Annals of Forest Science

, Volume 65, Issue 3, pp 311–311 | Cite as

Functional traits and plasticity linked to seedlings’ performance under shade and drought in Mediterranean woody species

  • David Sánchez-GómezEmail author
  • Miguel A. Zavala
  • Fernando Valladares
Original Article


Interspecific differences in morphology, biomass allocation and phenotypic plasticity along an experimental irradiance gradient and two contrasting water regimes were studied for eight Mediterranean woody species at the seedling stage; a critical demographic stage in Mediterranean plant communities. We tested whether species variation in these traits can explain previously reported interspecific differences in performance under shade and drought. Four irradiance levels (1%, 6%, 20% and 100% of full sunlight) and two water regimes (well watered and water-stressed conditions) in 6% and 100% irradiance levels were established. Quercus species exhibited the largest seeds, the highest total dry mass and also the highest root-shoot ratio, but their leaf mass fraction (LMF) and leaf area ratio (LAR) were low. Pistacia terebinthus, and Arbutus unedo exhibited the opposite traits. From those traits that correlated with seed size only LAR resulted significantly linked to survival in deep shade. None of the traits studied correlated with survival under water-stressed conditions. Overall phenotypic plasticity was negatively correlated with survival in deep shade but no correlation was found with survival under water-stressed conditions. Our results highlight the importance of low LAR and low phenotypic plasticity as potential determinants of enhanced performance under shade during the very early seedling stages of Mediterranean woody species. Low LAR was also positively correlated with seed size and consequently, its relationship with enhanced performance under shade might change at later life stages of the plant when seed reserves are no longer available.

conservative resource-use strategy leaf area ratio root-shoot ratio seed size specific leaf area 

Traits fonctionnels et plasticité en relation avec les performances de semis de ligneux méditerranéens sous ombrage et en situation de sécheresse


Les différences interspécifiques de morphologie, d’allocation de biomasse et de plasticité phénotypique ont été étudiées pour des semis de huit espèces ligneuses méditerranéennes sous un gradient d’ombrage et soumis à deux régimes d’alimentation hydrique. Le stade semis est un stade critique pour la démographie des communautés végétales méditerranéennes. Nous avons testé l’hypothèse que des différences dans ces traits pouvaient expliquer les différences inter-spécifiques de performances souvent décrites sous ombrage et sous sécheresse. Nous avons imposé quatre niveaux d’ombrage (1 %, 6 %, 20 % and 100 % du rayonnement incident) et deux régimes hydriques (irrigation abondante et déficit hydrique pour les traitements 6 % et 100 %). Les chênes présentaient les graines les plus grosses, la plus forte biomasse et également le rapport racine/parties aériennes le plus élevé, mais leurs rapports (biomasse foliaire/biomasse totale) et (surface foliaire/biomasse totale) (LAR) étaient faibles. Pistacia terebinthus, et Arbutus unedo présentaient des caractéristiques opposées. Parmi ces traits liés à la taille des graines, seul LAR était fortement corrélé à la survie sous ombre forte. Aucun des traits mesurés n’était corrélé à la survie sous sécheresse. Le degré de plasticité phénotypique était corrélé négativement avec la survie sous ombre forte, mais aucune corrélation n’a pu être détectée avec la survie sous sécheresse. Ces résultats soulignent l’importance d’un LAR faible et d’une faible plasticité phénotypique comme déterminants d’une survie sous fort ombrage pendant les tous premiers stades de développement des semis de ligneux méditerranéens. De faibles valeurs de LAR étaient également associées à de fortes biomasses initiales des graines; son effet sur la performance des semis à l’ombre risque de ce fait de disparaître lors des stades de développement ultérieurs quand les réserves des graines sont épuisées.

stratégie conservatrice d’utilisation des ressources rapport surface foliaire biomasse totale rapport racine parties aériennes dimensions des graines surface spécifique 


  1. [1]
    Ackerly D., Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance, Ecol. Monogr. 74 (2004) 25–44.CrossRefGoogle Scholar
  2. [2]
    Antúnez I., Retamosa E.C., Villar R., Relative growth rate in phylogenetically related deciduous and evergreen woody species, Oecologia 128 (2001) 172–180.CrossRefGoogle Scholar
  3. [3]
    Aschman H., Distribution and peculiarity of Mediterranean ecosystems, in: di Castri F., Mooney H.A. (Eds.), Mediterranean type ecosystems: origin and structure, Springer-Verlag, Berlin, 1973, pp. 11–19.Google Scholar
  4. [4]
    Broncano M.J., Riba M., Retana J., Seed germination and seedling performance of two Mediterranean tree species, holm oak (Quercus ilex) and Aleppo pine (Pinus halepensis): a multifactor experimental approach, Plant Ecol. 1 (1998) 17–26.CrossRefGoogle Scholar
  5. [5]
    Canham C.D., Berkowitz A.R., Kelly V.R., Lovett G.M., Ollinger S.V., Schnurr J., Biomass allocation and multiple resource limitation in tree seedlings, Can. J. For. Res. 26 (1996) 1521–1530.CrossRefGoogle Scholar
  6. [6]
    Castro J., Zamora R., Hódar J.A., Gómez J.M., 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 (2004) 266–277.CrossRefGoogle Scholar
  7. [7]
    Castro-Diez P., Navarro J., Pintado A., Sancho L.G., Maestro M., Interactive effects of shade and irrigation on the performance of seedlings of three Mediterranean Quercus species, Tree Physiol. 26 (2006) 389–400.PubMedCrossRefGoogle Scholar
  8. [8]
    Catalán Bachiller G., Semillas de árboles y arbustos forestales, ICONA, Madrid, 1993.Google Scholar
  9. [9]
    Chapin F.S., Autumn K., Pugnaire F.I., Evolution of suites of traits in response to environmental-stress, Am. Nat. 142S (1993) S78-S92.Google Scholar
  10. [10]
    Cochard H., Lemoine D., Dreyer E., The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L., Plant Cell Environ. 22 (1999) 101–108.CrossRefGoogle Scholar
  11. [11]
    Coomes D.A., Grubb P.J., Impacts of root competition in forests and woodlands: A theoretical framework and review of experiments, Ecol. Monogr. 70 (2000) 171–207.CrossRefGoogle Scholar
  12. [12]
    Coomes D.A., Grubb P.J., Colonization, tolerance, competition and seed-size variation within functional groups, Trends Ecol. Evol. 18 (2003) 283–291.CrossRefGoogle Scholar
  13. [13]
    Cornelissen J.H.C., Castro Diez P., Hunt R., Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types, J. Ecol. 84 (1996) 755–765.CrossRefGoogle Scholar
  14. [14]
    Deka R.N., Wairiu M., Mtakwa P.W., Mullins C.E., Veenendaal E.M., Townend J., Use and accuracy of the filter-paper technique for measurement of soil matric potential, Eur. J. Soil Sci. 46 (1995) 233–238.CrossRefGoogle Scholar
  15. [15]
    Givnish T.J., Adaptation to sun and shade: a whole-plant perspective, Aust. J. Plant Physiol. 15 (1988) 63–92.CrossRefGoogle Scholar
  16. [16]
    Gomez J.M., Valladares F., Puerta-Piñero C., Differences between structural and functional heterogeneity caused by seed dispersal, Funct. Ecol. 18 (2004) 787–792.CrossRefGoogle Scholar
  17. [17]
    Gratani L., Canopy structure, vertical radiation profile and photosynthetic function in a Quercus ilex evergreen forest, Photosynthetica 33 (1997) 139–149.CrossRefGoogle Scholar
  18. [18]
    Grime J.P., Plant strategies, vegetation processes, and ecosystem properties, John Wiley & Sons, Ltd, Chichester, GB, 2001.Google Scholar
  19. [19]
    Grubb P.J., The maintenance of species-richness in plant communities: the importance of the regeneration niche, Biol. Rev. 52 (1977) 107–145.CrossRefGoogle Scholar
  20. [20]
    Grubb P.J., Metcalfe D.J., Adaptation and inertia in the Australian tropical lowland rain-forest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand, Funt. Ecol. 10 (1996) 512–520.CrossRefGoogle Scholar
  21. [21]
    Hewitt N., Seed size and shade-tolerance: a comparative analysis of North American temperate trees, Oecologia 114 (1998) 432–440.CrossRefGoogle Scholar
  22. [22]
    Instituto-Nacional-de-Meteorología, Calendario meteorológico 2002, Ministerio de Medio Ambiente, Madrid, 2002.Google Scholar
  23. [23]
    Kawecki T.J., The evolution of genetic canalization under fluctuating selection, Evolution 54 (2000) 1–12.PubMedGoogle Scholar
  24. [24]
    Kitajima K., Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees, Oecologia 98 (1994) 419–428.CrossRefGoogle Scholar
  25. [25]
    Kobe R.K., Pacala S.W., Silander J.A.J., Juvenile tree survivorship as a component of shade tolerance, Ecol. Appl. 5 (1995) 517–532.CrossRefGoogle Scholar
  26. [26]
    Ludlow M.M., Strategies of response to water stress, in: Kreeb K.H., Richter H., Hinckley T.M. (Eds.), Structural and functional responses to environmental stresses, SPB Academic Publishing, The Hague, 1989, pp. 269–281.Google Scholar
  27. [27]
    Niinemets Ü, The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited, J. Ecol. 94 (2006) 464–470.CrossRefGoogle Scholar
  28. [28]
    Pigott C.D., Pigott S., Water as a determinant of the distribution of trees at the boundary of the Mediterranean zone, J. Ecol. 81 (1993) 557–566.CrossRefGoogle Scholar
  29. [29]
    Poorter L., Light-dependent changes in biomass allocation and their importance for growth of rain forest tree species, Funct. Ecol. 15 (2001) 113–123.CrossRefGoogle Scholar
  30. [30]
    Reich P.B., Walters M.B., Ellsworth D.S., Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems, Ecol. Monogr. 62 (1992) 365–392.CrossRefGoogle Scholar
  31. [31]
    Reich P.B., Wright I.J., Cavender-Bares J., Craine M., Oleksyn J., Westoby M., Walters M.B., The evolution of plant functional variation: traits, spectra and strategies, Int. J. Plant Sci. 164 (2003) S143-S164.CrossRefGoogle Scholar
  32. [32]
    Rickleffs R.E., Environmental heterogeneity and plant species diversity: A hypothesis, Am. Nat. 111 (1977) 376–381.CrossRefGoogle Scholar
  33. [33]
    Sack L., Grubb P.J., The combined impacts of deep shade and drought on the growth and biomass allocation of shade-tolerant woody seedlings, Oecologia 131 (2002) 175–185.CrossRefGoogle Scholar
  34. [34]
    Sack L., Grubb P.J., Maranon T., The functional morphology of juvenile plants tolerant of strong summer drought in shaded forest understories in southern Spain, Plant Ecol. 168 (2003) 139–163.CrossRefGoogle Scholar
  35. [35]
    Sánchez-Gómez D., Valladares F., Zavala M.A., Functional traits and plasticity in response to light in seedlings of four Iberian forest tree species, Tree Physiol. 26 (2006) 1425–1433.PubMedGoogle Scholar
  36. [36]
    Sánchez-Gómez D., Valladares F., Zavala M.A., 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 (2006) 795–806.PubMedCrossRefGoogle Scholar
  37. [37]
    Smith T., Huston M., A theory of the spatial and temporal dynamics of plant communities, Vegetatio 83 (1989) 49–69.CrossRefGoogle Scholar
  38. [38]
    Sultan S.E., What has survived of Darwin’s theory? Phenotypic plasticity and the Neo-Darwinian legacy, Evol.Trend Plant 6 (1992) 61–71.Google Scholar
  39. [39]
    Tilman D., Plant strategies and the dynamics and structure of plant communities, Princeton University Press, Princeton, New Jersey, USA, 1988.Google Scholar
  40. [40]
    Tilman D., Constraints and tradeoffs: toward a predictive theory of competition and succession, Oikos 58 (1990) 3–15.CrossRefGoogle Scholar
  41. [41]
    Valladares F., Global change and radiation in Mediterranean forest ecosystems: a meeting point for ecology and management, in: Arianoutsou M., Papanastasis V. (Eds.), Ecology, conservation and sustainable managements of Mediterranean type ecosystems of the world, Millpress, Rotterdam, 2004, pp. 1–4.Google Scholar
  42. [42]
    Valladares F., Balaguer L., Martínez-Ferri E., Pérez-Corona E., Manrique E., Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems, New Phytol. 156 (2002) 457–467.CrossRefGoogle Scholar
  43. [43]
    Valladares F., Martinez-Ferri E., Balaguer L., Perez-Corona E., Manrique E., Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy?, New Phytol. 148 (2000) 79–91.CrossRefGoogle Scholar
  44. [44]
    Valladares F., Sánchez-Gómez D., Ecophysiological traits associated with drought in Mediterranean tree seedlings: Individual responses versus interspecific trends in eleven species, Plant Biol. 8 (2006) 688–697.PubMedCrossRefGoogle Scholar
  45. [45]
    Valladares F., Sánchez-Gómez D., Zavala M.A., Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications, J. Ecol. 94 (2006) 1103–1116.CrossRefGoogle Scholar
  46. [46]
    Valladares F., Wright S.J., Lasso E., Kitajima K., Pearcy R.W., Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest, Ecology 81 (2000) 1925–1936.CrossRefGoogle Scholar
  47. [47]
    Veneklaas E.J., Poorter L., Growth and carbon partitioning of tropical tree seedlings in contrasting light environments, in: Lambers H., Poorter H., Van Vuuren M.M.I. (Eds.), Inherent variation in plant growth: physiological mechanisms and ecological consequences, Backhuys, Leiden, NL, 1998, pp. 337–361.Google Scholar
  48. [48]
    Walters M.B., Reich P.B., Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ?, New Phytol. 143 (1999) 143–154.CrossRefGoogle Scholar
  49. [49]
    West-Eberhard M.J., Phenotypic plasticity and the origins of diversity, Ann. Rev. Ecol. Syst. 20 (1989) 249–278.CrossRefGoogle Scholar
  50. [50]
    Zar J.H., Biostatistical analysis, Prentice Hall, New Jersey, 1999.Google Scholar
  51. [51]
    Zavala M.A., Bravo de la Parra R., A mechanistic model of tree competition and facilitation for Mediterranean forests: Scaling from leaf physiology to stand dynamics, Ecol. Model. 188 (2005) 76–92.CrossRefGoogle Scholar
  52. [52]
    Zavala M.A., Espeita J.M., Retana J., Constraints and trade-offs in Mediterranean plant communities: the case of Holm oak-Aleppo pine forests, Bot. Rev. 66 (2000) 119–149.CrossRefGoogle Scholar
  53. [53]
    Zavala M.A., Zea G.E., Mechanisms maintaining biodiversity in Mediterranean pine-oak forests: insights from a spatial simulation model, Plant Ecol. 171 (2004) 197–207.CrossRefGoogle Scholar

Copyright information

© Springer S+B Media B.V. 2008

Authors and Affiliations

  • David Sánchez-Gómez
    • 1
    Email author
  • Miguel A. Zavala
    • 1
    • 2
  • Fernando Valladares
    • 3
    • 4
  1. 1.Instituto Nacional de Investigatión y Tecnología Agraria y AlimentariaMadridSpain
  2. 2.Departamento de Ecología, Edificio de CienciasUniversidad de Alcalá. Alcalá de HenaresMadridSpain
  3. 3.Centro de Ciencias Medioambientales C.S.I.C.Instituto de Recursos NaturalesMadridSpain
  4. 4.Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y TecnológicasUniversidad Rey Juan CarlosMóstolesSpain

Personalised recommendations