Skip to main content

Advertisement

Log in

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

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Data availability

The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • 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, Madrid

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218

    Article  Google Scholar 

  • 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 153–170

    Google Scholar 

  • 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., Barcelona

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Burdett AN (1990) Physiological processes in plantation establishment and the development of specifications for forest planting stock. Can J For Res 20:415–427

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, USA, p 488

    Google Scholar 

  • 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:eR02S

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • 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 81:7–30

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum tree species rate among 11 mature temperate. Funct Ecol 18:388–397

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 Heidelberg

    Google Scholar 

  • De Luis M, Verdú M, Raventós J (2008) Early to rise makes a plant healthy, wealthy, and wise. Ecology 89:3061–3071

    Article  Google Scholar 

  • 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 1–20

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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 38:507–516

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gonzalo J (2008) Diagnosis fitoclimática de la España peninsular. Actualización y análisis geoestadístico aplicado. Universidad Politécnica de Madrid, Madrid

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Grossnickle SC (2012) Why seedlings survive: influence of plant attributes. New For 43:711–738

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Körner CH, Renhardt U (1987) Dry matter partitioning and root length/leaf area ratios in herbaceous perennial plants with diverse altitudinal distribution. Oecologia 74:411–418

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Volume II. Water, radiation, salt, and other stresses, 2nd edn. Academic Press, New York

    Google Scholar 

  • Lyr H (1996) Effect of the root temperature on growth parameters of various European tree species. In: Annales des sciences forestières. EDP Sciences, pp 317–323

  • 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

    Article  Google Scholar 

  • 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 105:32–38

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mitrakos K (1980) A theory for Mediterranean plant life. Acta Oecol Oecol Plant 1:245–252

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 12:327–338

    Article  Google Scholar 

  • 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 169:269–279

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 13:045004

    Article  CAS  Google Scholar 

  • 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 24:4069–4083

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 108:503–511

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 38:96–108

    Article  CAS  PubMed  Google Scholar 

  • 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 215:1562–1573

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert Savé.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Nardini.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 789 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andivia, E., Zuccarini, P., Grau, B. et al. Rooting big and deep rapidly: the ecological roots of pine species distribution in southern Europe. Trees 33, 293–303 (2019). https://doi.org/10.1007/s00468-018-1777-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-018-1777-x

Keywords

Profiles

  1. Enrique Andivia