Skip to main content
Log in

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

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 14:2709–2726

    Google Scholar 

  • Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–31

    Article  CAS  Google Scholar 

  • 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 124:476–486

    Article  Google Scholar 

  • Chabot BF, Chabot JF (1977) Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26:363–377

    Article  Google Scholar 

  • Chapmann HD, Pratt PF (1973) Methods of analysis for soils, plants and water. University of California, Riverside

    Google Scholar 

  • Chmielewski FM, Rötzer T (2001) Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–112

    Article  Google Scholar 

  • 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 25:1127–1137

    Article  CAS  Google Scholar 

  • Fitter AH, Hay RKM (2002) Environmental physiology of plants, 3rd edn. Academic Press, London, p 423

    Google Scholar 

  • Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Adv Ecol Res 20:59–124

    Article  Google Scholar 

  • Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743

    Google Scholar 

  • Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195

    Article  Google Scholar 

  • Griffith M, Brown GN (1982) Cell wall deposits in winter rye Secale cereale L. “Puma” during cold acclimation. Bot Gaz 143:486–490

    Article  Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • Jian Q, Keming M, Yuxin Z (2009) Leaf-trait relationships of Quercus liaotungensis along an altitudinal gradient in Dongling Mountain, Beijing. Ecol Res 24:1243–1250

    Article  Google Scholar 

  • Jonas GS, Geber MA (1999) Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients. Am J Bot 86:333–343

    Article  CAS  Google Scholar 

  • Kodra E, Steinhaeuser K, Ganguly AR (2011) Persisting cold extremes under 21st-century warming scenarios. Geophys Res Lett 38:1–5

    Article  Google Scholar 

  • Körner CH, Larcher W (1988) Plant life in cold climates. Symp Soc Exp Biol 42:25–57

    Google Scholar 

  • Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91:1939–1948

    Article  Google Scholar 

  • 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 148:59–67

    Article  CAS  Google Scholar 

  • 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 40:5–13

    Google Scholar 

  • Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytol 108:267–276

    Article  Google Scholar 

  • 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 159:203–211

    Article  Google Scholar 

  • Mediavilla S, Escudero A, Heilmeier H (2001) Internal leaf anatomy and photosynthetic resource-use efficiency: interspecific and intraspecific comparisons. Tree Physiol 21:251–259

    Article  CAS  Google Scholar 

  • 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 134:471–479

    Article  CAS  Google Scholar 

  • 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 144:35–47

    Article  Google Scholar 

  • Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469

    Article  Google Scholar 

  • Niinemets Ü, Sack L (2006) Structural determinants of leaf light-harvesting capacity and photosynthetic potentials. Progress Bot 67:385–419

    Article  CAS  Google Scholar 

  • Nobel PS (2005) Physicochemical and environmental plant physiology. Academic Press, San Diego

    Google Scholar 

  • 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 31:168–173

    Article  Google Scholar 

  • 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 12:573–590

    Article  Google Scholar 

  • 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 21:97–107

    Article  Google Scholar 

  • 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 82:307–318

    Article  Google Scholar 

  • 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 182:565–588

    Article  Google Scholar 

  • 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 111:605–612

    CAS  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS 101:11001–11006

    Article  CAS  Google Scholar 

  • Reiter WD (1998) The molecular analysis of cell wall components. Trends Plant Sci 3:27–32

    Article  Google Scholar 

  • Schulze ED, Mooney HA (1993) Biodiversity and ecosystem function. Springer, Berlin

    Book  Google Scholar 

  • Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plantarum 119:253–262

    Article  CAS  Google Scholar 

  • 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 84:313–319

    Article  Google Scholar 

  • 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 3:108–115

    Article  Google Scholar 

  • 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 18:149–157

    Article  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • Tinker PB, Nye PH (2000) Solute movement in the rizosphere. Oxford University Press, New York

    Google Scholar 

  • Turner NC (1986) Adaptation to water deficits: a changing perspective. Aust J Plant Physiol 13:175–190

    Article  Google Scholar 

  • Turner IM (1994a) Sclerophylly: primarily protective? Funct Ecol 8:669–675

    Article  Google Scholar 

  • Turner IM (1994b) A quantitative analysis of leaf form in woody plants from the world’s major broadleaved forest types. J Biogeogr 21:413–419

    Article  Google Scholar 

  • 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

  • Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13 C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84:362–370

    Google Scholar 

  • 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 37:29–38

    Article  CAS  Google Scholar 

  • Walther GR (2000) Climatic forcing on the dispersal of exotic species. Phytocoenologia 30:409–430

    Google Scholar 

  • 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 146:389–395

    Article  Google Scholar 

  • Weih M, Karlsson PS (1999) The nitrogen economy of mountain birch seedlings: implications for winter survival. J Ecol 87:211–219

    Article  Google Scholar 

  • 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 150:147–155

    Article  Google Scholar 

  • Westoby M, Warton D, Reich PB (2000) The time value of leaf area. Am Nat 155:649–656

    Article  Google Scholar 

  • Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493

    Google Scholar 

  • 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 17:237–245

    Article  Google Scholar 

  • 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 90:534–543

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  Google Scholar 

  • Yates MJ, Verboom GA, Rebelo AG, Cramer MD (2010) Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region. Funct Ecol 24:485–492

    Article  Google Scholar 

Download references

Acknowledgments

This paper has received financial support from the Spanish Ministerio de Ciencia e Innovación—EU-FEDER (Project No. CGL2006-04281 and CGL2010-21187), the Regional Government of Castilla-León (Project No. SA126A08) and Miguel Casado S José Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sonia Mediavilla.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mediavilla, S., Gallardo-López, V., González-Zurdo, P. et al. Patterns of leaf morphology and leaf N content in relation to winter temperatures in three evergreen tree species. Int J Biometeorol 56, 915–926 (2012). https://doi.org/10.1007/s00484-011-0498-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-011-0498-2

Keywords

Navigation