Abstract
Dendroclimatology generally assumes that climate–growth relationships are age and size independent. However, there is evidence that climate response can be unstable across different age/size classes. In addition, the occurrence of some anatomical features, such as intra-annual density fluctuations (IADFs), is age dependent. The present study investigates whether the climate–growth responses and the occurrence of IADFs in an even-aged stand of Pinus pinaster Ait., growing under Mediterranean climate, are also size-dependent. We randomly selected 60 P. pinaster trees falling within two stem diameter classes: small (<27 cm) and large (>35 cm). Tree rings were crossdated, measured and IADFs identified according to their position within the ring. The residual chronologies of both size classes were strongly correlated, suggesting a common signal. In fact, similar growth–climate relationships were observed in large and small trees. The frequency of IADFs was higher in large than in small trees, suggesting that IADFs were more likely to occur in wider rings of fast-growing trees. In both size classes, most of the IADFs were found in latewood. Latewood IADFs were triggered by the combination of dry June, wet September, and warm December, whereas IADFs located at the end of earlywood were triggered by previous winter precipitation and favorable conditions before summer (high precipitation for large trees and lower temperature for small trees). Our results suggest that IADFs can be a mechanism used at the individual level for adaptation to drought in P. pinaster. The climatic signal of IADFs between earlywood and latewood was mediated by stem size suggesting that future tree-ring studies should include trees stratified by size to better estimate the sensitivity of IADFs to climate.
Similar content being viewed by others
References
Abe H, Nakai T (1999) Effect of the water status within a tree on tracheid morphogenesis in Cryptomeria japonica D. Don. Trees 14:124–129. doi:10.1007/PL00009758
Andreu L, Gutiérrez E, Macias M, Ribas M, Bosh O, Camarero JJ (2007) Climate increases regional tree-growth variability in Iberian pine forests. Glob Change Biol 13:804–815. doi:10.1111/j.1365-2486.2007.01322.x
Battipaglia G, De Micco V, Brand WA, Linke P, Aronne G, Saurer M, Cherubini P (2010) Variations of vessel diameter and δ13C in false rings of Arbutus unedo L. reflect different environmental conditions. New Phytol 188:1099–1112. doi:10.1111/j.1469-8137.2010.03443.x
Bogino SM, Bravo F (2008) Growth response of Pinus pinaster Ait. to climatic variables in central Spanish forests. Ann For Sci 65:506. doi:10.1051/forest
Bogino S, Bravo F (2009) Climate and intraannual density fluctuations in Pinus pinaster subsp. mesogeensis in Spanish woodlands. Can J For Res 39:1557–1565
Briffa KR, Jones PD (1990) Basic chronology statistics and assessment. In: Cook ER, Kairiukstis LA (eds) Methods of dendrochronology: applications in the environmental sciences. Kluwer Academic Publishers, Boston, pp 137–152
Bunn A (2008) A dendrochronology program library in R (dplR). Dendrochronologia 26:115–124. doi:10.1016/j.dendro.2008.01.002
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
Campelo F, Nabais C, Freitas H, Gutiérrez E (2007) Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal. Ann For Sci 64:229–238. doi:10.1051/forest
Campelo F, García-González I, Nabais C (2012) detrendeR—a graphical user interface to process and visualize tree-ring data using R. Dendrochronologia 30:57–60. doi:10.1016/j.dendro.2011.01.010
Carrer M, Urbinati C (2004) Age-dependent tree-ring growth responses to climate in Larix decidua and Pinus cembra. Ecology 85:730–740. doi:10.1890/02-0478
Chhin S, Hogg E, Lieffers V, Huang S (2008) Potential effects of climate change on the growth of lodgepole pine across diameter size classes and ecological regions. For Ecol Manag 256:1692–1703. doi:10.1016/j.foreco.2008.02.046
De Luis M, Gričar J, Čufar K, Raventós J (2007) Seasonal dynamics of wood formation: a comparison between pinning, microcoring and dendrometer measurements. IAWA J 28:389–404
De Luis M, Novak K, Čufar K, Raventós J (2009) Size mediated climate–growth relationships in Pinus halepensis and Pinus pinea. Trees 23:1065–1073. doi:10.1007/s00468-009-0349-5
De Luis M, Novak K, Raventós J, Gričar J, Prislan P, Čufar K (2011) Climate factors promoting intra-annual density fluctuations in Aleppo pine (Pinus halepensis) from semiarid sites. Dendrochronologia 29:163–169. doi:10.1016/j.dendro.2011.01.005
De Micco V, Saurer M, Aronne G, Tognetti R, Cherubini P (2007) Variations of wood anatomy and δ13C within-tree rings of coastal Pinus pinaster showing intra-annual density fluctuations. IAWA J 28:61–74
De Micco V, Battipaglia G, Brand WA, Linke P, Saurer M, Aronne G, Cherubini P (2012) Discrete versus continuous analysis of anatomical and δ13C variability in tree rings with intra-annual density fluctuations. Trees 26:513–524. doi:10.1007/s00468-011-0612-4
Deslauriers A, Rossi S, Anfodillo T, Saracino A (2008) Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiol 28:863–871
Domec J-C, Gartner BL (2002) How do water transport and water storage differ in coniferous earlywood and latewood? J Exp Bot 53:2369–2379. doi:10.1093/jxb/erf100
Dorado Liñán I, Gutiérrez E, Heinrich I, Andreu-Hayles L, Muntán E, Campelo F, Helle G (2011) 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. doi:10.1007/s10342-011-0566-5
Edmondson J (2010) The meteorological significance of false rings in eastern redcedar (Juniperus virginiana L.) from the southern Great Plains, U.S.A. Tree Ring Res 66:19–33
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. doi:10.1016/j.foreco.2008.03.015
Griffin D, Meko DM, Touchan R, Leavitt SW, Woodhouse CA (2011) Latewood chronology development for summer-moisture reconstruction in the U.S. Southwest. Tree Ring Res 67:87–101. doi:10.3959/2011-4.1
He J-S, Zhang Q-B, Bazzaz FA (2005) Differential drought responses between saplings and adult trees in four co-occurring species of New England. Trees 19:442–450. doi:10.1007/s00468-004-0403-2
Hoffer M, Tardif JC (2009) False rings in jack pine and black spruce trees from eastern Manitoba as indicators of dry summers. Can J For Res 39:1722–1736. doi:10.1139/X09-088
Jayawickrama KJS, Mckeand SE, Jett JB, Wheeler EA (1997) Date of earlywood–latewood transition in provenances and families of loblolly pine, and its relationship to growth phenology and juvenile wood specific gravity. Can J For Res 27:1245–1253
Larson PR (1994) The vascular cambium: development and structure. Springer, Berlin
Linares JC, Camarero JJ, Carreira JA (2009) Plastic responses of Abies pinsapo xylogenesis to drought and competition. Tree Physiol 29:1525–1536. doi:10.1093/treephys/tpp084
Liu C (1986) Rectifying radii on off-center increment cores. For Sci 32:1058–1061
Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ 33:1721–1730. doi:10.1111/j.1365-3040.2010.02176.x
Martinez-Meier A, Sanchez L, Pastorino M, Gallo L, Rozenberg P (2008) What is hot in tree rings? The wood density of surviving Douglas-firs to the 2003 drought and heat wave. For Ecol Manag 256:837–843. doi:10.1016/j.foreco.2008.05.041
Masiokas M, Villalba R (2004) Climatic significance of intra-annual bands in the wood of Nothofagus pumilio in southern Patagonia. Trees 18:696–704. doi:10.1007/s00468-004-0355-6
Medlyn BE, Loustau D, Delzon S (2002) Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant Cell Environ 25:1155–1165. doi:10.1046/j.1365-3040.2002.00890.x
Mérian P, Lebourgeois F (2011) Size-mediated climate–growth relationships in temperate forests: a multi-species analysis. For Ecol Manag 261:1382–1391. doi:10.1016/j.foreco.2011.01.019
Meyer FD, Braker OU (2001) Climate response in dominant and suppressed spruce trees, Picea abies (L.) Karst., on a subalpine and lower montane site in Switzerland. Ecoscience 8:105–114
Osborn TJ, Briffa KR, Jones PD (1997) Adjusting variance for sample-size in tree-ring chronologies and other regional mean time series. Dendrochronologia 15:89–99
Paiva JAP, Garnier-Géré PH, Rodrigues JC, Alves A, Santos S, Graça J, Le Provost G, Chaumeil G, Da Silva-Perez D, Bosc A, Fevereiro P, Plomion C (2008) Plasticity of maritime pine (Pinus pinaster) wood-forming tissues during a growing season. New Phytol 179:1080–1094. doi:10.1111/j.1469-8137.2008.02536.x
Pereira JS (2002) Pinus pinaster. In: Pines of silvicultural importance: compiled from the Forestry Compendium, CAB International. CABI Publishing, New York, pp 316–328
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. doi:10.1016/j.foreco.2007.02.007
Rathgeber CBK, Misson L, Nicault A, Guiot J (2005) Bioclimatic model of tree radial growth: application to the French Mediterranean Aleppo pine forests. Trees 19:162–176. doi:10.1007/s00468-004-0378-z
Rathgeber CBK, Rossi S, Bontemps J-D (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438. doi:10.1093/aob/mcr168
Rigling A, Waldner PO, Forster T, Bräker OU, Pouttu A (2001) Ecological interpretation of tree-ring width and intraannual density fluctuations in Pinus sylvestris on dry sites in the central Alps and Siberia. Can J For Res 31:18–31. doi:10.1139/cjfr-31-1-18
Rinn F (2003) TSAP-Win: Time series analysis and presentation for dendrochronology and related applications. Version 0.53 for Microsoft Windows. User Reference. Rinntech Heidelberg, Heidelberg, p 91
Rossi S, Deslauriers A, Anfodillo T, Carrer M (2008) Age-dependent xylogenesis in timberline conifers. New Phytol 177:199–208. doi:10.1111/j.1469-8137.2007.02235.x
Rozas V, García-González I, Zas R (2011) Climatic control of intra-annual wood density fluctuations of Pinus pinaster in NW Spain. Trees 25:443–453. doi:10.1007/s00468-010-0519-5
Stokes MA, Smiley TC (1996) An introduction to tree-ring dating. The University of Arizona Press, Tucson
Szeicz JM, MacDonald GM (1994) Age-dependent tree-ring growth responses of subarctic white spruce to climate. Can J For Res 24:120–132
Touchan R, Shishov VV, Meko DM, Nouiri I, Grachev A (2012) Process based model sheds light on climate sensitivity of Mediterranean tree-ring width. Biogeosciences 9:965–972. doi:10.5194/bg-9-965-2012
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
Utsumi Y, Sano Y, Funada R, Ohtani J, Fujikawa S (2003) Seasonal and perennial changes in the distribution of water in the sapwood of conifers in a sub-frigid zone. Plant Physiol 131:1826–1833. doi:10.1104/pp.102.014795.large
Vaganov E, Hughes M, Shashkin A (2006) (2006) Growth dynamics of conifer tree rings. Springer, Heidelberg
Vieira J, Campelo F, Nabais C (2009) Age-dependent responses of tree-ring growth and intra-annual density fluctuations of Pinus pinaster to Mediterranean climate. Trees 23:257–265. doi:10.1007/s00468-008-0273-0
Vieira J, Campelo F, Nabais C (2010) Intra-annual density fluctuations of Pinus pinaster are a record of climatic changes in the western Mediterranean region. Can J For Res 40:1567–1575. doi:10.1139/X10-096
Wang X, Zhang Y, McRae DJ (2009) Spatial and age-dependent tree-ring growth responses of Larix gmelinii to climate in northeastern China. Trees 23:875–885. doi:10.1007/s00468-009-0329-9
Wigley TML, Briffa KR, Jones PD (1984) On the average value correlated time series, with applications in dendrochronology and hydrometeorology. J Clim Appl Meteorol 23:201–2013
Wimmer R (2002) Wood anatomical features in tree-rings as indicators of environmental change. Dendrochronologia 20:21–36. doi:10.1078/1125-7865-00005
Wimmer R, Strumia G, Holawe F (2000) Use of false rings in Austrian pine to reconstruct early growing season precipitation. Can J For Res 30:1691–1697. doi:10.1139/cjfr-30-11-1691
Xing P, Zhang Q, Baker PJ (2012) Age and radial growth pattern of four tree species in a subtropical forest of China. Trees 26:283–290. doi:10.1007/s00468-011-0590-6
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. doi:10.1007/s00468-007-0170-y
Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin
Zweifel R, Zimmermann L, Zeugin F, Newbery DM (2006) Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. J Exp Bot 57:1445–1459. doi:10.1093/jxb/erj125
Acknowledgments
The authors wish to thank the communicating editor and two anonymous reviewers for their suggestions and comments that helped to improve the original version of the paper. This study was supported by the Portuguese Foundation for Science and Technology (FCT), through a postdoctoral research grant (SFRH/BPD/47822/2008) attributed to Filipe Campelo and a PhD grant (SFRH/BD/48089/2008) attributed to Joana Vieira, with funds from POPH (Portuguese Operational Human Potential Program) and QREN Portugal (Portuguese National Strategic Reference Framework).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Leavitt.
Rights and permissions
About this article
Cite this article
Campelo, F., Vieira, J. & Nabais, C. Tree-ring growth and intra-annual density fluctuations of Pinus pinaster responses to climate: does size matter?. Trees 27, 763–772 (2013). https://doi.org/10.1007/s00468-012-0831-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-012-0831-3