Geographically Structured Growth decline of Rear-Edge Iberian Fagus sylvatica Forests After the 1980s Shift Toward a Warmer Climate

Abstract

Warming-related growth decrease on southern Fagus sylvatica forests has been observed in different regions; however, whether it is a generalized fact or not remains unclear. Here we investigate the geographical pattern on growth response of the southwestern European beech forests to the warming climate shift which started in the 1980s. We sampled 15 beech forests (215 trees) across four climatically contrasting regions (Mediterranean, Pyrenean, low- and high-elevation Atlantic areas) near the southern distribution limit of the species in the Iberian Peninsula. Dendrochronological analyses were carried out to evaluate the growth of European beech since the 1950s. Growth responses quantified as pointer years, abrupt growth changes and long-term growth trends were compared between periods (before and after the 1980s climate shift), geographical regions and tree sizes. Analyses of the studied variables indicated a growth decrease in basal area increment after the climate shift in three of the four studied regions. Pyrenean stands were not negatively influenced by the climate shift, although an increase in the frequency of negative abrupt growth changes was also found there. Growth after the climate shift presented divergent patterns depending on the geographical region. Although Mediterranean and Atlantic stands presented different indicators of constrained growth, Pyrenean stands showed rising long-term growth trends. Such results suggest that regional characteristics differentially determine the growth response of the southern European beech forests to recent warming periods. Iberian beech forests located at the Pyrenees would benefit from forecasted warming conditions, whereas Atlantic and Mediterranean forests would be more prone to suffer warming-related growth decline.

This is a preview of subscription content, log in to check access.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

References

  1. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Camilo Villegas J, Breshears DD, Zou CB, Troch PA, Huxman TE. 2009. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Natl Acad Sci USA 106:7063–6. https://doi.org/10.1073/pnas.0901438106.

    Article  PubMed  Google Scholar 

  2. Adams HD, Zeppel MJB, Anderegg WRL, Hartmann H, Landhäusser SM, Tissue DT, Huxman TE, Hudson PJ, Franz TE, Allen CD et al. 2017. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol 1:1285–91. https://doi.org/10.1038/s41559-017-0248-x.

    Article  PubMed  Google Scholar 

  3. Adams HR, Barnard HR, Loomis AK. 2014. Topography alters tree growth-climate relationships in a semi-arid forested catchment. Ecosphere 11:1–16. https://doi.org/10.1890/ES14/00296.1.

    Article  Google Scholar 

  4. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell NG, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–84. https://doi.org/10.1016/jforeco.2009.09.001.

    Article  Google Scholar 

  5. Allen CD, Breshears DD, McDowell NG. 2015. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:1–55. https://doi.org/10.1890/ES15-00203.1.

    Article  Google Scholar 

  6. Anderegg WRL, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak E, Ogle K, Shaw JD, Shevliakova E, Williams AP et al. 2015. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349:528–32. https://doi.org/10.1126/science.aab1833.

    Article  CAS  Google Scholar 

  7. Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. 2015. Larger trees suffer most during drought in forests worldwide. Nat Plants 28:1–15139. https://doi.org/10.1038/NPLANTS.2015.139.

    Article  Google Scholar 

  8. Benito-Garzón M, Sánchez de Dios R, Sainz-Ollero H. 2008. Effects of climate change on the distribution of Iberian tree species. Appl Veg Sci 11:169–78. https://doi.org/10.3170/2008-7-18348.

    Article  Google Scholar 

  9. Biondi F, Qeadan F. 2008. A theory-driven approach to tree-ring standardization: defining the biological trend from expected basal area increment. Tree-Ring Res 64:81–96. https://doi.org/10.3959/2008-6.1.

    Article  Google Scholar 

  10. Bunn A, Korpela M, Biondi F, Campelo F, Mérian P, Qeadan F, Zang C, Pucha-Cofrep D, Wernicke J. 2018. dplR: Dendrochronology Program Library in R. R package version 1.6.8. https://r-forge.r-project.org/projects/dplr/.

  11. Camarero JJ, Bigler C, Linares JC, Gil-Pelegrín E. 2011. Synergistic effects of past historical logging and drought on the decline of Pyrenean silver fir forests. For Ecol Manag 262:759–69.

    Article  Google Scholar 

  12. Camarero JJ, Gazol A, Sangüesa-Barreda G, Oliva J, Vicente-Serrano SM. 2015. To die or not to die: early-warning signals of dieback in response to a severe drought. J Ecol 103:44–57.

    Article  CAS  Google Scholar 

  13. Camarero JJ, Gazol A, Sangüesa-Barreda G, Cantero A, Sánchez-Salguero R, Sánchez-Miranda A, Granda E, Serra-Maluquer X, Ibáñez R. 2018. Forest growth responses to drought at short- and long-term scales in Spain: squeezing the stress memory from tree rings. Front Ecol Evolut 6:9. https://doi.org/10.3389/fevo.2018.00009.

    Article  Google Scholar 

  14. Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J. 2011. Widespread crown condition decline, food weeb disruption and amplified tree mortality with increased climate change type drought. Proc Natl Acad Sci USA 108:1474–8. https://doi.org/10.1073/pnas.1010070108.

    Article  CAS  PubMed  Google Scholar 

  15. Cavin L, Jump AS. 2017. Highest drought sensitivity and lowest resistance to growth suppression are found in the range core of the tree Fagus sylvatica L. not the equatorial range edge. Glob Change Biol 23:362–79. https://doi.org/10.1111/gcb.13366.

    Article  Google Scholar 

  16. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–6. https://doi.org/10.1126/science.1206432.

    Article  CAS  Google Scholar 

  17. Colangelo M, Camarero JJ, Borghetti M, Gazol A, Gentilesca T, Ripullone F. 2017. Size matters a lot: drought-affected Italian oaks are smaller and show lower growth prior to tree death. Front Plant Sci 8:135.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Cropper JP. 1979. Tree-ring skeleton plotting by computer. Tree-Ring Bull 39:47–59.

    Google Scholar 

  19. Dittmar C, Zech W, Elling W. 2003. Growth variations of common beech (Fagus sylvatica L.) under climatic and environmental conditions in Europe—a dendroecological study. For Ecol Manag 173:63–78. https://doi.org/10.1016/S0378-1127(01)00816-7.

    Article  Google Scholar 

  20. Dorado-Liñán I, Akhmetzyanov L, Menzel A. 2017. Climate threats on growth of rear-edge European beech peripheral populations in Spain. Int J Biometeorol 61:2097–110. https://doi.org/10.1007/s00484-017-1410-5.

    Article  PubMed  Google Scholar 

  21. Dulamsuren C, Hauck M, Kopp G, Ruff M, Leuschner C. 2016. European beech responds to climate change with growth decline at lower, and growth increase at higher elevations in the center of its distribution range (SW Germany). Trees 31:673–86. https://doi.org/10.1007/s00468-016-1499-x.

    Article  Google Scholar 

  22. Galván JD, Camarero JJ, Sangüesa-Barreda G, Alla AQ, Gutiérrez E. 2012. Sapwood area drives growth in mountain conifer forests. J Ecol 100:1233–44.

    Article  Google Scholar 

  23. Garamszegi B, Kern Z. 2014. Climate influence on radial growth of Fagus sylvatica growing near the edge of its distribution in Bükk Mts, Hungary. Dendrobiology 72:93–102.

    Article  Google Scholar 

  24. Gazol A, Camarero JJ, Gutiérrez E, Popa I, Andreu-Hayles L, Motta R, Nola P, Ribas M, Sangüesa-Barreda G, Urbinati C et al. 2015. Distinct effects of climate warming on populations of silver fir (Abies alba) across Europe. J Biogeogr 42:1150–62.

    Article  Google Scholar 

  25. Gazol A, Camarero JJ, Anderegg WRL, Vicente-Serrano SM. 2017. Impacts of droughts on the growth resilience of the Northern Hemisphere forests. Glob Ecol Biogeogr 26:166–76.

    Article  Google Scholar 

  26. Gazol A, Camarero JJ, Vicente-Serrano SM, Sánchez-Salguero R, Gutiérrez E, de Luis M, Sangüesa-Barreda G, Novak K, Rozas V, Tíscar PA et al. 2018. Forest resilience to drought varies across biomes. Glob Change Biol 24:2143–58. https://doi.org/10.1111/gcb.14082.

    Article  Google Scholar 

  27. Gonzalez-Hidalgo JC, Peña-Angulo D, Brunetti M, Cortesi N. 2015. Recent trend in temperature evolution in Spanish mainland (1951–2010): from warming to hiatus. Int J Climatol 36:2405–16. https://doi.org/10.1002/joc.4519.

    Article  Google Scholar 

  28. Greenwood S, Ruiz-Benito P, Martínez-Vilalta J, Lloret F, Kitzberger T, Allen CD, Fensham R, Laughlin DC, Kattge J, Bönisch G et al. 2017. Tree mortality across biomes is promoted by drought intensity, lower wood density and higher specific leaf area. Ecol Lett 20:539–53. https://doi.org/10.10111/ele.12748.

    Article  PubMed  Google Scholar 

  29. Gutiérrez E. 1988. Dendroecological study of Fagus sylvatica L. in the Montseny Mountains (Spain). Acta Oecol 9:301–9.

    Google Scholar 

  30. Hacket-Pain AJ, Cavin L, Friend AD, Jump AS. 2016. Consistent limitation of growth by high temperature and low precipitation from range core to southern edge of European beech indicates widespread vulnerability to changing climate. Eur J For Res 135:897–909.

    Article  Google Scholar 

  31. Hacket-Pain AJ, Friend AD. 2017. Increased growth and reduced summer drought limitation at the southern limit of Fagus sylvatica L., despite regionally warmer and drier conditions. Dendrochronologia 44:22–30. https://doi.org/10.1016/j.dendro.2017.02.005.

    Article  Google Scholar 

  32. Harris IC, Jone PD. 2017. CRU TS4.01: Climatic Research unit (CRU) Time Series (TS) version 4.01 of high resolution gridded data of month-by-month variation in climate (Jan 1901–Dec 2016). Centre for Environmental Data analyses, 04 December 2017. https://doi.org/10.5285/58a8802721c94c66ae45c3baa4d814d0.

  33. Holmes RL. 1983. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:69–78.

    Google Scholar 

  34. Hurrell JW. 1996. Influence of variations in extratropical wintertime teleconnections on Northern Hemisphere temperature. Geophys Res Lett 23:665–8.

    Article  Google Scholar 

  35. IPCC. 2014. Climate Change 2014: Synthesis Report. In: Puchauri RK, Meyer LA, Eds. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Geneva: IPCC. p. 151.

  36. Jump AS, Hunt MJ, Peñuelas J. 2006. Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Change Biol 12:2163–74. https://doi.org/10.1111/j.1365-2486.2006.01250x.

    Article  Google Scholar 

  37. Köcher P, Gebauer T, Horna V, Leuschner C. 2009. Leaf water status and stem xylem flux in relation to soil drought in five temperate broad-leaved tree species with contrasting water use strategies. Ann For Sci 66:101.

    Article  Google Scholar 

  38. Knutzen F, Meier IC, Leuschner C. 2015. Does reduced precipitation trigger physiological and morphological drought adaptations in European beech (Fagus sylvatica L.)? Comparing provenances across precipitation gradient. Tree Physiol 35:949–63. https://doi.org/10.1093/treephys/tpv057.

    Article  CAS  PubMed  Google Scholar 

  39. Knutzen F, Dulamsuren C, Meier IC, Leuschner C. 2017. Recent climate warming-related growth decline impairs European Beech in the center of its distribution range. Ecosystems 20:1494–511. https://doi.org/10.1007/s10021-017-0128-x.

    Article  CAS  Google Scholar 

  40. Lendzion J, Leuschner C. 2008. Growth of European beech (Fagus sylvatica L.) saplings is limited by elevated atmospheric vapour pressure deficits. For Ecol Manag 256:648–55. https://doi.org/10.1016/j.foreco.2008.05.008.

    Article  Google Scholar 

  41. Lenth R. 2018. emmeans: Estimated marginal means, aka least-square means. R package version 1.1. https://CRAN.R-project.org/package=emmeans.

  42. Linares JC, Camarero JJ. 2012. From pattern to process: linking intrinsic water use efficiency to drought-induced forest decline. GlobChange Biol 18:1000–15. https://doi.org/10.1111/j.1365-2486.2011.02566.x.

    Article  Google Scholar 

  43. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: Why do some plants survive, while others succumb to drought? N Phytol 178:719–39. https://doi.org/10.10111/j.1469-8137.2008.02436.x.

    Article  Google Scholar 

  44. Peltier DMP, Fell M, Ogle K. 2016. Legacy effects of drought in the southwestern United States: a multi species synthesis. Ecol Monogr 86:312–26. https://doi.org/10.1002/ecm.1219.

    Article  Google Scholar 

  45. Pinheiro J, Bates D, Debroy S, Sarkar D, R Core Team. 2017. nlme: Linear mixed effects models. R package version 3.1-131. https://CRAN.R-project.org/package=nlme.

  46. Piovesan G, Biondi F, Di Filippo A, Alessandrini A, Maugeri M. 2008. Drought-driven growth reduction in old beech (Fagus sylvatica L.) forests of the central Apennines, Italy. Glob Change Biol 14:1265–81. https://doi.org/10.1111/j.1365.2486.2008.01570.x.

    Article  Google Scholar 

  47. Príncipe A, van der Maaten E, van der Maaten-Theunissen M, Struwe T, Wilmking M, Kreyling J. 2017. Low resistance but high resilience in growth of a major deciduous forest tree (Fagus sylvatica L.) in response to late spring frost in southern Germany. Trees 31:743–51.

    Article  Google Scholar 

  48. R core Team. 2017. R: A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. R foundation for Satatistical Computing. Retrieved from https://www.R-project.org/.

  49. Reid PC, Hari RE, Beaugrand G, Livingstone DM, Marty C, Straile D, Barichivich J, Goberville E, Adrian R, Aono Y et al. 2016. Global impacts of the 1980s regime shift. Glob Change Biol 22:682–703. https://doi.org/10.1111/gcb.13106.

    Article  Google Scholar 

  50. Rogers BM, Solvik K, Hogg EH, Ju J, Masek JG, Michaelian M, Berner LT, Goetz SJ. 2018. Detecting early warning signals of tree mortality in boreal North America using multiscale satellite data. Glob Change Biol 24:2284–304. https://doi.org/10.10111/gcb.14107.

    Article  Google Scholar 

  51. Rozas V. 2015. Individual-based approach as useful tool to disentangle the relative importance of tree age, size and inter-tree competition in dendroclimatic studies. iForest 8:187–94. https://doi.org/10.3832/ifor1249-007.

    Article  Google Scholar 

  52. Rozas V, Camarero JJ, Sangüesa-Barreda G, Souto M, García-González I. 2015. Summer drought and ENSO-related cloudiness distinctly drive Fagus sylvatica growth near the species rear-edge in the northern Spain. Agric For Meteorol 201:153–64.

    Article  Google Scholar 

  53. Ryan MG, Phillips N, Bond BJ. 2006. The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–81. https://doi.org/10.1111/j.1365-3040.2005.01478.x.

    Article  PubMed  Google Scholar 

  54. Sánchez-Salguero R, Camarero JJ, Gutiérrez E, González-Rouco F, Gazol A, Sangüesa-Barreda G, Andreu-Hayles L, Linares JC, Seftigen K. 2017. Assessing forest vulnerability to climate warming using a process based model of tree growth: bad prospects for rear-edges. Glob Change Biol 23:2705–19. https://doi.org/10.10111/gcb.13541.

    Article  Google Scholar 

  55. Schwalm CR, Anderegg WRL, Michalak AM, Fisher JB, Biondi F, Koch G, Litvak M, Ogle K, Shaw JD, Wolf A et al. 2017. Global patterns of drought recovery. Nature 548:202–5. https://doi.org/10.1038/nature23021.

    Article  CAS  PubMed  Google Scholar 

  56. Schweingruber FH, Eckstein D, Serre-Bachet F, Bräker OU. 1990. Identification, presentation and interpretation of event years and pointer years in dendrochronology. Dendrochronologia 8:9–38.

    Google Scholar 

  57. Tegel W, Seim A, Hakelberg D, Hoffmann S, Panev M, Westphal T, Büntgen U. 2014. A recent growth increase of European beech (Fagus sylvatica L.) at its Mediterranean distribution limit contradicts drought stress. Eur J For Res 133:61–71. https://doi.org/10.1007/s10342-013-0737-7.

    Article  Google Scholar 

  58. Thiel D, Kreyling J, Backhaus S, Beierkuhnlein C, Buhk C, Egen K, Huber G, Konnert M, Nagy L, Jentsch A. 2014. Different reactions of central and marginal provenances of Fagus sylvatica to experimental drought. Eur J For Res 133:247–60. https://doi.org/10.1007/s10342-013-0750-x.

    Article  Google Scholar 

  59. Tuhkanen S. 1980. Climatic parameters and indices in plant geography. Acta Phytogeogr Suec 67:1–105.

    Google Scholar 

  60. Van der Maaten-Theunissen M, van der Maaten E, Bouriaud O. 2015. pointRes: An R package to analyze pointer years and components of resilience. Dendrochronologia 35:34–8. https://doi.org/10.1016/j.dendro.2015.05.006.

    Article  Google Scholar 

  61. Van der Werf GW, Sass-Klaassen UGW, Mohren GMJ. 2007. The impact of the 2003 summer drought on the intra-annual growth pattern of beech (Fagus sylvatica L.) and oak (Quercus robur L.) On a dry site in the Netherlands. Dendrochronologia 25:103–12. https://doi.org/10.1016/j.dendro.2007.03.004.

    Article  Google Scholar 

  62. Vanoni M, Bugmann H, Nötzli M, Bigler C. 2016. Drought and frost contribute to abrupt growth decreases before tree mortality in nine temperate tree species. For Ecol Manag 382:51–63.

    Article  Google Scholar 

  63. Vicente-Serrano SM, Beguería S, López-Moreno JI. 2010. A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J Clim 23:1696–718.

    Article  Google Scholar 

  64. Weber P, Bugmann H, Pluess AR, Walthert L, Rigling A. 2013. Drought response and changing mean sensitivity of European beech close to the dry distribution limit. Trees 27:171–81. https://doi.org/10.1007/s00468-012-0786-4.

    Article  Google Scholar 

  65. Zeileis A, Kleiber C, Krämer W, Hornik K. 2003. Testing and dating structural changes in practice. Comput Stat Data Anal 44:109–23. https://doi.org/10.1016/S0167-9473(03)00030-6.

    Article  Google Scholar 

  66. Zimmermann J, Hauck M, Dulamsuren C, Leuschner C. 2015. Climate warming-related growth decline affects Fagus sylvatica, but not other broad-leaved tree species in central European forests. Ecosystems 18:560–72. https://doi.org/10.10007/s10021-015-9849-x.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Pere Casals who helped us during the fieldwork on the Montsec site. This study was supported by project FunDiver (CGL2015-69186-C2-1-R) funded by the Spanish Ministry of Economy, Industry and Competitiveness (MINECO), INIA (RTA 2006-00117) and CANOPEE (Interreg V-A POCTEFA 2014-2020-FEDER funds). XSM is supported by FPI grant from the Spanish Ministry of Economy, Industry and Competitiveness (BES-2016-077676). GSB and RSS are supported by “Juan de la Cierva” grants (FJCI 2016-30121, IJCI-2015-25845, respectively, FEDER funds). We thank the editorial tasks of two anonymous reviewers and the editor. We also thank all regional administrations for providing sampling permissions (Gobierno de Navarra, Gobierno de Aragón, HAZI, Gobierno de Euskadi, Junta de Castilla y León and Generalitat de Catalunya).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Xavier Serra-Maluquer.

Additional information

Author Contributions

XSM, AG and JJC conceived the ideas. JJC, GSB, RSS, MC, VR, XSM and EG conducted fieldwork and tree-ring data processing. XSM and AG analyzed the data. XSM led the writing with assistance of all authors. All the authors contributed to the discussion, read and approved the final draft.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 471 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Serra-Maluquer, X., Gazol, A., Sangüesa-Barreda, G. et al. Geographically Structured Growth decline of Rear-Edge Iberian Fagus sylvatica Forests After the 1980s Shift Toward a Warmer Climate. Ecosystems 22, 1325–1337 (2019). https://doi.org/10.1007/s10021-019-00339-z

Download citation

Keywords

  • climate warming
  • dendroecology
  • growth decline
  • tree rings
  • climate shift
  • beech
  • Iberian Peninsula