International Journal of Biometeorology

, Volume 56, Issue 5, pp 915–926 | Cite as

Patterns of leaf morphology and leaf N content in relation to winter temperatures in three evergreen tree species

  • Sonia Mediavilla
  • Victoria Gallardo-López
  • Patricia González-Zurdo
  • Alfonso Escudero
Original Paper

Abstract

The competitive equilibrium between deciduous and perennial species in a new scenario of climate change may depend closely on the productivity of leaves along the different seasons of the year and on the morphological and chemical adaptations required for leaf survival during the different seasons. The aim of the present work was to analyze such adaptations in the leaves of three evergreen species (Quercus ilex, Q. suber and Pinus pinaster) and their responses to between-site differences in the intensity of winter harshness. We explore the hypothesis that the harshness of winter would contribute to enhancing the leaf traits that allow them to persist under conditions of stress. The results revealed that as winter harshness increases a decrease in leaf size occurs in all three species, together with an increase in the content of nitrogen per unit leaf area and a greater leaf mass per unit area, which seems to be achieved only through increased thickness, with no associated changes in density. P. pinaster was the species with the most intense response to the harshening of winter conditions, undergoing a more marked thickening of its needles than the two Quercus species. Our findings thus suggest that lower winter temperatures involve an increase in the cost of leaf production of evergreen species, which must be taken into account in the estimation of the final cost and benefit balance of evergreens. Such cost increases would be more pronounced for those species that, like P. pinaster, show a stronger response to the winter cold.

Keywords

Leaf density Leaf mass per unit area Leaf N content Leaf thickness Winter temperature gradient 

References

  1. Atkin OK, Atkinson LJ, Fisher R, Campbell CD, Zaragoza-Castells J, Pitchford JW, Woodward FI, Hurry V (2008) Using temperature-dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate–vegetation model. Glob Change Biol 14:2709–2726Google Scholar
  2. Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–31CrossRefGoogle Scholar
  3. Castro-Díez P, Puyravaud JP, Cornelissen JHC (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124:476–486CrossRefGoogle Scholar
  4. Chabot BF, Chabot JF (1977) Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26:363–377CrossRefGoogle Scholar
  5. Chapmann HD, Pratt PF (1973) Methods of analysis for soils, plants and water. University of California, RiversideGoogle Scholar
  6. Chmielewski FM, Rötzer T (2001) Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–112CrossRefGoogle Scholar
  7. Coste S, Roggy JC, Imbert P, Born C, Bonal D, Dreyer E (2005) Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance. Tree Physiol 25:1127–1137CrossRefGoogle Scholar
  8. Fitter AH, Hay RKM (2002) Environmental physiology of plants, 3rd edn. Academic Press, London, p 423Google Scholar
  9. Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Adv Ecol Res 20:59–124CrossRefGoogle Scholar
  10. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743Google Scholar
  11. Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195CrossRefGoogle Scholar
  12. Griffith M, Brown GN (1982) Cell wall deposits in winter rye Secale cereale L. “Puma” during cold acclimation. Bot Gaz 143:486–490CrossRefGoogle Scholar
  13. IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge, University Press, CambridgeGoogle Scholar
  14. Jian Q, Keming M, Yuxin Z (2009) Leaf-trait relationships of Quercus liaotungensis along an altitudinal gradient in Dongling Mountain, Beijing. Ecol Res 24:1243–1250CrossRefGoogle Scholar
  15. Jonas GS, Geber MA (1999) Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients. Am J Bot 86:333–343CrossRefGoogle Scholar
  16. Kodra E, Steinhaeuser K, Ganguly AR (2011) Persisting cold extremes under 21st-century warming scenarios. Geophys Res Lett 38:1–5CrossRefGoogle Scholar
  17. Körner CH, Larcher W (1988) Plant life in cold climates. Symp Soc Exp Biol 42:25–57Google Scholar
  18. Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91:1939–1948CrossRefGoogle Scholar
  19. Kubacka-Zebalska M, Kacperska A (1999) Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape (Brassica napus L. var oleifera L.). Plant Sci 148:59–67CrossRefGoogle Scholar
  20. Li C, Zhang X, Liu X, Luukkanen O, Berninger F (2006) Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fenn 40:5–13Google Scholar
  21. Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytol 108:267–276CrossRefGoogle Scholar
  22. 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
  23. Mediavilla S, Escudero A, Heilmeier H (2001) Internal leaf anatomy and photosynthetic resource-use efficiency: interspecific and intraspecific comparisons. Tree Physiol 21:251–259CrossRefGoogle Scholar
  24. Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ13C of Alchemilla alpine. New Phytol 134:471–479CrossRefGoogle Scholar
  25. Niinemets U (1999) Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144:35–47CrossRefGoogle Scholar
  26. Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  27. Niinemets Ü, Sack L (2006) Structural determinants of leaf light-harvesting capacity and photosynthetic potentials. Progress Bot 67:385–419CrossRefGoogle Scholar
  28. Nobel PS (2005) Physicochemical and environmental plant physiology. Academic Press, San DiegoGoogle Scholar
  29. Ogaya R, Peñuelas J (2007) Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures. Acta Oecol 31:168–173CrossRefGoogle Scholar
  30. Oleksyn J, Modrzynski J, Tjoelker MG, Zytkowiak R, Reich PB, Karolewski P (1998) Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation. Funct Ecol 12:573–590CrossRefGoogle Scholar
  31. Oliveira G, Peñuelas J (2000) Comparative photochemical and phenomorphological responses to winter stress of an evergreen (Quercus ilex L) and a semi-deciduous (Cistus albidus L) Mediterranean woody species. Acta Oecol 21:97–107CrossRefGoogle Scholar
  32. Parsons AN, Welker JM, Wookey PA, Press MC, Callaghan TV, Lee JA (1994) Growth responses of four sub-Arctic dwarf shrubs to simulated environmental change. J Ecol 82:307–318CrossRefGoogle Scholar
  33. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588CrossRefGoogle Scholar
  34. Rajashekar CB, Lafta A (1996) Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and cell cultures. Plant Physiol 111:605–612Google Scholar
  35. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS 101:11001–11006CrossRefGoogle Scholar
  36. Reiter WD (1998) The molecular analysis of cell wall components. Trends Plant Sci 3:27–32CrossRefGoogle Scholar
  37. Schulze ED, Mooney HA (1993) Biodiversity and ecosystem function. Springer, BerlinCrossRefGoogle Scholar
  38. Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plantarum 119:253–262CrossRefGoogle Scholar
  39. Stefanowska M, Kuras M, Kubacka-Zebalska M, Kacperska A (1999) Low temperature affects pattern on leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var oleifera L.). Ann Bot 84:313–319CrossRefGoogle Scholar
  40. Suzuki S, Kudo G (1997) Short-term effects of simulated environmental change on phenology, leaf traits, and shoot growth of alpine plants on a temperate mountain, northern Japan. Glob Change Biol 3:108–115CrossRefGoogle Scholar
  41. Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18:149–157CrossRefGoogle Scholar
  42. Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054CrossRefGoogle Scholar
  43. Tinker PB, Nye PH (2000) Solute movement in the rizosphere. Oxford University Press, New YorkGoogle Scholar
  44. Turner NC (1986) Adaptation to water deficits: a changing perspective. Aust J Plant Physiol 13:175–190CrossRefGoogle Scholar
  45. Turner IM (1994a) Sclerophylly: primarily protective? Funct Ecol 8:669–675CrossRefGoogle Scholar
  46. Turner IM (1994b) A quantitative analysis of leaf form in woody plants from the world’s major broadleaved forest types. J Biogeogr 21:413–419CrossRefGoogle Scholar
  47. Uğurlu E, Oldeland J (2010) Species response curves of oak species along climatic gradients in Turkey. Int J Biometeorol. doi:10.1007/s00484-010-0399-9
  48. Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13 C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84:362–370Google Scholar
  49. Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38CrossRefGoogle Scholar
  50. Walther GR (2000) Climatic forcing on the dispersal of exotic species. Phytocoenologia 30:409–430Google Scholar
  51. Walther GR, Post E, Convey P, Menzel A, Parmesank C, Beebee T, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 146:389–395CrossRefGoogle Scholar
  52. Weih M, Karlsson PS (1999) The nitrogen economy of mountain birch seedlings: implications for winter survival. J Ecol 87:211–219CrossRefGoogle Scholar
  53. Weih M, Karlsson PS (2001) Growth response of Mountain birch to air and soil temperature: is increasing leaf-nitrogen content an acclimation to lower air temperature? New Phytol 150:147–155CrossRefGoogle Scholar
  54. Westoby M, Warton D, Reich PB (2000) The time value of leaf area. Am Nat 155:649–656CrossRefGoogle Scholar
  55. Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493Google Scholar
  56. Woods HA, Makino W, Cotner JB, Hobbie SE, Harrison JF, Acharya K, Elser JJ (2003) Temperature and the chemical composition of poikilothermic organisms. Funct Ecol 17:237–245CrossRefGoogle Scholar
  57. Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J Ecol 90:534–543CrossRefGoogle Scholar
  58. Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefGoogle Scholar
  59. Yates MJ, Verboom GA, Rebelo AG, Cramer MD (2010) Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region. Funct Ecol 24:485–492CrossRefGoogle Scholar

Copyright information

© ISB 2011

Authors and Affiliations

  • Sonia Mediavilla
    • 1
  • Victoria Gallardo-López
    • 1
  • Patricia González-Zurdo
    • 1
  • Alfonso Escudero
    • 1
  1. 1.Departamento de Ecología, Facultad de BiologíaUniversidad de SalamancaSalamancaSpain

Personalised recommendations