Abstract
We investigated the influence of climate on the ring width and xylem anatomy of two co-occurring pines (Pinus nigra Arn. and P. sylvestris L.) in the mountains of east-central Spain in order to test their utility for dendroclimatic reconstructions. We developed chronologies of ring width, mean lumen diameter and mean cell-wall thickness (in the earlywood, latewood, and the total annual ring) and the number of cells between 1960 and 2006. Drought, expressed as the standardized precipitation-evapotranspiration index (SPEI), was the main climatic driver of tree radial growth, although trees were also sensitive to temperature (negative effect in previous autumn and current summer) and precipitation (with a general positive effect). P. sylvestris response was stronger to climate of the current year, whereas the effect of previous-year climate was more important for P. nigra. Warm and dry summers reduced ring width, tracheid lumen, and wall thickness in both species, whereas warm winter-spring temperatures had the opposite effect, primarily for P. sylvestris. Previous-year or early-season conditions mainly affected earlywood features, whereas latewood was more responsive to summer climate. Overall, climate appeared to be a stronger limiting factor for P. sylvestris. During periods of drought, cell-wall thickness was reduced while lumen width increased in the latewood of P. sylvestris. This could compromise its hydraulic safety against drought-induced cavitation as our site was close to the southern and dry edge of the species distribution area. Our results suggest that anatomical variables record different and stronger climate information than ring width variables, especially in P. sylvestris. Reconstruction models for SPEI at the 3-month scale were developed for July–August and September–October using principal components regression. The best models included anatomical and width variables of both pine species suggesting that tracheid chronologies can be useful for drought reconstructions especially at mesic sites or with species that encode a mixed drought and temperature-precipitation signal.
Similar content being viewed by others
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723
Andreu L, Gutierrez E, Macias M, Ribas M, Bosch O, Camarero JJ (2007) Climate increases regional tree-growth variability in Iberian pine forests. Glob Change Biol 13:1–12
Andreu-Hayles L, Rosanne DA, Anchukaitis KJ, Beck PSA, Frank D, Goetz S (2011) Varying boreal forest response to Arctic environmental change at the Firth River. Alaska. Env Res Let 6(4):045503
Assmann E (1970) The principles of forest yield study. Pergamon Press Ltd., Oxford
Attolini MR, Calvani F, Galli M, Nanni T, Ruggiero L, Schaer E, Zuanni F (1990) The relationship between climate variables and wood structure in Pinus halepensis Mill. Theor Appl Climatol 41:121–127
Barbéro M, Losiel R, Queézel P, Richardson DM, Romane F (1998) Pines of the mediterranean basin. In: Richardson DM (ed) Ecology and biogeography of pinus. Cambridge University Press, Cambridge
Beeckman H, Van der Mijnsbrugge K (1993) Redundancy analysis and the evolutionary learning algorithm as complementary mathematical processing tools for dendrochronological data sets. Silva Gandavensis 58:101–113
Brodribb T, Hill RS (1999) The importance of xylem constraints in the distribution of conifer species. New Phytol 143(2):365–372
Bunn AG (2008) A dendrochronology program library in R (dplR). Dendrochronologia 26(2):115–124
Camarero JJ, Guerrrero-Campo J, Gutiérrez E (1998) Tree ring growth and structure of Pinus uncinata and Pinus sylvestris in the central Spanish Pyrenees. Arct Alp Res 30(1):1–10
Campelo F, Nabais C, Gutiérrez E, Freitas H, García-González I (2010) Vessel features of Quercus ilex L. growing under Mediterranean climate have a better climatic signal than tree-ring width. Trees 24(3):463–470
Cherubini P, Gartner BL, Tognetti R, Bräker OU, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from mediterranean climates. Biol Rev 78:119–148
Cinnirella S, Magnani F, Saracino A, Borghetti M (2002) Response of a mature Pinus laricio plantation to a three-year restriction of water supply: structural and functional acclimation to drought. Tree Physiol 22:21–30
Cook ER, Pederson N (2010) Uncertainty, emergence, and statistics in dendrochronology. In: Hughes MK, Swetnam TW, Diaz HF (eds) Dendroclimatology: progress and prospects, developments in paleoecological research. Springer, Berlin
Cook ER, Meko DM, Stahle DW, Cleaveland MK (1999) Drought reconstructions for the continental United States. J Clim 12:1145–1162
Cook ER, Esper J, D’Arrigo RD (2004) Extra-tropical Northern Hemisphere land temperature variability over the past 1000 years. Quat Sci Rev 23(20–22):2063–2074
Cook ER, Anchukaitis KJ, Buckley BM, D’Arrigo RD, Jacoby GC, Wright WE (2010) Asian monsoon failure and mega drought during the last millennium. Science 328(5977):486–489
D’Arrigo R, Wilson R, Jacoby G (2006) On the long-term context for late twentieth century warming. J Geophys Res 111(D3):D03103
De Grandpré L, Tardif JC, Hessl A, Pederson N, Conciatori F, Green TR, Oyunsanaa B, Baatarbileg N (2011) Seasonal shift in the climate responses of Pinus sibirica, Pinus sylvestris, and Larix sibirica trees from semi-arid, north-central Mongolia. Can J For Res 41(6):1242–1255
De Micco V, Saurer M, Aronne G, Tognetti R, Cherubini P (2007) Variations of wood anatomy and ∂13C within-tree rings of coastal Pinus pinaster showing intra-annual density fluctuations. IAWA J 28(1):61–74
Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees 19(4):402–408
Dewar RC, Ludlow AR, Dougherty PM (1994) Environmental influences on carbon allocation in pines. Ecol Bull 43:92–101
Donaldson LA (2002) Abnormal lignin distribution in wood from severely drought stressed Pinus radiata trees. IAWA J 23(2):161–178
Eckstein D (2004) Change in past environments—secrets of the tree hydrosystem. New Phytol 163:1–4
Eilmann B, Zweifel R, Buchmann N, Fonti P, Rigling A (2009) Drought-induced adaptation of the xylem in scots pine and pubescent oak. Tree Physiol 29:1011–1020
Esper J, Cook ER, Schweingruber FH (2002) Low-frequency signals in long tree-ring chronologies for reconstructing past temperature variability. Science 295(5563):2250–2253
Esteban-Parra MJ, Rodrigo FS, Castro-Diez Y (1998) Spatial and temporal patterns of precipitation in Spain for the period 1880–1992. Int J Climatol 18:1557–1574
Filion L, Cournoyer L (1995) Variation in wood structure of eastern larch defoliated by the larch sawfly in subarctic Quebec. Can. Can J For Res 25(8):1263–1268
Fonti P, García-Gonzalez I (2004) Suitability of chestnut earlywood vessel chronologies for ecological studies. New Phytol 163:77–86
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(1):42–53
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 Manag 262(9):1807–1816
Gea-Izquierdo G, Fonti P, Cherubini P, Martin-Benito D, Chaar H, Cañellas I (2012) Xylem hydraulic adjustment and growth response of Quercus canariensis wild to climatic variability. Tree Physiol 32(4):401–413
Gindl W, Grabner M, Wimmer R (2000) The influence of temperature on latewood lignin content in treeline Norway spruce compared with maximum density and ring width. Trees 14:409–414
Gricar J, Zupancic M, Cufar K, Koch G, Schmitt UWE, Oven P (2006) Effect of local heating and cooling on cambial activity and cell differentiation in the stem of Norway spruce (Picea abies). Ann Bot 97(6):943–951
Gruber A, Strobl S, Veit B, Oberhuber W (2010) Impact of drought on the temporal dynamics of wood formation in Pinus sylvestris. Tree Physiol 30(4):490–501
Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4(2):97–115
Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant, Cell Environ 26(7):1067–1081
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:69–78
Hughes MK (2002) Dendrochronology in climatology—the state of the art. Dendrochronologia 20(1–2):95–116
Hughes MK, Xiangding W, Xuemei S, Garfin GM (1994) A preliminary reconstruction of rainfall in north-central China since A.D. 1600 from tree-ring density and width. Quatern Res 42(1):88–99
Irvine J, Perks MP, Magnani F, Grace J (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18:393–402
Jones H (1998) Stomatal control of photosynthesis and transpiration. J Exp Bot 49:387–398
Kirdyanov A, Hughes M, Vaganov E, Schweingruber F, Silkin P (2003) The importance of early summer temperature and date of snow melt for tree growth in the Siberian Subarctic. Trees 17(1):61–69
Körner C (2003) Carbon limitation in trees. J Ecol 91(1):4–17
Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science BV, Amsterdam
Liang C, Filion L, Cournoyer L (1997) Wood structure of biotically and climatically induced light rings in eastern larch (Larix laricina). Can J For Res 27:1538–1547
Maherali H, DeLucia EH (2000) Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiol 20:859–867
Martín-Benito D, del Rio M, Cañellas I (2010) Black pine (Pinus nigra Arn.) growth divergence along a latitudinal gradient in Western Mediterranean mountains. Ann For Sci 67(4):401
Martínez-Vilalta J, Piñol J (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manag 161(1–3):247–256
Maxwell RS, Hessl AE, Cook ER, Pederson N (2011) A multispecies tree ring reconstruction of Potomac River stream flow (950–2001). Water Resour Res 47(5):W05512
McCarroll D, Jalkanen R, Hicks S, Tuovinen M, Gagen M, Pawellek F, Eckstein D, Schmitt U, Autio J, Heikkinen O (2003) Multiproxy dendroclimatology: a pilot study in northern Finland. The Holocene 13(6):829–838
Meehl GA, Tebaldi C (2004) More Intense, more frequent, and longer lasting heat waves in the 21st century. Science 305(5686):994–997
Navarro Cerrillo RM, Varo MA, Lanjeri S, Hernández Clemente R (2007) Cartografía de defoliación en los pinares de pino silvestre (Pinus sylvestris L.) y pino salgareño (Pinus nigra Arnold.) en la Sierra de los Filabres. Ecosistemas 16(3):163–171
Nicault A, Alleaume S, Brewer S, Carrer M, Nola P, Guiot J (2008) Mediterranean drought fluctuation during the last 500 years based on tree-ring data. Clim Dynam 31(2):227–245
Nikolov N, Helmisaari H (1992) Silvics of the circumpolar boreal forest tree species. In: Shugart HH, Leemans R, Bonan GB (eds) A systems analysis of the global boreal forest. Cambridge University Press, Cambridge, pp 13–84
Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2008) Vegan: community ecology package. R package version 1.15-0. http://cran.r-project.org/, http://vegan.r-forge.r-project.org/
Panyushkina IP, Hughes MK, Vaganov EA, Munro MAR (2003) Summer temperature in northeastern Siberia since 1642 reconstructed from tracheid dimensions and cell numbers of Larix cajanderi. Can J For Res 33:1905–1914
Pichler P, Oberhuber W (2007) Radial growth response of coniferous forest trees in an inner Alpine environment to heat-wave in 2003. For Ecol Manag 242:688–699
Piovesan G, Biondi F, Di Filippo A, Alessandrini A, Maugeri M (2008) Drought-driven growth reduction in old beech (Fagus sylvatica) forests of the central Apennines, Italy. Glob Change Biol 14:1265–1281
Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH (2006) Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant, Cell Environ 29:1618–1628
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Rasband WS (1997) ImageJ (1.38x). U.S. National Institutes of Health, Bethesda, Maryland, USA
Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R, Borghetti M (2006) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol 170(2):301–310
Rossi S, Deslauriers A, Gričar J, Seo J-W, Rathgeber CB, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R (2008) Critical temperatures for xylogenesis in conifers of cold climates. Glob Ecol Biogeogr 17(6):696–707
Rötzer T, Grote R, Pretzsch (2004) The timing of bud burst and its effect on tree growth. Int J Biometeorol 48:109–118
Schmitz N, Verheyden A, Kairo JG, Beeckman H, Koedam N (2007) Successive cambia development in Avicennia marina (Forssk.) Vierh. is not climatically driven in the seasonal climate at Gazi Bay, Kenya. Dendrochronologia 25:87–96
St-Germain J-L, Krause C (2008) Latitudinal variation in tree-ring and wood cell characteristics of Picea mariana across the continuous boreal forest in Quebec. Can J For Res 38(6):397–1405
Stokes MA, Smiley TL (1968) An introduction to tree-ring dating. University of Chicago Press, Chicago
Tardif J, Conciatori F (2006) Influence of climate on tree rings and vessel features in red oak and white oak growing near their northern distribution limit, Southwestern Quebec, Canada. Can J For Res 36:2317–2330
Ter Braak CJF (1994) Canonical community ordination. Part I: basic theory and linear methods. Ecoscience 1(2):127–140
Trigo IF, Davies TD, Bigg GR (1999) Objective climatology of cyclones in the mediterranean region. J Clim 12(6):1685–1696
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer Verlag, New York
Uggla C, Magel E, Moritz T, Sundberg B (2001) Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in scots pine. Plant Physiol 125:2029–2039
Vaganov EA, Hughes MK, Shaskin AV (2006) Growth dynamics of conifer tree rings-images of past and futures environments. Springer, Heidelberg
Vicente-Serrano SM, Beguería S, López-Moreno JI (2010) A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J Clim 23(7):1696–1718
Vysotskaya LG, Vaganov EA (1989) Components of the variability of radial cell size in tree rings of conifers. IAWA Bulletin 10:417–428
Wang L, Payette S, Bégin Y (2002) Relationships between anatomical and densitometric characteristics of black spruce and summer temperature at tree line in northern Quebec. Can J For Res 32(3):477–486
Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195(2):285–289
Wimmer R, Grabner M (2000) A comparison of tree-ring features in Picea abies as correlated with climate. IAWA J 21(4):403–416
Yasue K, Funada R, Kobayashi O, Ohtani J (2000) The effects of tracheid dimensions on variations in maximum density of Picea glehnii and relationships to climatic factors. Trees 14:223–229
Acknowledgments
The authors wish to thank Nele Schmitz for her help and advice on wood sample preparation. Caroline Leland provided critical feedback that improved an earlier version of this manuscript. The Spanish National Meteorological Agency (AEMET) provided climate data. Two anonymous reviewers provided suggestions that helped improve an earlier version of this manuscript. Lamont-Doherty Earth Observatory Contribution No. 7598. This work has been supported by the Spanish Ministry of Science of Education through project AGL2010.21153.02.01. D. M-B was supported by a Fulbright-MICIIN postdoctoral fellowship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Matyssek.
Rights and permissions
About this article
Cite this article
Martin-Benito, D., Beeckman, H. & Cañellas, I. Influence of drought on tree rings and tracheid features of Pinus nigra and Pinus sylvestris in a mesic Mediterranean forest. Eur J Forest Res 132, 33–45 (2013). https://doi.org/10.1007/s10342-012-0652-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10342-012-0652-3