, Volume 26, Issue 2, pp 621–630 | Cite as

Growth patterns in relation to drought-induced mortality at two Scots pine (Pinus sylvestris L.) sites in NE Iberian Peninsula

  • Ana-Maria HereşEmail author
  • Jordi Martínez-Vilalta
  • Bernat Claramunt López
Original Paper


Drought-related tree mortality has become a widespread phenomenon. Scots pine (Pinus sylvestris L.) is a boreal species with high ecological amplitude that reaches its southwestern limit in the Iberian Peninsula. Thus, Iberian Scots pine populations are particularly good models to study the effects of the increase in aridity predicted by climate change models. A total of 78 living and 39 dead Scots pines trees were sampled at two sites located in the NE of the Iberian Peninsula, where recent mortality events have been recorded. Annual tree rings were used to (1) date dead trees; (2) investigate if there was an association between the occurrence of tree death and severe drought periods characterized by exceptionally low ratios of summer precipitation to potential evapotranspiration (P/PET); and (3) to compare the growth patterns of trees that died with those of surviving ones. Mixed models were used to describe the relationships between tree growth (in terms of basal area increment, BAI, and the percentage of latewood, LW%) and climate variables. Our results showed a direct association between Scots pine mortality and severe drought periods characterized by low summer water availability. At the two sites, the growth patterns of dead trees were clearly distinguishable from those of the trees that survived. In particular, the BAI of dead trees was more sensitive to climate dryness (low P/PETsummer, high temperatures) and started to decline below the values of surviving neighbors 15–40 years before the time of death, implying a slow process of growth decline preceding mortality.


Scots pine Mortality Drought Tree rings Climate–growth relationships 



We would like to thank Miquel Ninyerola and the Servei Meteorològic de Catalunya (SMC) for providing the climatic datasets used in this study. We are indebted to Dr. M. Mencuccini for field work and interesting discussions related to the study. Two anonymous referees are thanked for their thorough review and useful suggestions. Field and laboratory assistance of A. Vilà and M. Sabaté is very much appreciated. This study was supported by the Spanish Ministry of Science and Innovation via the competitive projects CGL2007-60120 and CSD2008-0040, and by the Spanish Ministry of Education via a FPU scholarship.

Supplementary material

468_2011_628_MOESM1_ESM.jpg (1.2 mb)
Correlation coefficients of growth indices with precipitation and temperature data corresponding to August (Year prior to growth) to December (Year of growth) period, for Prades (a) and Arcalís (b). Climate and growth indices data are from the period 1952 to 2008. Asterisks indicate significant relationships (p < 0.05) (JPEG 1.15 MB)
468_2011_628_MOESM2_ESM.jpg (910 kb)
Temporal (1951–2008) growth trends (RW) of Scots pine trees from Prades (JPEG 909 KB)
468_2011_628_MOESM3_ESM.jpg (851 kb)
Temporal (1951–2008) growth trends (RW) of Scots pine trees from Arcalís (JPEG 851 KB)


  1. Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci USA 95:14839–14842. doi: 10.1073/pnas.95.25.14839 PubMedCrossRefGoogle Scholar
  2. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. doi: 10.1016/j.foreco.2009.09.001 CrossRefGoogle Scholar
  3. Amoroso MM, Daniels LD (2010) Cambial mortality in declining Austrocedrus chilensis forests: implications for stand dynamics. Can J For Res 40:885–893. doi: 10.1139/X10-042 CrossRefGoogle Scholar
  4. Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean Basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University, Cambridge, pp 153–170Google Scholar
  5. Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (2008) Climate change and water. Technical paper VI of the intergovernmental panel on climate change. IPCC Secretariat, Geneva, pp 210Google Scholar
  6. Bigler C, Bugmann H (2003) Growth-dependent tree mortality models based on tree rings. Can J For Res 33:210–221. doi: 10.1139/X02-180 CrossRefGoogle Scholar
  7. Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosyst 9:330–343. doi: 10.1007/s10021-005-0126-2 CrossRefGoogle Scholar
  8. Bigler C, Gavin DG, Gunning C, Veblen TT (2007) Drought induces lagged tree mortality in a subalpine forest in the Rocky Mountains. Oikos 116:1983–1994. doi: 10.1111/j.2007.0030-1299.16034.x CrossRefGoogle Scholar
  9. Biondi F (1999) Comparing tree-ring chronologies and repeated timber inventories as forest monitoring tools. Ecol Appl 9:216–227. doi: 10.1890/1051-0761(1999)009[0216:CTRCAR]2.0.CO;2 CrossRefGoogle Scholar
  10. Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon WT, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: The physical science basis. contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University, Cambridge, pp 847–940Google Scholar
  11. Das AJ, Battles JJ, Stephenson NL, van Mantgem PJ (2007) The relationship between tree growth patterns and likelihood of mortality: a study of two tree species in the Sierra Nevada. Can J For Res 37:580–597. doi: 10.1139/X06-262 CrossRefGoogle Scholar
  12. Dobbertin M (2005) Tree growth as indicator of tree vitality and of tree reaction to environmental stress: a review. Eur J For Res 124:319–333. doi: 10.1007/s10342-005-0085-3 CrossRefGoogle Scholar
  13. Douville H, Chauvin F, Planton S, Royer JF, Salas-Mélia D, Tyteca S (2002) Sensitivity of the hydrological cycle to increasing amounts of greenhouse gases and aerosols. Clim Dyn 20:45–68. doi: 10.1007/s00382-002-0259-3 CrossRefGoogle Scholar
  14. Drobyshev I, Linderson H, Sonesson K (2007) Temporal mortality pattern of pedunculate oaks in southern Sweden. Dendrochronol 24:97–108. doi: 10.1016/j.dendro.2006.10.004 CrossRefGoogle Scholar
  15. 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. doi: 10.1093/treephys/tpp035 PubMedCrossRefGoogle Scholar
  16. Ellenberg H (1988) Vegetation ecology of Central Europe. Cambridge University, CambridgeGoogle Scholar
  17. Fritts HC (2001) Tree rings and climate (Reprint of second printing). Blackburn, New JerseyGoogle Scholar
  18. Galiano L, Martínez-Vilalta J, Lloret F (2010) Drought-induced multifactor decline of Scots pine in the Pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosyst 13:978–991. doi: 10.1007/s10021-010-9368-8 CrossRefGoogle Scholar
  19. Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol. doi: 10.1111/j.1469-8137.2010.03628.x
  20. Gruber A, Strobl S, Veit B, Oberhuber W (2010) Impact of drought on the temporal dynamics of wood formation in Pinus sylvestris. Tree Physiol 30:490–501. doi: 10.1093/treephys/tpq003 PubMedCrossRefGoogle Scholar
  21. Grudd H, Briffa KR, Karlén W, Bartholin TS, Jones PD, Kromer B (2002) A 7400-year tree-ring chronology in northern Swedish Lapland: natural climatic variability expressed on annual to millennial timescales. Holocene 12:657–665. doi: 10.1191/0959683602hl578rp CrossRefGoogle Scholar
  22. Guarín A, Taylor AH (2005) Drought triggered tree mortality in mixed conifer forests in Yosemite National Park, California, USA. For Ecol Manag 218:229–244. doi: 10.1016/j.foreco.2005.07.014 CrossRefGoogle Scholar
  23. Gutiérrez E (1989) Dendroclimatological study of Pinus sylvestris L. in Southern Catalonia (Spain). Tree Ring Bull 49:1–9Google Scholar
  24. Helama S, Lindholm M, Timonen M, Meriläinen J, Eronen M (2002) The supra-long Scots pine tree-ring record for Finnish Lapland: Part 2, interannual to centennial variability in summer temperatures for 7500 years. Holocene 12:681–687. doi: 10.1191/0959683602hl581rp CrossRefGoogle Scholar
  25. Helama S, Timonen M, Holopainen J, Ogurtsov MG, Mielikäinen K, Eronen M, Lindholm M, Meriläinen J (2009) Summer temperature variations in Lapland during the Medieval Warm Period and the Little Ice Age relative to natural instability of thermohaline circulation on multi-decadal and multi-centennial scales. J Quat Sci 24:450–456. doi: 10.1002/jqs.1291 CrossRefGoogle Scholar
  26. Hereter A, Sánchez JR (1999) Experimental areas of Prades and Montseny. In: Rodà F, Retana J, Gracia CA, Bellot J (eds) Ecology of Mediterranean Evergreen Oak forests. Springer Press, Berlin, pp 15–27CrossRefGoogle Scholar
  27. Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-ring Bull 43:69–78Google Scholar
  28. IPCC (2007) Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  29. 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. doi: 10.1093/treephys/18.6.393 PubMedGoogle Scholar
  30. Linares JC, Camarero JJ, Carreira JA (2010) Competition modulates the adaptation capacity of forests to climatic stress: insights from recent growth decline and death in relict stands of the Mediterranean fir Abies pinsapo. J Ecol 98:592–603. doi: 10.1111/j.1365-2745.2010.01645.x CrossRefGoogle Scholar
  31. Manion PD (1991) Tree disease concepts. Prentice Hall, New JerseyGoogle Scholar
  32. Martín-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. doi: 10.1007/s00468-007-0191-6 CrossRefGoogle Scholar
  33. Martínez-Vilalta J, Piñol J (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manag 161:247–256. doi: 10.1016/S0378-1127(01)00495-9 CrossRefGoogle Scholar
  34. 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 14:1–14. doi: 10.1111/j.1365-2486.2008.01685.x CrossRefGoogle Scholar
  35. McDowell N (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. doi: 10.1104/pp.110.170704 PubMedCrossRefGoogle Scholar
  36. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. doi: 10.1111/j.1469-8137.2008.02436.x PubMedCrossRefGoogle Scholar
  37. McDowell N, Allen CD, Marshall L (2010) Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus ponderosa elevational transect. Glob Change Biol 16:399–415. doi: 10.1111/j.1365-2486.2009.01994.x CrossRefGoogle Scholar
  38. Ninyerola M, Pons X, Roure JM (2000) A methodological approach of climatological modelling of air temperature and precipitation through GIS techniques. Int J Climatol 20:1823–1841. doi: 10.1002/10970088(20001130)20:14<1823:AID-JOC566>3.0.CO;2-B CrossRefGoogle Scholar
  39. Ninyerola M, Pons X, Roure JM (2007a) Monthly precipitation mapping of the Iberian Peninsula using spatial interpolation tools implemented in a Geographic Information System. Theoret Appl Climatol 89:195–209. doi: 10.1007/s00704-006-0264-2 CrossRefGoogle Scholar
  40. Ninyerola M, Pons X, Roure JM (2007b) Objective air temperature mapping for the Iberian Peninsula using spatial interpolation and GIS. Int J Climatol 27:1231–1242. doi: 10.1002/joc.1462 CrossRefGoogle Scholar
  41. Ogle K, Whitham TG, Cobb NS (2000) Tree-ring variation in pinyon predicts likelihood of death following severe drought. Ecol 81:3237–3243. doi: 10.1890/0012-9658(2000)081[3237:TRVIPP]2.0.CO;2 CrossRefGoogle Scholar
  42. Pedersen BS (1998) The role of stress in the mortality of Midwestern oaks as indicated by growth prior to death. Ecology 79:79–93. doi: 10.1890/0012-9658(1998)079[0079:TROSIT]2.0.CO;2 CrossRefGoogle Scholar
  43. Pedersen BS (1999) The mortality of Midwestern overstory oaks as a bioindicator of environmental stress. Ecol Appl 9:1017–1027. doi: 10.1890/1051-0761(1999)009[1017:TMOMOO]2.0.CO;2 CrossRefGoogle Scholar
  44. Pilcher JR (1990) Sample Preparation, Cross-dating, and Measurements. In: Cook ER, Kairiukstis LA (eds) Methods of dendrochronology—applications in the environmental sciences. Kluwer Academic, Dordrecht, pp 40–50Google Scholar
  45. Piñol J, Lledó MJ, Escarré A (1991) Hydrological balance of two Mediterranean forested catchments (Prades, northeast Spain). Hydrol Sci J 36:95–107. doi: 10.1080/02626669109492492 CrossRefGoogle Scholar
  46. Pons X (1996) Estimación de la radiación solar a partir de modelos digitales de elevaciones. Propuesta metodológica. In: Juaristi J, Moro I (eds) VII Coloquio de Geografίa Cuantitativa, Sistemas de Información Geográfica y Teledetección. Vitoria-Gasteiz, Spain, pp 87–97Google Scholar
  47. Poyatos R, Latron J, Llorens P (2003) Land use and land cover change after agricultural abandonment—the case of a Mediterranean mountain area (Catalan Pre-Pyrenees). Mt Res Dev 23:362–368. doi: 10.1659/0276-4741(2003)023[0362:LUALCC]2.0.CO;2 CrossRefGoogle Scholar
  48. Régent Instruments Inc (2004) WinDendro For Tree-Ring Analysis, Régent Instruments Quebec, CanadaGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. Rigling A, Bräker O, Schneiter G, Schweingruber F (2002) Intra-annual tree-ring parameters indicating differences in drought stress of Pinus sylvestris forests within the Erico-Pinion in the Valais (Switzerland). Plant Ecol 163:105–121. doi: 10.1023/A:1020355407821 CrossRefGoogle Scholar
  51. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281. doi: 10.1111/j.1469-8137.2009.03167.x PubMedCrossRefGoogle Scholar
  52. SPSS Inc (2006) SPSS Base 15.0 for Windows User’s Guide. SPSS Inc Chicago IL, USAGoogle Scholar
  53. Suarez ML, Ghermandi L, Kitzberger T (2004) Factors predisposing episodic drought-induced tree mortality in Nothofagus–site, climatic sensitivity and growth trends. Ecol 92:954–966. doi: 10.1111/j.1365-2745.2004.00941.x CrossRefGoogle Scholar
  54. Thornthwaite CW (1948) An approach toward a rational classification of climate. Geogr Rev 38:55–94CrossRefGoogle Scholar
  55. Vaganov EA, Hughes MK, Shashkin AV (2006) Growth dynamics of conifer tree rings images of past and future environments. Springer, BerlinGoogle Scholar
  56. van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH, Veblen TT (2009) Widespread increase of tree mortality rates in the Western United States. Science 323:521–524. doi: 10.1126/science.1165000 PubMedCrossRefGoogle Scholar
  57. Vilà-Cabrera A, Martínez-Vilalta J, Vayreda J, Retana J (2011) Structural and climatic determinants of demographic rates of Scots pine forests across the Iberian Península. Ecol Appl. doi: 10.1890/10-0647.1
  58. Villalba R, Veblen TT (1998) Influences of large-scale climatic variability on episodic tree mortality in northern Patagonia. Ecol 79:2624–2640. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  59. Weber P, Bugmann H, Rigling A (2007) Radial growth response to drought of Pinus sylvestris and Quercus pubescens in an inner-Alpine dry valley. J Veg Sci 18:777–792. doi: 10.1658/1100-9233(2007)18[777:RGRTDO]2.0.CO;2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ana-Maria Hereş
    • 1
    Email author
  • Jordi Martínez-Vilalta
    • 1
  • Bernat Claramunt López
    • 1
  1. 1.CREAF/Unitat d’Ecologia, Departament de Biologia Animal, Biologia Vegetal y EcologiaUniversitat Autònoma de Barcelona, Edifici C (Facultat de Ciències)BarcelonaSpain

Personalised recommendations