Abstract
Aging in trees implies a progressive reduction in the growth rate, related to a shortening of the growing period and changes in the photosynthetic capability and efficiency. These changes may continue during the old-growth life stages following the juvenile phase and are reflected in tree-ring properties such as growth increment, density or stable isotopes. We studied possible climate age effects in time series of several tree-ring parameters (ring width, wood density and stable carbon and oxygen isotopes) of mature individuals from two age groups of Pinus uncinata and P. nigra at two locations in Spain. The aim was to test whether age differences in trees in the old-growth life stages could lead to diverging climate responses. The results show some differences in response to climate between age groups at a monthly level, but most of these divergences are not significant for seasonal climate variables. Regardless of the age group, the main limiting climate factors constrained tree growth equally. Although our findings do not support the idea of an age-dependent response to climate that may lead to inaccurate climate reconstructions, further studies using tree-ring density and stable isotope series are urgently needed to verify the current results.
Similar content being viewed by others
References
Andreu L, Gutiérrez E, Macias M, Ribas M, Bosch O, Camarero JJ (2007) Climate increases regional tree-growth variability in Iberian pine forests. Glob Change Biol 13:804–815
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
Andreu-Hayles L, Planells O, Gutiérrez E, Muntán 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. doi:10.1111/j.1365-2486.2010.02373.x
Battipaglia G, Saurer M, Cherubini P, Siegwolf RTW, Cotrufo MF (2009) Tree rings indicate different drought resistance of a native (Abies alba Mill.) and a nonnative (Picea abies (L.) Karst.) species co-occurring at a dry site in Southern Italy. For Ecol Manage 257:820–828
Becker P, Meinzer FC, Wullschleger SD (2000) Hydraulic limitation of tree height: a critique. Funct Ecol 14:4–11
Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353
Briffa KR, Osborn TJ, Schweingruber FH (2004) Large-scale temperature inferences from tree rings: a review. Glob Planet Change 40:11–26
Buchmann N, Ehleringer JR (1998) CO2 concentration profiles, and carbon and oxygen isotopes in C3 and C4 crop canopies. Agric For Meteorol 89:45–58
Büntgen U, Frank DC, Verstege A, Nievergelt D, Esper J (2007) Climatic response of multiple tree-ring parameters from the Central Spanish Pyrenees. Trace 5:60–72
Büntgen U, Frank DC, Grudd H, Esper J (2008) Long-term summer temperature variations in the Pyrenees. Clim Dyn 31:615–631
Büntgen U, Frank DC, Trouet V, Esper J (2010) Diverse climate sensitivity of Mediterranean tree-ring width and density. Trees Struct Funct 24:261–273
Carrer M, Urbinati C (2004) Age-dependent tree-ring growth responses to climate in Larix decidua and Pinus cembra. Ecology 85:730–740
Cook ER (1985) A time series approach to tree-ring standardization. Ph.D., dissertation. University of Arizona
Cook ER, Kairiukstis LA (1990) Methods of dendrochronology: applications in the environmental sciences. International Institute for Applied Systems Analysis, Kluwer, Boston
Cook ER, Briffa KR, Meko DM, Graybill DA, Funkhouser G (1995) The ‘segment length curse’ in long tree-ring chronology development for palaeoclimatic studies. Holocene 5:229–237
D’Arrigo R, Wilson R, Jacoby G (2006) On the long-term context for late twentieth century warming. J Geophys Res 111: D03103
Day ME, Greenwood MS, Diaz-Sala C (2002) Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol 22:507–513
Esper J, Cook ER, Schweingruber FH (2002) Low-frequency signals in long tree-ring chronologies and the reconstruction of past temperature variability. Science 295:2250–2253
Esper J, Niederer R, Bebi P, Frank D (2008) Climate signal age effects—evidence from young and old trees in the Swiss Engadin. For Ecol Manage 255:3783–3789
Esper J, Frank DC, Battipaglia G, Büntgen U, Holert C, Treydte K et al (2010) Low frequency noise in δ 13C and δ 18O tree-ring data: a case study of Pinus uncinata. Glob Biochem Cycles 24:GB4018
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
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
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
Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31
Freyer HD (1979) On the 13C record in tree rings: Part I. 13C variations in northern hemispheric trees during the last 150 years. Tellus 31:124–137
Fritts HC (1976) Tree rings and climate. Academic Press, New York
Gagen M, McCarroll D, Edouard JL (2004) The effect of site conditions on pine tree ring width, density and δ 13C series. Arctic, Antarctic and. Alpine Res 36(2):166–171
Gagen M, McCarroll D, Edouard JL (2006) Combining tree ring width, density and stable carbon isotope series to enhance the climate signal in tree rings: an example from the French Alps. Clim Change 78:363–379
Gagen M, McCarroll D, Loader NJ, Robertson I, Jalkanen R, Anchukaitis KJ (2007) Exorcising the ‘segment length curse’: summer temperature reconstruction since AD 1640 using non-detrended stable carbon isotope ratios from pine trees in northern Finland. Holocene 17:435–446
Gagen M, McCarroll D, Robertson I, Loader NJ, Jalkanen R (2008) Do tree ring δ 13C series from Pinus sylvestris in northern Fennoscandia contain long-term non-climatic trends? Chem Geol 252:42–51
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43:69–78
Jyske T (2008) The effects of thinning and fertilisation on wood and tracheid properties of Norway spruce (Picea abies)—the results of long-term experiments. Dissertationes Forestales 55, University of Helsinki, 59 p
Koga S, Zhang SY (2004) Inter-tree and intra-tree variations in ring width and wood density components in balsam fir (Abies balsamea). Wood Sci Technol 38:149–162
Leavitt SW, Long A (1984) Sampling strategy for stable carbon isotope analysis of tree rings in pine. Nature 301:145–147
Leavitt SW, Long A (1989) Drought indicated in carbon-13/carbon-12 ratios of southwestern tree rings. Water Res Bull 25:341–347
Lerman JC, Long A (1979) Carbon-13 in tree rings: local or canopy effect? In: Proceedings of the international meeting on stable isotopes in tree ring research, New York, pp 22–32
Linderholm HW, Linderholm K (2004) Age-dependent climate sensitivity of Pinus sylvestris L. in the central Scandinavian Mountains. Boreal Environ Res 9:307–317
Loader NJ, Robertson I, Barker AC, Switsur VR, Waterhouse JS (1997) A modified method for the batch processing of small wholewood samples to α-cellulose. Chem Geol (Isot Geosci) 136:313–317
Mann ME, Bradley RS, Hughes MG (1999) Northern Hemisphere temperature during the last millennium: inferences, uncertainties and limitations. Geophys Res Lett 26:759–762
Marshall JD, Monserud RA (2006) Co-occurring species differ in tree-ring δ 18O trends. Tree Physiol 26:1055–1066
Martin-Benito D, Cherubini P, Del Río M, Cañellas I (2008) Growth response to climate and drought in Pinus nigra Arn. trees of different crown classes. Trees 22:363–373
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801
Peñuelas J (2005) Plant physiology: a big issue for trees. Nature 437(7061):965–966
Polge H (1965) Study of wood density variations by densitometric analysis of X-ray negative of samples taken with a pressler auger. Paper presented at meeting of IUFRO section 41
Rinn F (2003) TSAP-win professional time series analysis and presentation for dendrochronology and related applications. Version 0.3, Quick reference
Rivas-Martínez S (1983) Pisos bioclimáticos de España. Lazaroa 5:33–43
Rossi S, Deslauriers A, Anfodillo T, Carrer M (2008) Age-dependent xylogenesis in timberline conifers. New Phytol 177:199–208
Rozas V, DeSoto L, Olano JM (2009) Sex-specific age-dependent sensitivity of tree-ring growth to climate in the dioecious tree Juniperus thurifera L. New Phytol 182:687–697
Rozas V, Zas R, Garcıía-González I (2010) Contrasting effects of water availability on Pinus pinaster radial growth near the transition between the Atlantic and Mediterranean biogeographical regions in NW Spain. Eur J For Res. doi:10.1007/s10342-011-0494-4
Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. BioSci 47:235–242
Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381
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. Glob Change Biol 10(12):2109–2120
Saurer M, Cherubini P, Reynolds-Henne CE, Treydte KS, Anderson WT, Siegwolf RTW (2008) An investigation of the common signal in tree-ring stable isotope chronologies at temperate sites. J Geophy Res Biogeosci 113:G02019
Schleser GH (1992) d13C pattern in a forest tree as an indicator of carbon transfer in trees. Ecology 73:1922–1925
Schleser GH (1999) 13C/12C in growth rings and leaves: carbon distribution in trees. In: Jones TP, Rowe NP (eds) Fossil plants and spores: modern techniques. Geol Soc, London, pp 306–309
Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Physiol Ecol 155(3):441–454
Stokes MA, Smiley TL (1968) Introduction to tree-ring dating. University of Chicago Press, Chicago
Szeicz JM, MacDonald GM (1994) Age dependent tree ring growth responses of subarctic white spruce to climate. Can J For Res 24:120–132
Szeicz JM, MacDonald GM (1995) Dendroclimatic reconstruction of summer temperatures in northwestern Canada since AD 1638 based on age-dependent modeling. Quat Res 44:257–266
Tardif J, Camarero JJ, Ribas M, Gutiérrez E (2003) Spatiotemporal variability in tree growth in the Central Pyrenees: climatic and site influences. Ecol Monogr 73:241–257
Treydte K, Schleser GH, Helle G, Frank DC, Winiger M, Haug GH, Esper J (2006) The twentieth century was the wettest period in northern Pakistan over the past millennium. Nature 440:1179–1182
Treydte KS, Frank D, Esper J et al (2007) Signal strength and climate calibration of a European tree-ring isotope network. Geophys Res Lett 34(24):L24302
Treydte K, Frank DC, Saurer M, Helle G, Schleser G, Esper J (2009) Impact of climate and CO2 on a millennium-long tree-ring carbon isotope record. Geochim Cosmochim Acta 73:4635–4647
Voltas J, Chambel MR, Prada MA, Ferrio JP (2008) Climate-related variability in carbon and oxygen stable isotopes among populations of Aleppo pine grown in common-garden tests. Trees 22(6):759–769
Wigley TML, Briffa KR, Jones PD (1984) On the average of value of correlated time series, with applications in dendroclimatology and hydrometeorology. J Clim Appl Meteorol 23:201–213
Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates of old trees. For Sci 40:513–527
Zweifel R, Zimmerman L, Zeugin F, Newbery DM (2006) Intra-annual radial growth and water relations of trees: implication towards a growth mechanism. J Exp Bot 57:1445–1459
Acknowledgments
We thank Carmen Bürger and Christoph Küppers for the isotope analyses and Björn Günther for performing all density measurements. This research was funded by EU project MILLENNIUM (017008-2).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Brazaitis.
Rights and permissions
About this article
Cite this article
Dorado Liñán, I., Gutiérrez, E., Heinrich, I. et al. Age effects and climate response in trees: a multi-proxy tree-ring test in old-growth life stages. Eur J Forest Res 131, 933–944 (2012). https://doi.org/10.1007/s10342-011-0566-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10342-011-0566-5