KEY MESSAGE: The temperature sensitivity of maximum latewood density measurements in pine trees from a high-elevation site in the Spanish Pyrenees increases with tree age. Detrending modulates the intensity of the effect. ABSTRACT: Tree-rings are the prime archive for high-resolution climate information over the past two millennia. However, the accuracy of annually resolved reconstructions from tree-rings can be constrained by what is known as climate signal age effects (CSAE), encompassing changes in the sensitivity of tree growth to climate over their lifespans. Here, we evaluate CSAE in Pinus uncinata from an upper tree line site in the Spanish central Pyrenees, Lake Gerber, which became a key location for reconstructing western Mediterranean summer temperatures at annual resolution. We use tree-ring width (TRW) and maximum latewood density (MXD) measurements from 50 pine trees with individual ages ranging from 7 to 406 years. For MXD, temperature sensitivity increases significantly (p < 0.01) with tree age from r = 0.31 in juvenile rings with a cambial age < 100 years to r = 0.49 in adult rings > 100 years. Similar CSAE are not detected in TRW, likely affected by the overall lower temperature signal (r TRW = 0.45 vs. r MXD = 0.81 from 1951 to 2020). The severity of CSAE is influenced by the approach used to remove ontogenetic trends, highlighting the need to assess and consider potential biases during tree-ring standardization. Our findings reveal CSAE to add uncertainty in MXD-based climate reconstructions in the Mediterranean. We recommend studying CSAE by sampling diverse age classes in dendroclimatic field campaigns. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00468-024-02598-3.

Department of Geography Johannes Gutenberg University 55099 Mainz Germany

Department of Geography University of Cambridge Cambridge CB2 3EN UK

Department of Geology National Museum of Natural Sciences Spanish National Research Council Madrid Spain

Faculty of Science Department of Geography Masaryk University 61137 Brno Czech Republic

Global Change Research Institute of the Czech Academy of Sciences 60300 Brno Czech Republic

Oeschger Centre for Climate Change Research University of Bern 3012 Bern Switzerland

Zobrazit více v PubMed

Babushkina EA, Vaganov EA, Belokopytova LV, Shishov VV, Grachev AM (2015) Competitive strength effect in the climate response of scots pine radial growth in south-central siberia forest-steppe. Tree-Ring Res 71:106–117. 10.3959/1536-1098-71.2.106

Barichivich J, Osborn TJ, Harris I, van der Schrier G, Jones PD (2022) Monitoring global drought using the self-calibrating Palmer Drought Severity Index. State of the Climate in 2021. Bull Am Meteorol Soc 103:S66–S67. 10.1175/BAMS-D-22-0092.1

Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353. 10.1016/S1360-1385(00)01691-5 PubMed

Bunn AG (2008) A dendrochronology program library in R (dplR). Dendrochronologia 26:115–124. 10.1016/j.dendro.2008.01.002

Büntgen U, Esper J (2024) Physiological meaning of bimodal tree growth-climate response patterns. Int J Biometeorol. 10.1007/s00484-024-02706-5 PubMed PMC

Büntgen U, Frank D, Trouet V, Esper J (2010) Diverse climate sensitivity of Mediterranean tree-ring width and density. Trees 24:261–273. 10.1007/s00468-009-0396-y

Büntgen U, Krusic PJ, Verstege A, Sangüesa-Barreda G, Wagner S, Camarero JJ, Ljungqvist FC, Zorita E, Oppenheimer C, Konter O, Tegel W, Gärtner H, Cherubini P, Reinig F, Esper J (2017) New tree-ring evidence from the pyrenees reveals western mediterranean climate variability since medieval times. J Clim 30:5295–5318. 10.1175/JCLI-D-16-0526.1

Büntgen U, Reinig F, Verstege A, Piermattei A, Kunz M, Krusic P, Slavin P, Štěpánek P, Torbenson M, Martinez del Castillo E, Arosio T, Kirdyanov A, Oppenheimer C, Trnka M, Palosse A, Bebchuk T, Camarero JJ, Esper J (2024) Recent summer warming over the western Mediterranean region is unprecedented since medieval times. Glob Planet Change 232:104336. 10.1016/j.gloplacha.2023.104336

Camarero JJ, Guerrero-Campo J, Gutierrez E (1998) Tree-ring growth and structure of Pinus uncinata and Pinus sylvestris in the Central Spanish Pyrenees. Arct Alp Res 30:1. 10.2307/1551739

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

Carrer M, Urbinati C (2004) Age-dependent tree-ring growth responses to climate in Larix decidua and Pinus cembra. Ecology 85:730–740. 10.1890/02-0478

Cook E, Krusic PJ, Peters K, Holmes RL (2017) Program ARSTAN (49v1b) Autoregressive tree-ring standardization program

Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree-Ring Bull 41:45–53

Cook E, Peters K (1997) Calculating unbiased tree-ring indices for the study of climatic and environmental change. Holocene 7:361–370. 10.1177/095968369700700314

Cook E (1985) A time series analysis approach to tree ring standardization. The University of Arizona

Copenheaver CA, Crawford CJ, Fearer TM (2011) Age-specific responses to climate identified in the growth of Quercus alba. Trees 25:647–653. 10.1007/s00468-011-0541-2

Cuny HE, Rathgeber CB (2016) Xylogenesis: coniferous trees of temperate forests are listening to the climate tale during the growing season but only remember the last words! Plant Physiol 171:306–317. 10.1104/pp.16.00037 PubMed PMC

Domec JC, Lachenbruch B, Pruyn ML, Spicer R (2012) Effects of age-related increases in sapwood area, leaf area, and xylem conductivity on height-related hydraulic costs in two contrasting coniferous species. Ann For Sci 69:17–27. 10.1007/s13595-011-0154-3

Dorado Liñán I, Gutiérrez E, Heinrich I, Andreu-Hayles L, Muntán E, Campelo F, Helle G (2012) Age effects and climate response in trees: a multi-proxy tree-ring test in old-growth life stages. Eur J for Res 131:933–944. 10.1007/s10342-011-0566-5

Eschbach W, Nogler P, Schär E, Schweingruber FH (1995) Technical advances in the radiodensitometrical determination of wood density. Dendrochronologia 13:155–168

Esper J, Cook ER, Krusic PJ, Peters K, Schweingruber FH (2003) Tests of the RCS method for preserving low-frequency variability in long tree-ring chronologies. Tree-Ring Res 59:81–98

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 Manag 255:3783–3789. 10.1016/j.foreco.2008.03.015

Esper J, Frank DC, Timonen M, Zorita E, Wilson RJ, Luterbacher J, Holzkämper S, Fischer N, Wagner S, Nievergelt D, Verstege A, Büntgen U (2012) Orbital forcing of tree-ring data. Nature Clim Change 2:862–866. 10.1038/nclimate1589

Esper J, Krusic PJ, Ljungqvist FC, Luterbacher J, Carrer M, Cook E, Davi NK, Hartl-Meier C, Kirdyanov A, Konter O, Myglan V, Timonen M, Treydte K, Trouet V, Villalba R, Yang B, Büntgen U (2016) Ranking of tree-ring based temperature reconstructions of the past millennium. Quat Sci Rev 145:134–151. 10.1016/j.quascirev.2016.05.009

Esper J, Hartl C, Tejedor E, De Luis M, Günther B, Büntgen U (2020) High-resolution temperature variability reconstructed from black pine tree ring densities in Southern Spain. Atmos 11:748. 10.3390/atmos11070748

Esper J, Torbenson M, Büntgen U (2024) 2023 summer warmth unparalleled over the past 2000 years. Nature. 10.1038/s41586-024-07512-y PubMed

Gallardo VB, Hadad MA, Ribas-Fernández YA, Roig FA, Tardif JC (2022) Age-related tree-ring sensitivity at the dry forest-steppe boundary in Northwestern Patagonia. Trees 36:1607–1620. 10.1007/s00468-022-02312-1

Gao X, Giorgi F (2008) Increased aridity in the Mediterranean region under greenhouse gas forcing estimated from high resolution simulations with a regional climate model. Glob Planet Change 62:195–209. 10.1016/j.gloplacha.2008.02.002

Gazol A, Camarero JJ, Sangüesa-Barreda G, Serra-Maluquer X, Sánchez-Salguero R, Coll L, Casals P (2020) Tree species are differently impacted by cumulative drought stress and present higher growth synchrony in dry places. Front For Glob Change 3:573346. 10.3389/ffgc.2020.573346

Giorgi F (2006) Climate change hot-spots. Geophys Res Lett 33:L08707. 10.1029/2006GL025734

Gryc V, Horáček P (2007) Variability in density of spruce (Picea abies [L.] Karst.) wood with the presence of reaction wood. J For Sci 53:129–137. 10.17221/2146-JFS

Harris I, Osborn TJ, Jones P, Lister D (2020) Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci Data 7:109. 10.1038/s41597-020-0453-3 PubMed PMC

Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:51–67

Konter O, Büntgen U, Carrer M, Timonen M, Esper J (2016) Climate signal age effects in boreal tree-rings: Lessons to be learned for paleoclimatic reconstructions. Quat Sci Rev 142:164–172. 10.1016/j.quascirev.2016.04.020

Li X, Liang E, Gričar J, Prislan P, Rossi S, Čufar K (2013) Age dependence of xylogenesis and its climatic sensitivity in Smith fir on the south-eastern Tibetan Plateau. Tree Physiol 33:48–56. 10.1093/treephys/tps113 PubMed

Ljungqvist FC, Piermattei A, Seim A, Krusic PJ, Büntgen U, He M, Kirdyanov A, Luterbacher J, Schneider L, Seftigen K, Stahle D, Villalba R, Yang B, Esper J (2020) Ranking of tree-ring based hydroclimate reconstructions of the past millennium. Quat Sci Rev 230:106074. 10.1016/j.quascirev.2019.106074

Madrigal-González J, Zavala MA (2014) Competition and tree age modulated last century pine growth responses to high frequency of dry years in a water limited forest ecosystem. Agric for Meteorol 192:18–26. 10.1016/j.agrformet.2014.02.011

Marqués L, Camarero JJ, Zavala MA, Stoffel M, Ballesteros-Cánovas JA, Sancho-García C, Madrigal-Gonzáles J (2021) Evaluating tree-to-tree competition during stand development in a relict Scots pine forest: how much does climate matter? Trees 35:1207–1219. 10.1007/s00468-021-02109-8

Olson ME, Soriano D, Rosell JA, Anfodillo T, Donoghue MJ, Edwards EJ, León-Gómez C, Dawson T, Camarero Martínez JJ, Castorena M, Echeverría A, Espinosa CI, Fajardo A, Gazol A, Isnard S, Lima RS, Marcati CR, Méndez-Alonzo R (2018) Plant height and hydraulic vulnerability to drought and cold. Proc Natl Acad Sci USA 115:7551–7556. 10.1073/pnas.1721728115 PubMed PMC

PAGES 2k Consortium (2013) Continental-scale temperature variability during the past two millennia. Nature Geosci 6:339–346. 10.1038/ngeo1797

Piermattei A, von Arx G, Avanzi C, Fonti P, Gärtner H, Piotti A, Urbinati C, Vendramin GG, Büntgen U, Crivellaro A (2020) Functional relationships of wood anatomical traits in Norway spruce. Front Plant Sci 11:683. 10.3389/fpls.2020.00683 PubMed PMC

Prendin AL, Mayr S, Beikircher B, Von Arx G, Petit G (2018) Xylem anatomical adjustments prioritize hydraulic efficiency over safety as Norway spruce trees grow taller. Tree Physiol 38:1088–1097. 10.1093/treephys/tpy065 PubMed

Rennie JJ, Lawrimore JH, Gleason BE, Thorne PW, Morice CP, Menne MJ, Williams CN, Almeida WG, Christy JR, Flannery M, Ishihara M, Kamiguchi K, Klein‐Tank AMG, Mhanda A, Lister DH, Razuvaev V, Renom M, Rusticucci M, Tandy J, Worley SJ, Venema V, Angel W, Brunet M, Dattore B Diamond H, Lazzara MA, Le Blancq F, Luterbacher J, Mächel H, Revadekar J, Vose RS, Yin X (2014) The international surface temperature initiative global land surface databank: monthly temperature data release description and methods. Geosci Data J 1:75–102. 10.1002/gdj3.8

Rossi S, Deslauriers A, Anfodillo T, Carrer M (2008) Age-dependent xylogenesis in timberline conifers. New Phytol 177:199–208. 10.1111/j.1469-8137.2007.02235.x PubMed

Royo-Navascues M, Martínez Del Castillo E, Tejedor E, Serrano-Notivoli R, Longares LA, Saz MA, Novak K, de Luis M (2022) The imprint of droughts on Mediterranean pine forests. Forests 13:1396. 10.3390/f13091396

Ruiz-Benito P, Madrigal-González J, Young S, Mercatoris P, Cavin L, Huang TJ, Chen JC, Jump AS (2015) Climatic stress during stand development alters the sign and magnitude of age-related growth responses in a subtropical mountain pine. PLoS One 10:e0126581. 10.1371/journal.pone.0126581 PubMed PMC

Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. BioSci 47:235–242. 10.2307/1313077

Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381. 10.1111/j.1365-3040.2005.01478.x PubMed

Seim A, Treydte K, Trouet V, Frank D, Fonti P, Tegel W, Panayotov M, Fernández-Donado L, Krusic P, Büntgen U (2015) Climate sensitivity of Mediterranean pine growth reveals distinct east–west dipole. Int J Climatol 35:2503–2513. 10.1002/joc.4137

Serrano Notivoli R, Beguería S, de Luis M (2019a) STEAD: a high-resolution daily gridded temperature dataset for Spain. Earth Syst Sci Data 11:1171–1188. 10.5194/essd-11-1171-2019

Serrano Notivoli R, de Luis M, Beguería S, Saz MÁ (2016) SPREAD (Spanish PREcipitation at daily scale). 10.20350/DIGITALCSIC/7393

Serrano Notivoli R, de Luis M, Beguería S (2019b) STEAD (Spanish TEmperature At Daily scale). 10.20350/DIGITALCSIC/8622

St. George S (2014) An overview of tree-ring width records across the Northern Hemisphere. Quat Sci Rev 95:132–150. 10.1016/j.quascirev.2014.04.029

Stephenson N, Das A, Condit R, Russo SE, Baker PJ, Beckman NG, Coomes DA, Lines ER, Morris WK, Rüger N, Álvarez E, Blundo C, Bunyavejchewin S, Chuyong G, Davies SJ, Duque Á, Ewango CN, Flores O, Franklin JF, Grau HR, Hao Z, Harmon ME, Hubbell SP, Kenfack D, Lin Y, Makana JR, Malizia A, Malizia LR, Pabst RJ, Pongpattananurak N, Su SH, Sun IF, Tan S, Thomas D, van Mantgem PJ, Wang X, Wiser SK, Zavala MA (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507:90–93. 10.1038/nature12914 PubMed

Trouet V, Van Oldenborgh GJ (2013) KNMI climate explorer: a web-based research tool for high-resolution paleoclimatology. Tree-Ring Res 69:3–13. 10.3959/1536-1098-69.1.3

Trouillier M, Van Der Maaten-Theunissen M, Scharnweber T, Würth D, Burger A, Schnittler M, Wilmking M (2019) Size matters—a comparison of three methods to assess age- and size-dependent climate sensitivity of trees. Trees 33:183–192. 10.1007/s00468-018-1767-z

Van Der Schrier G, Barichivich J, Briffa KR, Jones PD (2013) A scPDSI-based global data set of dry and wet spells for 1901–2009. JGR Atmos 118:4025–4048. 10.1002/jgrd.50355

Voelker SL (2011) Age-dependent changes in environmental influences on tree growth and their implications for forest responses to climate change. In: Meinzer F, Lachenbruch B, Dawson T (eds) Size- and age-related changes in tree structure and function. Tree Physiol 4. Springer, Dordrecht. 10.1007/978-94-007-1242-3_17

Wigley TM, Briffa KR, Jones PD (1984) On the average value of correlated time series, with applications in dendroclimatology and hydrometeorology. J Appl Meteorol Climatol 23:201–213

Yu G, Liu Y, Wang X, Ma K (2008) Age-dependent tree-ring growth responses to climate in Qilian juniper (Sabina przewalskii Kom.). Trees 22:197–204. 10.1007/s00468-007-0170-y

Zang C, Biondi F (2015) treeclim: an R package for the numerical calibration of proxy-climate relationships. Ecography 38:431–436. 10.1111/ecog.01335

Ziaco E, Liu X, Biondi F (2023) Dendroanatomy of xylem hydraulics in two pine species: efficiency prevails on safety for basal area growth in drought-prone conditions. Dendrochronologia 81:126116. 10.1016/j.dendro.2023.126116