Abstract
Forest dynamics will depend upon the physiological performance of individual tree species under more stressful conditions caused by climate change. In order to compare the idiosyncratic responses of Mediterranean tree species (Quercus faginea, Pinus nigra, Juniperus thurifera) coexisting in forests of central Spain, we evaluated the temporal changes in secondary growth (basal area increment; BAI) and intrinsic water-use efficiency (iWUE) during the last four decades, determined how coexisting species are responding to increases in atmospheric CO2 concentrations (C a) and drought stress, and assessed the relationship among iWUE and growth during climatically contrasting years. All species increased their iWUE (ca. +15 to +21 %) between the 1970s and the 2000s. This increase was positively related to C a for J. thurifera and to higher C a and drought for Q. faginea and P. nigra. During climatically favourable years the study species either increased or maintained their growth at rising iWUE, suggesting a higher CO2 uptake. However, during unfavourable climatic years Q. faginea and especially P. nigra showed sharp declines in growth at enhanced iWUE, likely caused by a reduced stomatal conductance to save water under stressful dry conditions. In contrast, J. thurifera showed enhanced growth also during unfavourable years at increased iWUE, denoting a beneficial effect of C a even under climatically harsh conditions. Our results reveal significant inter-specific differences in growth driven by alternative physiological responses to increasing drought stress. Thus, forest composition in the Mediterranean region might be altered due to contrasting capacities of coexisting tree species to withstand increasingly stressful conditions.
Similar content being viewed by others
References
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(5):771–781. doi:10.1111/j.1600-0889.2008.00370.x
Andreu-Hayles L, Planells O, Gutiérrez E, Muntan E, Helle G, Anchukaitis KJ, Schleser GH (2011) Long tree-ring chronologies reveal 20th century increases in water-use efficiency but no enhancement of tree growth at five Iberian pine forests. Glob Change Biol 17(6):2095–2112. doi:10.1111/j.1365-2486.2010.02373.x
Beedlow PA, Tingey DT, Phillips DL, Hogsett WE, Olszyk DM (2004) Rising atmospheric CO2 and carbon sequestration in forests. Front Ecol Environ 2(6):315–322. doi:10.1890/1540-9295(2004)002[0315:racacs]2.0.co;2
Brueggemann N, Gessler A, Kayler Z, Keel SG, Badeck F, Barthel M, Boeckx P, Buchmann N, Brugnoli E, Esperschuetz J, Gavrichkova O, Ghashghaie J, Gomez-Casanovas N, Keitel C, Knohl A, Kuptz D, Palacio S, Salmon Y, Uchida Y, Bahn M (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences 8(11):3457–3489. doi:10.5194/bg-8-3457-2011
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Christensen JH, Hewitson B, Busuioc A, Gao Chen X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Rueda VM, Mearns L, Menéndez CG, Räisänen J, Rinke A, Whetton ASP (2007) Regional climate projections. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. In: Solomon S, Qin D, Manning M, et al. (eds) Climate change 2007: the physical science basis. Cambridge University Press, Cambridge, pp 847–943
Corcuera L, Camarero JJ, Gil-Pelegrin E (2004) Effects of a severe drought on growth and wood anatomical properties of Quercus faginea. Iawa J 25(2):185–204
Durante P, Oyonarte C, Valladares F (2009) Influence of land-use types and climatic variables on seasonal patterns of NDVI in Mediterranean Iberian ecosystems. Appl Veg Sci 12(2):177–185. doi:10.1111/j.1654-109X.2009.01012.x
Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15(2):105–111
Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the inter-cellular crabon-dioxide concentration in leaves. Aust J Plant Physiol 9(2):121–137
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443
Feng XH (1999) Trends in intrinsic water-use efficiency of natural trees for the past 100–200 years: a response to atmospheric CO2 concentration. Geochimi Cosmochim Acta 63(13–14):1891–1903. doi:10.1016/s0016-7037(99)00088-5
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 Ser B-Chem Phys Meteorol 57(2):164–173. doi:10.1111/j.1600-0889.2005.00137.x
Ferrio JP, Florit A, Vega A, Serrano L, Voltas J (2003) Delta(13)C and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis. Oecologia 137(4):512–518. doi:10.1007/s00442-003-1372-7
Francey RJ, Farquhar GD (1982) An explanation of C13/C12 variations in tree rings. Nature 297(5861):28–31. doi:10.1038/297028a0
Gea-Izquierdo G, Cherubini P, Cañellas I (2011) Tree-rings reflect the impact of climate change on Quercus ilex L. along a temperature gradient in Spain over the last 100 years. For Ecol Manage 262(9):1807–1816. doi:10.1016/j.foreco.2011.07.025
Gedalof Z, Berg AA (2010) Tree ring evidence for limited direct CO2 fertilization of forests over the 20th century. Glob Biogeochem Cycles 24. doi:10.1029/2009gb003699
Gimeno TE, Camarero JJ, Granda E, Pias 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(3):326–336. doi:10.1093/treephys/tps011
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:69–78
Huang JG, Bergeron Y, Denneler B, Berninger F, Tardif J (2007) Response of forest trees to increased atmospheric CO2. Crit Rev Plant Sci 26:265–283. doi:10.1080/07352680701626978
IAEA (1995) Reference and intercomparison materials for stable isotopes of light elements. International Atomic Energy Agency, Vienna
Jaccard J, Turrisi R (2003) Interaction effects in multiple regression, 2nd edn. Sage, Thousand Oaks
Klein T, Di Matteo G, Rotenberg E, Cohen S, Yakir D (2013) Differential ecophysiological response of a major Mediterranean pine species across a climatic gradient. Tree Physiol 33(1):26–36. doi:10.1093/treephys/tps116
Koutavas A (2008) Late 20th century growth acceleration in greek firs (Abies cephalonica) from Cephalonia Island, Greece: a CO2 fertilization effect? Dendrochronologia 26(1):13–19. doi:10.1016/j.dendro.2007.06.001
Lavorel S, Canadell J, Rambal S, Terradas J (1998) Mediterranean terrestrial ecosystems: research priorities on global change effects. Glob Ecol Biogeogr Lett 7(3):157–166. doi:10.2307/2997371
Leavitt SW, Danzer SR (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65(1):87–89. doi:10.1021/ac00049a017
Levanic T, Cater M, McDowell NG (2011) Associations between growth, wood anatomy, carbon isotope discrimination and mortality in a Quercus robur forest. Tree Physiol 31(3):298–308. doi:10.1093/treephys/tpq111
Linares JC, Camarero JJ (2012) From pattern to process: linking intrinsic water-use efficiency to drought-induced forest decline. Glob Change Biol 18(3):1000–1015. doi:10.1111/j.1365-2486.2011.02566.x
Linares JC, Tíscar PA (2010) Climate change impacts and vulnerability of the southern populations of Pinus nigra subsp. salzmannii. Tree Physiol 30(7):795–806. doi:10.1093/treephys/tpq052
Linares JC, Delgado-Huertas A, Julio Camarero J, 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(3):611–624. doi:10.1007/s00442-009-1409-7
Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, García-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manage 259(4):698–709. doi:10.1016/j.foreco.2009.09.023
Liu X, Shao X, Liang E, Zhao L, Chen T, Qin D, Ren J (2007) Species-dependent responses of juniper and spruce to increasing CO2 concentration and to climate in semi-arid and arid areas of northwestern China. Plant Ecol 193(2):195–209. doi:10.1007/s11258-006-9258-5
Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F (2012) Extreme climatic events and vegetation: the role of stabilizing processes. Glob Change Biol 18(3):797–805. doi:10.1111/j.1365-2486.2011.02624.x
Martínez-Vilalta J, López BC, Adell N, Badiella L, Ninyerola M (2008) Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Glob Change Biol 14(12):2868–2881. doi:10.1111/j.1365-2486.2008.01685.x
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(2):573–585. doi:10.1007/s00442-011-2010-4
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23(7–8):771–801. doi:10.1016/j.quascirev.2003.06.017
Morgan JA, Pataki DE, Korner C, Clark H, Del Grosso SJ, Grunzweig JM, Knapp AK, Mosier AR, Newton PCD, Niklaus PA, Nippert JB, Nowak RS, Parton WJ, Polley HW, Shaw MR (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140(1):11–25. doi:10.1007/s00442-004-1550-2
Nock CA, Baker PJ, Wanek W, Leis A, Grabner M, Bunyavejchewin S, Hietz P (2011) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Glob Change Biol 17(2):1049–1063. doi:10.1111/j.1365-2486.2010.02222.x
Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant, Cell Environ 22(6):683–714. doi:10.1046/j.1365-3040.1999.00391.x
Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci USA 102(50):18052–18056. doi:10.1073/pnas.0509478102
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. Glob Change Biol 14(5):1076–1088. doi:10.1111/j.1365-2486.2008.01563.x
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(4):597–608. doi:10.1111/j.1466-8238.2010.00608.x
Pias B, Matesanz S, Herrero A, Gimeno TE, Escudero A, Valladares F (2010) Transgenerational effects of three global change drivers on an endemic Mediterranean plant. Oikos 119(9):1435–1444. doi:10.1111/j.1600-0706.2010.18232.x
Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2000) nlme: Linear and nonlinear mixed effects models. R package version 3.1–108
Rathgeber C, Guiot J, Edouard JL (2000) Using a biogeochemical model in dendroecology. Application to Pinus cembra. C R Acad Sci Ser Iii-Sci Vie-Life Sci 323 (5). doi:10.1016/s0764-4469(00)00154-2
Robertson A, Overpeck J, Rind D, Mosley-Thompson E, Zielinski G, Lean J, Koch D, Penner J, Tegen I, Healy R (2001) Hypothesized climate forcing time series for the last 500 years. J Geophy Res-Atmos 106 (D14):14783–14803. doi:10.1029/2000jd900469
Sarris D, Christodoulakis D, Koerner C (2011) Impact of recent climatic change on growth of low elevation eastern Mediterranean forest trees. Clim Change 106(2):203–223. doi:10.1007/s10584-010-9901-y
Sarris D, Siegwolf R, Körner C (2013) Inter- and intra-annual stable carbon and oxygen isotope signals in response to drought in Mediterranean pines. Agric For Meteorol 168:59–68. doi:10.1016/j.agrformet.2012.08.007
Silva LCR, Anand M, Leithead MD (2010) Recent widespread tree growth decline despite increasing atmospheric CO2. PlOS One 5(7). doi:10.1371/journal.pone.0011543
Stokes MA, Smiley TL (1968) An introduction to tree ring dating. University Chicago Press, Chicago
Thornthwaite CW, Mather JR (1957) Instructions and tables for computing potential evapotranspiration and the water balance. Publ Climatol Lab Climatol Dresel Inst Technol 10(3):185–311
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(1) doi:10.1046/j.1469-8137.2000.00620.x
Voltas J, Camarero JJ, Carulla D, Aguilera M, Ortíz A, Ferrio JP (2013) A retrospective, dual-isotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of Scots pine. Plant Cell Environ. doi:10.1111/pce.12072
Wang G, Feng X (2012) Response of plants’ water use efficiency to increasing atmospheric CO2 concentration. Environ Sci Technol 46(16):8610–8620. doi:10.1021/es301323m
Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York
Acknowledgments
We thank the Junta de Castilla-La Mancha, the Director and park rangers of the Alto Tajo Natural Park for permission and facilities provided. Meteorological data were provided by the Spanish Agencia Estatal de Meteorología. We are very grateful to David L. Quiroga, Arben Q. Alla and Enrique Palma for their valuable support in the field, and to Adrián Escudero, Teresa E. Gimeno, Silvia Matesanz and three anonymous referees for suggestions that greatly improved the manuscript. This work was supported by the Spanish Ministry for Innovation and Science with the grants FPI (CGL2007-66066-C04-02) to E. G., Consolider Montes (CSD2008 00040) and VULGLO (CGL2010 22180 C03 03) and by the Community of Madrid grant REMEDINAL 2 (CM S2009 AMB 1783). J. J. Camarero acknowledges the support of ARAID. This study was conceived and performed within the Globimed network (www.globimed.net).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Dan Yakir.
Electronic supplementary material
Below is the link to the ESM.
Rights and permissions
About this article
Cite this article
Granda, E., Rossatto, D.R., Camarero, J.J. et al. Growth and carbon isotopes of Mediterranean trees reveal contrasting responses to increased carbon dioxide and drought. Oecologia 174, 307–317 (2014). https://doi.org/10.1007/s00442-013-2742-4
Received:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1007/s00442-013-2742-4