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Oecologia

, Volume 169, Issue 2, pp 565–577 | Cite as

Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought

  • Jean-Marc LimousinEmail author
  • Serge Rambal
  • Jean-Marc Ourcival
  • Jesus Rodríguez-Calcerrada
  • Ignacio M. Pérez-Ramos
  • Raquel Rodríguez-Cortina
  • Laurent Misson
  • Richard Joffre
Global change ecology - Original research

Abstract

Mediterranean trees must adjust their canopy leaf area to the unpredictable timing and severity of summer drought. The impact of increased drought on the canopy dynamics of the evergreen Quercus ilex was studied by measuring shoot growth, leaf production, litterfall, leafing phenology and leaf demography in a mature forest stand submitted to partial throughfall exclusion for 7 years. The leaf area index rapidly declined in the throughfall-exclusion plot and was 19% lower than in the control plot after 7 years of treatment. Consequently, leaf litterfall was significantly lower in the dry treatment. Such a decline in leaf area occurred through a change in branch allometry with a decreased number of ramifications produced and a reduction of the leaf area supported per unit sapwood area of the shoot (LA/SA). The leafing phenology was slightly delayed and the median leaf life span was slightly longer in the dry treatment. The canopy dynamics in both treatments were driven by water availability with a 1-year lag: leaf shedding and production were reduced following dry years; in contrast, leaf turnover was increased following wet years. The drought-induced decrease in leaf area, resulting from both plasticity in shoot development and slower leaf turnover, appeared to be a hydraulic adjustment to limit canopy transpiration and maintain leaf-specific hydraulic conductivity under drier conditions.

Keywords

Allometry Leaf area Leaf demography Litterfall Shoot growth 

Notes

Acknowledgments

This work was initiated within the framework of the UE project MIND (EVK2-CT-2002-000158). Additional support was provided by the French Research Agency (ANR) through the DROUGHT + project (ANR-06-VULN-003-01) and by the UE project Carbo-Extreme (FP7-ENV-2008-1-226701). The authors are grateful to Christian Collin and David Degueldre for their help with the installation of field experiments and to Prof. João Pereira, the editors and the anonymous reviewers for constructive comments on the manuscript.

References

  1. Allard V, Ourcival JM, Rambal S, Joffre R, Rocheteau A (2008) Seasonal and annual variation of carbon exchange in an evergreen Mediterranean forest in southern France. Glob Change Biol 14:714–725CrossRefGoogle Scholar
  2. Baldocchi DD, Xu L (2007) What limits evaporation from Mediterranean oak woodlands - The supply of moisture in the soil, physiological control by plants or the demand by the atmosphere? Adv Water Resour 30:2113–2122CrossRefGoogle Scholar
  3. Brando PM, Nepstad DC, Davidson EA, Trumbore SE, Ray D, Camargo P (2008) Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philos Trans R Soc Lond B 363:1839–1848CrossRefGoogle Scholar
  4. Bussotti F, Borghini F, Celesti C, Leonzio C, Cozzi A, Bettini D, Ferretti M (2003) Leaf shedding, crown condition and element return in two mixed holm oak forests in Tuscany, central Italy. For Ecol Manag 176:273–285CrossRefGoogle Scholar
  5. Campbell GS (1974) A simple method for determining unsaturated conductivity from moisture retention data. Soil Sci 117:311–314CrossRefGoogle Scholar
  6. Castro-Diez P, Montserrat-Marti G (1998) Phenological pattern of fifteen Mediterranean phanaerophytes from Quercus ilex communities of NE-Spain. Plant Ecol 139:103–112CrossRefGoogle Scholar
  7. Castro-Diez P, Villar-Salvador P, Pérez-Rontomé C, Maestro-Martinez M, Montserrat-Marti G (1997) Leaf morphology and leaf chemical composition in three Quercus (Fagaceae) species along a rainfall gradient in NE Spain. Trees 11:127–134Google Scholar
  8. Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259CrossRefGoogle Scholar
  9. Cherbuy B, Joffre R, Gillon D, Rambal S (2001) Internal remobilization of carbohydrates, lipids, nitrogen and phosphorus in the Mediterranean evergreen oak Quercus ilex. Tree Physiol 21:9–17PubMedCrossRefGoogle Scholar
  10. Cline MG (1997) Concepts and terminology of apical dominance. Am J Bot 84:1064–1069PubMedCrossRefGoogle Scholar
  11. Cochard H, Peiffer M, Le Gall K, Granier A (1997) Developmental control of xylem hydraulic resistances and vulnerability to embolism in Fraxinus excelsior L.: impacts on water relations. J Exp Bot 48:655–663CrossRefGoogle Scholar
  12. Cochard H, Coste S, Chanson B, Guehl JM, Nicolini E (2005) Hydraulic architecture correlates with bud organogenesis and primary shoot growth in beech (Fagus sylvatica). Tree Physiol 25:1545–1552PubMedCrossRefGoogle Scholar
  13. Dale JE (1988) The control of leaf expansion. Annu Rev Plant Physiol Plant Mol Biol 39:267–295CrossRefGoogle Scholar
  14. de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82PubMedCrossRefGoogle Scholar
  15. Eagleson PS (1982) Ecological optimality in water-limited natural soil-vegetation systems. 1. Theory and hypothesis. Water Resour Res 18:325–340CrossRefGoogle Scholar
  16. Fisher RA, Williams M, Lola da Costa A, Malhi Y, da Costa RF, Almeida S, Meir P (2007) The response of an Eastern Amazonian rain forest to drought stress: results and modelling analyses from a throughfall exclusion experiment. Glob Change Biol 13:2361–2378CrossRefGoogle Scholar
  17. Fontaine F, Chaar H, Colin F, Clement C, Burrus M, Druelle JL (1999) Preformation and neoformation of growth units on 3-year-old seedlings of Quercus petraea. Can J Bot 77:1623–1631CrossRefGoogle Scholar
  18. Gao XJ, Giorgi F (2008) Increased aridity in the Mediterranean region under greenhouse gas forcing estimated from high resolution simulations with a regional climate model. Glob Planet Change 62:195–209CrossRefGoogle Scholar
  19. Gao XJ, Pal JS, Giorgi F (2006) Projected changes in mean and extreme precipitation over the Mediterranean region from a high resolution double nested RCM simulation. Geophys Res Lett 33:L03706. doi: 10.1029/2005GL024954 CrossRefGoogle Scholar
  20. Gholz HL (1982) Environmental limits on aboveground net primary production, leaf area, and biomass in vegetation zones of the Pacific Northwest. Ecology 63:469–481CrossRefGoogle Scholar
  21. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63:90–104CrossRefGoogle Scholar
  22. Gratani L (1996) Leaf and shoot growth dynamics of Quercus ilex L. Acta Oecol 17:17–27Google Scholar
  23. Grier CC, Running SW (1977) Leaf area of mature coniferous forests: relation to site water balance. Ecology 58:893–899CrossRefGoogle Scholar
  24. Hättenschwiler S, Miglietta F, Raschi A, Körner C (1997) Morphological adjustments of mature Quercus ilex trees to elevated CO2. Acta Oecol 18:361–365CrossRefGoogle Scholar
  25. Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Ann Bot 95:521–533PubMedCrossRefGoogle Scholar
  26. Hoff C, Rambal S (2003) An examination of the interaction between climate, soil and leaf area index in a Quercus ilex ecosystem. Ann For Sci 60:153–161CrossRefGoogle Scholar
  27. Hsiao TC, Xu LK (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. J Exp Bot 51:1595–1616PubMedCrossRefGoogle Scholar
  28. Jasienski M, Bazzaz FA (1999) The fallacy of ratios and the testability of models in biology. Oikos 84:321–326CrossRefGoogle Scholar
  29. Joffre R, Rambal S (1993) How tree cover influences the water balance of Mediterranean rangelands. Ecology 74:570–582CrossRefGoogle Scholar
  30. Kikuzawa K (1991) A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Am Nat 138:1250–1263CrossRefGoogle Scholar
  31. Koch WG, Sillet SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854PubMedCrossRefGoogle Scholar
  32. Limousin JM, Rambal S, Ourcival JM, Joffre R (2008) Modelling rainfall interception in a Mediterranean Quercus ilex ecosystem: lesson from a throughfall exclusion experiment. J Hydrol 357:57–66CrossRefGoogle Scholar
  33. Limousin JM, Rambal S, Ourcival JM, Rocheteau A, Joffre R, Rodríguez-Cortina R (2009) Long-term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest. Glob Change Biol 15:2163–2175CrossRefGoogle Scholar
  34. Limousin JM, Longepierre D, Huc R, Rambal S (2010a) Change in hydraulic traits of Mediterranean Quercus ilex submitted to long-term throughfall exclusion. Tree Physiol 30:1026–1036PubMedCrossRefGoogle Scholar
  35. Limousin JM, Misson L, Lavoir AV, Martin NK, Rambal S (2010b) Do photosynthetic limitations of evergreen Quercus ilex leaves change with long-term increased drought severity? Plant Cell Environ 33:863–875PubMedGoogle Scholar
  36. Lockhart JA (1967) Physical nature of irreversible deformation of plant cells. Plant Physiol 42:1545–1552PubMedCrossRefGoogle Scholar
  37. Martinez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R (2009) Hydraulic adjustment of Scots pine across Europe. New Phytol 184:353–364PubMedCrossRefGoogle Scholar
  38. Mediavilla S, Escudero A (2003) Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytol 159:203–211CrossRefGoogle Scholar
  39. Milla R, Palacio S, Maestro-Martinez M, Montserrat-Marti G (2007) Leaf exchange in a Mediterranean shrub: water, nutrient, non-structural carbohydrate and osmolyte dynamics. Tree Physiol 27:951–960PubMedCrossRefGoogle Scholar
  40. Misson L, Rocheteau A, Rambal S, Ourcival JM, Limousin JM, Rodríguez-Cortina R (2010) Functional changes in the controls of carbon fluxes after 3 years of increased drought in a Mediterranean evergreen forest? Glob Change Biol 16:2461–2575Google Scholar
  41. Misson L, Degueldre D, Collin C, Rodríguez-Cortina R, Rocheteau A, Ourcival JM, Rambal S (2011) Phenological responses to extreme droughts in a Mediterranean forest. Glob Change Biol 17:1036–1048CrossRefGoogle Scholar
  42. Montserrat-Marti G, Camarero JJ, Palacio S, Pérez-Rontomé C, Milla R, Albuixech J, Maestro M (2009) Summer-drought constrains the phenology and growth of two coexisting Mediterranean oaks with contrasting leaf habit: implications for their persistence and reproduction. Trees 23:787–799CrossRefGoogle Scholar
  43. Myers BJ (1988) Water stress integral—a link between short-term stress and long-term growth. Tree Physiol 4:315–323PubMedGoogle Scholar
  44. Nardini A (2002) Relations between efficiency of water transport and duration of leaf growth in some deciduous and evergreen trees. Trees 16:417–422CrossRefGoogle Scholar
  45. Niinemets U, Cescatti A, Rodeghiero M, Tosens T (2005) Leaf internal diffusion limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant Cell Environ 28:1552–1566CrossRefGoogle Scholar
  46. Ogaya R, Peñuelas J (2006) Contrasting foliar responses to drought in Quercus ilex and Phillyrea latifolia. Biol Plant 50:373–382CrossRefGoogle Scholar
  47. Pearson M, Mansfield TA (1994) Effects of exposure to ozone and water stress on the following season’s growth of beech (Fagus sylvatica L.). New Phytol 126:511–515CrossRefGoogle Scholar
  48. Peñuelas J, Filella I, Zhang X, Llorens L, Ogaya R, Lloret F, Comas P, Estiarte M, Terradas J (2004) Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol 161:837–846CrossRefGoogle Scholar
  49. Pereira JS, Chaves MM (1993) Plant water deficits in Mediterranean ecosystems. In: Smith JAC, Griffiths H (eds) Water deficits: plant responses from cell to community. Bios Scientific Publishers, Oxford, pp 235–251Google Scholar
  50. Pérez-Ramos IM, Ourcival JM, Limousin JM, Rambal S (2010) Mast seeding under increasing drought: results from a long-term dataset and from a rainfall exclusion experiment. Ecology 91:3057–3068PubMedCrossRefGoogle Scholar
  51. Poole DK, Miller PC (1981) The distribution of plant water stress and vegetation characteristics in Southern California chaparral. Am Midl Nat 105:32–43CrossRefGoogle Scholar
  52. Preston KA, Ackerly DD (2003) Hydraulic architecture and the evolution of shoot allometry in contrasting climates. Am J Bot 90:1502–1512PubMedCrossRefGoogle Scholar
  53. Rambal S (1993) The differential role of mechanisms for drought resistance in a Mediterranean evergreen shrub: a simulation approach. Plant Cell Environ 16:35–44CrossRefGoogle Scholar
  54. Rambal S, Ourcival JM, Joffre R, Mouillot F, Nouvellon Y, Reichstein M, Rocheteau A (2003) Drought controls over conductance and assimilation of a Mediterranean evergreen ecosytem: scaling from leaf to canopy. Glob Change Biol 9:1813–1824CrossRefGoogle Scholar
  55. Rapp M (1969) Production de litière et apport au sol d’éléments minéraux dans deux écosystèmes méditerranéens: la forêt de Quercus ilex L. et la garrigue de Quercus coccifera L. Oecol Plant 4:377–410Google Scholar
  56. Reich PB, Borchert R (1984) Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J Ecol 72:61–74CrossRefGoogle Scholar
  57. Ripullone F, Borghetti M, Raddi S, Vicinelli E, Baraldi R, Guerrieri MR, Nolè A, Magnani F (2009) Physiological and structural changes in response to altered precipitation regimes in a Mediterranean macchia ecosystem. Trees 23:823–834CrossRefGoogle Scholar
  58. Rodríguez-Calcerrada J, Pérez-Ramos IM, Ourcival JM, Limousin JM, Joffre R, Rambal S (2011) Is selective thinning an adequate practice for adapting Quercus ilex coppices to climate change? Ann For Sci 68:575–585CrossRefGoogle Scholar
  59. Sanz-Pérez V, Castro-Diez P (2010) Summer water stress and shade alter bud size and budburst date in three Mediterranean Quercus species. Trees 24:89–97CrossRefGoogle Scholar
  60. Sheffield J, Wood EF (2008) Projected changes in drought occurence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations. Clim Dyn 31:79–105CrossRefGoogle Scholar
  61. Somot S, Sevault F, Deque M, Crepon M (2008) 21st century climate change scenario for the Mediterranean using a couple atmosphere-ocean regional climate model. Glob Planet Change 63:112–126CrossRefGoogle Scholar
  62. Specht RL (1972) Water use by perennial evergreen plant communities in Australia and Papua New Guinea. Aust J Bot 20:273–299CrossRefGoogle Scholar
  63. Tyree MT, Alexander JD (1993) Hydraulic conductivity of branch junctions in three temperate tree species. Trees 7:156–159CrossRefGoogle Scholar
  64. Tyree MT, Ewers FW (1991) Tansley Review No. 34. The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360CrossRefGoogle Scholar
  65. Villar-Salvador P, Castro-Diez P, Pérez-Rontomé C, Montserrat-Marti G (1997) Stem xylem features in three Quercus (Fagaceae) species along a climatic gradient in NE Spain. Trees 12:90–96Google Scholar
  66. Warton DI, Weber NC (2002) Common slope tests for bivariate structural relationships. Biometrical J 44:161–174CrossRefGoogle Scholar
  67. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291PubMedCrossRefGoogle Scholar
  68. Williams RJ, Myers BA, Muller WJ, Duff GA, Eamus D (1997) Leaf phenology of woody species in a North Australian tropical savanna. Ecology 78:2542–2558CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jean-Marc Limousin
    • 1
    • 2
    Email author
  • Serge Rambal
    • 1
  • Jean-Marc Ourcival
    • 1
  • Jesus Rodríguez-Calcerrada
    • 1
  • Ignacio M. Pérez-Ramos
    • 3
  • Raquel Rodríguez-Cortina
    • 1
  • Laurent Misson
    • 1
  • Richard Joffre
    • 1
  1. 1.Centre d’Ecologie Fonctionnelle et Evolutive CEFE CNRSMontpellier Cedex 5France
  2. 2.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  3. 3.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS, CSIC)SevilleSpain

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