seasonal drought? Oecologia 164:579–590.  https://doi.org/10.1007/s00442-010-1657-6 CrossRefGoogle Scholar
  60. Tíscar PA, Linares JC (2011) Structure and regeneration patterns of Pinus nigra subsp. Salzmannii natural forests: a basic knowledge for adaptive management in a changing climate. Forests 2:1013–1030.  https://doi.org/10.3390/f2041013 CrossRefGoogle Scholar
  61. Toca AO, Oliet JA, Villar-Salvador P, Maroto J, Jacobs DF (2018) Species ecology determines the role of nitrogen nutrition on the frost tolerance of pine seedlings. Tree Physiol 38:96–108CrossRefGoogle Scholar
  62. Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: The influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215:1562–1573CrossRefGoogle Scholar
  63. Vicente-Serrano SM, Gouveia C, Camarero JJ, Begueria S, Trigo R, Lopez-Moreno JI, Azorin-Molina C, Pasho E, Lorenzo-Lacruz J, Revuelto J, Moran-Tejeda E, Sanchez-Lorenzo A (2013) Response of vegetation to drought time-scales across global land biomes. Proc Natl Acad Sci 110:52–57.  https://doi.org/10.1073/pnas.1207068110 CrossRefGoogle Scholar
  64. Villar-Salvador P, Puértolas J, Cuesta B, Peñuelas JL, Uscola M, Heredia-Guerrero N, Rey Benayas JM (2012) Increase in size and nitrogen concentration enhances seedling survival in Mediterranean plantations. Insights from an ecophysiological conceptual model of plant survival. New For 43:755–770.  https://doi.org/10.1007/s11056-012-9328-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Forest Ecology and Restoration Group, Departmento de Ciencias de la VidaUniversidad de AlcaláMadridSpain
  2. 2.Plant Science AreaIRTA-Institut de Recerca i Tecnologia AgroalimentariesBarcelonaSpain
  3. 3.CREAFCampus de Bellaterra, Universitat Autònoma de BarcelonaBarcelonaSpain

Personalised recommendations