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Drought-induced increase in water-use efficiency reduces secondary tree growth and tracheid wall thickness in a Mediterranean conifer

  • Global change ecology - Original research
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Abstract

In order to understand the impact of drought and intrinsic water-use efficiency (iWUE) on tree growth, we evaluated the relative importance of direct and indirect effects of water availability on secondary growth and xylem anatomy of Juniperus thurifera, a Mediterranean anisohydric conifer. Dendrochronological techniques, quantitative xylem anatomy, and 13C/12C isotopic ratio were combined to develop standardized chronologies for iWUE, BAI (basal area increment), and anatomical variables on a 40-year-long annually resolved series for 20 trees. We tested the relationship between iWUE and secondary growth at short-term (annual) and long-term (decadal) temporal scales to evaluate whether gains in iWUE may lead to increases in secondary growth. We obtained a positive long-term correlation between iWUE and BAI, simultaneously with a negative short-term correlation between them. Furthermore, BAI and iWUE were correlated with anatomical traits related to carbon sink or storage (tracheid wall thickness and ray parenchyma amount), but no significant correlation with conductive traits (tracheid lumen) was found. Water availability during the growing season significantly modulated tree growth at the xylem level, where growth rates and wood anatomical traits were affected by June precipitation. Our results are consistent with a drought-induced limitation of tree growth response to rising CO2, despite the trend of rising iWUE being maintained. We also remark the usefulness of exploring this relationship at different temporal scales to fully understand the actual links between iWUE and secondary growth dynamics.

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References

  • Andreu L, Planells O, Gutierrez E, Helle G, Schleser GH (2008) Climatic significance of tree-ring width and δ13 C in a Spanish pine forest network. Tellus B 60:771–781

    Article  Google Scholar 

  • Arbuckle JL (2009) Amos 18 user’s guide. SPSS Inc, Chicago

    Google Scholar 

  • Barber VA, Juday GP, Finney BP (2000) Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. Nature 405:668–673. doi:10.1038/35015049

    Article  CAS  PubMed  Google Scholar 

  • Bert D, Leavitt SW, Dupouey J-L (1997) Variations of wood δ13C and water-use efficiency of Abies alba during the last century. Ecology 78:1588–1596. doi:10.1890/0012-9658(1997)078[1588:VOWCAW]2.0.CO;2

    Google Scholar 

  • Biondi F, Qeadan F (2008) A theory-driven approach to tree-ring standardization: defining the biological trend from expected basal area increment. Tree-Ring Res 64:81–96. doi:10.3959/2008-6.1

    Article  Google Scholar 

  • Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol 185:471–480. doi:10.1111/j.1469-8137.2009.03073.x

    Article  PubMed  Google Scholar 

  • Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366. doi:10.1111/j.1461-0248.2009.01285.x

    Article  PubMed  Google Scholar 

  • Cook ER, Holmes RL (1996) Guide for computer program ARSTAN. In: Grissino-Mayer HD, Holmes RL, Fritts HC (eds) The international tree ring data bank program library version 2.0 user’s manual. Laboratory of Tree-Ring Research, University of Arizona, Tucson, pp 75–87

  • Cuny HE, Rathgeber CBK, Kiesse TS, Hartmann FP, Barbeito I, Fournier M (2013) Generalized additive models reveal the intrinsic complexity of wood formation dynamics. J Exp Bot 64:1983–1994. doi:10.1093/jxb/ert057

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dawes M, Hagedorn F, Handa I, Streit K, Ekblad A, Rixen C, Körner C, Hättenschwiler S (2013) An alpine treeline in a carbon dioxide-rich world: synthesis of a nine-year free-air carbon dioxide enrichment study. Oecologia 171:623–637. doi:10.1007/s00442-012-2576-5

    Article  PubMed  Google Scholar 

  • Denne MP (1988) Definition of latewood according to Mork (1928). IAWA Bull 10:59–62

    Article  Google Scholar 

  • DeSoto L, de la Cruz M, Fonti P (2011) Intra-annual patterns of tracheid size in the Mediterranean tree Juniperus thurifera as an indicator for seasonal water stress. Can J For Res 41:1280–1294. doi:10.1139/X11-045

    Article  Google Scholar 

  • DeSoto L, Camarero JJ, Olano JM, Rozas V (2012) Geographically structured and temporally unstable growth responses of Juniperus thurifera to recent climate variability in the Iberian Peninsula. Eur J For Res 131:905–917. doi:10.1007/s10342-011-0564-7

    Article  Google Scholar 

  • Eilmann B, Buchmann N, Siegwolf R, Saurer M, Cherubini P, Rigling A (2010) Fast response of Scots pine to improved water availability reflected in tree-ring width and d13C. Plant Cell Environ 33:1351–1360. doi:10.1111/j.1365-3040.2010.02153.x

    CAS  PubMed  Google Scholar 

  • Eilmann B, Zweifel R, Buchmann N, Graf Pannatier E, Rigling A (2011) Drought alters timing, quantity, and quality of wood formation in Scots pine. J Exp Bot 62:2763–2771. doi:10.1093/jxb/erq443

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  CAS  Google Scholar 

  • Ferrio JP, Voltas J (2005) Carbon and oxygen isotope ratios in wood constituents of Pinus halepensis as indicators of precipitation, temperature and vapor pressure deficit. Tellus B 57:164–173. doi:10.1111/j.1600-0889.2005.00137.x

    Article  Google Scholar 

  • Fonti P, von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gärtner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53. doi:10.1111/j.1469-8137.2009.03030.x

    Article  PubMed  Google Scholar 

  • Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr. after a drought episode. New Phytol 190:750–759. doi:10.1111/j.1469-8137.2010.03628.x

    Article  CAS  PubMed  Google Scholar 

  • Gimeno TE, Camarero JJ, Granda E, Pías B, Valladares F (2012) Enhanced growth of Juniperus thurifera under a warmer climate is explained by a positive carbon gain under cold and drought. Tree Physiol 32:326–336. doi:10.1093/treephys/tps011

    Article  CAS  PubMed  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Granda E, Camarero JJ, Jimeno TE, Martínez-Fernández J, Valladares F (2013) Intensity and timing of warming and drought differentially affect growth patterns of co-occurring Mediterranean tree species. Eur J For Res 132:469–480. doi:10.1007/s10342-013-0687-0

    Article  Google Scholar 

  • Granda E, Rossatto DR, Camarero JJ, Voltas J, Valladares F (2014) Growth and carbon isotopes of Mediterranean trees reveal contrasting responses to increased carbon dioxide and drought. Oecologia 174:307–317. doi:10.1007/s00442-013-2742-4

    Article  PubMed  Google Scholar 

  • Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree-Ring Res 57:205–221

    Google Scholar 

  • Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–115. doi:10.1078/1433-8319-00017

    Article  Google Scholar 

  • Helama S, Lindholm M, Timonen M, Eronen M (2004) Detection of climate signal in dendrochronological data analysis: a comparison of tree-ring standardization methods. Theor Appl Climatol 79:239–254. doi:10.1007/s00704-004-0077-0

    Article  Google Scholar 

  • Helle G, Schleser GH (2004) Beyond CO2-fixation by RuBisCO: an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380. doi:10.1111/j.0016-8025.2003.01159.x

    Article  CAS  Google Scholar 

  • Heres AM, Voltas J, López BC, Martínez-Vilalta J (2013) Drought-induced mortality selectively affects Scots pine trees that show limited intrinsic water-use efficiency responsiveness to raising atmospheric CO2. Func Plant Biol 41:244–256. doi:10.1071/FP13067

    Article  Google Scholar 

  • IPCC (2013) Climate change 2013. The physical science basis. Working group I contribution to the fifth assessment report of the intergovernmental panel on climate change technical summary. Cambridge University Press, Cambridge

  • Kilpeläinen A, Zubizarreta-Gerendiain A, Luostarinen K, Peltola H, Kellomäki S (2007) Elevated temperature and CO2 concentration effects on xylem anatomy of Scots pine. Tree Physiol 27:1329–1338. doi:10.1093/treephys/27.9.1329

    Article  PubMed  Google Scholar 

  • Koehler IH, Macdonald A, Schnyder H (2012) Nutrient supply enhanced the increase in intrinsic water-use efficiency of a temperate seminatural grassland in the last century. Global Change Biol 18:3367–3376. doi:10.1111/j.1365-2486.2012.02781.x

    Article  Google Scholar 

  • Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619. doi:10.1890/1051-0761(2000)010[1590:BRTCE]2.0.CO;2

    Google Scholar 

  • Linares JC, Camarero JJ (2011) From pattern to process, linking intrinsic water-use efficiency to drought-induced forest decline. Global Change Biol 18:1000–1015. doi:10.1111/j.1365-2486.2011.02566.x

    Article  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. doi:10.1007/s00442-009-1409-7

    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. doi:10.1007/s00442-011-2010-4

    Article  PubMed  Google Scholar 

  • McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801. doi:10.1016/j.quascirev.2003.06.017

    Article  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. doi:10.1104/pp.110.170704

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Niinemets Ü, Flexas J, Peñuelas J (2011) Evergreens favored by higher responsiveness to increased CO2. Trends Ecol Evol 26:136–142. doi:10.1016/j.tree.2010.12.012

    Article  PubMed  Google Scholar 

  • Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. P Natl Acad Sci USA 107:19368–19373. doi:10.1073/pnas.1006463107

    Article  CAS  Google Scholar 

  • Offermann C, Ferrio JP, Holst J, Grote R, Siegwolf R, Kayler Z, Gessler A (2011) The long way down: are carbon and oxygen isotope signals in the tree ring uncoupled from canopy physiological processes? Tree Physiol 31:1088–1102. doi:10.1093/treephys/tpr093

    Article  CAS  PubMed  Google Scholar 

  • Olano JM, Rozas V, Bartolomé D, Sanz D (2008) Effects of changes in traditional management on height and radial growth patterns in a Juniperus thurifera L. woodland. For Ecol Manage 255:506–512. doi:10.1016/j.foreco.2007.09.015

    Article  Google Scholar 

  • Olano JM, Eugenio M, García-Cervigón AI, Folch M, Rozas V (2012) Quantitative tracheid anatomy reveals a complex environmental control of wood structure in continental Mediterranean climate. Int J Plant Sci 173:137–149. doi:10.1086/663165

    Article  Google Scholar 

  • Olano JM, Almería I, Eugenio M, von Arx G (2013a) Under pressure, how a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints. Funct Ecol 27:1295–1303. doi:10.1111/1365-2435.12144

    Article  Google Scholar 

  • Olano JM, Arzac A, García-Cervigón A, von Arx G, Rozas V (2013b) New star on the stage: amount of ray parenchyma in tree rings shows a link to climate. New Phytol 198:486–495. doi:10.1111/nph.12113

    Article  PubMed  Google Scholar 

  • Pasho E, Camarero JJ, De Luis M, Vicente-Serrano SM (2011) Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain. Agr For Meteorol 151:1800–1811. doi:10.1016/j.agrformet.2011.07.018

    Article  Google Scholar 

  • Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Global Ecol Biogeogr 20:597–608. doi:10.1111/j.1466-8238.2010.00608.x

    Article  Google Scholar 

  • Perry LG, Shafroth PB, Blumenthal DM, Morgan JA, LeCain DR (2013) Elevated CO2 does not offset greater water stress predicted under climate change for native and exotic riparian plants. New Phytol 197:532–543. doi:10.1111/nph.12030

    Article  CAS  PubMed  Google Scholar 

  • Ponton S, Dupouey JL, Breda N, Feuillat F, Bodenes C, Dreyer E (2001) Carbon isotope discrimination and wood anatomy variations in mixed stands of Quercus robur and Quercus petraea. Plant Cell Environ 24:861–868. doi:10.1046/j.0016-8025.2001.00733.x

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rathgeber CBK, Rossi S, Bontemps JD (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438. doi:10.1093/aob/mcr168

    Article  PubMed Central  PubMed  Google Scholar 

  • Roden JS, Farquhar GD (2012) A controlled test of the dual-isotope approach for the interpretation of stable carbon and oxygen isotope ratio variation in tree rings. Tree Physiol 32:490–503. doi:10.1093/treephys/tps019

    Article  CAS  PubMed  Google Scholar 

  • Rozas V, Olano JM (2013) Environmental heterogeneity and neighbourhood interference modulate the individual response of Juniperus thurifera tree-ring growth to climate. Dendrochronologia 31:105–113. doi:10.1016/j.dendro.2012.09.001

    Article  Google Scholar 

  • Rozas V, DeSoto L, Olano JM (2009) Sex-specific, age-dependent sensitivity of tree-ring growth to climate in the dioecious tree Juniperus thurifera. New Phytol 182:687–697. doi:10.1111/j.1469-8137.2009.02770.x

    Article  PubMed  Google Scholar 

  • Salleo S, Trifilo P, Esposito S, Nardini A, Lo Gullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36:815–825. doi:10.1071/FP09103

    Article  Google Scholar 

  • Saurer M, Siegwolf R, Schweingruber F (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Global Change Biol 10:2109–2120. doi:10.1111/j.1365-2486.2004.00869.x

    Article  Google Scholar 

  • Speed JDM, Austrheim G, Hester AJ, Mysterud A (2011) Browsing interacts with climate to determine tree-ring increment. Funct Ecol 25:1018–1023. doi:10.1111/j.1365-2435.2011.01877.x

    Article  Google Scholar 

  • Taylor AM, Brooks JR, Lachenbruch B, Morrell JJ, Voelker S (2008) Correlation of carbon isotope ratios in the cellulose and wood extractives of Douglas-fir. Dendrochronologia 26:125–131. doi:10.1016/j.dendro.2007.05.005

    Article  Google Scholar 

  • Tyree MT (2003) Hydraulic limits on tree performance: transpiration, carbon gain and growth of trees. Trees 17:95–100. doi:10.1007/s00468-002-0227-x

    Google Scholar 

  • Vicente-Serrano SM, Beguería S, López-Moreno JI (2010) A multi-scalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index (SPEI). J Climate 23:1696–1718. doi:10.1029/2003WR002610

    Article  Google Scholar 

  • Von Wilpert K (1991) Intra-annual variation of radial tracheid diameters as a monitor of site specific water stress. Dendrochronologia 9:95–114

    Google Scholar 

  • Waterhouse JS, Switsur VR, Barker AC, Carter AHC, Hemming DL, Loader NJ, Robertson I (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quat Sci Rev 23:803–810. doi:10.1016/j.quascirev.2003.06.011

    Article  Google Scholar 

  • Ze-Xin F, Shi-Bao Z, Guang-You H, Slik JWF, Cao K-F (2012) Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. J Ecol 100:732–741. doi:10.1111/j.1365-2745.2011.01939.x

    Article  Google Scholar 

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Acknowledgments

We are indebted to Ayuntamiento de Cabrejas del Pinar (Soria) for all the facilities provided during field work, Juan Carlos Rubio for assistance with stem disk preparation, and especially to Gonzalo Juste, Isabel Lorente, Maika Folch, and Enrique Marcos for the arduous task of microtomy, tracheid measurements, and isotope material preparation. David Brown edited the English. Comments and suggestions from Georg von Arx, David Tissue, and two anonymous reviewers greatly improved the paper. This work was supported by a FPI-EHU grant to A.A., a FPI-MICINN grant to A.I.G.-C. and projects CGL2012-34209 (Spanish Ministry of Economy and Competitivity) and VA006A10-2 (Junta de Castilla y León).

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Authors and Affiliations

  1. Departamento de Ciencias Agroforestales, EU de Ingenierías Agrarias, Universidad de Valladolid, Los Pajaritos s/n, 42004, Soria, Spain

    José Miguel Olano & Ana I. García-Cervigón

  2. Sustainable Forest Management Research Institute, Universidad de Valladolid-INIA, Valladolid, Spain

    José Miguel Olano & Ana I. García-Cervigón

  3. Área de Ecología, Universidad Pablo de Olavide, Ctra. Utrera km. 1, 41002, Seville, Spain

    Juan Carlos Linares

  4. Departamento de Biología Vegetal y Ecología, Facultad de Ciencia y Tecnología, Universidad del País Vasco, Barrio Sarriena s/n, 48940, Leioa, Bizkaia, Spain

    Alberto Arzac

  5. Instituto Andaluz de Ciencias de la Tierra (CSIC), 18100, Armilla, Granada, Spain

    Antonio Delgado

  6. Laboratorio de Dendrocronología, Facultad de Ciencias Forestales, Universidad Austral de Chile, Casilla 567, Valdivia, Chile

    Vicente Rozas

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  1. José Miguel Olano
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  2. Juan Carlos Linares
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  3. Ana I. García-Cervigón
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  4. Alberto Arzac
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  5. Antonio Delgado
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  6. Vicente Rozas
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Correspondence to José Miguel Olano.

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Communicated by David Tissue.

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Olano, J.M., Linares, J.C., García-Cervigón, A.I. et al. Drought-induced increase in water-use efficiency reduces secondary tree growth and tracheid wall thickness in a Mediterranean conifer. Oecologia 176, 273–283 (2014). https://doi.org/10.1007/s00442-014-2989-4

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