European Journal of Forest Research

, Volume 132, Issue 2, pp 325–333 | Cite as

How nutrient availability influences acclimation to shade of two (pioneer and late-successional) Mediterranean tree species?

  • Yogan Monnier
  • Anne Bousquet-Mélou
  • Bruno Vila
  • Bernard Prévosto
  • Catherine Fernandez
Original Paper

Abstract

Examining ecological limits to shade acclimation at whole-plant level is determinant for evaluating the success of sapling establishment in low-light environments. We studied nutritional effects on whole-plant development in response to shade in two Mediterranean forest tree species with different successional status: the early-successional Pinus halepensis Mill. and the late-successional Quercus pubescens Wild. Through a nursery-based factorial experimental design approach, we measured height increment along 2 years and final leaf, stem and root biomass in both species saplings subjected to two lights and two soil nutrient availability treatments. The shade avoidance response was exclusive to P. halepensis, appeared as timely dependent, and persisted longer in saplings exposed to higher nutrient availability. Q. pubescens benefited from the higher nutrient availability by lowering the light-driven plastic response in aerial support investment and belowground carbon allocation, whereas P. halepensis heightened its light-driven plastic response. These contrasted responses are thus clearly related to the shade acclimation strategy of each species: the shade-intolerant P. halepensis enhances shade avoidance when non-nutrient-limited, whereas the shade-tolerant Q. pubescens assumes a conservative strategy by limiting phenotypic plasticity-induced costs. Maintaining greater shade avoidance in non-nutrient-limited soil conditions might be an adaptive advantage for P. halepensis seedlings growing in the understory, in response to gap formation in the overstory. In contrast, the more conservative and less costly shade responsiveness of Q. pubescens may confer it a better adaptive advantage in long-term light-limited environments.

Keywords

Pinus halepensis Quercus pubescens Phenotypic plasticity Biomass partitioning Allocation Forest regeneration 

Supplementary material

10342_2012_677_MOESM1_ESM.pdf (12 kb)
ESM_1: Summary of biomass data. Supplementary material 1 (PDF 12 kb)

References

  1. Aphalo PJ, Lehto T (1997) Effects of light quality on growth and N accumulation in birch seedlings. Tree Physiol 17:125–132PubMedCrossRefGoogle Scholar
  2. Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond Ser B 277:503–511CrossRefGoogle Scholar
  3. Barbero M, Bonin G, Loisel R, Quézel P (1990) Changes and disturbances of forest ecosystems caused by human activities in the western part of the Mediterranean basin. Vegetatio 87:151–173CrossRefGoogle Scholar
  4. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155CrossRefGoogle Scholar
  5. Burton PJ, Bazzaz FA (1995) Ecophysiological responses of tree seedlings invading different patches of old-field vegetation. J Ecol 83:99–112CrossRefGoogle Scholar
  6. Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128CrossRefGoogle Scholar
  7. Causin HF, Wulff RD (2003) Changes in the responses to light quality during ontogeny in Chenopodium album. Can J Bot 81:152CrossRefGoogle Scholar
  8. Delagrange S, Messier C, Lechowicz MJ, Dizengremel P (2004) Physiological, morphological, and allocational plasticity in understory deciduous trees: importance of individual size and light availability. Tree Physiol 24:775–784PubMedCrossRefGoogle Scholar
  9. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81PubMedCrossRefGoogle Scholar
  10. Franklin KA (2008) Shade avoidance. New Phytol 179:930–944PubMedCrossRefGoogle Scholar
  11. Gasque M, García-Fayos P (2004) Interaction between Stipa tenacissima and Pinus halepensis: consequences for reforestation and the dynamics of grass steppes in semi-arid Mediterranean areas. For Ecol Manag 189:251–261CrossRefGoogle Scholar
  12. Gedroc JJ, McConnaughay KDM, Coleman JS (1996) Plasticity in root/shoot partitioning: optimal, ontogenetic, or both? Funct Ecol 10:44–50CrossRefGoogle Scholar
  13. Grassi G, Minotta G (2000) Influence of nutrient supply on shade–sun acclimation of Picea abies seedlings: effects on foliar morphology, photosynthetic performance and growth. Tree Physiol 20:645–652PubMedCrossRefGoogle Scholar
  14. Greenwood MS, Day ME, Berlyn GP (2009) Regulation of foliar plasticity in conifers: developmental and environmental factors. J Sustain For 28:48–62CrossRefGoogle Scholar
  15. Grime JP (1979) Plant strategies and vegetation processes. Wiley, ChichesterGoogle Scholar
  16. Henry HAL, Aarssen LW (1997) On the relationship between shade tolerance and shade avoidance strategies in woodland plants. Oikos 80:575–582CrossRefGoogle Scholar
  17. Henry HAL, Aarssen LW (2001) Inter- and intraspecific relationships between shade tolerance and shade avoidance in temperate trees. Oikos 93:477–487CrossRefGoogle Scholar
  18. King DA (1990) The adaptive significance of tree height. Am Nat 135:809–828CrossRefGoogle Scholar
  19. Lortie CJ, Aarssen LW (1996) The specialization hypothesis for phenotypic plasticity in plants. Int J Plant Sci 157:484–487CrossRefGoogle Scholar
  20. Lusk CH, Warton DI (2007) Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytol 176:764–774PubMedCrossRefGoogle Scholar
  21. Messier C, Nikinmaa E (2000) Effects of light availability and sapling size on the growth, biomass allocation, and crown morphology of understory sugar maple, yellow birch, and beech. Ecoscience 7:345–356Google Scholar
  22. Monnier Y, Vila B, Montès N, Bousquet-Mélou A, Prévosto B, Fernandez C (2011) Fertilization and allelopathy modify Pinus halepensis saplings crown acclimation to shade. Trees Struct Funct 25:497–507CrossRefGoogle Scholar
  23. Morgan DC, Smith H (1979) A systematic relationship between phytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta 145:253–258CrossRefGoogle Scholar
  24. Moriuchi KS, Winn AA (2005) Relationships among growth, development and plastic response to environment quality in a perennial plant. New Phytol 166:149–158PubMedCrossRefGoogle Scholar
  25. Niinemets Ü (2004) Adaptive adjustments to light in foliage and whole-plant characteristics depend on relative age in the perennial herb Leontodon hispidus. New Phytol 162:683–696CrossRefGoogle Scholar
  26. Niinemets Ü (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714CrossRefGoogle Scholar
  27. Niinemets Ü, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecol Monogr 76:521–547CrossRefGoogle Scholar
  28. Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486PubMedCrossRefGoogle Scholar
  29. Portsmuth A, Niinemets Ü (2007) Structural and physiological plasticity in response to light and nutrients in five temperate deciduous woody species of contrasting shade tolerance. Funct Ecol 21:61–77CrossRefGoogle Scholar
  30. Quézel P, Barbero M (1992) Le pin d’Alep et les espèces voisines: répartition et caractères écologiques généraux, sa dynamique récente en France méditerranéenne. Forêt méditerranéenne XIII:158–170Google Scholar
  31. Sanchez-Gomez D, Valladares F, Zavala MA (2006a) Functional traits and plasticity in response to light in seedlings of four Iberian forest tree species. Tree Physiol 26:1425–1433PubMedCrossRefGoogle Scholar
  32. Sanchez-Gomez D, Valladares F, Zavala MA (2006b) Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytol 170:795–805PubMedCrossRefGoogle Scholar
  33. Sumida A, Komiyama A (1997) Crown spread patterns for five deciduous broad-leaved woody species: ecological significance of the retention patterns of larger branches. Ann Bot 80:759–766Google Scholar
  34. Tilman D (1985) The resource-ratio hypothesis of plant succession. Am Nat 125:827–852CrossRefGoogle Scholar
  35. Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257CrossRefGoogle Scholar
  36. Valladares F, Martinez-Ferri E, Balaguer L, Perez-Corona E, Manrique E (2000) Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytol 148:79–91CrossRefGoogle Scholar
  37. Valladares F, Arrieta S, Aranda I, Lorenzo D, Sánchez-Gómez D, Tena D, Suárez F, Pardos JA (2005) Shade-tolerance, photoinhibition sensitivity and phenotypic plasticity of Ilex aquifolium in continental Mediterranean sites. Tree Physiol 25:1041–1052PubMedCrossRefGoogle Scholar
  38. 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
  39. Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763PubMedCrossRefGoogle Scholar
  40. Weinig C (2000) Plasticity versus Canalization: population differences in the timing of shade-avoidance responses. Evolution 54:441–451PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Yogan Monnier
    • 1
    • 2
  • Anne Bousquet-Mélou
    • 1
  • Bruno Vila
    • 1
  • Bernard Prévosto
    • 2
  • Catherine Fernandez
    • 1
  1. 1.Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE, UMR CNRS 7263)Aix-Marseille UniversitéMarseille Cedex 03France
  2. 2.IRSTEA-CEMAGREFUR EMAXCedex 5France

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