Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

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.

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 142:472–479

    Google Scholar 

  • Baquedano FJ, Castillo FJ (2007) Drought tolerance in the Mediterranean species Quercus coccifera, Quercus ilex, Pinus halepensis, and Juniperus phoenicea. Photosynthetica 45(2):229–238

    Article  Google Scholar 

  • Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94

    Article  CAS  Google Scholar 

  • 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 261:193–202

    Article  Google Scholar 

  • 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 188:1099–1112

    Article  CAS  PubMed  Google Scholar 

  • 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 197:544–554

    Article  CAS  PubMed  Google Scholar 

  • 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 37:382–391

    Article  CAS  PubMed  Google Scholar 

  • Battipaglia G, Micco V, Fournier T, Aronne G, Carcaillet C (2014b) Isotopic and anatomical signals for interpreting fire-related responses in Pinus halepensis. Trees 28:1095–1104

    Article  Google Scholar 

  • Biondi F (1999) Comparing tree-ring chronologies and repeated timber inventories as forest monitoring tools. Ecol Appl 9:216–227

    Article  Google Scholar 

  • 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 162:107–113

    Article  Google Scholar 

  • 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):4603–4612

    Article  CAS  PubMed  Google Scholar 

  • 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 177–210

    Chapter  Google Scholar 

  • 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):49–56

    Article  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Bio 30:239–264

    Article  CAS  Google Scholar 

  • 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 78:119–148

    Article  PubMed  Google Scholar 

  • Correia OA, Catarino FM (1994) Seasonal changes in soil-to-leaf resistance in Cistus sp. and Pistacia lentiscus. Acta Oecol 15:289–300

    Google Scholar 

  • Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95:565–574

    Article  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815

    Article  Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable Isotopes in Plant Ecology. Annu Rev Ecol Evol S 33:507–509

    Article  Google Scholar 

  • 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 34:1873–1892

    Article  Google Scholar 

  • Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15:105–111

    Article  PubMed  Google Scholar 

  • 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 9:121–137

    Article  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Phys 40:503–537

    Article  CAS  Google Scholar 

  • 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 107:277–283

    Article  Google Scholar 

  • 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 137:512–518

    Article  CAS  PubMed  Google Scholar 

  • 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 22:33–43

    Article  Google Scholar 

  • 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 51:170–193

    Article  Google Scholar 

  • 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 175:81–93

    Article  PubMed  Google Scholar 

  • 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 34:796–818

    Article  CAS  PubMed  Google Scholar 

  • Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global Planet Change 63:90–104

    Article  Google Scholar 

  • Gratani L, Varone L (2006) Long-time variations in leaf mass and area of Mediterranean evergreen broad-leaf and narrow-leaf maquis species. Photosynthetica 44:161–168

    Article  Google Scholar 

  • Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2010) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207:233–244

    Article  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends in Plant Sci 3:224–230

    Article  Google Scholar 

  • Kaennel M, Schweingruber FH (1995) Multilingual glossary of dendrochronology: terms and definitions in English, German, French, Spanish, Italian, Portuguese and Russian. Birmensdorf, Berne

  • 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 302:34–42

    Article  Google Scholar 

  • Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst Int J Deal Asp Plant Biol 134:279–295

    Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Academic Press, New York

    Google Scholar 

  • 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 29:79–86

    Article  Google Scholar 

  • 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 

  • 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 259:698–709

    Article  Google Scholar 

  • 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 20:131–138

    Article  PubMed  Google Scholar 

  • Martınez-Vilalta J, Poyatos R, Aguade D, Retana J, Mencuccini M (2014) A new look at water transport regulation in plants. New Phytol 204:105–115

    Article  PubMed  Google Scholar 

  • 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 167:573–585

    Article  PubMed  Google Scholar 

  • McCarrol D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801

    Article  Google Scholar 

  • 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 317:17–29

    Article  CAS  Google Scholar 

  • 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):2599–2610

    Article  Google Scholar 

  • 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 35:1026–1039

    Article  Google Scholar 

  • 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 196:489–496

    Article  PubMed  Google Scholar 

  • 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 29:15–25

    Article  Google Scholar 

  • Ogaya R, Peñuelas J (2008) Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability. Acta Oecol 34:331–338

    Article  Google Scholar 

  • 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 200:527–534

    Google Scholar 

  • 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 20:597–608

    Article  Google Scholar 

  • 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 12:303–316

    Article  Google Scholar 

  • 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 166:45–57

    Article  PubMed  Google Scholar 

  • 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 176:581–594

    Article  PubMed  Google Scholar 

  • Schweingruber FH (1996) Tree Rings and Environment. Dendroecology. Birmensdorf, Berne

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    Article  PubMed  Google Scholar 

  • 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 125:350–357

    Article  Google Scholar 

  • 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 49:419–432

    Article  Google Scholar 

  • 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 339–354

  • Tognetti R, Cherubini P, Innes JL (2000) Comparative stem-growth rates of Mediterranean trees under background and naturally enhanced ambient CO2 concentrations. New Phytol 146:59–74

    Article  Google Scholar 

  • 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 148:79–91

    Article  CAS  Google Scholar 

  • 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, Spain

  • Vilagrosa A, Cortina J, Gil-Pelegrin E, Bellot J (2003) Suitability of drought-preconditioning techniques in Mediterranean climate. Restor Ecol 11:208–216

    Article  Google Scholar 

  • Villar-Salvador P (2000) Estrategias ecolóagicas y funcionales del xilema en plantas lenósas mediterraneas. PhD thesis. Universidad de Valencia, Spain

  • 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):443–450

    Article  Google Scholar 

  • 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 66:157–160

    Article  Google Scholar 

  • 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 29:192–201

    Article  CAS  PubMed  Google Scholar 

  • 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 10:288–292

    Google Scholar 

  • 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 20:15–23

    Article  Google Scholar 

  • 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 212:127–142

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, Second University of Naples, via Vivaldi 43, 81100, Caserta, Italy

    Simona Altieri, Simona Castaldi, Carmina Sirignano, Carmine Lubritto & Giovanna Battipaglia

  2. Dipartimento di Scienze della Natura e del Territorio (DipNET), Università degli Studi di Sassari, Sassari, Italy

    Simone Mereu

  3. CMCC, Euro-Mediterranean Center on Climate Change, IAFES Division (Sassari), Sassari, Italy

    Simone Mereu

  4. Swiss Federal Research Institute, WSL, 8903, Birmensdorf, Switzerland

    Paolo Cherubini

  5. Ecole Pratique des Hautes Etudes (PALECO EPHE), Centre for Bio-Archaeology and Ecology, Institut de Botanique, University of Montpellier 2, 34090, Montpellier, France

    Giovanna Battipaglia

  6. Euro-Mediterranean Center on Climate Change (CMCC), Via Augusto Imperatore 16, 73100, Lecce, Italy

    Simona Castaldi & Giovanna Battipaglia

Authors
  1. Simona Altieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simone Mereu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paolo Cherubini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Simona Castaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carmina Sirignano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carmine Lubritto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giovanna Battipaglia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simona Altieri.

Additional information

Communicated by E. Liang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Altieri, S., Mereu, S., Cherubini, P. et al. Tree-ring carbon and oxygen isotopes indicate different water use strategies in three Mediterranean shrubs at Capo Caccia (Sardinia, Italy). Trees 29, 1593–1603 (2015). https://doi.org/10.1007/s00468-015-1242-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-015-1242-z

Keywords

Search

Navigation