, Volume 25, Issue 5, pp 873–884 | Cite as

The relevance of seed size in modulating leaf physiology and early plant performance in two tree species

  • Jesús Rodríguez-CalcerradaEmail author
  • Nikos Nanos
  • Ismael Aranda
Original Paper


The size of seeds and the microsite of seed dispersal may affect the early establishment of seedlings through different physiological processes. Here, we examined the effects of seed size and light availability on seedling growth and survival, and whether such effects were mediated by water use efficiency. Acorns of Quercus petraea and the more drought-tolerant Quercus pyrenaica were sowed within and around a tree canopy gap in a sub-Mediterranean forest stand. We monitored seedling emergence and measured predawn leaf water potential (Ψpd), leaf nitrogen per unit area (Na), leaf mass per area, leaf carbon isotope composition (δ13C) and plant growth at the end of the first summer. Survival was measured on the next year. Path analysis revealed a consistent pattern in both species of higher δ13C as Ψpd decreased and higher δ13C as seedlings emerged later in the season, indicating an increase in 13C as the growing season is shorter and drier. There was a direct positive effect of seed size on δ13C in Q. petraea that was absent in Q. pyrenaica. Leaf δ13C had no effect on growth but the probability of surviving until the second year was higher for those seedlings of Q. pyrenaica that had lower δ13C on the first year. In conclusion, leaf δ13C is affected by seed size, seedling emergence time and the availability of light and water, however, leaf δ13C is irrelevant for first year growth, which is directly dependent on the amount of seed reserves.


Phenology Water stress Recruitment Seedling survival 13



We thank Guillermo González Gordaliza and Jesús Alonso for their helpful assistance in the field and Matthew T. Robson and Javier Cano for helping measuring and sowing the acorns. We are also grateful to Ruben Milla for advice on path analysis and critical reading of the manuscript, and Nicolas Fanin for constructive comments on data analysis. This work was supported by funding from projects CCG07-UPM/AMB-1865 and SUM2008-00004-C03-01.

Conflict of interest


Supplementary material

468_2011_562_MOESM1_ESM.pdf (247 kb)
Supplementary Figures (PDF 246 kb)


  1. Aranda I, Pardos M, Puértolas J, Jiménez MD, Pardos JA (2007) Water-use efficiency in cork oak (Quercus suber) is modified by the interaction of water and light availabilities. Tree Physiol 27:671–677PubMedGoogle Scholar
  2. Arbuckle JL (2003) AMOS 5 user’s guide. Smallwaters Corportation, Chigago, ILGoogle Scholar
  3. Asbjornsen H, Vogt KA, Ashton MS (2004) Synergistic responses of oak, pine and shrub seedlings to edge environments and drought in a fragmented tropical highland oak forest, Oaxaca, Mexico. For Ecol Manag 192:313–334CrossRefGoogle Scholar
  4. Augspurger CK, Cheeseman JM, Salk CF (2005) Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct Ecol 19:537–546CrossRefGoogle Scholar
  5. Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412CrossRefGoogle Scholar
  6. Baraloto C, Forget P-M, Goldberg DE (2005) Seed mass, seedling size and neotropical tree seedling establishment. J Ecol 93:1156–1166CrossRefGoogle Scholar
  7. Bates DM (2005) Fitting linear mixed models in R. R News 5:27–30Google Scholar
  8. Bentler PM (1989) EQS structural equations program manual. BMDP Statistical software, Los AngelesGoogle Scholar
  9. Bonfil C (1998) The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceaea). Am J Bot 85:79–87PubMedCrossRefGoogle Scholar
  10. Brookes PC, Wigston DL, Bourne WF (1980) The dependence of Quercus robur and Quercus petraea seedlings on cotyledon potassium, magnesium, calcium, and phosphorus during the first year of growth. Forestry 53:167–177CrossRefGoogle Scholar
  11. Casper BB, Forseth IN, Wait DA (2005) Variation in carbon isotope discrimination in relation to plant performance in a natural population of Cryptantha flava. Oecologia 145:541–548PubMedCrossRefGoogle Scholar
  12. Castro J (2006) Short delay in timing of emergence determines establishment success in Pinus sylvestris across microhabitats. Ann Bot 98:1233–1240PubMedCrossRefGoogle Scholar
  13. Castro J, Reich PB, Sánchez-Miranda A, Guerrero JD (2008) Evidence that the negative relationship between seed mass and relative growth rate is not physiological but linked to species identity: a within-family analysis of Scots pine. Tree Physiol 28:1077–1082PubMedGoogle Scholar
  14. Cordell S, Goldstein G, Meinzer FC, Handley LL (1999) Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and δ13C along an altitudinal gradient. Funct Ecol 13:811–818CrossRefGoogle Scholar
  15. Damesin C, Lelarge C (2003) Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant Cell Environ 26:207–219CrossRefGoogle Scholar
  16. Damesin C, Rambal S, Joffre R (1998) Seasonal and annual changes in leaf δ13C in two co-occurring Mediterranean oaks: relations to leaf growth and drought progression. Funct Ecol 12:778–785CrossRefGoogle Scholar
  17. Du Y, Huang Z (2008) Effects of seed mass and emergence time on seedling performance in Castanopsis chinenesis. For Ecol Manag 255:2495–2501CrossRefGoogle Scholar
  18. Duan B, Li C, Zhang X, Korpelainen H (2009) Water deficit affects mesophyll limitation of leaves more strongly in sun than in shade in two contrasting Picea asperata populations. Tree Physiol 29:1551–1561PubMedCrossRefGoogle Scholar
  19. Dudley SA (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92–102CrossRefGoogle Scholar
  20. Eglin T, Fresneau C, Lelarge-Trouverie C, Francois C, Damesin C (2009) Leaf and twig δ13C during growth in relation to biochemical composition and respired CO2. Tree Physiol 29:777–788PubMedCrossRefGoogle Scholar
  21. Ehleringer JR (1993) Variation in leaf carbon isotope discrimination in Encelia farinosa: implications for growth, competition, and drought survival. Oecologia 95:340–346CrossRefGoogle Scholar
  22. Ehleringer JR, Cooper TA (1988) Correlations between carbon isotope ratio and microhabitat in desert plants. Oecologia 76:562–566Google Scholar
  23. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137CrossRefGoogle Scholar
  24. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  25. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189PubMedCrossRefGoogle Scholar
  26. Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. Int J Plant Sci 164(3 Suppl):S21–S42CrossRefGoogle Scholar
  27. Gómez-Aparicio L, Pérez-Ramos IM, Mendoza I, Matías L, Quero JL, Castro J, Zamora R, Marañón T (2008) Oak seedling survival and growth along resource gradients in Mediterranean forests: implications for regeneration in current and future scenarios. Oikos 117:1683–1699CrossRefGoogle Scholar
  28. Imaji A, Seiwa K (2010) Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species. Oecologia 162:273–281PubMedCrossRefGoogle Scholar
  29. Jones RH, Allen BP, Sharitz RR (1997) Why do early-emerging tree seedlings have survival advantages?: a test using Acer rubrum (Aceraceae). Am J Bot 84:1714–1718PubMedCrossRefGoogle Scholar
  30. Kennedy PG, Hausmann NJ, Wenk EH, Dawson TE (2004) The importance of seed reserves for seedling performance: an integrated approach using morphological, physiological, and stable isotope techniques. Oecologia 141:547–554PubMedCrossRefGoogle Scholar
  31. Khurana E, Singh JS (2004) Response of five dry tropical tree seedlings to elevated CO2: impacts of seed size and successional status. New For 27:139–157CrossRefGoogle Scholar
  32. Long TJ, Jones RH (1996) Seedling growth strategies and seed size effects in fourteen oak species native to different soil moisture habitats. Trees 11:1–8CrossRefGoogle Scholar
  33. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739PubMedCrossRefGoogle Scholar
  34. Mediavilla S, Escudero A (2003) Mature trees versus seedlings: differences in leaf traits and gas exchange patterns in three co-occurring Mediterranean oaks. Ann For Sci 60:455–460CrossRefGoogle Scholar
  35. Meziane D, Shipley B (2001) Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply. Ann Bot 88:915–927CrossRefGoogle Scholar
  36. Milla R, Escudero A, Iriondo JM (2009) Inherited variability in multiple traits determines fitness in populations of an annual legume from contrasting latitudinal origins. Ann Bot 103:1279–1289PubMedCrossRefGoogle Scholar
  37. Nanos N, Pardo F, Nager JA, Pardos JA, Gil L (2005) Using multivariate factorial kriging for multiscale ordination: a case study. Can J For Res 35:2860–2874CrossRefGoogle Scholar
  38. Nicotra AB, Davidson A (2010) Adaptive phenotypic plasticity and plant water use. Funct Plant Biol 37:117–127CrossRefGoogle Scholar
  39. Picotte JL, Rosenthal DM, Rhode JM, Cruzan MB (2007) Plastic responses to temporal variation in moisture availability: consequences for water use efficiency and plant performance. Oecologia 153:821–832PubMedCrossRefGoogle Scholar
  40. Ponton S, Dupouey J-L, Bréda N, Dreyer E (2002) Comparison of water-use efficiency of seedlings from two sympatric oak species: genotype × environment interactions. Tree Physiol 22:413–422PubMedGoogle Scholar
  41. Quero JL, Villar R, Marañón T, Zamora R, Poorter L (2007) Seed-mass effects in four Mediterranean Quercus species (Fagaceae) growing in contrasting light environments. Am J Bot 94:1795–1803PubMedCrossRefGoogle Scholar
  42. Ramel F, Sulmon C, Gouesbet G, Couée J (2009) Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent response to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 104:1323–1337PubMedCrossRefGoogle Scholar
  43. Rich PM (1990) Characterising plant canopies with hemispherical photographs. Remote Sens Rev 5:13–29Google Scholar
  44. Rodríguez-Calcerrada J, Pardos JA, Gil L, Reich PB, Aranda I (2008) Light response in seedlings of a temperate (Quercus petraea) and a sub-Mediterranean species (Quercus pyrenaica): contrasting ecological strategies as potential keys to regeneration performance in mixed marginal populations. Plant Ecol 195:273–285CrossRefGoogle Scholar
  45. Rodríguez-Calcerrada J, Cano FJ, Valbuena-Carabaña M, Gil L, Aranda I (2010) Functional performance of oak seedlings naturally regenerated across microhabitats of distinct overstorey canopy closure. New For 39:245–259CrossRefGoogle Scholar
  46. Sandquist DR, Ehleringer JR (2003) Carbon isotope discrimination differences within and between contrasting populations of Encelia farinose raised under common-environment conditions. Oecologia 134:463–470PubMedGoogle Scholar
  47. Seiwa K (1998) Advantages of early germination for growth and survival of seedlings of Acer mono under different overstorey phenologies in deciduous broad-leaved forests. J Ecol 86:219–228CrossRefGoogle Scholar
  48. Seiwa K (2000) Effects of seed size and emergence time on tree seedling establishment: importance of developmental constraints. Oecologia 123:208–215CrossRefGoogle Scholar
  49. Shipley B (2000) Cause and correlation in biology—a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, UKCrossRefGoogle Scholar
  50. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria.
  51. Tripathi RS, Khan ML (1990) Effects of weight and microsite characteristics on germination and seedling fitness in two species of Quercus in a subtropical wet hill forest. Oikos 57:289–296CrossRefGoogle Scholar
  52. Urbieta IR, Pérez-Ramos IM, Zavala MA, Marañón T, Kobe RK (2008) Soil water content and emergence time control seedling establishment in three co-occurring Mediterranean oak species. Can J For Res 38:2382–2393CrossRefGoogle Scholar
  53. Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394CrossRefGoogle Scholar
  54. Villar-Salvador P, Heredia N, Millard P (2010) Remobilization of acorn nitrogen for seedling growth in holm oak (Quercus ilex), cultivated with contrasting nutrient availability. Tree Physiol 30:257–263PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jesús Rodríguez-Calcerrada
    • 1
    Email author
  • Nikos Nanos
    • 2
  • Ismael Aranda
    • 3
  1. 1.Centre of Functional and Evolutionary Ecology, CNRSMontpellier Cedex 5France
  2. 2.School of Forest EngineeringTechnical University of MadridMadridSpain
  3. 3.CIFORNational Institute for Agricultural and Food Scientific Research and Technology (INIA)MadridSpain

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