, Volume 29, Issue 5, pp 1593–1603 | Cite as

Tree-ring carbon and oxygen isotopes indicate different water use strategies in three Mediterranean shrubs at Capo Caccia (Sardinia, Italy)

  • Simona Altieri
  • Simone Mereu
  • Paolo Cherubini
  • Simona Castaldi
  • Carmina Sirignano
  • Carmine Lubritto
  • Giovanna Battipaglia
Original Article
Part of the following topical collections:
  1. Tree Rings


Key message

Variations in stable carbon and oxygen isotope compositions of co-occurring plant species reflect their different water use strategies and indicate the importance of screening species’ WUE i to plan climate change adaptation strategies.


The different abilities of plant species to cope with drought have been associated with structural and ecophysiological constraints. In this paper, we evaluate interspecific differences in intrinsic water use efficiency (WUE i ) and the ratio of photosynthesis (A) to stomatal conductance (gs) in three co-occurring Mediterranean shrubs: two broad-leaved evergreen (Pistacia lentiscus and Phillyrea angustifolia) and one needle-like-leaved evergreen (Juniperus phoenicea). We used δ13C in rings to assess inter-annual changes in WUE i while the influence of the stomatal conductance was explored through δ18O. Our results indicate consistent differences in WUE i in the three species, largely determined by leaf traits and differences in stomatal conductance control. Juniperus phoenicea could be the most threatened by the current trend of increasing temperature and summers drought. Phillyrea angustifolia and P. lentiscus seem to be less affected by drought stress because of their tighter stomatal control and high survival rate under field conditions. Our study shows that shrubs with different leaf traits employ different plant ecophysiological strategies under drought stress.


Mediterranean species Tree rings Water use efficiency δ18



This research was supported financially by the MIUR (Italian Ministry of Education, Universities and Research) through the PRIN “CARBOTREES” project. This study is linked to activities conducted within the COST FP1106 ‘STReESS’ network. The authors thank Dr. Curtis Gautschi for the language revision.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Arena C, Vitale L, Virzo de Santo A (2008) Photosynthesis and photoprotective strategies in Laurus nobilis L. and Quercus ilex L. under summer drought and winter cold. Plant Biosyst Int J Deal Asp Plant Biol 142:472–479Google Scholar
  2. Baquedano FJ, Castillo FJ (2007) Drought tolerance in the Mediterranean species Quercus coccifera, Quercus ilex, Pinus halepensis, and Juniperus phoenicea. Photosynthetica 45(2):229–238CrossRefGoogle Scholar
  3. Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94CrossRefGoogle Scholar
  4. Battipaglia G, Jäggi M, Surer M, Siegwolf RTW, Cotrufo MF (2008) Climatic sensitivity of δ18O in the wood and cellulose of tree rings: results from a mixed stand of Acer pseudoplatanus L. and Fagus sylvatica. Palaeogeogr Palaeoclimatol Palaeoecol 261:193–202CrossRefGoogle Scholar
  5. Battipaglia G, De Micco V, Brand WA, Linke P, Aronne G, Saurer M, Cherubini P (2010) Variations of vessel diameter and delta 13C in false rings of Arbutus unedo L. reflect different environmental conditions. New Phytol 188:1099–1112CrossRefPubMedGoogle Scholar
  6. Battipaglia G, Saurer M, Cherubini P, Calfapietra C, McCarthy HR, Norby RJ, Cotrufo MF (2013) Elevated CO2 increases tree-level intrinsic water use efficiency: insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites. New Phytol 197:544–554CrossRefPubMedGoogle Scholar
  7. Battipaglia G, De Micco V, Brand WA, Saurer M, Aronne G, Linke P, Cherubini P (2014a) Drought impact on water use efficiency and intra-annual density fluctuations in Erica arborea on Elba (Italy). Plant Cell Environ 37:382–391CrossRefPubMedGoogle Scholar
  8. Battipaglia G, Micco V, Fournier T, Aronne G, Carcaillet C (2014b) Isotopic and anatomical signals for interpreting fire-related responses in Pinus halepensis. Trees 28:1095–1104CrossRefGoogle Scholar
  9. Biondi F (1999) Comparing tree-ring chronologies and repeated timber inventories as forest monitoring tools. Ecol Appl 9:216–227CrossRefGoogle Scholar
  10. Blanco MJ, Rodríguez P, Morales MA, Ortuño MF, Torrecillas A (2002) Comparative growth and water relations of Cistus albidus and Cistus montpeliensis plants during water deficit conditions and recovery. Plant Sci 162:107–113CrossRefGoogle Scholar
  11. Boettger T, Haupt M, Knöller K et al (2007) Wood cellulose preparation methods and mass spectrometric analyses of δ13C, δ18O, and nonexchangeable δ2H values in cellulose, sugar, and starch: an interlaboratory comparison. Anal Chem 79(12):4603–4612CrossRefPubMedGoogle Scholar
  12. Canadell J, Zedler PH (1995) Underground structures of woody plants in Mediterranean ecosystems of Australia, California, and Chile. In: Fox M, Kalin M, Zedler PH (eds) Ecology and biogeography of Mediterranean ecosystems in Chile, California and Australia. Verlag, Berlin, pp 177–210CrossRefGoogle Scholar
  13. Castillo JM, Rubio Casal AE, Luque CJ, Luque T, Figueroa ME (2002) Comparative field summer stress of three tree species co-occurring in Mediterranean coastal dunes. Photosintetica 40(1):49–56CrossRefGoogle Scholar
  14. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Bio 30:239–264CrossRefGoogle Scholar
  15. Cherubini P, Gartner BL, Tognetti R, Bräker OU, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from Mediterranean climate. Biol Rev 78:119–148CrossRefPubMedGoogle Scholar
  16. Correia OA, Catarino FM (1994) Seasonal changes in soil-to-leaf resistance in Cistus sp. and Pistacia lentiscus. Acta Oecol 15:289–300Google Scholar
  17. Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95:565–574CrossRefGoogle Scholar
  18. Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815CrossRefGoogle Scholar
  19. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable Isotopes in Plant Ecology. Annu Rev Ecol Evol S 33:507–509CrossRefGoogle Scholar
  20. Di Filippo A, Biondi F, Cufar K, de Luis M, Grabner M et al (2007) Bioclimatology of beech (Fagus sylvatica L.) in the Eastern Alps: spatial and altitudinal climatic signals identified through a tree-ring network. J Biogeogr 34:1873–1892CrossRefGoogle Scholar
  21. Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15:105–111CrossRefPubMedGoogle Scholar
  22. 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
  23. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Phys 40:503–537CrossRefGoogle Scholar
  24. Fernández JA, Balenzategui L, Bañón S, Franco JA (2006) Induction of drought tolerance by paclobutrazol and irrigation deficit in Phillyrea angustifolia during the nursery period. Sci Horticu 107:277–283CrossRefGoogle Scholar
  25. Ferrio JP, Florit A, Vega A, Serrano L, Voltas J (2003) Delta C-13 and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis. Oecologia 137:512–518CrossRefPubMedGoogle Scholar
  26. Flexas J, Gulías J, Jonasson S, Medrano H, Mus M (2001) Seasonal patterns and control of gas exchange in local populations of the Mediterranean evergreen shrub Pistacia lentiscus L. Acta Oecol 22:33–43CrossRefGoogle Scholar
  27. Francey RJ, Allison CE, Etheridge D, Trudinger CM, Enting IG, Leuenberger M, Langenfelds RL, Michel E, Steele LP (1999) A 1000-year high precision record of δ13C in atmospheric CO2. Tellus B 51:170–193CrossRefGoogle Scholar
  28. Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93CrossRefPubMedGoogle Scholar
  29. Gessler A, Ferrio JP, Hommel R, Treydte K, Werner RA, Monson RK (2014) Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood. Tree Physiol 34:796–818CrossRefPubMedGoogle Scholar
  30. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global Planet Change 63:90–104CrossRefGoogle Scholar
  31. Gratani L, Varone L (2006) Long-time variations in leaf mass and area of Mediterranean evergreen broad-leaf and narrow-leaf maquis species. Photosynthetica 44:161–168CrossRefGoogle Scholar
  32. Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2010) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207:233–244CrossRefGoogle Scholar
  33. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends in Plant Sci 3:224–230CrossRefGoogle Scholar
  34. Kaennel M, Schweingruber FH (1995) Multilingual glossary of dendrochronology: terms and definitions in English, German, French, Spanish, Italian, Portuguese and Russian. Birmensdorf, BerneGoogle Scholar
  35. Klein T, Shpringer I, Fikler B, Elbaz G, Cohen S, Yakir D (2013) Relationship between stomatal regulation, water-use, and water-use efficiency of two coexisting key Mediterranean tree species. Forest Ecol Manag 302:34–42CrossRefGoogle Scholar
  36. Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst Int J Deal Asp Plant Biol 134:279–295Google Scholar
  37. Levitt J (1980) Responses of plants to environmental stresses. Academic Press, New YorkGoogle Scholar
  38. Liang E, Liu W, Ren P, Dawadi B, Eckstein D (2015) The alpine dwarf shrub Cassiope fastigiata in the Himalayas: does it reflect site-specific climatic signals in its annual growth rings? Trees 29:79–86CrossRefGoogle Scholar
  39. Linares JC, Camarero JJ (2012) Silver fir defoliation likelihood is related to negative growth trends and high warming sensitivity at their southernmost distribution limit. ISRN For. doi: 10.5402/2012/437690 Google Scholar
  40. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer M, Marchetti M (2010) Climate change impacts, adaptive capacity and vulnerability of European forest ecosystems. Forest Ecol Manag 259:698–709CrossRefGoogle Scholar
  41. Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerance tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138CrossRefPubMedGoogle Scholar
  42. Martınez-Vilalta J, Poyatos R, Aguade D, Retana J, Mencuccini M (2014) A new look at water transport regulation in plants. New Phytol 204:105–115CrossRefPubMedGoogle Scholar
  43. Maseyk K, Hemming D, Angert A, Leavitt SW, Yakir D (2011) Increase in water-use efficiency and underlying processes in pine forests across a precipitation gradient in the dry Mediterranean region over the past 30 years. Oecologia 167:573–585CrossRefPubMedGoogle Scholar
  44. McCarrol D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801CrossRefGoogle Scholar
  45. Medrano H, Flexas J, Galmés J (2009) Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. Plant Soil 317:17–29CrossRefGoogle Scholar
  46. Mereu S, Salvatori E, Fusaro L, Gerosa G, Muys B, Manes F (2009) An integrated approach shows different use of water resources from Mediterranean maquis species in a coastal dune ecosystem. Biogeosciences 6(11):2599–2610CrossRefGoogle Scholar
  47. Moreno-Gutiérrez C, Battipaglia G, Cherubini P, Saurer M, Nicolás E, Contreras S, Querejeta JI (2012a) Stand structure modulates the longterm vulnerability of Pinus halepensis to climatic drought in a semiarid Mediterranean ecosystem. Plant, Cell Environ 35:1026–1039CrossRefGoogle Scholar
  48. Moreno-Gutiérrez C, Dawson TE, Nicolás E, Querejeta JI (2012b) Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytol 196:489–496CrossRefPubMedGoogle Scholar
  49. Moreno-Gutiérrez C, Battipaglia G, Cherubini P, Delgado Huertas A, Querejeta JI (2015) Pine afforestation decreases the long-term performance of understorey shrubs in a semi-arid Mediterranean ecosystem: a stable isotope approach. Funct Ecol 29:15–25CrossRefGoogle Scholar
  50. Ogaya R, Peñuelas J (2008) Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability. Acta Oecol 34:331–338CrossRefGoogle Scholar
  51. Palacio S, Milla RN, Montserrat-Mart G (2005) A phenological hypothesis on the thermophilous distribution of Pistacia lentiscus L. Flora—Morphology, Distribution, Functional. Ecol Plants 200:527–534Google Scholar
  52. Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Glob Ecol Biogeogr 20:597–608CrossRefGoogle Scholar
  53. Pumo D, Viola F, Noto LV (2008) Ecohydrology in Mediterranean areas: a numerical model to describe growing seasons out of phase with precipitations. Hydrol Earth Syst Sc 12:303–316CrossRefGoogle Scholar
  54. Quero JL, Sterch FJ, Martínez-Vilalta J, Villar R (2011) Water-use strategies of six co-existing Mediterranean woody species during a summer drought. Oecologia 166:45–57CrossRefPubMedGoogle Scholar
  55. Scartazza A, Vaccari FP, Bertolini T, Di Tommasi P, Lautieri M, Miglietta F, Brugnoli E (2014) Comparing integrated stable isotope and eddy covariance estimates of water-use efficiency on a Mediterranean successional sequence. Oecologia 176:581–594CrossRefPubMedGoogle Scholar
  56. Schweingruber FH (1996) Tree Rings and Environment. Dendroecology. Birmensdorf, BerneGoogle Scholar
  57. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454CrossRefPubMedGoogle Scholar
  58. Sheidegger Y, Saurer M, Bahn M, Siegwolf RTW (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357CrossRefGoogle Scholar
  59. Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand, modeling isohydric and anisohydric behaviors. J Exp Bot 49:419–432CrossRefGoogle Scholar
  60. Tenhunen JD, Harley PC, Beyschlag W, Lange OL (1987) A model of net photosynthesis for leaves of the sclerophyll Quercus coccifera. In: Tenhunen J, Catarino F, Lange O, Oechel W (eds) Plant response to stress. NATO ASI Series, Vol. G15. Verlag, Berlin, pp 339–354Google Scholar
  61. Tognetti R, Cherubini P, Innes JL (2000) Comparative stem-growth rates of Mediterranean trees under background and naturally enhanced ambient CO2 concentrations. New Phytol 146:59–74CrossRefGoogle Scholar
  62. Valladares F, Martínez-Ferri E, Balaguer L, Perez-Corona E, Manrique E (2000) Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytol 148:79–91CrossRefGoogle Scholar
  63. Vilagrosa A (2002) Estrategias de Resistencia al Déficit Hídrico en Pistacia lentiscus L. y Quercus coccifera L. Implicaciones en la repoblacion forestal. PhD thesis. Universidad de Alicante, SpainGoogle Scholar
  64. Vilagrosa A, Cortina J, Gil-Pelegrin E, Bellot J (2003) Suitability of drought-preconditioning techniques in Mediterranean climate. Restor Ecol 11:208–216CrossRefGoogle Scholar
  65. Villar-Salvador P (2000) Estrategias ecolóagicas y funcionales del xilema en plantas lenósas mediterraneas. PhD thesis. Universidad de Valencia, SpainGoogle Scholar
  66. Vitale L, Arena C, Virzo De Santo A (2012) Seasonal change in photosynthetic activity and photochemical efficiency of the Mediterranean shrub Phillyrea angustifolia L. Plant Biosyst 146(2):443–450CrossRefGoogle Scholar
  67. Waring RH, McDonald AJS, Larsson S, Ericcson T, Wiren A, Ericcson A, Lohammar T (1985) Differences in chemical compositions of plants grown at constant relative growth rates with stable mineral nutrition. Oecologia 66:157–160CrossRefGoogle Scholar
  68. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201CrossRefPubMedGoogle Scholar
  69. Werner C, Correia O (1996) Photoinhibition in cork-oak leaves under stress: influence of the bark-stripping on the chlorophyll fluorescence emission in Quercus suber L. Trees Struct Funct 10:288–292Google Scholar
  70. Werner C, Correia O, Beyschlag W (1999) Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol 20:15–23CrossRefGoogle Scholar
  71. Zunzunegui M, Díaz Barradas MC, Ain-Lhout F, Alvarez-Cansino L, Esquivias MP, García Novo F (2011) Seasonal physiological plasticity and recovery capacity after summer stress in Mediterranean scrub communities. Plant Ecol 212:127–142CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Simona Altieri
    • 1
  • Simone Mereu
    • 2
    • 3
  • Paolo Cherubini
    • 4
  • Simona Castaldi
    • 1
    • 6
  • Carmina Sirignano
    • 1
  • Carmine Lubritto
    • 1
  • Giovanna Battipaglia
    • 1
    • 5
    • 6
  1. 1.Department of Environmental, Biological and Pharmaceutical Sciences and TechnologiesSecond University of NaplesCasertaItaly
  2. 2.Dipartimento di Scienze della Natura e del Territorio (DipNET)Università degli Studi di SassariSassariItaly
  3. 3.CMCC, Euro-Mediterranean Center on Climate Change, IAFES Division (Sassari)SassariItaly
  4. 4.Swiss Federal Research InstituteWSLBirmensdorfSwitzerland
  5. 5.Ecole Pratique des Hautes Etudes (PALECO EPHE), Centre for Bio-Archaeology and Ecology, Institut de BotaniqueUniversity of Montpellier 2MontpellierFrance
  6. 6.Euro-Mediterranean Center on Climate Change (CMCC)LecceItaly

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