European Journal of Forest Research

, Volume 127, Issue 6, pp 495–506 | Cite as

Phenotypic plasticity blurs ecotypic divergence in the response of Quercus coccifera and Pinus halepensis to water stress

  • Francisco J. Baquedano
  • Fernando Valladares
  • Federico J. CastilloEmail author
Original Paper


The Mediterranean evergreen woody plants Quercus coccifera and Pinus halepensis grow in a range of environments where selection by drought, heat and high irradiance can drive genetic and phenotypic differentiation of populations. However, the role of these stresses in filtering out maladaptive genotypes remains unknown. We hypothesize that this filtering is an important process for woody Mediterranean species due to their low phenotypic plasticity reported in previous studies. We have studied the response of saplings of Q. coccifera and P. halepensis, originating from two contrasting populations (a rock outcrop and a garrigue formation), to water stress. Isozyme characterization of genetic diversity was done to determine whether populations were genetically distinct. Water response analysis was based on water relations, gas exchange, chlorophyll a fluorescence, pigment content, antioxidant status and morphological and structural parameters. Ecotypic differentiation was found for both Q. coccifera and P. halepensis populations, with a higher population isozyme similarity and a higher frequency of dominance of a few genotypes at the rock outcrop in both the species. P. halepensis exhibited small but significant differences between populations for plastic responses to water, with lower phenotypic plasticity in saplings from the rock outcrop. Although it was not found in Q. coccifera, this pattern suggests that ecotypic differentiation rendering stress-tolerant ecotypes involves a decreased plasticity. Phenotypic plasticity was not high but it explained over 75% of the total variability among individual plants. Thus, and although evidence for ecotypic divergence was found in both the species, saplings were plastic enough to blur ecotypic differentiation.


Drought Ecotype Genetic variability Mediterranean species Phenotypic plasticity 



This research was founded by the Spanish CICYT (CLI97-0735-C03-03 and AMB1999-0293), Universidad Pública de Navarra and Gobierno de Navarra. We thank M. Lubias, J.J. Echaniz, I. Redín and L. Sánchez for their contribution to obtain experimental data. Collaborative research and data analysis was made possible by the Spanish thematic network GLOBIMED (

Supplementary material

10342_2008_232_MOESM1_ESM.pdf (60 kb)
Electronic supplementary material (PDF 60 kb)


  1. Abrams MD (1994) Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiol 14:833–842PubMedGoogle Scholar
  2. Acherar M, Rambal S (1992) Comparative water relations of four Mediterranean oak species. Vegetation 99–100:177–184. doi: 10.1007/BF00118224 CrossRefGoogle Scholar
  3. Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402–407. doi: 10.1016/S0169-5347(00)89156-9 CrossRefGoogle Scholar
  4. Bailey JD, Harrington CA (2006) Temperature regulation of bud-burst phenology within and among years in a young Douglas-fir (Pseudotsuga menziesii) plantation in western Washington, USA. Tree Physiol 26:421–430PubMedGoogle Scholar
  5. Balaguer L, Martínez-Ferri E, Valladares F, Pérez-Corona ME, Baquedano FJ, Castillo FJ et al (2001) Population divergence in the plasticity of the response of Quercus coccifera to the light environment. Funct Ecol 15:124–135. doi: 10.1046/j.1365-2435.2001.00505.x CrossRefGoogle Scholar
  6. Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100. doi: 10.1016/0098-8472(92)90034-Y CrossRefGoogle Scholar
  7. Bogdan S, Katicic-Trupcevic I, Kajba D (2004) Genetic variation in growth traits in a Quercus robur L. open-pollinated progeny test of the Slavonian provenance. Silvae Genet 53:198–201Google Scholar
  8. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155. doi: 10.1016/S0065-2660(08)60048-6 CrossRefGoogle Scholar
  9. Buschmann C (1995) Variation of the quenching of chlorophyll fluorescence under different intensities of the actinic light in wild type plants of tobacco and in an Aurea mutant deficient of light-harvesting-complex. J Plant Physiol 145:245–252Google Scholar
  10. Cano A, Hernández-Ruíz J, García-Cánovas F, Acosta M, Arnao MB (1998) An end-point method for estimation of the total antioxidant activity in plant material. Phytochem Anal 9:196–202. doi:10.1002/(SICI)1099-1565(199807/08)9:4<196::AID-PCA395>3.0.CO;2-WCrossRefGoogle Scholar
  11. Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environ Exp Bot 28:231–238. doi: 10.1016/0098-8472(88)90033-0 CrossRefGoogle Scholar
  12. Castillo FJ, Penel C, Greppin H (1984) Peroxidases release induced by ozone in Sedum album leaves. Plant Physiol 74:846–851PubMedGoogle Scholar
  13. Castro-Díez P, Navarro J, Pintado A, Sancho LG, Maestro M (2006) Interactive effects of shade and irrigation on the performance of seedlings of three Mediterranean Quercus species. Tree Physiol 26:389–400PubMedGoogle Scholar
  14. Cregg BM (1992) Leaf area estimation of mature foliage of Juniperus. For Sci 38:61–67Google Scholar
  15. Dodd RS, Rafii ZA, Power AB (1998) Ecotypic adaptation in Austrocedrus chilensis in cuticular hydrocarbon composition. New Phytol 138:699–708. doi: 10.1046/j.1469-8137.1998.00142.x CrossRefGoogle Scholar
  16. Donohue K, Polisetty CR, Wender NJ (2005) Genetic basis and consequences of niche construction: plasticity-induced genetic constraints on the evolution of seed dispersal in Arabidopsis thaliana. Am Nat 165:537–550. doi: 10.1086/429162 PubMedCrossRefGoogle Scholar
  17. Einhorn KS, Rosenqvist E, Leverenz JW (2004) Photoinhibition in seedlings of Fraxinus and Fagus under natural light conditions: implications for forest regeneration? Oecologia 140(2):241–251. doi: 10.1007/s00442-004-1591-6 PubMedCrossRefGoogle Scholar
  18. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 42:313–349Google Scholar
  19. Gianoli E (2004) Plasticity of traits and correlations in two populations of Convolvulus arvensis (Convolvulaceae) differing in environmental heterogeneity. Int J Plant Sci 165:825–832. doi: 10.1086/422050 CrossRefGoogle Scholar
  20. González AV, Gianoli E (2004) Morphological plasticity in response to shading in three Convolvulus species of different ecological breadth. Acta Oecol 26:185–190. doi: 10.1016/j.actao.2004.05.001 CrossRefGoogle Scholar
  21. Gratani L, Meneghini M, Pesoli A, Crescente MF (2003) Structural and functional plasticity of Quercus ilex saplings of different provenances in Italy. Trees (Berl) 17:515–521. doi: 10.1007/s00468-003-0269-8 Google Scholar
  22. Harwite W (ed) (1980) Official methods of analysis of the Association of Official Analytical Chemists, 13th edn. Washington D.C., pp 117–123Google Scholar
  23. Kawecki TJ (2000) The evolution of genetic canalization under fluctuating selection. Evol Int J Org Evol 54:1–12Google Scholar
  24. Kyparissis A, Drilias P, Manetas Y (2000) Seasonal fluctuations in photoprotective (xantophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Aust J Plant Physiol 27:264–272Google Scholar
  25. Lauteri M, Pliura A, Monteverdi MC, Brugnoli E, Villani F, Eriksson G (2004) Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. J Evol Biol 17:1286–1296. doi: 10.1111/j.1420-9101.2004.00765.x PubMedCrossRefGoogle Scholar
  26. Lin MJ, Hsu BD (2004) Photosynthetic plasticity of Phalaenopsis in response to different light environments. J Plant Physiol 161:1259–1268. doi: 10.1016/j.jplph.2004.05.009 PubMedCrossRefGoogle Scholar
  27. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277. doi: 10.1146/annurev.ecolsys.27.1.237 CrossRefGoogle Scholar
  28. Lortie CJ, Aarssen LW (1996) The specialization hypothesis for phenotypic plasticity in plants. Int J Plant Sci 157:484–487. doi: 10.1086/297365 CrossRefGoogle Scholar
  29. MAFF (1986) The analysis of agricultural material. Ministry of Agriculture Fisheries and Food, Reference book 427, HMSO, London, UK, pp 156–157Google Scholar
  30. Maherali H, Williams BL, Paige KN, Delucia EH (2002) Hydraulic differentiation of Ponderosa pine populations along a climate gradient is not associated with ecotypic divergence. Funct Ecol 16:510–521. doi: 10.1046/j.1365-2435.2002.00645.x CrossRefGoogle Scholar
  31. Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138PubMedGoogle Scholar
  32. Matthes-Sears U, Larson DW (1999) Limitations to sapling growth and survival by the quantity and quality of rooting space: implications for the establishment of Thuja occidentalis on cliff faces. Int J Plant Sci 160:122–128. doi: 10.1086/314105 CrossRefGoogle Scholar
  33. McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymatic function for erythrocuprin (hemocuprin). J Biol Chem 224:6049–6055Google Scholar
  34. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692. doi: 10.1016/j.tree.2005.08.002 PubMedCrossRefGoogle Scholar
  35. Navas ML, Garnier E (2002) Plasticity of whole plant and leaf traits in Rubia peregrina in response to light, nutrient and water availability. Acta Oceol 23:375–383. doi: 10.1016/S1146-609X(02)01168-2 CrossRefGoogle Scholar
  36. Peters JL, Castillo FJ, Heath RL (1989) Alteration of extracellular enzymes in pinto bean leaves upon exposure to air pollutants, ozone and sulphur dioxide. Plant Physiol 89:159–164PubMedCrossRefGoogle Scholar
  37. Robinson D, Rorison IH (1988) Plasticity in grass species in relation to nitrogen supply. Funct Ecol 2:249–257. doi: 10.2307/2389701 CrossRefGoogle Scholar
  38. Ronsheim ML, Bever JD (2000) Genetic variation and evolutionary trade-offs for sexual and asexual reproductive modes in Allium vineale (Lillaceae). Am J Bot 87:1769–1777. doi: 10.2307/2656827 PubMedCrossRefGoogle Scholar
  39. Saldaña A, Gianoli E, Lusk CH (2005) Ecophysiological responses to light availability in three Blechnum species (Pteridophyta, Blechnaceae) of different ecological breadth. Oecologia 145:252–257. doi: 10.1007/s00442-005-0116-2 PubMedCrossRefGoogle Scholar
  40. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, SunderlandGoogle Scholar
  41. Schnitzer M (1982) Organic matter characterization. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbiological properties. Soil Science Society of America, Madison, WI, pp 581–594Google Scholar
  42. Scholander PF, Harmall HT, Baastreet ED, Hemminger EA (1965) Sap pressure in vascular plants. Science 148:339–346. doi: 10.1126/science.148.3668.339 PubMedCrossRefGoogle Scholar
  43. Sleeman JD, Dudley SA (2001) Phenotypic plasticity in carbon acquisition of rapid cycling Brassica rapa L. in response to light quality and water availability. Int J Plant Sci 162:297–307. doi: 10.1086/319584 CrossRefGoogle Scholar
  44. Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. WH Freeman Co., San FranciscoGoogle Scholar
  45. Sultan SE (1996) Phenotypic plasticity for offspring traits in Polygonum persicaria. Ecology 77:1791–1807. doi: 10.2307/2265784 CrossRefGoogle Scholar
  46. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542. doi: 10.1016/S1360-1385(00)01797-0 PubMedCrossRefGoogle Scholar
  47. Terradas J (1999) Holm oak and Holm oak forests: an introduction.In: Rodá F, Retana J, Gracia CA, Bellot JE (eds) Ecology of Mediterranean evergreen oak forests. Springer, Belin, pp 3–14Google Scholar
  48. van Tienderen PH (1997) Generalists, specialists, and the evolution of phenotypic plasticity in symmetric populations of distinct species. Evol Int J Org Evol 51:1372–1380. doi: 10.2307/2411189 Google Scholar
  49. Treseder KK, Vitousek PM (2001) Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii. Oecologia 126:266–275. doi: 10.1007/s004420000523 CrossRefGoogle Scholar
  50. Valladares F, Martínez-Ferri E, Balaguer L, Perez-Corona E, Manrique E (2000a) Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytol 148:79–91. doi: 10.1046/j.1469-8137.2000.00737.x CrossRefGoogle Scholar
  51. Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000b) Plastic phenotypic response to light of 16 congeneric shrubs from Panamanian rainforest. Ecology 81:1925–1936CrossRefGoogle Scholar
  52. Valladares F, Balaguer L, Martínez-Ferri E, Perez-Corona E, Manrique E (2002a) Plasticity, instability and canalization: is the phenotypic variation in saplings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytol 256:457–467. doi: 10.1046/j.1469-8137.2002.00525.x CrossRefGoogle Scholar
  53. Valladares F, Chico JM, Aranda I, Balaguer L, Dizengremel P, Manrique E et al (2002b) The greater sapling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees (Berl) 16:395–403Google Scholar
  54. 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 94:1103–1116. doi: 10.1111/j.1365-2745.2006.01176.x CrossRefGoogle Scholar
  55. Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. Tansley review. New Phytol 176:749–763. doi: 10.1111/j.1469-8137.2007.02275.x PubMedCrossRefGoogle Scholar
  56. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313Google Scholar
  57. Yamashita N, Koike N, Ishida A (2002) Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant Cell Environ 25:1341–1356. doi: 10.1046/j.1365-3040.2002.00907.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Francisco J. Baquedano
    • 1
  • Fernando Valladares
    • 2
    • 3
  • Federico J. Castillo
    • 4
    Email author
  1. 1.Departamento de Ciencias del Medio NaturalUniversidad Pública de NavarraPamplonaSpain
  2. 2.Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, CSICMadridSpain
  3. 3.Departamento de Biología y Geología. Escuela Superior de Ciencias Experimentales y TecnológicasUniversidad Rey Juan CarlosMóstolesSpain
  4. 4.Departamento de Ciencias del Medio NaturalUniversidad Pública de NavarraPamplonaSpain

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