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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

  • Global change ecology - Original Paper
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Abstract

Motivated by persistent predictions of warming and drying in the entire Mediterranean and other regions, we have examined the interactions of intrinsic water-use efficiency (W i) with environmental conditions in Pinus halepensis. We used 30-year (1974–2003) tree-ring records of basal area increment (BAI) and cellulose 13C and 18O composition, complemented by short-term physiological measurements, from three sites across a precipitation (P) gradient (280–700 mm) in Israel. The results show a clear trend of increasing W i in both the earlywood (EW) and latewood (LW) that varied in magnitude depending on site and season, with the increase ranging from ca. 5 to 20% over the study period. These W i trends were better correlated with the increase in atmospheric CO2 concentration, C a, than with the local increase in temperature (~0.04°C year−1), whereas age, height and density variations had minor effects on the long-term isotope record. There were no trends in P over time, but W i from EW and BAI were dependent on the interannual variations in P. From reconstructed C i values, we demonstrate that contrasting gas-exchange responses at opposing ends of the hydrologic gradient underlie the variation in W i sensitivity to C a between sites and seasons. Under the mild water limitations typical of the main seasonal growth period, regulation was directed at increasing C i/C a towards a homeostatic set-point observed at the most mesic site, with a decrease in the W i response to C i with increasing aridity. With more extreme drought stress, as seen in the late season at the drier sites, the response was W i driven, and there was an increase in the W i sensitivity to C a with aridity and a decreasing sensitivity of C i to C a. The apparent C a-driven increases in W i can help to identify the adjustments to drying conditions that forest ecosystems can make in the face of predicted atmospheric change.

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References

  • Affek HP, Krisch MJ, Yakir D (2006) Effects of intraleaf variations in carbonic anhydrase activity and gas exchange on leaf C18OO isoflux in Zea mays. New Phytol 169:321–329

    Article  PubMed  CAS  Google Scholar 

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–371

    Article  PubMed  Google Scholar 

  • Andreu L, Planells O, Gutiérrez E, Helle G, Schleser GH (2008) Climatic significance of tree-ring width and δ13C in a Spanish pine forest network. Tellus B 60:771–781

    Article  Google Scholar 

  • Angert A, Biraud S, Bonfils C, Henning CC, Buermann W, Pinzon J, Tucker CJ, Fung I (2005) Drier summers cancel out the CO2 uptake enhancement induced by warmer springs. Proc Natl Acad Sci USA 102:10823–10827

    Google Scholar 

  • Bar Massada A (2004) Multi-temporal assessment of above-ground forest biomass using allometric equations and aerial photographs (Masters thesis). Technion—Israel Institute of Technology, Haifa

  • Bert D, Leavitt SW, Dupouey JL (1997) Variations of wood δ13C and water-use efficiency of Abies alba during the last century. Ecology 78:1588–1596

    Google Scholar 

  • Betts RA, Boucher O, Collins M, Cox PM, Falloon PD, Gedney N, Hemming DL, Huntingford C, Jones CD, Sexton DMH, Webb MJ (2007) Projected increase in continental runoff due to plant responses to increasing carbon dioxide. Nature 448:1035–1037

    Google Scholar 

  • Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase oxygenase and the rate of respiration in the light—estimates from gas-exchange measurements on spinach. Planta 165:397–406

    Google Scholar 

  • Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley Centre climate model. J Hydrometeorol 7:1113–1125

    Google Scholar 

  • Cao L, Bala G, Caldeira K, Nemani R, Ban-Weiss G (2010) Importance of carbon dioxide physiological forcing to future climate change. Proc Natl Acad Sci USA 107:9513–9518

    Article  PubMed  CAS  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Rueda VM, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S et al. (eds) 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

  • Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533

    Google Scholar 

  • Dawson TE, Ward JK, Ehleringer JR (2004) Temporal scaling of physiological responses from gas exchange to tree rings: a gender-specific study of Acer negundo (Boxelder) growing under different conditions. Funct Ecol 18:212–222

    Article  Google Scholar 

  • de Luis M, Gričar J, Čufar K, Raventós J (2007) Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain. IAWA J 28:389–404

    Google Scholar 

  • Duquesnay A, Breda N, Stievenard M, Dupouey JL (1998) Changes of tree-ring δ13C and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell Environ 21:565–572

    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

    PubMed  Google Scholar 

  • Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13:281–292

    Article  CAS  Google Scholar 

  • Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effect in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic, San Diego, pp 47–70

  • 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 

  • Feng XH (1999) Trends in intrinsic water-use efficiency of natural trees for the past 100–200 years: a response to atmospheric CO2 concentration. Geochim Cosmochim Acta 63:1891–1903

    Google Scholar 

  • Ferrio JP, Voltas J (2005) Carbon and oxygen isotope ratios in wood constituents of Pinus halepensis as indicators of precipitation, temperature and vapour pressure deficit. Tellus Series B Chem Phys Meteorol 57:164–173

    Google Scholar 

  • Ferrio JP, Florit A, Vega A, Serrano L, Voltas J (2003) Δ13C and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis. Oecologia 137:512–518

    Article  PubMed  CAS  Google Scholar 

  • Field CB, Jackson RB, Mooney HA (1995) Stomatal responses to increased CO2—implications from the plant to the global-scale. Plant Cell Environ 18:1214–1225

    Google Scholar 

  • Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31

    Article  CAS  Google Scholar 

  • Gagen M, Finsinger W, Wagner-Cremer F, McCarroll D, Loader NJ, Robertson I, Jalkanen R, Young G, Kirchhefer A (2011) Evidence of changing intrinsic water-use efficiency under rising atmospheric CO2 concentrations in boreal Fennoscandia from subfossil leaves and tree ring δ13C ratios. Glob Chang Biol 17:1064–1072

    Google Scholar 

  • Gelfand I, Yakir D (2008) Influence of nitrite accumulation in association with seasonal patterns and mineralization of soil nitrogen in a semi-arid pine forest. Soil Biol Biochem 40:415–424

    Article  CAS  Google Scholar 

  • Gessler A, Brandes E, Buchmann N, Helle G, Rennenberg H, Barnard RL (2009) Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant Cell Environ 32:780–795

    Article  PubMed  CAS  Google Scholar 

  • Gindel J (1944) Aleppo pine as a medium for tree-ring analysis. Tree-Ring Bulltein 11:6–8

    Google Scholar 

  • Grünzweig JM, Lin T, Rotenberg E, Schwartz A, Yakir D (2003) Carbon sequestration in arid-land forest. Global Change Biology 9:791–799

    Article  Google Scholar 

  • Grünzweig JM, Gelfand I, Fried Y, Yakir D (2007) Biogeochemical factors contributing to enhanced carbon storage following afforestation of a semi-arid shrubland. Biogeosciences 4:891–904

    Article  Google Scholar 

  • Harley PC, Loreto F, Dimarco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436

    Article  PubMed  CAS  Google Scholar 

  • Hemming DL, Switsur VR, Waterhouse JS, Heaton THE, Carter AHC (1998) Climate variation and the stable carbon isotope composition of tree ring cellulose: an intercomparison of Quercus robur, Fagus sylvatica and Pinus silvestris. Tellus Series B Chem Phys Meteorol 50:25–33

    Google Scholar 

  • Hemming D, Fritts HC, Leavitt SW, Wright W, Long A, Shashkin A (2001) Modelling tree-ring δ13C. Dendrochronologia 19:23–38

    Google Scholar 

  • Hemming D, Yakir D, Ambus P, Aurela M, Besson C, Black K, Buchmann N, Burlett R, Cescatti A, Clement R, Gross P, Granier A, Grunwald T, Havrankova K, Janous D, Janssens IA, Knohl A, Ostner BK, Kowalski A, Laurila T, Mata C, Marcolla B, Matteucci G, Moncrieff J, Moors EJ, Osborne B, Pereira JS, Pihlatie M, Pilegaard K, Ponti F, Rosova Z, Rossi F, Scartazza A, Vesala T (2005) Pan-European δ13C values of air and organic matter from forest ecosystems. Glob Chang Biol 11:1065–1093

    Google Scholar 

  • Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bulletin 43:69–75

    Google Scholar 

  • Klein T, Hemming D, Lin TB, Grunzweig JM, Maseyk K, Rotenberg E, Yakir D (2005) Association between tree-ring and needle δ13C and leaf gas exchange in Pinus halepensis under semi-arid conditions. Oecologia 144:45–54

    Google Scholar 

  • Kohler IH, Poulton PR, Auerswald K, Schnyder H (2010) Intrinsic water-use efficiency of temperate seminatural grassland has increased since 1857: an analysis of carbon isotope discrimination of herbage from the Park Grass Experiment. Global Change Biology 16:1531–1541

    Article  Google Scholar 

  • Leavitt SW (2010) Tree-ring C–H–O isotope variability and sampling. Sci Total Environ 408:5244–5253

    Article  PubMed  CAS  Google Scholar 

  • Leavitt SW, Danzer SR (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65:87–89

    Article  CAS  Google Scholar 

  • Leavitt SW, Lara A (1994) South-American tree rings show declining δ13C trend. Tellus Series B Chem Phys Meteorol 46:152–157

    Google Scholar 

  • Leavitt SW, Long A (1991) Seasonal stable-carbon isotope variability in tree rings—possible paleoenvironmental signals. Chem Geol 87:59–70

    CAS  Google Scholar 

  • Leavitt SW, Wright WE, Long A (2002) Spatial expression of ENSO, drought, and summer monsoon in seasonal δ13C of ponderosa pine tree rings in southern Arizona and New Mexico. J Geophys Res Atmospheres 107:110

    Google Scholar 

  • Leavitt SW, Idso SB, Kimball BA, Burns JM, Sinha A, Stott L (2003) The effect of long-term atmospheric CO2 enrichment on the intrinsic water-use efficiency of sour orange trees. Chemosphere 50:217–222

    Article  PubMed  CAS  Google Scholar 

  • Linares JC, Delgado-Huertas A, Camarero JJ, Merino J, Carreira JA (2009) Competition and drought limit the response of water-use efficiency to rising atmospheric carbon dioxide in the Mediterranean fir Abies pinsapo. Oecologia 161:611–624

    Article  PubMed  Google Scholar 

  • Liphschitz N, Levyadun S, Rosen E, Waisel Y (1984) The annual rhythm of activity of the lateral meristems (cambium and phellogen) in Pinus halepensis Mill and Pinus pinea L. IAWA Bull 5:263–274

  • Marshall JD, Monserud RA (1996) Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105:13–21

    Article  Google Scholar 

  • Maseyk K, Grunzweig JM, Rotenberg E, Yakir D (2008a) Respiration acclimation contributes to high carbon-use efficiency in a seasonally dry pine forest. Global Change Biology 14:1553–1567

    Article  Google Scholar 

  • Maseyk KS, Lin T, Rotenberg E, Gruenzweig JM, Schwartz A, Yakir D (2008b) Physiology–phenology interactions in a productive semi-arid pine forest. New Phytol 178:603–616

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

    Google Scholar 

  • McDowell NG, Licata J, Bond BJ (2005) Environmental sensitivity of gas exchange in different-sized trees. Oecologia 145:9–20

    Article  PubMed  Google Scholar 

  • McDowell NG, Adams HD, Bailey JD, Hess M, Kolb TE (2006) Homeostatic maintenance of ponderosa pine gas exchange in response to stand density changes. Ecol Appl 16:1164–1182

    Article  PubMed  Google Scholar 

  • Monserud RA, Marshall JD (2001) Time-series analysis of δ13C from tree rings. I. Time trends and autocorrelation. Tree Physiol 21:1087–1102

    PubMed  CAS  Google Scholar 

  • Ne’eman G, Trabaud L (eds) (2000) Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean Basin. Backhuys, Laiden

  • Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280

    Article  Google Scholar 

  • Ogée J, Cuntz M, Peylin P, Bariac T (2007) Non-steady-state, non-uniform transpiration rate and leaf anatomy effects on the progressive stable isotope enrichment of leaf water along monocot leaves. Plant Cell Environ 30:367–387

    Article  PubMed  Google Scholar 

  • Ogée J, Barbour MM, Wingate L, Bert D, Bosc A, Stievenard M, Lambrot C, Pierre M, Bariac T, Loustau D, Dewar RC (2009) A single-substrate model to interpret intra-annual stable isotope signals in tree-ring cellulose. Plant Cell Environ 32:1071–1090

    Google Scholar 

  • Peñuelas J, Hunt JM, Ogaya R, Jump AS (2008) Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Global Change Biology 14:1076–1088

    Article  Google Scholar 

  • Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361:61–64

    Article  Google Scholar 

  • Robertson I, Switsur VR, Carter AHC, Barker AC, Waterhouse JS, Briffa KR, Jones PD (1997) Signal strength and climate relationships in C-13/C-12 ratios of tree ring cellulose from oak in east England. J Geophys Res Atmospheres 102:19507–19516

    Google Scholar 

  • Rotenberg E, Yakir D (2010) Contribution of semi-arid forests to the climate system. Science 327:451–454

    Article  PubMed  CAS  Google Scholar 

  • Sarris D, Christodoulakis D, Korner C (2007) Recent decline in precipitation and tree growth in the eastern Mediterranean. Global Change Biology 13:1187–1200

    Article  Google Scholar 

  • Saurer M, Siegwolf RTW, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Global Change Biology 10:2109–2120

    Article  Google Scholar 

  • Seibt U, Wingate L, Berry JA, Lloyd J (2006) Non-steady state effects in diurnal 18O discrimination by Picea sitchensis branches in the field. Plant Cell Environ 29:928–939

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Sternberg LSL (1989) Oxygen and hydrogen isotope measurements in plant cellulose analysis. In: Linskens HF, Jackson JF (eds) Plant fibres: modern methods of plant analysis. Springer, Berlin

  • Tognetti R, Michelozzi M, Giovannelli A (1997) Geographical variation in water relations, hydraulic architecture and terpene composition of Aleppo pine seedlings from Italian provenances. Tree Physiol 17:241–250

    PubMed  CAS  Google Scholar 

  • Trenberth KE, Jones PD, Ambenje P, Bojariu R, Easterling D, Tank AK, Parker D, Rahimzadeh F, Renwick JA, Rusticucci M, Soden B, Zhai P (2007) Observations: surface and atmospheric climate change. In: Solomon S et al. (eds) 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, pp 235–336

  • Voltas J, Chambel M, Prada M, Ferrio J (2008) Climate-related variability in carbon and oxygen stable isotopes among populations of Aleppo pine grown in common-garden tests. Trees-Struct Funct 22:759–769

    CAS  Google Scholar 

  • Walcroft AS, Silvester WB, Whitehead D, Kelliher FM (1997) Seasonal changes in stable carbon isotope ratios within annual rings of Pinus radiata reflect environmental regulation of growth processes. Aust J Plant Physiol 24:57–68

    Google Scholar 

  • Ward JK, Dawson TE, Ehleringer JR (2002) Responses of Acer negundo genders to interannual differences in water availability determined from carbon isotope ratios of tree ring cellulose. Tree Physiol 22:339–346

    PubMed  CAS  Google Scholar 

  • Warren CR, McGrath JF, Adams MA (2001) Water availability and carbon isotope discrimination in conifers. Oecologia 127:476–486

    Article  Google Scholar 

  • Waterhouse JS, Switsur VR, Barker AC, Carter AHC, Hemming DL, Loader NJ, Robertson I (2004) Northern European trees show a progressive diminishing response to increasing atmospheric carbon dioxide concentrations. Quat Sci Rev 23:803–810

    Google Scholar 

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Acknowledgments

Jim Burns of the Laboratory of Tree-Ring Research dated the samples and measured ring widths. Pablo Garcia of LTRR helped to prepare the α-cellulose from the rings. This research was supported by grants from the International Arid Land Consortium (IALC) and GLOWA-Jordan River, The Henry Gutwirth Fund for Research and the Philip M. Klutznick Fund for Research. DH and DY acknowledge the financial support provided through the European Community’s Human Potential Programme under contract HPRN-CT-1999-00059, NETCARB. AA was supported by a Weizmann Institute Postdoctoral Fellowship. We also thank three anonymous reviewers and the Handling Editor whose comments have helped produce a better manuscript.

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  1. Kadmiel Maseyk

    Present address: BIOEMCO (UMR 7618), Université Pierre et Marie Curie, 78850, Thiverval-Grignon, France

  2. Debbie Hemming

    Present address: Met Office Hadley Centre, Fitzroy Road, Exeter, UK

  3. Alon Angert

    Present address: Institute of Earth Sciences, Hebrew University, Jerusalem, Israel

Authors and Affiliations

  1. Department of Environmental Sciences and Energy Research, Weizmann Institute of Science, 76100, Rehovot, Israel

    Kadmiel Maseyk, Debbie Hemming, Alon Angert & Dan Yakir

  2. Laboratory of Tree-Ring Research, University of Arizona, Tucson, AZ, 85721, USA

    Steven W. Leavitt

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  1. Kadmiel Maseyk
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Correspondence to Dan Yakir.

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Communicated by Todd Dawson.

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Maseyk, K., Hemming, D., Angert, A. et al. 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 (2011). https://doi.org/10.1007/s00442-011-2010-4

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